Publikationsserver der Universitätsbibliothek Marburg

Titel:Recruitment of erythrocyte membrane components by apicomplexan parasites Babesia divergens and Plasmodium falciparum
Autor:Gangopadhyay, Preetish
Weitere Beteiligte: Lingelbach,Klaus (Prof. Dr.)
Veröffentlicht:2015
URI:https://archiv.ub.uni-marburg.de/diss/z2015/0410
DOI: https://doi.org/10.17192/z2015.0410
URN: urn:nbn:de:hebis:04-z2015-04109
DDC: Biowissenschaften, Biologie
Titel (trans.):Rekrutierung von Erythrozytenmembran Komponenten durch Apicomplexan Parasites Babesia divergens und Plasmodium falciparum
Publikationsdatum:2015-12-16
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Parasitologie, microscopy,cell biology,Plasmodium falciparum, Mikroskopie, Parasitoloy, Babesia divergens

Summary:
There are a few parasitic protozoa that infect erythrocyte and the erythrocyte does not play any essential or even obligatory role in the parasite survival and subsequent development for most of these, but for two apicomplexan parasites of the genera Plasmodium and Babesia. For these parasites, the host erythrocyte plays a vital role in survival and in associated pathogenicity (directly or indirectly). Moreover these two parasites are also known to alter the host cell differentially; for what seems customising it to specific requirements. Of these alterations one prominent is the formation of the unique vacuolar compartment ‘parasitophorus vacuole’ surrounded by ‘parasitophorus vacuole membrane. However our idea about the contribution of the host cell towards the PVM is limited. In absence of any marker for PVM, the formation and the fate too had not been studied in details but in a few apicomplexa. I took the advantage of a Babesia divergens strain, adapted to human erythrocytes (B. divergens normally infect cattle or immuno-suppressed humans) and used Plasmodium falciparum clone 3D7 (routinely cultured in human erythrocyte) and did a detailed comparative analysis between the PVM formed the invasion of these two related obligate intracellular apicomplexa in identical host cell (erythrocyte). Ultrastructure analysis of infected erythrocytes revealed that unlike Plasmodium falciparum, which remained inside the PV all along the intra-erythrocytic development, the Babesia divergens lost its PVM sometime soon after invasion: an observation, possibly indicating that the maintenance of the PV per se as a protective environment is not a prerequisite for this parasite growth. Thereafter with a strict selection of erythrocyte membrane proteins (membrane anchor containing, membrane spanning, cytoskeletal, cytoskeleton associated and erythrocyte surface receptor), reportedly internalized or discounted during the invasion by P. falciparum and present or absent on the newly formed PVM based on their association with erythrocyte cytoskeleton, I performed epifluorescence microscopy and biochemical analysis. I aimed to demonstrate the fate of these proteins parallaly in P. falciparum and B. divergens infected erythrocytes. I took help of immuno-electron microscopy to confirm my results. With fluorescence microscopy, I could show that both of the parasites took up labelled lipid components were from the labelled erythrocyte surface and recruited them onto their respective PVMs. However there was a difference in the recruitment of proteins between these two. A high copy number, erythrocyte membrane protein (Band 3) and a cytoskeletal protein (Spectrin) was found present in the PVM of Babesia divergens but not in PVM of Plasmodium falciparum. Parallel to this in B. divergens infected erythrocytes; PVM-localization could not be confirmed for few proteins, for which incorporation into the PVM of P. falciparum had been suggested in several reports. Altogether the results obtained from this study suggest that the recruitment or exclusion of specific membrane components is determined in a parasite specific manner and is not regulated by the intrinsic properties of the erythrocyte membrane. However incorporation or exclusion of different proteins may also reflect difference in the preferred entry sites for these parasites, leading ultimately to the difference in components of the PVM and show the possibility of using such parasites as molecular tools for understanding the inducible physiological processes, generally silent in such quiescent cells (erythrocyte).

Bibliographie / References

  1. LAEMMLI, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-5.
  2. PLATTNER, F. & SOLDATI-FAVRE, D. 2008. Hijacking of host cellular functions by the Apicomplexa. Annu Rev Microbiol, 62, 471-87.
  3. TOPOLSKA, A. E., LIDGETT, A., TRUMAN, D., FUJIOKA, H. & COPPEL, R. L. 2004. Characterization of a membrane-associated rhoptry protein of Plasmodium falciparum. J Biol Chem, 279, 4648-56.
  4. COOKE, B. M., MOHANDAS, N., COWMAN, A. F. & COPPEL, R. L. 2005. Cellular adhesive phenomena in apicomplexan parasites of red blood cells. Vet Parasitol, 132, 273-95.
  5. M. 2005. Adhesion of Plasmodium falciparum-infected red blood cells to CD36 under flow is enhanced by the cerebral malaria-protective trait South-East Asian ovalocytosis. Mol Biochem Parasitol, 142, 252-7.
  6. COOKE, B. M., MOHANDAS, N. & COPPEL, R. L. 2001. The malaria-infected red blood cell: structural and functional changes. Adv Parasitol, 50, 1-86.
  7. GILLIGAN, D. M. & BENNETT, V. 1993. The junctional complex of the membrane skeleton. Semin Hematol, 30, 74-83.
  8. MORDUE, D. G., DESAI, N., DUSTIN, M. & SIBLEY, L. D. 1999. Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J Exp Med, 190, 1783-92.
  9. LEY, V., ROBBINS, E. S., NUSSENZWEIG, V. & ANDREWS, N. W. 1990. The exit of Trypanosoma cruzi from the phagosome is inhibited by raising the pH of acidic compartments. J Exp Med, 171, 401-13.
  10. OLLOMO, B., DURAND, P., PRUGNOLLE, F., DOUZERY, E., ARNATHAU, C., NKOGHE, D., LEROY, E. & RENAUD, F. 2009. A new malaria agent in African hominids. PLoS Pathog, 5, e1000446.
  11. SCHROEDER, G. N. & HILBI, H. 2008. Molecular pathogenesis of Shigella spp.: controlling host cell signaling, invasion, and death by type III secretion. Clin Microbiol Rev, 21, 134- 56.
  12. URSITTI, J. A., PUMPLIN, D. W., WADE, J. B. & BLOCH, R. J. 1991. Ultrastructure of the human erythrocyte cytoskeleton and its attachment to the membrane. Cell Motil Cytoskeleton, 19, 227-43.
  13. YU, J., FISCHMAN, D. A. & STECK, T. L. 1973. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J Supramol Struct, 1, 233-48.
  14. HSU, C. J., LEMAY, A., ESHDAT, Y. & MARCHESI, V. T. 1979. Substructure of human erythrocyte spectrin. J Supramol Struct, 10, 227-39.
  15. SUAREZ, C. E., THOMPSON, S. M., MCELWAIN, T. F., HINES, S. A. & PALMER, G. H. 1994. Conservation of oligopeptide motifs in rhoptry proteins from different genera of erythroparasitic protozoa. Exp Parasitol, 78, 246-51.
  16. OGUN, S. A. & HOLDER, A. A. 1994. Plasmodium yoelii: brefeldin A-sensitive processing of proteins targeted to the rhoptries. Exp Parasitol, 79, 270-8.
  17. NDENGELE, M. M., MESSINEO, D. G., SAM-YELLOWE, T. & HARWALKAR, J. A. 1995. Plasmodium falciparum: effects of membrane modulating agents on direct binding of rhoptry proteins to human erythrocytes. Exp Parasitol, 81, 191-201.
  18. RUDZINSKA, M. A., TRAGER, W., LEWENGRUB, S. J. & GUBERT, E. 1976. An electron microscopic study of Babesia microti invading erythrocytes. Cell Tissue Res, 169, 323- 34.
  19. SCHOLTYSECK, E. & MEHLHORN, H. 1970. Ultrastructural study of characteristic organelles (paired organelles, micronemes, micropores) of sporozoa and related organisms. Z Parasitenkd, 34, 97-127.
  20. MARCHESI, V. T. 1979. Spectrin: present status of a putative cyto-skeletal protein of the red cell membrane. J Membr Biol, 51, 101-31.
  21. KAWAI, S., IGARASHI, I., ABGAANDORJIIN, A., MIYAZAWA, K., IKADAI, H., NAGASAWA, H., FUJISAKI, K., MIKAMI, T., SUZUKI, N. & MATSUDA, H. 1999. Ultrastructural characteristics of Babesia caballi in equine erythrocytes in vitro. Parasitol Res, 85, 794-9.
