The cell biology of malaria infection of mosquito: Advances and opportunities

Cellular Microbiology

Volumn 17, Issue 4, 2015, Pages 451-466

  Sinden, R E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AXONEME; CYTOLOGY; CYTOPLASM; DISEASE CARRIER; ERYTHROCYTE; FERTILIZATION; GAMETE; GAMETOCYTE; GAMETOGENESIS; GENE REPLICATION; HOST; MALARIA; MOSQUITO; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; ANIMAL; DISEASE TRANSMISSION; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; PARASITOLOGY; PLASMODIUM; PREVENTION AND CONTROL; TRANSMISSION;

ANIMALS; CULICIDAE; DISEASE TRANSMISSION, INFECTIOUS; HOST-PATHOGEN INTERACTIONS; HUMANS; MALARIA; PLASMODIUM;

EID: 84924453761     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12413     Document Type: Review

References (204)

1. Aguilar, R., Magallon-Tejada, A., Achtman, A.H., Moraleda, C., Joice, R., Cisteró, P., etal. (2014) Molecular evidence for the localization of Plasmodium falciparum immature gametocytes in bone marrow. Blood 123: 959-966.
2. Aikawa, M., Huff, C.G., and Sprinz, H. (1969) Comparative fine structure study of the gametocytes of avian, reptilian and mammalian malaria parasites. J Ultrastruct Res 26: 316-331.
3. Aikawa, M., Carter, R., Ito, Y., and Nijhout, M. (1984) New observations on gametogenesis, fertilization, and zygote transformation in Plasmodium gallinaceum. J Protozool 31: 403-413.
4. Akinosoglou, K.A., Bushell, E.S., Ukegbu, C.V., Schlegelmilch, T., Cho, J.S., Redmond, S., etal. (2015) Characterization of Plasmodium developmental transcriptomes in Anopheles gambiae midgut reveals novel regulators of malaria transmission. Cell Microbiol 17: 254-268.
5. Alano, P. (2014) The sound of sexual commitment breaks the silencing of malaria parasites. Trends Parasitol 30: 509-510.
6. Alano, P., Read, D., Bruce, M., Aikawa, M., Kaido, T., Tegoshi, T., etal. (1995) COS cell expression cloning of Pfg377, a Plasmodium falciparum gametocyte antigen associated with osmiophilic bodies. Mol Biochem Parasitol 74: 143-156.
7. Alonso, P.L., Brown, G., Arevalo-Herrera, M., Binka, F., Chitnis, C., Collins, F., etal. (2011) A research agenda to underpin malaria eradication. PLoS Med 8: e1000406.
8. Andenmatten, N., Egarter, S., Jackson, A.J., Jullien, N., Herman, J.P., and Meissner, M. (2012) Conditional genome engineering in Toxoplasma gondii uncovers alternative invasion mechanisms. Nat Methods 10: 125-127.
9. Anderson, R.A., Koella, J.C., and Hurd, H. (1999) The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proc R Soc Lond B 266: 1729-1733.
10. Armistead, J.S., Morlais, I., Mathias, D.K., Jardim, J.G., Joy, J., Fridman, A., etal. (2013) Antibodies to a single, conserved epitope in Anopheles APN1 inhibit universal transmission of falciparum and vivax malaria. Infect Immun 82: 818-829.
11. Baker, D.A. (2010) Malaria gametocytogenesis. Mol Biochem Parasitol 172: 57-65.
12. Batista, E., Costa, E., and Silva, A. (2014) Anopheles darlingi (Diptera: Culicidae) displays increased attractiveness to infected individuals with Plasmodium vivax gametocytes. Parasit Vect 7: 251.
13. Beetsma, A.L., van de Viel, T.J.J.M., Sauerwein, R.W., and Eling, W.M.C. (1998) Plasmodium berghei ANKA: purification of large numbers of infectious gametocytes. Exp Parasitol 88: 69-72.
14. Bhasin, V.K., and Trager, W. (1984) Gametocyte-forming and non-gametocyte-forming clones of Plasmodium falciparum. Am J Trop Med Hyg 33: 534-537.
15. Billker, O., Shaw, M.K., Margos, G., and Sinden, R.E. (1997) The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 115: 1-7.
16. Billker, O., Lindo, V., Panico, M., Etienne, A.E., Paxton, T., Dell, A., etal. (1998) Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito. Nature 392: 289-292.
17. Billker, O., Dechamps, S., Tewari, R., Wenig, G., Franke-Fayard, B., and Brinkman, V. (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117: 503-514.
