Origins and evolution of antigenic diversity in malaria parasites

Current Molecular Medicine

Volumn 7, Issue 6, 2007, Pages 588-602

  Ferreira, Marcelo U ^a   Zilversmit, Martine ^b   Wunderlich, Gerhard ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Antigenic diversity; Antigenic variation; Evolution; Malaria; Vaccine

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1; MALARIA VACCINE; MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 1; MEROZOITE SURFACE PROTEIN 2; PARASITE ANTIGEN; RIFIN; STEVOR; SURFIN; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ANTIGENIC VARIATION; CELL ADHESION; CELLULAR IMMUNITY; GENE CONVERSION; GENE FREQUENCY; GENE SEQUENCE; GENE SWITCHING; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MALARIA; MOLECULAR PHYLOGENY; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; REVIEW; TANDEM REPEAT;

ANIMALS; ANTIGENIC VARIATION; ANTIGENS, PROTOZOAN; EVOLUTION, MOLECULAR; HUMANS; MALARIA VACCINES; PLASMODIUM FALCIPARUM;

BACTERIA (MICROORGANISMS);

EID: 35448976513     PISSN: 15665240     EISSN: None     Source Type: Journal    
DOI: 10.2174/156652407781695756     Document Type: Review

References (150)

1. Snow, R.W., Guerra, C.A., Noor, A.M., Myint, H.Y. and Hay, S.I. (2005) Nature, 434, 214-217.
2. Guerin, P.J., Olliaro, P., Nosten, F., Druilhe, P., Laxminarayan, R., Binka, F., Kilama, W.L., Ford, N. and White, N.J. (2002) Lancet Infect. Dis., 2, 564-573.
3. Day, K.P. and Marsh, K. (1991) Immunol. Today, 12, A68-71.
4. Gupta, S. and Day, K.P. (1994) Parasite Immunol., 16, 361-370.
5. Bull, P.C. and Marsh, K. (2002) Trends Microbiol., 10, 55-58.
6. Mota, M.M. and Rodriguez, A. (2004) Cell Microbiol., 6, 1113-1118.
7. Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F. and Menard, R. (2006) Nat. Med., 12, 220-224.
8. Karunaweera, N.D., Wijesekera, S.K., Wanasekera, D., Mendis, K.N. and Carter, R. (2003) Trends Parasitol., 19, 188-193.
9. Tsuji, M. and Zavala, F. (2003) Trends Parasitol., 19, 88-93.
10. Yoshida, N., Nussenzweig, R.S., Potocnjak, P., Nussenzweig, V. and Aikawa, M. (1980) Science, 207, 71-73.
11. Cavinato, R.A., Bastos, K.R., Sardinha, L.R., Elias, R.M., Alvarez, J.M. and d'Imperio Lima, M.R. (2001) Parasite Immunol., 23, 587-597.
12. Groux, H. and Gysin, J. (1990) Res. Immunol., 141, 529-542.
13. Bouharoun-Tayoun, H., Attanath, P., Sabchareon, A., Chongsuphajaisiddhi, T. and Druilhe, P. (1990) J. Exp. Med., 172, 1633-1641.
14. Bouharoun-Tayoun, H., Oeuvray, C., Lunel, F. and Druilhe, P. (1995) J. Exp. Med., 182, 409-418.
15. Costa, F.T., Fusai, T., Parzy, D., Sterkers, Y., Torrentino, M., Douki, J.B., Traore, B., Petres, S., Scherf, A. and Gysin, J. (2003) J. Infect. Dis., 188, 153-164.
16. Staalsoe, T., Shulman, C.E., Bulmer, J.N., Kawuondo, K., Marsh, K. and Hviid, L. (2004) Lancet, 363, 283-289.
17. Berzins, K. and Anders, R.F., in Malaria - Molecular and Clinical Aspects Wahlgren, M. andPerlemann, P., Eds. (Harwood Academic Publishers, Amsterdam, 1999) pp. 181-216.
18. Rich, S.M., Licht, M.C., Hudson, R.R. and Ayala, F.J. (1998) Proc. Natl. Acad. Sci. USA, 95, 4425-4430.
19. Volkman, S.K., Barry, A.E., Lyons, E.J., Nielsen, K.M., Thomas, S.M., Choi, M., Thakore, S.S., Day, K.P., Wirth, D.F. and Hartl, D.L. (2001) Science, 293, 482-484.