  22. GORDESKY, S. E. & MARINETTI, G. V. 1973. The asymetric arrangement of phospholipids in the human erythrocyte membrane. Biochem Biophys Res Commun, 50, 1027-31.
  23. LANGRETH, S. G., NGUYEN-DINH, P. & TRAGER, W. 1978b. Plasmodium falciparum: merozoite invasion in vitro in the presence of chloroquine. Exp Parasitol, 46, 235-8.
  24. PARRODI, F., WRIGHT, I. G., BOURNE, A. S. & DOBSON, C. 1989. In vitro adherence of bovine erythrocytes infected with Babesia bovis to thrombospondin and laminin. Int J Parasitol, 19, 567-9.
  25. UPSTON, J. M. & GERO, A. M. 1990. Increased glucose permeability in Babesia bovis-infected erythrocytes. Int J Parasitol, 20, 69-76.
  26. WRIGHT, I. G., GOODGER, B. V., BUFFINGTON, G. D., CLARK, I. A., PARRODI, F. & WALTISBUHL, D. J. 1989. Immunopathophysiology of babesial infections. Trans R Soc Trop Med Hyg, 83 Suppl, 11-3.
  27. LUSTIGMAN, S., ANDERS, R. F., BROWN, G. V. & COPPEL, R. L. 1988. A component of an antigenic rhoptry complex of Plasmodium falciparum is modified after merozoite invasion. Mol Biochem Parasitol, 30, 217-24.
  28. SUAREZ, C. E., MCELWAIN, T. F., STEPHENS, E. B., MISHRA, V. S. & PALMER, G. H. 1991a. Sequence conservation among merozoite apical complex proteins of Babesia bovis, Babesia bigemina and other apicomplexa. Mol Biochem Parasitol, 49, 329-32.
  29. GUNTHER, K., TUMMLER, M., ARNOLD, H. H., RIDLEY, R., GOMAN, M., SCAIFE, J. G. & LINGELBACH, K. 1991. An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein. Mol Biochem Parasitol, 46, 149-57.
  30. JASMER, D. P., REDUKER, D. W., HINES, S. A., PERRYMAN, L. E. & MCGUIRE, T. C. 1992. Surface epitope localization and gene structure of a Babesia bovis 44-kilodalton variable merozoite surface antigen. Mol Biochem Parasitol, 55, 75-83.
  31. GRURING, C. & SPIELMANN, T. 2012. Imaging of live malaria blood stage parasites. Methods Enzymol, 506, 81-92.
  32. COWMAN, A. F. & CRABB, B. S. 2006. Invasion of red blood cells by malaria parasites. Cell, 124, 755-66.
  33. TOMLEY, F. 2009. Apicomplexan biology in the post-genomic era: perspectives from the European COST Action 857. Int J Parasitol, 39, 133-4.
  34. KANEKO, O., YIM LIM, B. Y., IRIKO, H., LING, I. T., OTSUKI, H., GRAINGER, M., TSUBOI, T., ADAMS, J. H., MATTEI, D., HOLDER, A. A. & TORII, M. 2005. Apical expression of three RhopH1/Clag proteins as components of the Plasmodium falciparum RhopH complex. Mol Biochem Parasitol, 143, 20-8.
  35. VINCENSINI, L., FALL, G., BERRY, L., BLISNICK, T. & BRAUN BRETON, C. 2008. The RhopH complex is transferred to the host cell cytoplasm following red blood cell invasion by Plasmodium falciparum. Mol Biochem Parasitol, 160, 81-9.
  36. XIAO, Y. P., AL-KHEDERY, B. & ALLRED, D. R. 2010. The Babesia bovis VESA1 virulence factor subunit 1b is encoded by the 1beta branch of the ves multigene family. Mol Biochem Parasitol, 171, 81-8.
  37. SAM-YELLOWE, T. Y. 2009. The role of the Maurer's clefts in protein transport in Plasmodium falciparum. Trends Parasitol, 25, 277-84.
  38. WEED, R. I. 1970. The importance of erythrocyte deformability. Am J Med, 49, 147-50.
  39. PORCHET-HENNERE, E. & NICOLAS, G. 1983. Are rhoptries of Coccidia really extrusomes? J Ultrastruct Res, 84, 194-203.
  40. RUEF, B. J., DOWLING, S. C., CONLEY, P. G., PERRYMAN, L. E., BROWN, W. C., JASMER, D. P. & RICE-FICHT, A. C. 2000. A unique Babesia bovis spherical body protein is conserved among geographic isolates and localizes to the infected erythrocyte membrane. Mol Biochem Parasitol, 105, 1-12.
  41. PREISER, P., KAVIRATNE, M., KHAN, S., BANNISTER, L. & JARRA, W. 2000. The apical organelles of malaria merozoites: host cell selection, invasion, host immunity and immune evasion. Microbes Infect, 2, 1461-77.
  42. MARECHAL, E. & CESBRON-DELAUW, M. F. 2001. The apicoplast: a new member of the plastid family. Trends Plant Sci, 6, 200-5.
  43. GARCIA, C. R., DE AZEVEDO, M. F., WUNDERLICH, G., BUDU, A., YOUNG, J. A. & BANNISTER, L. 2008. Plasmodium in the postgenomic era: new insights into the molecular cell biology of malaria parasites. Int Rev Cell Mol Biol, 266, 85-156.
  44. POUVELLE, B., SPIEGEL, R., HSIAO, L., HOWARD, R. J., MORRIS, R. L., THOMAS, A. P. & TARASCHI, T. F. 1991. Direct access to serum macromolecules by intraerythrocytic malaria parasites. Nature, 353, 73-5.
  45. MILLER, L. H., BARUCH, D. I., MARSH, K. & DOUMBO, O. K. 2002a. The pathogenic basis of malaria. Nature, 415, 673-9.
  46. SHENAI, B. R., SIJWALI, P. S., SINGH, A. & ROSENTHAL, P. J. 2000. Characterization of native and recombinant falcipain-2, a principal trophozoite cysteine protease and essential hemoglobinase of Plasmodium falciparum. J Biol Chem, 275, 29000-10.
  47. NYALWIDHE, J., BAUMEISTER, S., HIBBS, A. R., TAWILL, S., PAPAKRIVOS, J., VOLKER, U. & LINGELBACH, K. 2002. A nonpermeant biotin derivative gains access to the parasitophorous vacuole in Plasmodium falciparum-infected erythrocytes permeabilized with streptolysin O. J Biol Chem, 277, 40005-11.
  48. NYALWIDHE, J., MAIER, U. G. & LINGELBACH, K. 2003. Intracellular parasitism: cell biological adaptations of parasitic protozoa to a life inside cells. Zoology (Jena), 106, 341-8.
  49. COX-SINGH, J., DAVIS, T. M., LEE, K. S., SHAMSUL, S. S., MATUSOP, A., RATNAM, S., RAHMAN, H. A., CONWAY, D. J. & SINGH, B. 2008. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis, 46, 165- 71.
  50. & LANG, F. 2002. Plasmodium falciparum activates endogenous Cl(-) channels of human erythrocytes by membrane oxidation. EMBO J, 21, 22-30.
  51. REPNIK, U., GANGOPADHYAY, P., BIETZ, S., PRZYBORSKI, J. M., GRIFFITHS, G. & LINGELBACH, K. 2015. The apicomplexan parasite Babesia divergens internalizes band 3, glycophorin A and spectrin during invasion of human red blood cells. Cell Microbiol.
  52. LEVINE, N. D. & IVENS, V. 1988. Cross-transmission of Eimeria spp. (Protozoa, Apicomplexa) of rodents--a review. J Protozool, 35, 434-7.
  53. CURSINO-SANTOS, J. R., HALVERSON, G., RODRIGUEZ, M., NARLA, M. & LOBO, C. A. 2014b. Identification of binding domains on red blood cell glycophorins for Babesia divergens. Transfusion, 54, 982-9.
  54. SIBLEY, L. D. 2004. Intracellular parasite invasion strategies. Science, 304, 248-53.
  55. KYES, S., HORROCKS, P. & NEWBOLD, C. 2001. Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol, 55, 673-707.
  56. GLENISTER, F. K., COPPEL, R. L., COWMAN, A. F., MOHANDAS, N. & COOKE, B. M. 2002. Contribution of parasite proteins to altered mechanical properties of malaria- infected red blood cells. Blood, 99, 1060-3.