18. Birago, C., Bucci, A., Dore, E., Frontali, C., and Zenobi, P. (1982) Mosquito infectivity is directly related to the proportion of repetitive DNA in Plasmodium berghei. Mol Biochem Parasitol 6: 1-12.
19. Blagborough, A.M., and Sinden, R.E. (2009) Plasmodium berghei HAP2 induces strong malaria transmission-blocking immunity in vivo and in vitro. Vaccine 27: 5187-5194.
20. Boisbouvier, J., Prochnika-Chalufour, A., Nieto, A.R., Torres, J.A., Nanard, N., Rodriguez, M.H., etal. (1998) Structural information on a cercropin-like synthetic peptide, Shiva 3 toxic to the sporogonic development of Plasmodium berghei. Eur J Biochem 257: 263-273.
21. Boisson, B., Lacroix, C., Bischoff, E., Gueirard, P., Bargieri, D.Y., Franke-Fayard, B., etal. (2011) The novel putative transporter NPT1 plays a critical role in early stages of Plasmodium berghei sexual development. Mol Microbiol 81: 1343-1357.
22. Bousema, T., and Drakeley, C. (2011) Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 24: 1-35.
23. Bousema, T., Griffin, J.T., Sauerwein, R.W., Smith, D.L., Churcher, T.S., Takken, W., etal. (2012) Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med 9: e1001165.
24. Brancucci, N.M., Bertschi, N.L., Zhu, L., Niederwieser, I., Chin, W.H., Wampfler, R., etal. (2014) Heterochromatin protein 1 secures survival and transmission of malaria parasites. Cell Host Microbe 16: 165-176.
25. 2 signals at key decision points in the life cycle of malaria parasites. PLoS Biol 12: e1001806.
26. Bruce, M.C., Carter, R.N., Nakamura, K., Aikawa, M., and Carter, R. (1994) Cellular location and temporal expression of the Plasmodium falciparum sexual stage antigen pfs16. Mol Biochem Parasitol 65: 11-22.
27. Canning, E.U., and Sinden, R.E. (1973) The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67: 29-40.
28. Carter, L.M., Kafsack, B.F.C., Llinás, M., Mideo, N., Pollitt, L.C., and Reece, S.E. (2013) Stress and sex in malaria parasites: why does commitment vary? Evol, Med Public Health 2013: 135-147.
29. Carter, R., and Miller, L.H. (1979) Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bull World Health Organ 57: 37-52.
30. Carter, R., Mendis, K.N., Miller, L.H., Molineaux, L., and Saul, A. (2000) Malaria transmission-blocking vaccines - how can their development be supported? Nat Med 241-244.
31. Christophides, G. (2005) Transgenic mosquitoes and malaria transmission. Cell Microbiol 7: 325-333.
32. Churcher, T.S., Bousema, T., Walker, M., Drakeley, C., Schneider, P., Ouedraogo, A.L., and Basanez, M.G. (2013). Predicting mosquito infection from Plasmodium falciparum gametocyte density and estimating the reservoir of infection. eLife 2, e00626.
33. Coleman, B.I., Skillman, K.M., Jiang, R.H., Childs, L.M., Altenhofen, L.M., Ganter, M., etal. (2014) A Plasmodium falciparum histone deacetylase regulates antigenic variation and gametocyte conversion. Cell Host Microbe 16: 177-186.
34. Cornelissen, A.W.C.A. (1988) Sex determination and sexual differentiation in malaria parasites. Biol Rev 63: 379-394.
35. Creasey, A.M., Ranfordcartwright, L.C., Moore, D.J., Williamson, D.H., Wilson, R.J.M., Walliker, D., and Carter, R. (1993) Uniparental inheritance of the mitochondrial gene cytochrome-b in Plasmodium falciparum. Curr Genet 23: 360-364.
36. Day, K.P., Karamalis, F., Thompson, J., Barnes, D.A., Peterson, C., Brown, H., etal. (1993) Genes necessary for expression of a virulence determinant and for transmission of Plasmodium falciparum are located on a 0.3-Megabase region of chromosome-9. Proc Natl Acad Sci U S A 90: 8292-8296.
37. Dearsly, A.L., Sinden, R.E., and Self, I. (1990) Sexual development in malarial parasites: gametocyte production, fertility and infectivity to the mosquito vector. Parasitology 100: 359-368.