20. Joy, D.A., Feng, X., Mu, J., Furuya, T., Chotivanich, K., Krettli, A.U., Ho, M., Wang, A., White, N.J., Suh, E., Beerli, P. and Su, X.Z. (2003) Science, 300, 318-321.
21. Hartl, D.L. (2004) Nat. Rev. Microbiol., 2, 15-22.
22. Volkman, S.K., Hartl, D.L., Wirth, D.F., Nielsen, K.M., Choi, M., Batalov, S., Zhou, Y., Plouffe, D., Le Roch, K.G., Abagyan, R. and Winzeler, E.A. (2002) Science, 298, 216-218.
23. Rich, S.M. and Ayala, F.J. (2000) Proc. Natl. Acad. Sci. USA, 97, 6994-7001.
24. Tanabe, K., Mackay, M., Goman, M. and Scaife, J.G. (1987) J. Mol. Biol., 195, 273-287.
25. Locher, C.P., Tam, L.Q., Chang, S.P., McBride, J.S. and Siddiqui, W.A. (1996) Exp. Parasitol., 84, 74-83.
26. Conway, D.J., Cavanagh, D.R., Tanabe, K., Roper, C., Mikes, Z.S., Sakihama, N., Bojang, K.A., Oduola, A.M., Kremsner, P.G., Arnot, D.E., Greenwood, B.M. and McBride, J.S. (2000) Nat. Med., 6, 689-692.
27. Ferreira, M.U. and Hartl, D.L. (2007) Exp. Parasitol., 115, 32-40.
28. Epping, R.J., Goldstone, S.D., Ingram, L.T., Upcroft, J.A., Ramasamy, R., Cooper, J.A., Bushell, G.R. and Geysen, H.M. (1988) Mol. Biochem. Parasitol., 28, 1-10.
29. Rzepczyk, C.M., Ramasamy, R., Mutch, D.A., Ho, P.C., Battistutta, D., Anderson, K.L., Parkinson, D., Doran, T.J. and Honeyman, M. (1989) Eur. J. Immunol., 19, 1797-1802.
30. al-Yaman, F., Genton, B., Anders, R.F., Falk, M., Triglia, T., Lewis, D., Hii, J., Beck, H.P. and Alpers, M.P. (1994) Am. J. Trop. Med. Hyg., 51, 593-602.
31. Ekala, M.T., Jouin, H., Lekoulou, F., Mercereau-Puijalon, O. and Ntoumi, F. (2002) Clin. Exp. Immunol., 129, 326-331.
32. al-Yaman, F., Genton, B., Anders, R., Taraika, J., Ginny, M., Mellor, S. and Alpers, M.P. (1995) Parasite Immunol., 17, 493-501.
33. Metzger, W.G., Okenu, D.M., Cavanagh, D.R., Robinson, J.V., Bojang, K.A., Weiss, H.A., McBride, J.S., Greenwood, B.M. and Conway, D.J. (2003) Parasite Immunol., 25, 307-312.
34. Polley, S.D., Conway, D.J., Cavanagh, D.R., McBride, J.S., Lowe, B.S., Williams, T.N., Mwangi, T.W. and Marsh, K. (2006) Vaccine, 24, 4233-4246.
35. Taylor, R.R., Allen, S.J., Greenwood, B.M. and Riley, E.M. (1998) Am. J. Trop. Med. Hyg., 58, 406-413.
36. Roy, S.W., Ferreira, M.U. and Hartl, D.L. (2007) Heredity, in press.
37. Pearce, J.A., Triglia, T., Hodder, A.N., Jackson, D.C., Cowman, A.F. and Anders, R.F. (2004) Infect. Immun., 72, 2321-2328.