  57. WETZEL, D. M., CHEN, L. A., RUIZ, F. A., MORENO, S. N. & SIBLEY, L. D. 2004. Calcium-mediated protein secretion potentiates motility in Toxoplasma gondii. J Cell Sci, 117, 5739-48.
  58. HAKANSSON, S., CHARRON, A. J. & SIBLEY, L. D. 2001. Toxoplasma evacuoles: a two- step process of secretion and fusion forms the parasitophorous vacuole. EMBO J, 20, 3132-44.
  59. WICKHAM, M. E., RUG, M., RALPH, S. A., KLONIS, N., MCFADDEN, G. I., TILLEY, L. & COWMAN, A. F. 2001. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J, 20, 5636-49.
  60. PRZYBORSKI, J. M., MILLER, S. K., PFAHLER, J. M., HENRICH, P. P., ROHRBACH, P., CRABB, B. S. & LANZER, M. 2005. Trafficking of STEVOR to the Maurer's clefts in Plasmodium falciparum-infected erythrocytes. EMBO J, 24, 2306-17.
  61. SCHRIER, S. L. 1985. Red cell membrane biology--introduction. Clin Haematol, 14, 1-12.
  62. COMMINS, M. A., GOODGER, B. V., WALTISBUHL, D. J. & WRIGHT, I. G. 1988. Babesia bovis: studies of parameters influencing microvascular stasis of infected erythrocytes.
  63. WEBSTER, P., DOBBELAERE, D. A. & FAWCETT, D. W. 1985. The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Immunoelectron microscopic observations. Eur J Cell Biol, 36, 157-62.
  64. SCHOLTYSECK, E. & PIEKARSKI, G. 1965. [Electron microscopic studies on merozoites of Eimeria (Eimeria perforans and E. stidae) and Toxoplasma gondii. On the systematic position of T. gondii]. Z Parasitenkd, 26, 91-115.
  65. SARGEANT, T. J., MARTI, M., CALER, E., CARLTON, J. M., SIMPSON, K., SPEED, T. P. & COWMAN, A. F. 2006. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol, 7, R12.
  66. TONKIN, C. J., VAN DOOREN, G. G., SPURCK, T. P., STRUCK, N. S., GOOD, R. T., HANDMAN, E., COWMAN, A. F. & MCFADDEN, G. I. 2004. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol, 137, 13-21.
  67. KIRK, K. & SALIBA, K. J. 2007. Targeting nutrient uptake mechanisms in Plasmodium. Curr Drug Targets, 8, 75-88.
  68. DE KONING-WARD, T. F., GILSON, P. R., BODDEY, J. A., RUG, M., SMITH, B. J., PAPENFUSS, A. T., SANDERS, P. R., LUNDIE, R. J., MAIER, A. G., COWMAN, A. F. & CRABB, B. S. 2009. A newly discovered protein export machine in malaria parasites. Nature, 459, 945-9.
  69. MAIER, A. G., RUG, M., O'NEILL, M. T., BROWN, M., CHAKRAVORTY, S., SZESTAK, T., CHESSON, J., WU, Y., HUGHES, K., COPPEL, R. L., NEWBOLD, C., BEESON, J. G., CRAIG, A., CRABB, B. S. & COWMAN, A. F. 2008. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell, 134, 48-61.
  70. O'CONNOR, R. M., LONG, J. A. & ALLRED, D. R. 1999. Cytoadherence of Babesia bovis- infected erythrocytes to bovine brain capillary endothelial cells provides an in vitro model for sequestration. Infect Immun, 67, 3921-8.
  71. VAN DER GOOT, F. G. & GRUENBERG, J. 2006. Intra-endosomal membrane traffic. Trends Cell Biol, 16, 514-21.
  72. SIM, B. K., ORLANDI, P. A., HAYNES, J. D., KLOTZ, F. W., CARTER, J. M., CAMUS, D., ZEGANS, M. E. & CHULAY, J. D. 1990. Primary structure of the 175K Plasmodium falciparum erythrocyte binding antigen and identification of a peptide which elicits antibodies that inhibit malaria merozoite invasion. J Cell Biol, 111, 1877-84.
  73. WARD, G. E., MILLER, L. H. & DVORAK, J. A. 1993. The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. J Cell Sci, 106 ( Pt 1), 237-48.
  74. LINGELBACH, K. & JOINER, K. A. 1998. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J Cell Sci, 111 ( Pt 11), 1467-75.
  75. TELFORD, S. R., 3RD & SPIELMAN, A. 1993. Reservoir competence of white-footed mice for Babesia microti. J Med Entomol, 30, 223-7.
  76. JOHNSON, D., GUNTHER, K., ANSORGE, I., BENTING, J., KENT, A., BANNISTER, L., RIDLEY, R. & LINGELBACH, K. 1994. Characterization of membrane proteins exported from Plasmodium falciparum into the host erythrocyte. Parasitology, 109 ( Pt 1), 1-9.
  77. MOSSER, D. M. & BRITTINGHAM, A. 1997. Leishmania, macrophages and complement: a tale of subversion and exploitation. Parasitology, 115 Suppl, S9-23.
  78. LOBO, C. A., RODRIGUEZ, M. & CURSINO-SANTOS, J. R. 2012. Babesia and red cell invasion. Curr Opin Hematol, 19, 170-5.
  79. GORENFLOT, A., BRASSEUR, P., PRECIGOUT, E., L'HOSTIS, M., MARCHAND, A. & SCHREVEL, J. 1991. Cytological and immunological responses to Babesia divergens in different hosts: ox, gerbil, man. Parasitol Res, 77, 3-12.
  80. LANGE, Y. & STECK, T. L. 1984. Mechanism of red blood cell acanthocytosis and echinocytosis in vivo. J Membr Biol, 77, 153-9.
  81. SCHWARTZMAN, J. D. & SAFFER, L. D. 1992. How Toxoplasma gondii gets in and out of host cells. Subcell Biochem, 18, 333-64.
  82. SMITH, A. D. & STUBBS, C. D. 1987. Modulation of membrane protein function by bilayer lipids. Basic Res Cardiol, 82 Suppl 1, 93-7.
  83. MCLAREN, D. J., BANNISTER, L. H., TRIGG, P. I. & BUTCHER, G. A. 1977. A freeze- fracture study on the parasite-erythrocyte interrelationship in Plasmodium knowlesi infections. Bull World Health Organ, 55, 199-203.
  84. LAUER, S. A., RATHOD, P. K., GHORI, N. & HALDAR, K. 1997. A membrane network for nutrient import in red cells infected with the malaria parasite. Science, 276, 1122-5.
  85. SPIELMANN, T. & BECK, H. P. 2000. Analysis of stage-specific transcription in plasmodium falciparum reveals a set of genes exclusively transcribed in ring stage parasites. Mol Biochem Parasitol, 111, 453-8.
  86. TRIGLIA, T., HEALER, J., CARUANA, S. R., HODDER, A. N., ANDERS, R. F., CRABB, B. S. & COWMAN, A. F. 2000. Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol, 38, 706-18.
  87. GALINSKI, M. R., MEDINA, C. C., INGRAVALLO, P. & BARNWELL, J. W. 1992. A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell, 69, 1213- 26.
  88. MILLER, S. K., GOOD, R. T., DREW, D. R., DELORENZI, M., SANDERS, P. R., HODDER, A. N., SPEED, T. P., COWMAN, A. F., DE KONING-WARD, T. F. & CRABB, B. S. 2002b. A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J Biol Chem, 277, 47524-32.
  89. DELBECQ, S., PRECIGOUT, E., VALLET, A., CARCY, B., SCHETTERS, T. P. & GORENFLOT, A. 2002. Babesia divergens: cloning and biochemical characterization of Bd37. Parasitology, 125, 305-12.
  90. QUICK, R. E., HERWALDT, B. L., THOMFORD, J. W., GARNETT, M. E., EBERHARD, M. L., WILSON, M., SPACH, D. H., DICKERSON, J. W., TELFORD, S. R., 3RD, STEINGART, K. R., POLLOCK, R., PERSING, D. H., KOBAYASHI, J. M., JURANEK, D. D. & CONRAD, P. A. 1993. Babesiosis in Washington State: a new species of Babesia? Ann Intern Med, 119, 284-90.
  91. HUNFELD, K. P., HILDEBRANDT, A. & GRAY, J. S. 2008. Babesiosis: recent insights into an ancient disease. Int J Parasitol, 38, 1219-37.