38. Deligianni, E., Morgan, R.N., Bertuccini, L., Wirth, C.C., Silmon de Monerri, N.C., Spanos, L., etal. (2013) A perforin-like protein mediates disruption of the erythrocyte membrane during egress of Plasmodium berghei male gametocytes. Cell Microbiol 15: 1438-1455.
39. Delves, M., Plouffe, D., Scheurer, C., Meister, S., Wittlin, S., Winzeler, E.A., etal. (2012) The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med 9: e1001169.
40. Dessens, J.T., Mendoza, J., Claudianos, C., Vinetz, J.M., Khater, E., Hassard, S., etal. (2001) Knockout of the rodent malaria parasite chitinase PbCHT1 reduces infectivity to mosquitoes. Infect Immun 69: 4041-4047.
41. Dimopoulos, G. (2003) Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiol 5: 3-14.
42. Dixon, M.W.A., Dearnley, M.K., Hanssen, E., Gilberger, T., and Tilley, L. (2012) Shape-shifting gametocytes: how and why does P.falciparum go banana-shaped? Trends Parasitol 28: 471-478.
43. Dubremetz, J.F. (1975) La genese des merozoites chez la Coccidie Eimeria necatrix. Etude ultrastructurale. J Protozool 22: 71-84.
44. Dyer, M., and Day, K.P. (2000) Commitment to gametocytogenesis in Plasmodium falciparum. Parasitol Today 16: 102-107.
45. Ecker, A., Pinto, S.B., Baker, K.W., Kafatos, F.C., and Sinden, R.E. (2007) Plasmodium berghei: Plasmodium perforin-like protein 5 is required for mosquito midgut invasion in Anopheles stephensi. Exp Parasitol 116: 504-508.
46. Eichner, M., Diebner, H.H., Molineux, L., Collins, W.E., Jeffery, G.M., and Dietz, K. (2001) Genesis, sequestration and survival of Plasmodium falciparum gametocytes: parameter estimates from fitting a model to malaria therapy data. Trans R Soc Trop Med Hyg 95: 497-501.
47. Eksi, S., Morahan, B.J., Haile, Y., Furuya, T., Jiang, H., Ali, O., etal. (2012) Plasmodium falciparum gametocyte development 1 (Pfgdv1) and gametocytogenesis early gene identification and commitment to sexual development. PLoS Pathog 8: e1002964.
48. Fang, W., Vega-Rodríguez, J., Ghosh, A.K., Jacobs-Lorena, M., Kang, A., and St Leger, R.J. (2011) Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science 331: 1074-1077.
49. Farfour, E., Charlotte, F., Settegrana, C., Miyara, M., and Buffet, P. (2012) The extravascular compartment of the bone. Malar J 11: 285.
50. Feachem, R.G.A., Phillips, A.A., Hwang, J., Cotter, C., Wielgosz, B., Greenwood, B.M., etal. (2010) Shrinking the malaria map: progress and prospects. Lancet 376: 1566-1578.
51. Fowler, R.E., Sinden, R.E., and Pudney, M. (1995) Inhibitory activity of the anti-malarial atovaquone (566C80) against ookinetes, oocysts, and sporozoites of Plasmodium berghei. J Parasitol 81: 452-458.
52. Fraiture, M., Baxter, R.H.G., Steinert, S., Chelliah, Y., Frolet, C., Quispe-Tintaya, W., etal. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273-284.
53. Fry, M., and Pudney, M. (1992) Site of action of the antimalarial hydroxynaphthoquinone, 2-[trans-4-(4′-chlorophenyl)cyclohexyl]-3-hydroxy-1, 4-naphthoquin one (566C80). Biochem Pharmacol 43: 1545-1553.
54. Garnham, P.C.C. (1965) The structure of the early sporogonic stages of Plasmodium berghei. Ann Soc Belg Med Trop 45: 259-265.
55. Garnham, P.C.C., Bird, R.G., and Baker, J.R. (1967). Electron microscope studies of motile stages of malaria parasites. V. Exflagellation in plasmodium, hepatocystis and leucocytozoon. Trans R Soc Trop Med Hyg 61, 58-68.
56. Gass, R.F. (1977) Influences of blood digestion on the development of Plasmodium gallinaceum (Brumpt) in the midgut of Aedes aegypti (L.). Acta Trop 34: 127-140.
57. Gass, R.F., and Yeates, R.A. (1979) In vitro damaged of cultured ookinetes of Plasmodium gallinaceum by digestive proteinases from susceptible Aedes aegypti. Acta Trop 36: 243-252.
58. Ghosh, A.K., Coppens, I., Gardsvoll, H., Ploug, M., and Jacobs-Lorena, M. (2011) Plasmodium ookinetes coopt mammalian plasminogen to invade the mosquito midgut. PNAS 108: 17153-17158.