38. Singh, S., Soe, S., Roussilhon, C., Corradin, G. and Druilhe, P. (2005) Infect. Immun., 73, 1235-1238.
39. McConkey, G.A., Waters, A.P. and McCutchan, T.F. (1990) Annu. Rev. Microbiol., 44, 479-498.
40. Felger, I., Marshal, V.M., Reeder, J.C., Hunt, J.A., Mgone, C.S. and Beck, H.P. (1997) J. Mol. Evol., 45, 154-160.
41. Ferreira, M.U., Ribeiro, W.L., Tonon, A.P., Kawamoto, F. and Rich, S.M. (2003) Gene, 304, 65-75.
42. Rosario, V. (1981) Science, 212, 1037-1038.
43. Hoffmann,, E.H., Malafronte, R.S., Moraes-Avila, S.L., Osakabe, A.L., Wunderlich, G., Durham, A.M., Ribolla, P.E., del Portillo, H.A. and Ferreira, M.U. (2006) Gene, 376, 224-230.
44. Guttman, D.S. and Dykhuizen, D.E. (1994) Science, 266, 1380-1383.
45. Su, X., Ferdig, M.T., Huang, Y., Huynh, C.Q., Liu, A., You, J., Wootton, J.C. and Wellems, T.E. (1999) Science, 286, 1351-1353.
46. Cortes, A. (2005) Int. J. Parasitol., 35, 125-130.
47. DePristo, M.A., Zilversmit, M.M. and Hartl, D.L. (2006) Gene, 378, 19-30.
48. Wootton, J.C. (1993) Comput. Chem., 17, 149-163.
49. Wootton, J.C. (1994) Comput. Chem., 18, 269-285.
50. Altschul, S.F., Boguski, M.S., Gish, W. and Wootton, J.C. (1994) Nat. Genet., 6, 119-129.
51. Pizzi, E. and Frontali, C. (2001) Genome Res., 11, 218-229.
52. Xue, H.Y. and Forsdyke, D.R. (2003) Mol. Biochem. Parasitol., 128, 21-32.
53. Lavstsen, T., Salanti, A., Jensen, A.T., Arnot, D.E. and Theander, T.G. (2003) Malar. J., 2, 27.
54. Triglia, T., Thompson, J., Caruana, S.R., Delorenzi, M., Speed, T. and Cowman, A.F. (2001) Infect. Immun., 69, 1084-1092.
55. Rayner, J.C., Huber, C.S., Galinski, M.R. and Barnwell, J.W. (2004) Mol. Biochem. Parasitol., 133, 287-296.
56. Duraisingh, M.T., Triglia, T., Ralph, S.A., Rayner, J.C., Barnwell, J.W., McFadden, G.I. and Cowman, A.F. (2003) EMBO J., 22, 1047-1057.
57. Lobo, C.A., Rodriguez, M., Struchiner, C.J., Zalis, M.G. and Lustigman, S. (2006) Mol. Biochem. Parasitol., 149, 246-251.
58. Jennings, C.V., Ahouidi, A.D., Zilversmit, M., Bei, A., Rayner, J., Sarr, O., Ndir, O., Wirth, D.F., Mboup, S. and Duraisingh, M.T. (2007) Infect Immun., 75, 3531-3538.
59. Zilversmit, M. (2007), PhD dissertation, Harvard University.
60. Ferreira, M.U., da Silva Nunes, M. and Wunderlich, G. (2004) Clin. Diagn. Lab. Immunol., 11, 987-995.
61. Schofield, L. (1991) Parasitol. Today, 7, 269-275.
62. Mond, J.J., Lees, A. and Snapper, C.M. (1995) Annu. Rev. Immunol., 13, 655-692.
63. Anders, R.F. (1986) Parasite Immunol., 8, 529-539.
64. Ahlborg, N., Berzins, K. and Perlmann, P. (1991) Mol. Biochem. Parasitol., 46, 89-95.
65. Cavanagh, D.R., Dobano, C., Elhassan, I.M., Marsh, K., Elhassan, A., Hviid, L., Khalil, E.A., Theander, T.G., Arnot, D.E. and McBride, J.S. (2001) Infect. Immun., 69, 1207-1211.
66. Da Silveira, L.A., Dorta, M.L., Kimura, E.A., Katzin, A.M., Kawamoto, F., Tanabe, K. and Ferreira, M.U. (1999) Infect. Immun., 67, 5906-5916.
67. Rzepczyk, C.M., Hale, K., Woodroffe, N., Bobogare, A., Csurhes, P., Ishii, A. and Ferrante, A. (1997) Infect. Immun., 65, 1098-1100.