  92. COSSART, P. & SANSONETTI, P. J. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science, 304, 242-8.
  93. SHAW, M. K. 2003. Cell invasion by Theileria sporozoites. Trends Parasitol, 19, 2-6.
  94. KRISHNAMURTHY, K., WANG, G., SILVA, J., CONDIE, B. G. & BIEBERICH, E. 2007. Ceramide regulates atypical PKCzeta/lambda-mediated cell polarity in primitive ectoderm cells. A novel function of sphingolipids in morphogenesis. J Biol Chem, 282, 3379-90.
  95. WAYS, P. & HANAHAN, D. J. 1964. Characterization and quantification of red cell lipids in normal man. J Lipid Res, 5, 318-28.
  96. ZINTL, A., WESTBROOK, C., SKERRETT, H. E., GRAY, J. S. & MULCAHY, G. 2002b. Chymotrypsin and neuraminidase treatment inhibits host cell invasion by Babesia divergens (Phylum Apicomplexa). Parasitology, 125, 45-50.
  97. SIMPSON, C. F., KIRKHAM, W. W. & KLING, J. M. 1967. Comparative morphologic features of Babesia caballi and Babesia equi. Am J Vet Res, 28, 1693-7.
  98. Curriculum Vitae Personal data Name: Preetish Gangopadhyay Date of birth: 15 th September 1983
  99. HOYTE, H. M. 1971. Differential diagnosis of Babesia argentina and Babesia bigemina infections in cattle using thin blood smears and brain smears. Aust Vet J, 47, 248-50.
  100. YOKOYAMA, N., OKAMURA, M. & IGARASHI, I. 2006. Erythrocyte invasion by Babesia parasites: current advances in the elucidation of the molecular interactions between the protozoan ligands and host receptors in the invasion stage. Vet Parasitol, 138, 22-32.
  101. SMITH, J. E. 1987. Erythrocyte membrane: structure, function, and pathophysiology. Vet Pathol, 24, 471-6.
  102. HAAS, A. 2009. Everybody has a Home of Their Own – " The Phagosome Zoo " . Intracellular Niches of Microbes. Wiley-VCH Verlag GmbH & Co. KGaA.
  103. LANGRETH, S. G. 1976. Feeding mechanisms in extracellular Babesia microti and Plasmodium lophurae. J Protozool, 23, 215-23.
  104. LANGRETH, S. G., JENSEN, J. B., REESE, R. T. & TRAGER, W. 1978a. Fine structure of human malaria in vitro. J Protozool, 25, 443-52.
  105. MENARD, R. 2001. Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite. Cell Microbiol, 3, 63-73.
  106. GORENFLOT, A., MOUBRI, K., PRECIGOUT, E., CARCY, B. & SCHETTERS, T. P. 1998. Human babesiosis. Ann Trop Med Parasitol, 92, 489-501.
  107. KARA, U., PYE, D., LORD, R., PAM, C., GOULD, H., GEYSEN, M., JONES, G., STENZEL, D., KIDSON, C. & SAUL, A. 1989. Immune response to a synthetic peptide corresponding to an epitope of a parasitophorous vacuole membrane antigen from Plasmodium falciparum. J Immunol, 143, 1334-9.
  108. Master of Science in Biotechnology Faculty of Biotechnology and Microbiology, Bangalore University, Bangalore, Karnataka, India Master thesis: at Department of Immunology and Molecular biology; AMC College, Bangalore, India.
  109. KRUGLIAK, M., ZHANG, J. & GINSBURG, H. 2002. Intraerythrocytic Plasmodium falciparum utilizes only a fraction of the amino acids derived from the digestion of host cell cytosol for the biosynthesis of its proteins. Mol Biochem Parasitol, 119, 249-56.
  110. ZINTL, A., WESTBROOK, C., MULCAHY, G., SKERRETT, H. E. & GRAY, J. S. 2002a. Invasion, and short-and long-term survival of Babesia divergens (Phylum Apicomplexa) cultures in non-bovine sera and erythrocytes. Parasitology, 124, 583-8.
  111. HALDAR, K., ELMENDORF, H. G., DAS, A., LI, W. L., FERGUSON, D. J. & ELFORD, B. C. 1994. In vitro secretory assays with erythrocyte-free malaria parasites. Methods Cell Biol, 45, 221-46.
  112. SAFFER, L. D., MERCEREAU-PUIJALON, O., DUBREMETZ, J. F. & SCHWARTZMAN, J. D. 1992. Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. J Protozool, 39, 526-30.
  113. Place of birth: Calcutta, West Bengal, India University education January 2012-2015
  114. LEECH, J. H., ALEY, S. B., MILLER, L. H. & HOWARD, R. J. 1984. Plasmodium falciparum malaria: cytoadherence of infected erythrocytes to endothelial cells and associated changes in the erythrocyte membrane. Prog Clin Biol Res, 155, 63-77.
  115. LUSE, S. A. & MILLER, L. H. 1971. Plasmodium falciparum malaria. Ultrastructure of parasitized erythrocytes in cardiac vessels. Am J Trop Med Hyg, 20, 655-60.
  116. SAM-YELLOWE, T. Y., FUJIOKA, H., AIKAWA, M. & MESSINEO, D. G. 1995. Plasmodium falciparum rhoptry proteins of 140/130/110 kd (Rhop-H) are located in an electron lucent compartment in the neck of the rhoptries. J Eukaryot Microbiol, 42, 224- 31.
  117. CREWTHER, P. E., CULVENOR, J. G., SILVA, A., COOPER, J. A. & ANDERS, R. F. 1990. Plasmodium falciparum: two antigens of similar size are located in different compartments of the rhoptry. Exp Parasitol, 70, 193-206.
  118. Pr86 to schizont rhoptries and p67 to free merozoites. Mol Biochem Parasitol, 92, 111- 22.
  119. Preparation of doctoral thesis in the research group of Prof. Dr. Klaus Lingelbach Philipps-University of Marburg, Department of Parasitology, Faculty of Biology Title of dissertation: " Recruitment of erythrocyte membrane components by apicomplexan parasites Plasmodium falciparum and Babesia divergens " October 2010-September 2011
  120. GEHDE, N., HINRICHS, C., MONTILLA, I., CHARPIAN, S., LINGELBACH, K. & PRZYBORSKI, J. M. 2009. Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum. Mol Microbiol, 71, 613-28.
  121. WRIGHT, I. G. & GOODGER, B. V. 1973. Proteolytic enzyme activity in the intra-erythrocytic parasites Babesia argentina and Babesia bigemina. Z Parasitenkd, 42, 213-20.
  122. GERO, A. M. & O'SULLIVAN, W. J. 1990. Purines and pyrimidines in malarial parasites. Blood Cells, 16, 467-84; discussion 485-98.
  123. MOHANDAS, N. & CHASIS, J. A. 1993. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol, 30, 171-92.
  124. PAUL, F., ROATH, S., MELVILLE, D., WARHURST, D. C. & OSISANYA, J. O. 1981. Separation of malaria-infected erythrocytes from whole blood: use of a selective high- gradient magnetic separation technique. Lancet, 2, 70-1.
  125. HABERMAN, S., BLANTON, P. & MARTIN, J. 1967. Some observations on the ABO antigen sites of the erythrocyte membranes of adults and newborn infants. J Immunol, 98, 150-60.
  126. GALLAGHER, P. G. & FORGET, B. G. 1993. Spectrin genes in health and disease. Semin Hematol, 30, 4-20.
  127. CRABB, B. S., TRIGLIA, T., WATERKEYN, J. G. & COWMAN, A. F. 1997. Stable transgene expression in Plasmodium falciparum. Mol Biochem Parasitol, 90, 131-44.
  128. MARTI, M., GOOD, R. T., RUG, M., KNUEPFER, E. & COWMAN, A. F. 2004. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science, 306, 1930-3.
  129. LEE, M. D., KING, L. S. & AGRE, P. 1997. The aquaporin family of water channel proteins in clinical medicine. Medicine (Baltimore), 76, 141-56.
  130. VERKLEIJ, A. J., ZWAAL, R. F., ROELOFSEN, B., COMFURIUS, P., KASTELIJN, D. & VAN DEENEN, L. L. 1973. The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim Biophys Acta, 323, 178-93.
  131. SAMUEL, B. U., MOHANDAS, N., HARRISON, T., MCMANUS, H., ROSSE, W., REID, M. & HALDAR, K. 2001. The role of cholesterol and glycosylphosphatidylinositol-anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J Biol Chem, 276, 29319-29.