68. Scopel, K.K., Fontes, C.J., Ferreira, M.U. and Braga, E.M. (2005) Exp. Parasitol., 109, 124-134.
69. Scopel, K.K., Fontes, C.J., Ferreira, M.U. and Braga, E.M. (2006) Clin. Vaccine Immunol., 13, 810-813.
70. Tongren, J.E., Drakeley, C.J., McDonald, S.L., Reyburn, H.G., Manjurano, A., Nkya, W.M., Lemnge, M.M., Gowda, C.D., Todd, J.E., Corran, P.H. and Riley, E.M. (2006) Infect. Immun., 74, 257-264.
71. Ferrante, A. and Rzepczyk, C.M. (1997) Parasitol. Today, 13, 145-148.
72. Miller, L.H., Roberts, T., Shahabuddin, M. and McCutchan, T.F. (1993) Mol. Biochem. Parasitol., 59, 1-14.
73. Snewin, V.A., Herrera, M., Sanchez, G., Scherf, A., Langsley, G. and Herrera, S. (1991) Mol. Biochem. Parasitol., 49, 265-275.
74. Hughes, A.L. (1992) Mol. Biol. Evol., 9, 381-393.
75. Conway, D.J. and Baum, J. (2002) Trends Parasitol., 18, 351-355.
76. Polley, S.D., Weedall, G.D., Thomas, A.W., Golightly, L.M. and Conway, D.J. (2005) Mol. Biochem. Parasitol., 142, 25-31.
77. Tanabe, K., Sakihama, N., Hattori, T., Ranford-Cartwright, L., Goldman, I., Escalante, A.A. and Lal, A.A. (2004) J. Mol. Evol., 59, 687-694.
78. Volkman, S.K., Sabeti, P.C., DeCaprio, D., Neafsey, D.E., Schaffner, S.F., Milner, D.A., Jr., Daily, J.P., Sarr, O., Ndiaye, D., Ndir, O., Mboup, S., Duraisingh, M.T., Lukens, A., Derr, A., Stange-Thomann, N., Waggoner, S., Onofrio, R., Ziaugra, L., Mauceli, E., Gnerre, S., Jaffe, D.B., Zainoun, J., Wiegand, R.C., Birren, B.W., Hartl, D.L., Galagan, J.E., Lander, E.S. and Wirth, D.F. (2007) Nat. Genet., 39, 113-119.
79. McKenzie, F.E., Ferreira, M.U., Baird, J.K., Snounou, G. and Bossert, W.H. (2001) Evol. Int. J. Org. Evol., 55, 1299-1307.
80. Frontali, C. (1994) Genetica, 94, 91-100.
81. Fenton, B., Clark, J.T., Khan, C.M., Robinson, J.V., Walliker, D., Ridley, R., Scaife, J.G. and McBride, J.S. (1991) Mol. Cell. Biol., 11, 963-974.
82. Richman, A. (2000) Mol. Ecol., 9, 1953-1963.
83. Cavanagh, D.R., Elhassan, I.M., Roper, C., Robinson, V.J., Giha, H., Holder, A.A., Hviid, L., Theander, T.G., Arnot, D.E. and McBride, J.S. (1998) J. Immunol., 161, 347-359.
84. Felger, I., Steiger, S., Hatz, C., Smith, T. and Beck, H.P. (2003) Parasite Immunol., 25, 531-543.
85. Franks, S., Baton, L., Tetteh, K., Tongren, E., Dewin, D., Akanmori, B.D., Koram, K.A., Ranford-Cartwright, L. and Riley, E.M. (2003) Infect. Immun., 71, 3485-3495.
86. Scopel, K.K., da Silva-Nunes, M., Malafronte, R. S., Braga, E. M., Ferreira, M. U. (2007) Am. J. Trop. Med. Hyg., 76, 1084-1091.
87. Genton, B., Betuela, I., Felger, I., Al-Yaman, F., Anders, R.F., Saul, A., Rare, L., Baisor, M., Lorry, K., Brown, G.V., Pye, D., Irving, D.O., Smith, T.A., Beck, H.P. and Alpers, M.P. (2002) J. Infect Dis., 185, 820-827.