  132. PETERS, C., AEBISCHER, T., STIERHOF, Y. D., FUCHS, M. & OVERATH, P. 1995. The role of macrophage receptors in adhesion and uptake of Leishmania mexicana amastigotes. J Cell Sci, 108 ( Pt 12), 3715-24.
  133. KIRK, K., HORNER, H. A., ELFORD, B. C., ELLORY, J. C. & NEWBOLD, C. I. 1994. Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel. J Biol Chem, 269, 3339-47.
  134. POOLE, R. C. & HALESTRAP, A. P. 1993. Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am J Physiol, 264, C761-82.
  135. RUDZINSKA, M. A. 1976. Ultrastructure of intraerythrocytic Babesia microti with emphasis on the feeding mechanism. J Protozool, 23, 224-33.
  136. NAGATA, Y. & BURGER, M. M. 1974. Wheat germ agglutinin. Molecular characteristics and specificity for sugar binding. J Biol Chem, 249, 3116-22.
  137. SKRABALO, Z. & DEANOVIC, Z. 1957. Piroplasmosis in man; report of a case. Doc Med Geogr Trop, 9, 11-6.
  138. MORRISSETTE, N. S. & SIBLEY, L. D. 2002. Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev, 66, 21-38; table of contents.
  139. JACKSON, A. P., OTTO, T. D., DARBY, A., RAMAPRASAD, A., XIA, D., ECHAIDE, I. E., FARBER, M., GAHLOT, S., GAMBLE, J., GUPTA, D., GUPTA, Y., JACKSON, L., MALANDRIN, L., MALAS, T. B., MOUSSA, E., NAIR, M., REID, A. J., SANDERS, M., SHARMA, J., TRACEY, A., QUAIL, M. A., WEIR, W., WASTLING, J. M., HALL, N., WILLADSEN, P., LINGELBACH, K., SHIELS, B., TAIT, A., BERRIMAN, M., ALLRED, D. R. & PAIN, A. 2014. The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction. Nucleic Acids Res, 42, 7113-31.
  140. NYALWIDHE, J. & LINGELBACH, K. 2006. Proteases and chaperones are the most abundant proteins in the parasitophorous vacuole of Plasmodium falciparum-infected erythrocytes. Proteomics, 6, 1563-73.
  141. DELPLACE, P., BHATIA, A., CAGNARD, M., CAMUS, D., COLOMBET, G., DEBRABANT, A., DUBREMETZ, J. F., DUBREUIL, N., PRENSIER, G., FORTIER, B. & ET AL. 1988. Protein p126: a parasitophorous vacuole antigen associated with the release of Plasmodium falciparum merozoites. Biol Cell, 64, 215-21.
  142. KNUEPFER, E., RUG, M., KLONIS, N., TILLEY, L. & COWMAN, A. F. 2005. Trafficking determinants for PfEMP3 export and assembly under the Plasmodium falciparum- infected red blood cell membrane. Mol Microbiol, 58, 1039-53.
  143. SPIELMANN, T., GARDINER, D. L., BECK, H. P., TRENHOLME, K. R. & KEMP, D. J. 2006a. Organization of ETRAMPs and EXP-1 at the parasite-host cell interface of malaria parasites. Mol Microbiol, 59, 779-94.
  144. HUTCHINGS, C. L., LI, A., FERNANDEZ, K. M., FLETCHER, T., JACKSON, L. A., MOLLOY, J. B., JORGENSEN, W. K., LIM, C. T. & COOKE, B. M. 2007. New insights into the altered adhesive and mechanical properties of red blood cells parasitized by Babesia bovis. Mol Microbiol, 65, 1092-105.
  145. KHATTAB, A. & KLINKERT, M. Q. 2006. Maurer's clefts-restricted localization, orientation and export of a Plasmodium falciparum RIFIN. Traffic, 7, 1654-65.
  146. KIRK, K. 2001. Membrane transport in the malaria-infected erythrocyte. Physiol Rev, 81, 495- 537.
  147. MURPHY, S. C., HILLER, N. L., HARRISON, T., LOMASNEY, J. W., MOHANDAS, N. & HALDAR, K. 2006. Lipid rafts and malaria parasite infection of erythrocytes. Mol Membr Biol, 23, 81-8.
  148. KOUSSIS, K., WITHERS-MARTINEZ, C., YEOH, S., CHILD, M., HACKETT, F., KNUEPFER, E., JULIANO, L., WOEHLBIER, U., BUJARD, H. & BLACKMAN, M. J. 2009. A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO J, 28, 725-35.
  149. MONTERO, E., GONZALEZ, L. M., RODRIGUEZ, M., OKSOV, Y., BLACKMAN, M. J. & LOBO, C. A. 2006. A conserved subtilisin protease identified in Babesia divergens merozoites. J Biol Chem, 281, 35717-26.
  150. NICHOLS, B. J., KENWORTHY, A. K., POLISHCHUK, R. S., LODGE, R., ROBERTS, T. H., HIRSCHBERG, K., PHAIR, R. D. & LIPPINCOTT-SCHWARTZ, J. 2001. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol, 153, 529-41.
  151. LINGWOOD, D. & SIMONS, K. 2010. Lipid rafts as a membrane-organizing principle. Science, 327, 46-50.
  152. SINAI, A. P. & JOINER, K. A. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol, 51, 415-62.
  153. SPIELMAN, A., WILSON, M. L., LEVINE, J. F. & PIESMAN, J. 1985. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annu Rev Entomol, 30, 439-60.
  154. LEW, V. L., TIFFERT, T. & GINSBURG, H. 2003. Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells. Blood, 101, 4189- 94.
  155. MURPHY, S. C., SAMUEL, B. U., HARRISON, T., SPEICHER, K. D., SPEICHER, D. W., REID, M. E., PROHASKA, R., LOW, P. S., TANNER, M. J., MOHANDAS, N. & HALDAR, K. 2004. Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood, 103, 1920-8.
  156. VAN WIJK, R. & VAN SOLINGE, W. W. 2005. The energy-less red blood cell is lost: erythrocyte enzyme abnormalities of glycolysis. Blood, 106, 4034-42.
  157. GLENISTER, F. K., FERNANDEZ, K. M., KATS, L. M., HANSSEN, E., MOHANDAS, N., COPPEL, R. L. & COOKE, B. M. 2009. Functional alteration of red blood cells by a megadalton protein of Plasmodium falciparum. Blood, 113, 919-28.
  158. SALZER, U. & PROHASKA, R. 2001. Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood, 97, 1141-3.
  159. PASVOL, G., WILSON, R. J., SMALLEY, M. E. & BROWN, J. 1978. Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Ann Trop Med Parasitol, 72, 87-8.
  160. JOINER, K. A. 1991. Rhoptry lipids and parasitophorous vacuole formation: a slippery issue. Parasitol Today, 7, 226-7.
  161. SPEICHER, D. W., WEGLARZ, L. & DESILVA, T. M. 1992. Properties of human red cell spectrin heterodimer (side-to-side) assembly and identification of an essential nucleation site. J Biol Chem, 267, 14775-82.
  162. SAJID, M., WITHERS-MARTINEZ, C. & BLACKMAN, M. J. 2000. Maturation and specificity of Plasmodium falciparum subtilisin-like protease-1, a malaria merozoite subtilisin-like serine protease. J Biol Chem, 275, 631-41.
  163. ROUDIER, N., BAILLY, P., GANE, P., LUCIEN, N., GOBIN, R., CARTRON, J. P. & RIPOCHE, P. 2002. Erythroid expression and oligomeric state of the AQP3 protein. J Biol Chem, 277, 7664-9.
  164. SPYCHER, C., KLONIS, N., SPIELMANN, T., KUMP, E., STEIGER, S., TILLEY, L. & BECK, H. P. 2003. MAHRP-1, a novel Plasmodium falciparum histidine-rich protein, binds ferriprotoporphyrin IX and localizes to the Maurer's clefts. J Biol Chem, 278, 35373-83.
  165. WICKHAM, M. E., CULVENOR, J. G. & COWMAN, A. F. 2003. Selective inhibition of a two- step egress of malaria parasites from the host erythrocyte. J Biol Chem, 278, 37658-63.
  166. RAGHEB, D., DALAL, S., BOMPIANI, K. M., RAY, W. K. & KLEMBA, M. 2011. Distribution and biochemical properties of an M1-family aminopeptidase in Plasmodium falciparum indicate a role in vacuolar hemoglobin catabolism. J Biol Chem, 286, 27255- 65.