88. Polley, S.D., Tetteh, K.K., Cavanagh, D.R., Pearce, R.J., Lloyd, J.M., Bojang, K.A., Okenu, D.M., Greenwood, B.M., McBride, J.S. and Conway, D.J. (2003) Infect. Immun., 71, 1833-1842.
89. Sows, K.M., Cavanagh, D.R., Creasey, A.M., Raats, J., McBride, J., Sauerwein, R., Roeffen, W.F. and Arnot, D.E. (2001) Mol. Biochem. Parasitol., 112, 143-147.
90. Ranford-Cartwright, L.C., Taylor, R.R., Asgari-Jirhandeh, N., Smith, D.B., Roberts, P.E., Robinson, V.I., Babiker, H.A., Riley, E.M., Walliker, D. and McBride, J.S. (1996) Parasite Immunol., 18, 411-420.
91. Tonhosolo, R., Wunderlich, G. and Ferreira, M.U. (2001) J. Eukaryot. Microbiol., 48, 556-564.
92. Tonon, A.P., Hoffmann, E.H., Silveira, L.A., Ribeiro, A.G., Goncalves, C.R., Ribolla, P.E., Wunderlich, G. and Ferreira, M.U. (2004) Exp. Parasitol., 108, 114-125.
93. Kanunfre, K.A., Leoratti, F.M., Hoffmann, E.H., Durlacher, R.R., Ferreira, A.W., Moraes-Avila, S.L. and Ferreira, M.U. (2003) Clin. Diagn. Lab. Immunol., 10, 973-976.
94. Weisman, S., Wang, L., Billman-Jacobe, H., Nhan, D.H., Richie, T.L. and Coppel, R.L. (2001) Infect. Immun., 69, 959-967.
95. Miller, L.H., Baruch, D.I., Marsh, K. and Doumbo, O.K. (2002) Nature, 415, 673-679.
96. David, P.H., Hommel, M., Miller, L.H., Udeinya, I.J. and Oligino, L.D. (1983) Proc. Natl. Acad. Sci. USA, 80, 5075-5079.
97. Saul, A. (1999) Parasitol. Today, 15, 455-457.
98. Leech, J.H., Barnwell, J.W., Miller, L.H. and Howard, R.J. (1984) J. Exp. Med., 159, 1567-1575.
99. Kyes, S.A., Rowe, J.A., Kriek, N. and Newbold, C.I. (1999) Proc. Natl. Acad. Sci. USA, 96, 9333-9338.
100. Winter, G., Kawai, S., Haeggstrom, M., Kaneko, O., von Euler, A., Kawazu, S., Palm, D., Fernandez, V. and Wahlgren, M. (2005) J. Exp. Med., 201, 1853-1863.
101. Kaviratne, M., Khan, S.M., Jarra, W. and Praiser, P.R. (2002) Eukaryot. Cell, 1, 926-935.
102. Hui, G.S. and Siddiqui, W.A. (1988) Mol. Biochem. Parasitol., 29, 283-263.
103. McRobert, L., Preiser, P., Sharp, S., Jarra, W., Kaviratne, M., Taylor, M.C., Renia, L. and Sutherland, C.J. (2004) Infect. Immun., 72, 6597-6602.
104. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J.M., Pain, A., Nelson, K.E., Bowman, S., Paulsen, I.T., James, K., Eisen, J.A., Rutherford, K., Salzberg, S.L., Craig, A., Kyes, S., Chan, M.S., Nene, V., Shallom, S.J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M.W., Vaidya, A.B., Martin, D.M., Fairlamb, A.H., Fraunholz, M.J., Roos, D.S., Ralph, S.A., McFadden, G.I., Cummings, L.M., Subramanian, G.M., Mungall, C., Venter, J.C., Carucci, D.J., Hoffman, S.L., Newbold, C., Davis, R.W., Fraser, C.M. and Barrell, B. (2002) Nature, 419, 498-511.
105. Luse, S.A. and Miller, L.H. (1971) Am. J. Trop. Med. Hyg., 20, 655-660.
106. Oquendo, P., Hundt, E., Lawler, J. and Seed, B. (1989) Cell, 58, 95-101.
107. Berendt, A.R., Simmons, D.L., Tansey, J., Newbold, C.I. and Marsh, K. (1989) Nature, 341, 57-59.
108. Rogerson, S.J., Chalyaroj, S.C., Ng, K., Reeder, J.C. and Brown, G.V. (1995) J. Exp. Med., 182, 15-20.
109. Ockenhouse, C.F., Tegoshi, T., Maeno, Y., Benjamin, C., Ho, M., Kan, K.E., Thway, Y., Win, K., Aikawa, M. and Lobb, R.R. (1992) J. Exp. Med., 176, 1183-1189.
110. Beeson, J.G., Rogerson, S.J., Cooke, B.M., Reeder, J.C., Chai, W., Lawson, A.M., Molyneux, M.E. and Brown, G.V. (2000) Nat. Med., 6, 86-90.
111. Vogt, A.M., Barragan, A., Chen, Q., Kironde, F., Spillmann, D. and Wahlgren, M. (2003) Blood, 101, 2405-2411.
112. Rowe, J.A., Moulds, J.M., Newbold, C.I. and Miller, L.H. (1997) Nature, 388, 292-295.
113. Flick, K., Scholander, C., Chen, Q., Fernandez, V., Pouvelle, B., Gysin, J. and Wahlgren, M. (2001) Science, 293, 2098-2100.
114. Barragan, A., Kremsner, P.G., Wahlgren, M. and Carlson, J. (2000) Infect. Immun., 68, 2971-2975.
115. Fried, M. and Duffy, P.E. (1996) Science 272, 1502-1504.
116. Baruch, D.I., Pasloske, B.L., Singh, H.B., Bi, X., Ma, X.C., Feldman, M., Taraschi, T.F. and Howard, R.J. (1995) Cell, 82, 77-87.
117. Thompson, J.K., Rubio, J.P., Caruana, S., Brockman, A., Wickham, M.E. and Cowman, A.F. (1997) Mol. Biochem. Parasitol., 87, 49-60.
118. Crabb, B.S., Cooke, B.M., Reeder, J.C., Waller, R.F., Caruana, S.R., Davem, K.M., Wickham, M.E., Brown; G.V., Coppel, R.L. and Cowman, A.F. (1997) Cell, 89, 287-296.
119. Chen, Q., Fernandez, V., Sundstrom, A., Schlichtherle, M., Datta, S., Hagblom, P. and Wahlgren, M. (1998) Nature, 394, 392-395.
120. Ralph, S.A. and Scharf, A. (2005) Curr. Opin. Microbiol., 8, 434-440.
121. Freitas-Junior, L.H., Hernandez-Rivas, R., Ralph, S.A., Montiel-Condado, D., Ruvalcaba-Salazar, O.K., Rojas-Meza, A.P., Mancio-Silva, L., Leal-Silvestre, R.J., Gontijo, A.M., Shorts, S. and Scherf, A. (2005) Cell, 121, 25-36.
122. Chookajorn, T., Dzikowski, R., Frank, M., Li, F., Jiwani, A.Z., Hartl, D.L. and Deitsch, K.W. (2007) Proc. Natl. Acad. Sci. USA, 104, 899-902.
123. Cui, L., Miao, J. and Cui, L. (2007) Antimicrob. Agents Chemother., 51, 488-494.
124. Choi, S.W., Keyes, M.K. and Horrocks, P. (2006) Mol. Biochem. Parasitol., 150, 350-352.
125. Roberts, D.J., Craig, A.G., Berendt, A.R., Pinches, R., Nash, G., Marsh, K. and Newbold, C.I. (1992) Nature, 357, 689-692.
126. Peters, J., Fowler, E., Gatton, M., Chen, N., Saul, A. and Chong, Q. (2002) Proc. Natl. Acad. Sci. USA, 99, 10689-10694.
127. Scherf, A., Figueiredo, L.M. and Freitas-Junior, L.H. (2001) Curr. Opin. Microbiol., 4, 409-414.
128. Fowler, E.V., Peters, J.M., Gatton, M.L., Chen, N. and Chang, Q. (2002) Mol. Biochem. Parasitol., 120, 117-126.
129. Bull, P.C., Berriman, M., Kyes, S., Quail, M.A., Hall, N., Kortok, M.M., Marsh, K. and Newbold, C.I. (2005) PLoS Pathog., 1, e26.