  167. MALPEDE, B. M., LIN, D. H. & TOLIA, N. H. 2013. Molecular basis for sialic acid-dependent receptor recognition by the Plasmodium falciparum invasion protein erythrocyte-binding antigen-140/BAEBL. J Biol Chem, 288, 12406-15.
  168. O'CONNOR, R. M. & ALLRED, D. R. 2000. Selection of Babesia bovis-infected erythrocytes for adhesion to endothelial cells coselects for altered variant erythrocyte surface antigen isoforms. J Immunol, 164, 2037-45.
  169. PERKINS, S. L. & AUSTIN, C. C. 2009. Four new species of Plasmodium from New Guinea lizards: integrating morphology and molecules. J Parasitol, 95, 424-33.
  170. JENSEN, J. B. & TRAGER, W. 1977. Plasmodium falciparum in culture: use of outdated erthrocytes and description of the candle jar method. J Parasitol, 63, 883-6.
  171. LAMBROS, C. & VANDERBERG, J. P. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol, 65, 418-20.
  172. KABANOVA, S., KLEINBONGARD, P., VOLKMER, J., ANDREE, B., KELM, M. & JAX, T. W. 2009. Gene expression analysis of human red blood cells. Int J Med Sci, 6, 156-9.
  173. SPIELMANN, T., FERGUSEN, D. J. & BECK, H. P. 2003. etramps, a new Plasmodium falciparum gene family coding for developmentally regulated and highly charged membrane proteins located at the parasite-host cell interface. Mol Biol Cell, 14, 1529-44.
  174. SPIELMANN, T., HAWTHORNE, P. L., DIXON, M. W., HANNEMANN, M., KLOTZ, K., KEMP, D. J., KLONIS, N., TILLEY, L., TRENHOLME, K. R. & GARDINER, D. L. 2006b. A cluster of ring stage-specific genes linked to a locus implicated in cytoadherence in Plasmodium falciparum codes for PEXEL-negative and PEXEL- positive proteins exported into the host cell. Mol Biol Cell, 17, 3613-24.
  175. PASVOL, G., WAINSCOAT, J. S. & WEATHERALL, D. J. 1982b. Erythrocytes deficiency in glycophorin resist invasion by the malarial parasite Plasmodium falciparum. Nature, 297, 64-6.
  176. POLOGE, L. G. & RAVETCH, J. V. 1986. A chromosomal rearrangement in a P. falciparum histidine-rich protein gene is associated with the knobless phenotype. Nature, 322, 474-7.
  177. YOSHIDA, H., KAWANE, K., KOIKE, M., MORI, Y., UCHIYAMA, Y. & NAGATA, S. 2005. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature, 437, 754-8.
  178. ROY, C. R. & MOCARSKI, E. S. 2007. Pathogen subversion of cell-intrinsic innate immunity. Nat Immunol, 8, 1179-87.
  179. MAIER, A. G., COOKE, B. M., COWMAN, A. F. & TILLEY, L. 2009. Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol, 7, 341-54.
  180. Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science, 309, 134-7.
  181. CURSINO-SANTOS, J. R., ALHASSAN, A., SINGH, M. & LOBO, C. A. 2014a. Babesia: impact of cold storage on the survival and the viability of parasites in blood bags. Transfusion, 54, 585-91.
  182. DAS, A., ELMENDORF, H. G., LI, W. I. & HALDAR, K. 1994. Biosynthesis, export and processing of a 45 kDa protein detected in membrane clefts of erythrocytes infected with Plasmodium falciparum. Biochem J, 302 ( Pt 2), 487-96.
  183. MERCIER, C., DUBREMETZ, J. F., RAUSCHER, B., LECORDIER, L., SIBLEY, L. D. & CESBRON-DELAUW, M. F. 2002. Biogenesis of nanotubular network in Toxoplasma parasitophorous vacuole induced by parasite proteins. Mol Biol Cell, 13, 2397-409.
  184. LORIA, P., MILLER, S., FOLEY, M. & TILLEY, L. 1999. Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. Biochem J, 339 ( Pt 2), 363-70.
  185. WETZEL, D. M., SCHMIDT, J., KUHLENSCHMIDT, M. S., DUBEY, J. P. & SIBLEY, L. D. 2005. Gliding motility leads to active cellular invasion by Cryptosporidium parvum sporozoites. Infect Immun, 73, 5379-87.
  186. CORBETT, J. D., CHO, M. R. & GOLAN, D. E. 1994b. Deoxygenation affects fluorescence photobleaching recovery measurements of red cell membrane protein lateral mobility. Biophys J, 66, 25-30.
  187. MOSQUEDA, J., MCELWAIN, T. F., STILLER, D. & PALMER, G. H. 2002. Babesia bovis merozoite surface antigen 1 and rhoptry-associated protein 1 are expressed in sporozoites, and specific antibodies inhibit sporozoite attachment to erythrocytes. Infect Immun, 70, 1599-603.
  188. KAVIRATNE, M., KHAN, S. M., JARRA, W. & PREISER, P. R. 2002. Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryot Cell, 1, 926-35.
  189. RICHIER, E., BIAGINI, G. A., WEIN, S., BOUDOU, F., BRAY, P. G., WARD, S. A., PRECIGOUT, E., CALAS, M., DUBREMETZ, J. F. & VIAL, H. J. 2006. Potent antihematozoan activity of novel bisthiazolium drug T16: evidence for inhibition of phosphatidylcholine metabolism in erythrocytes infected with Babesia and Plasmodium spp. Antimicrob Agents Chemother, 50, 3381-8.
  190. S. 2002. Functional analysis of Plasmodium falciparum merozoite antigens: implications for erythrocyte invasion and vaccine development. Philos Trans R Soc Lond B Biol Sci, 357, 25-33.
  191. MURPHY, S. C., FERNANDEZ-POL, S., CHUNG, P. H., PRASANNA MURTHY, S. N., MILNE, S. B., SALOMAO, M., BROWN, H. A., LOMASNEY, J. W., MOHANDAS, N. & HALDAR, K. 2007. Cytoplasmic remodeling of erythrocyte raft lipids during infection by the human malaria parasite Plasmodium falciparum. Blood, 110, 2132-9.
  192. WATERKEYN, J. G., WICKHAM, M. E., DAVERN, K. M., COOKE, B. M., COPPEL, R. L., REEDER, J. C., CULVENOR, J. G., WALLER, R. F. & COWMAN, A. F. 2000. Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. EMBO J, 19, 2813- 23.
  193. ZWEIG, S. & SINGER, S. J. 1979. Concanavalin A-induced endocytosis in rabbit reticulocytes, and its decrease with reticulocyte maturation. J Cell Biol, 80, 487-91.
  194. GAZARINI, M. L., THOMAS, A. P., POZZAN, T. & GARCIA, C. R. 2003. Calcium signaling in a low calcium environment: how the intracellular malaria parasite solves the problem. J Cell Biol, 161, 103-10.
  195. GRELLIER, P., RIGOMIER, D., CLAVEY, V., FRUCHART, J. C. & SCHREVEL, J. 1991. Lipid traffic between high density lipoproteins and Plasmodium falciparum-infected red blood cells. J Cell Biol, 112, 267-77.
  196. KUNDU, M., LINDSTEN, T., YANG, C. Y., WU, J., ZHAO, F., ZHANG, J., SELAK, M. A., NEY, P. A. & THOMPSON, C. B. 2008. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood, 112, 1493-502.
  197. MOHANDAS, N. & GALLAGHER, P. G. 2008. Red cell membrane: past, present, and future. Blood, 112, 3939-48.
  198. RICHARD, D., KATS, L. M., LANGER, C., BLACK, C. G., MITRI, K., BODDEY, J. A., COWMAN, A. F. & COPPEL, R. L. 2009. Identification of rhoptry trafficking determinants and evidence for a novel sorting mechanism in the malaria parasite Plasmodium falciparum. PLoS Pathog, 5, e1000328.
  199. MONTERO, E., RODRIGUEZ, M., OKSOV, Y. & LOBO, C. A. 2009. Babesia divergens apical membrane antigen 1 and its interaction with the human red blood cell. Infect Immun, 77, 4783-93.
  200. MACKELLAR, D. C., O'NEILL, M. T., ALY, A. S., SACCI, J. B., JR., COWMAN, A. F. & KAPPE, S. H. 2010. Plasmodium falciparum PF10_0164 (ETRAMP10.3) is an essential parasitophorous vacuole and exported protein in blood stages. Eukaryot Cell, 9, 784-94.
  201. KAFSACK, B. F. & CARRUTHERS, V. B. 2010. Apicomplexan perforin-like proteins. Commun Integr Biol, 3, 18-23.
  202. CORBETT, J. D., AGRE, P., PALEK, J. & GOLAN, D. E. 1994a. Differential control of band 3 lateral and rotational mobility in intact red cells. J Clin Invest, 94, 683-8.
  203. SHOHET, S. B., NATHAN, D. G. & KARNOVSKY, M. L. 1968. Stages in the incorporation of fatty acids into red blood cells. J Clin Invest, 47, 1096-108.
  204. WALLER, R. F., REED, M. B., COWMAN, A. F. & MCFADDEN, G. I. 2000. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J, 19, 1794-802.
  205. LAUER, S., VANWYE, J., HARRISON, T., MCMANUS, H., SAMUEL, B. U., HILLER, N. L., MOHANDAS, N. & HALDAR, K. 2000. Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J, 19, 3556-64.
  206. MACKELLAR, D. C., VAUGHAN, A. M., ALY, A. S., DELEON, S. & KAPPE, S. H. 2011. A systematic analysis of the early transcribed membrane protein family throughout the life cycle of Plasmodium yoelii. Cell Microbiol, 13, 1755-67.
  207. TONKIN, M. L., CRAWFORD, J., LEBRUN, M. L. & BOULANGER, M. J. 2013. Babesia divergens and Neospora caninum apical membrane antigen 1 structures reveal selectivity and plasticity in apicomplexan parasite host cell invasion. Protein Science : A Publication of the Protein Society, 22, 114-127.
  208. SIBLEY, L. D. 2011. Invasion and intracellular survival by protozoan parasites. Immunol Rev, 240, 72-91.
  209. LOBO, C. A., CURSINO-SANTOS, J. R., ALHASSAN, A. & RODRIGUES, M. 2013. Babesia: an emerging infectious threat in transfusion medicine. PLoS Pathog, 9, e1003387.
  210. COPPEL, R. L., FAVALORO, J. M., CREWTHER, P. E., BURKOT, T. R., BIANCO, A. E., STAHL, H. D., KEMP, D. J., ANDERS, R. F. & BROWN, G. V. 1985. A blood stage antigen of Plasmodium falciparum shares determinants with the sporozoite coat protein. Proc Natl Acad Sci U S A, 82, 5121-5.
  211. RUDZINSKA, M. A., SPIELMAN, A., LEWENGRUB, S., TRAGER, W. & PIESMAN, J. 1983. Sexuality in piroplasms as revealed by electron microscopy in Babesia microti. Proc Natl Acad Sci U S A, 80, 2966-70.
  212. TOWBIN, H., STAEHELIN, T. & GORDON, J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A, 76, 4350-4.
  213. KILEJIAN, A. 1979. Characterization of a protein correlated with the production of knob-like protrusions on membranes of erythrocytes infected with Plasmodium falciparum. Proc Natl Acad Sci U S A, 76, 4650-3.
  214. LOBO, C. A. 2005. Babesia divergens and Plasmodium falciparum use common receptors, glycophorins A and B, to invade the human red blood cell. Infect Immun, 73, 649-51.
  215. SIMMONS, D., WOOLLETT, G., BERGIN-CARTWRIGHT, M., KAY, D. & SCAIFE, J. 1987. A malaria protein exported into a new compartment within the host erythrocyte. EMBO J, 6, 485-91.
  216. SUAREZ, C. E., FLORIN-CHRISTENSEN, M., HINES, S. A., PALMER, G. H., BROWN, W. C. & MCELWAIN, T. F. 2000. Characterization of allelic variation in the Babesia bovis merozoite surface antigen 1 (MSA-1) locus and identification of a cross-reactive inhibition-sensitive MSA-1 epitope. Infect Immun, 68, 6865-70.
  217. CONBOY, J. G. 1993. Structure, function, and molecular genetics of erythroid membrane skeletal protein 4.1 in normal and abnormal red blood cells. Semin Hematol, 30, 58-73.
  218. SOLDATI-FAVRE, D. 2008. Molecular dissection of host cell invasion by the apicomplexans: the glideosome. Parasite, 15, 197-205.
  219. MESPLET, M., ECHAIDE, I., DOMINGUEZ, M., MOSQUEDA, J. J., SUAREZ, C. E., SCHNITTGER, L. & FLORIN-CHRISTENSEN, M. 2010. Bovipain-2, the falcipain-2 ortholog, is expressed in intraerythrocytic stages of the tick-transmitted hemoparasite Babesia bovis. Parasit Vectors, 3, 113.
  220. MORTENSEN, M., FERGUSON, D. J., EDELMANN, M., KESSLER, B., MORTEN, K. J., KOMATSU, M. & SIMON, A. K. 2010. Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc Natl Acad Sci U S A, 107, 832-7.
  221. SUSS-TOBY, E., ZIMMERBERG, J. & WARD, G. E. 1996. Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci U S A, 93, 8413-8.
  222. KNOWLES, D. W., TILLEY, L., MOHANDAS, N. & CHASIS, J. A. 1997. Erythrocyte membrane vesiculation: model for the molecular mechanism of protein sorting. Proc Natl Acad Sci U S A, 94, 12969-74.
  223. SIMONS, K. & IKONEN, E. 1997. Functional rafts in cell membranes. Nature, 387, 569-72.
  224. MACEDO, C. S., SCHWARZ, R. T., TODESCHINI, A. R., PREVIATO, J. O. & MENDONCA-PREVIATO, L. 2010. Overlooked post-translational modifications of proteins in Plasmodium falciparum: N-and O-glycosylation --a review. Mem Inst Oswaldo Cruz, 105, 949-56.
  225. SINGER, K. A. & MORRISON, M. 1976. Effect of metabolic state on agglutination of human erythrocytes by concanavalin A. Biochim Biophys Acta, 426, 123-31.
  226. UPSTON, J. M. & GERO, A. M. 1995. Parasite-induced permeation of nucleosides in Plasmodium falciparum malaria. Biochim Biophys Acta, 1236, 249-58.
  227. CULVENOR, J. G., LANGFORD, C. J., CREWTHER, P. E., SAINT, R. B., COPPEL, R. L., KEMP, D. J., ANDERS, R. F. & BROWN, G. V. 1987. Plasmodium falciparum: identification and localization of a knob protein antigen expressed by a cDNA clone. Exp Parasitol, 63, 58-67.
  228. SU, X. Z., HEATWOLE, V. M., WERTHEIMER, S. P., GUINET, F., HERRFELDT, J. A., PETERSON, D. S., RAVETCH, J. A. & WELLEMS, T. E. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell, 82, 89-100.
  229. SMITH, J. D., CHITNIS, C. E., CRAIG, A. G., ROBERTS, D. J., HUDSON-TAYLOR, D. E., PETERSON, D. S., PINCHES, R., NEWBOLD, C. I. & MILLER, L. H. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell, 82, 101-10.
  230. GINSBURG, H., KRUGLIAK, M., EIDELMAN, O. & CABANTCHIK, Z. I. 1983. New permeability pathways induced in membranes of Plasmodium falciparum infected erythrocytes. Mol Biochem Parasitol, 8, 177-90.
  231. KNAPP, B., HUNDT, E., NAU, U. & KUPPER, H. A. 1989. Molecular cloning, genomic structure and localization in a blood stage antigen of Plasmodium falciparum characterized by a serine stretch. Mol Biochem Parasitol, 32, 73-83.
  232. KILEJIAN, A., RASHID, M. A., AIKAWA, M., AJI, T. & YANG, Y. F. 1991. Selective association of a fragment of the knob protein with spectrin, actin and the red cell membrane. Mol Biochem Parasitol, 44, 175-81.
  233. SUAREZ, C. E., PALMER, G. H., JASMER, D. P., HINES, S. A., PERRYMAN, L. E. & MCELWAIN, T. F. 1991b. Characterization of the gene encoding a 60-kilodalton Babesia bovis merozoite protein with conserved and surface exposed epitopes. Mol Biochem Parasitol, 46, 45-52.
  234. POUVELLE, B., GORMLEY, J. A. & TARASCHI, T. F. 1994. Characterization of trafficking pathways and membrane genesis in malaria-infected erythrocytes. Mol Biochem Parasitol, 66, 83-96.