130. Albrecht, L., Merino, E.F., Hoffmann, E.H., Ferreira, M.U., de Mattos Ferreira, R.G., Osakabe, A.L., Dalla Martha, R.C., Ramharter, M., Durham, A.M., Ferreira, J.E., Del Portillo, H.A. and Wunderlich, G. (2006) Mol. Biochem. Parasitol., 150, 157-165.
131. Barry, A.E., Leliwa-Sytek, A., Tavul, L., Imrie, H., Migot-Nabias, F., Brown, S.M., McVean, G.A. and Day, K.P. (2007) PLoS Pathog., 3, e34.
132. Razakandrainibe, F.G., Durand, P., Koella, J.C., De Meeus, T., Rousset, F., Ayala, F.J. and Renaud, F. (2005) Proc. Natl. Acad. Sci. USA, 102, 17388-17393.
133. Jensen, A.T., Magistrado, P., Sharp, S., Joergensen, L., Lavstsen, T., Chiucchiuini, A., Salanti, A., Vestergaard, L.S., Lusingu, J.P., Hermsen, R., Sauerwein, R., Christensen, J., Nielsen, M.A., Hviid, L., Sutherland, C., Staalsoe, T. and Theander, T.G. (2004), J. Exp. Med., 199, 1179-1190.
134. Lavstsen, T., Magistrado, P., Hermsen, C.C., Salanti, A., Jensen, A.T., Sauerwein, R., Hviid, L., Theander, T.G. and Staalsoe, T. (2005) Malar. J., 4, 21.
135. Magistrado, P.A., Lusingu, J., Vestergaard, L.S., Lemnge, M., Lavstsen, T., Turner, L., Hviid, L., Jensen, A.T. and Theander, T.G. (2007) Infect. Immun., 75, 2415-2420.
136. Kirchgatter, K. and Portillo Hdel, A. (2002) Mol. Med., 8, 16-23.
137. Kaestli, M., Cockburn, I.A., Cortes, A., Baea, K., Rowe, J.A. and Beck, H.P. (2006) J. Infect. Dis. 193, 1567-1574.
138. Carlson, J. (1993) Scand. J. Infect. Dis. Suppl., 86, 1-79.
139. Bull, P.C., Lowe, B.S., Kortok, M., Molyneux, C.S., Newbold, C.I. and Marsh, K. (1998) Nat Med., 4, 358-360.
140. Gupta, S., Snow, R.W., Donnelly, C.A., Marsh, K. and Newbold, C. (1999) Nat. Med., 5, 340-348.
141. Oguariri, R.M., Borrmann S., Klinkert, M.Q., Kremsner, P.G. and Kun, J.F. (2001) Infect. Immu., 69, 7603-7609.
142. Gamain, B., Miller, L.H. and Baruch, D.I. (2001) Proc. Natl. Acad. Sci. USA, 98, 2664-2669.
143. Yipp, B.G., Baruch, D.J., Brady, C., Murray, A.G., Looareesuwan, S., Kubes, P. and Ho, M. (2003) Blood, 101, 331-337.
144. Lekana Douki, J.B., Traore, B., Costa, F.T., Fusai, T., Pouvelle, B., Sterkers, Y., Scherf, A. and Gysin, J. (2002) Blood, 100, 1478-1483.
145. Kyes, S., Pinches, R. and Newbold, C. (2000) Mol. Biochem. Parasitol., 105, 311-315.
146. Fernandez-Becerra, C., Pein, O., de Oliveira, T.R.; Yamamoto, M.M., Cassola, A.C., Rocha, C., Soares, I.S., de Braganca Pereira, C.A. and del Portillo, H.A. (2005) Mol. Microbiol., 58, 648-658.
147. Abdel-Latif, M.S., Dietz, K., Issifou, S., Kremsner, P.G. and Klinkert, M.Q. (2003) Infect. Immun. 71, 6229-6233.
148. Weber, J.L. (1988) Mol. Biochem. Parasitol., 29, 117-124.
149. Sharp, S., Lavstsen, T., Fivelman, Q.L., Saeed, M., McRobert, L., Templeton, T.J., Jensen, A.T., Baker, D.A., Theander, T.G. and Sutherland, C.J. (2006) Eukaryot. Cell, 5, 1206-1214.
150. Lavazec, C., Sanyal, S. and Templeton, T.J. (2007) Mol. Microbiol., 64, 1621-1634.