  235. DEITSCH, K. W. & WELLEMS, T. E. 1996. Membrane modifications in erythrocytes parasitized by Plasmodium falciparum. Mol Biochem Parasitol, 76, 1-10.
  236. PERKINS, M. E. 1992. Rhoptry organelles of apicomplexan parasites. Parasitol Today, 8, 28- 32.
  237. COOKE, B. M. & COPPEL, R. L. 1995. Cytoadhesion and falciparum malaria: going with the flow. Parasitol Today, 11, 282-7.
  238. LINGELBACH, K. R. 1993. Plasmodium falciparum: a molecular view of protein transport from the parasite into the host erythrocyte. Exp Parasitol, 76, 318-27.
  239. MA, J., RAHLFS, S., JORTZIK, E., SCHIRMER, R. H., PRZYBORSKI, J. M. & BECKER, K. 2012. Subcellular localization of adenylate kinases in Plasmodium falciparum. FEBS Lett, 586, 3037-43.
  240. TENTER, A. M., HECKEROTH, A. R. & WEISS, L. M. 2000. Toxoplasma gondii: from animals to humans. Int J Parasitol, 30, 1217-58.
  241. SALIBA, K. J. & KIRK, K. 2001. Nutrient acquisition by intracellular apicomplexan parasites: staying in for dinner. Int J Parasitol, 31, 1321-30.
  242. MERCIER, C., ADJOGBLE, K. D., DAUBENER, W. & DELAUW, M. F. 2005. Dense granules: are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites? Int J Parasitol, 35, 829-49.
  243. Maurer's clefts: a novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes. Int J Parasitol, 36, 23-36.
  244. STAINES, H. M., ALKHALIL, A., ALLEN, R. J., DE JONGE, H. R., DERBYSHIRE, E., EGEE, S., GINSBURG, H., HILL, D. A., HUBER, S. M., KIRK, K., LANG, F., LISK, G., OTENG, E., PILLAI, A. D., RAYAVARA, K., ROUHANI, S., SALIBA, K. J., SHEN, C., SOLOMON, T., THOMAS, S. L., VERLOO, P. & DESAI, S. A. 2007. Electrophysiological studies of malaria parasite-infected erythrocytes: current status. Int J Parasitol, 37, 475-82.
  245. YEOH, S., O'DONNELL, R. A., KOUSSIS, K., DLUZEWSKI, A. R., ANSELL, K. H., OSBORNE, S. A., HACKETT, F., WITHERS-MARTINEZ, C., MITCHELL, G. H., BANNISTER, L. H., BRYANS, J. S., KETTLEBOROUGH, C. A. & BLACKMAN, M. J. 2007. Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell, 131, 1072-83.
  246. NGUITRAGOOL, W., BOKHARI, A. A., PILLAI, A. D., RAYAVARA, K., SHARMA, P., TURPIN, B., ARAVIND, L. & DESAI, S. A. 2011. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell, 145, 665- 77.
  247. PASVOL, G., JUNGERY, M., WEATHERALL, D. J., PARSONS, S. F., ANSTEE, D. J. & TANNER, M. J. 1982a. Glycophorin as a possible receptor for Plasmodium falciparum. Lancet, 2, 947-50.
  248. PRZYBORSKI, J. M., WICKERT, H., KROHNE, G. & LANZER, M. 2003. Maurer's clefts--a novel secretory organelle? Mol Biochem Parasitol, 132, 17-26.
  249. SLAVIC, K., DERBYSHIRE, E. T., NAFTALIN, R. J., KRISHNA, S. & STAINES, H. M. 2009. Comparison of effects of green tea catechins on apicomplexan hexose transporters and mammalian orthologues. Mol Biochem Parasitol, 168, 113-6.
  250. WAN, K. L., CARRUTHERS, V. B., SIBLEY, L. D. & AJIOKA, J. W. 1997. Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol Biochem Parasitol, 84, 203-14.
  251. POUVELLE, B. & GYSIN, J. 1997. Presence of the parasitophorous duct in Plasmodium falciparum and P. vivax parasitized Saimiri monkey red blood cells. Parasitol Today, 13, 357-61.
  252. UILENBERG, G. 2006. Babesia--a historical overview. Vet Parasitol, 138, 3-10.
  253. GLUSHAKOVA, S., YIN, D., LI, T. & ZIMMERBERG, J. 2005. Membrane transformation during malaria parasite release from human red blood cells. Curr Biol, 15, 1645-50.
  254. KEELEY, A. & SOLDATI, D. 2004. The glideosome: a molecular machine powering motility and host-cell invasion by Apicomplexa. Trends Cell Biol, 14, 528-32.
  255. SANSONETTI, P. 2001. Phagocytosis of bacterial pathogens: implications in the host response. Semin Immunol, 13, 381-90.
  256. SHARMA, P. & CHITNIS, C. E. 2013. Key molecular events during host cell invasion by Apicomplexan pathogens. Curr Opin Microbiol, 16, 432-7.
  257. SPIELMANN, T., MONTAGNA, G. N., HECHT, L. & MATUSCHEWSKI, K. 2012. Molecular make-up of the Plasmodium parasitophorous vacuolar membrane. Int J Med Microbiol, 302, 179-86.
  258. TOMLEY, F. M. & SOLDATI, D. S. 2001. Mix and match modules: structure and function of microneme proteins in apicomplexan parasites. Trends Parasitol, 17, 81-8.
  259. PASVOL, G. 2003. How many pathways for invasion of the red blood cell by the malaria parasite? Trends Parasitol, 19, 430-2.
  260. CRABB, B. S. & COOKE, B. M. 2004. Molecular approaches to malaria: MAM 2004 and beyond. Trends Parasitol, 20, 547.
  261. COOKE, B. M., LINGELBACH, K., BANNISTER, L. H. & TILLEY, L. 2004. Protein trafficking in Plasmodium falciparum-infected red blood cells. Trends Parasitol, 20, 581- 9.
  262. SOLDATI, D., FOTH, B. J. & COWMAN, A. F. 2004. Molecular and functional aspects of parasite invasion. Trends Parasitol, 20, 567-74.
  263. WICKERT, H. & KROHNE, G. 2007. The complex morphology of Maurer's clefts: from discovery to three-dimensional reconstructions. Trends Parasitol, 23, 502-9.
  264. TYLER, J. S., TREECK, M. & BOOTHROYD, J. C. 2011. Focus on the ringleader: the role of AMA1 in apicomplexan invasion and replication. Trends Parasitol, 27, 410-20.
  265. THAM, W. H., HEALER, J. & COWMAN, A. F. 2012. Erythrocyte and reticulocyte binding- like proteins of Plasmodium falciparum. Trends Parasitol, 28, 23-30.
  266. UDEINYA, I. J., SCHMIDT, J. A., AIKAWA, M., MILLER, L. H. & GREEN, I. 1981. Falciparum malaria-infected erythrocytes specifically bind to cultured human endothelial cells. Science, 213, 555-7.
  267. WALLIKER, D., QUAKYI, I. A., WELLEMS, T. E., MCCUTCHAN, T. F., SZARFMAN, A., LONDON, W. T., CORCORAN, L. M., BURKOT, T. R. & CARTER, R. 1987. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science, 236, 1661-6.
  268. GINSBURG, H. 1994. Transport pathways in the malaria-infected erythrocyte. Their characterization and their use as potential targets for chemotherapy. Biochem Pharmacol, 48, 1847-56.
  269. MERCKX, A., BOUYER, G., THOMAS, S. L., LANGSLEY, G. & EGEE, S. 2009. Anion channels in Plasmodium-falciparum-infected erythrocytes and protein kinase A. Trends Parasitol, 25, 139-44.
  270. MARGOS, G., BANNISTER, L. H., DLUZEWSKI, A. R., HOPKINS, J., WILLIAMS, I. T. & MITCHELL, G. H. 2004. Correlation of structural development and differential expression of invasion-related molecules in schizonts of Plasmodium falciparum. Parasitology, 129, 273-87.
  271. LING, I. T., FLORENS, L., DLUZEWSKI, A. R., KANEKO, O., GRAINGER, M., YIM LIM, B. Y., TSUBOI, T., HOPKINS, J. M., JOHNSON, J. R., TORII, M., BANNISTER, L. H., YATES, J. R., 3RD, HOLDER, A. A. & MATTEI, D. 2004. The Plasmodium falciparum clag9 gene encodes a rhoptry protein that is transferred to the host erythrocyte upon invasion. Mol Microbiol, 52, 107-18.


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