59. Gozar, M.M.G., Price, V.L., and Kaslow, D.C. (1998) Saccharomyces cerevisiae-secreted fusion proteins Pfs25 and Pfs28 elicit potent Plasmodium falciparum transmission- blocking antibodies in mice. Infect Immun 66: 59-64.
60. Grotendorst, C.A., and Carter, R. (1987) Complement effects on the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes. II. Changes in sensitivity to complement-like factors during zygote development. J Parasitol 73: 980-984.
61. Guerreiro, A., Deligianni, E., Santos, J.M., Silva, P.A., Louis, C., Pain, A., etal. (2014) Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte. Genome Biol 15: 493.
62. Guttery, D.S., Ferguson, D.J.P., Poulin, B., Xu, Z., Straschil, U., Klop, O., etal. (2012a) A putative homologue of CDC20/CDH1 in the malaria parasite is essential for male gamete development. PLoS Pathog 8: e1002554.
63. Guttery, D.S., Poulin, B., Ferguson, D.J., Szoor, B., Wickstead, B., Carroll, P.L., etal. (2012b) A unique protein phosphatase with kelch-like domains (PPKL) in Plasmodium modulates ookinete differentiation, motility and invasion. PLoS Pathog 8: e1002948.
64. 2+ during sexual development. PLoS Pathog 9: e1003191.
65. Guttery, D.S., Poulin, B., Ramaprasad, A., Wall, R.J., Ferguson, D.J.P., Brady, D., etal. (2014) Genome-wide functional analysis of Plasmodium protein phosphatases reveals key regulators of parasite development and differentiation. Cell Host Microbe 16: 128-140.
66. Hall, N., Karras, M., Raine, J.D., Carlton, J.M., Kooij, T.W., Berriman, M., etal. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82-86.
67. Han, Y.S., and Barillas-Mury, C. (2002) Implications of time bomb model of ookinete invasion of midgut cells. Insect Biochem Mol Biol 32: 1311-1316.
68. Hawking, F., Wilson, M.E., and Gammage, K. (1971) Evidence for the cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Trans R Soc Trop Med Hyg 65: 549-559.
69. Hayward, R.E., DeRisi, J.L., Alfadhli, S., Kaslow, D.C., Brown, P.O., and Rathod, P.K. (2000) Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol Microbiol 35: 6-14.
70. Hliscs, M., Millet, C., Dixon, M.W., Siden-Kiamos, I., McMillan, P., and Tilley, L. (2015) Organisation and function of an actin cytoskeleton in Plasmodium falciparum gametocytes. Cell Microbiol 17: 207-225.
71. Ikadai, H., Shaw Saliba, K., Kanzok, S.M., McLean, K.J., Tanaka, T.Q., Cao, J., etal. (2013) Transposon mutagenesis identifies genes essential for Plasmodium falciparum gametocytogenesis. PNAS 110: E1676-E1684.
72. James, S.P. (1928) Ross's 'black spores' in the stomach and salivary glands of malaria-infected mosquitoes. Trans R Soc of Trop Med Hyg XXI (4): 258.
73. Janse, C.J., Rouwenhorst, R.J., van der Klooster, P.F.J., van der Kaay, H.J., and Overdulve, J.P. (1985) Development of Plasmodium berghei ookinetes in the midgut of Anopheles atroparvus mosquitoes and in vitro. Parasitology 91: 219-225.
74. Janse, C.J., van der Klooster, P.F., van der Kaay, H.J., van der Ploeg, M., and Overdulve, J.P. (1986a) Mitomycin-C is an unreliable inhibitor for study of DNA synthesis in Plasmodium. Mol Biochem Parasitol 21: 33-36.
75. Janse, C.J., van der Klooster, P.F.J., van der Kaay, H.J., van der Ploeg, M., and Overdulve, J.P. (1986b) Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei. Trans R Soc Trop Med Hyg 80: 154-157.
76. Janse, C.J., Boorsma, E.G., Ramesar, J., van Vianen, P., van der Meer, R., Zenobi, P., etal. (1989) Plasmodium berghei: gametocyte production, DNA content, and chromosome-size polymorphisms during asexual multiplication in vivo. Exp Parasitol 68: 274-282.
77. Jensen, J.B. (1979) Observations on gametogenesis in Plasmodium falciparum from continuous culture. J Protozool 26: 129-132.
78. Joice, R., Nilsson, S.K., Montgomery, J., Dankwa, S., Egan, E., Morahan, B., etal. (2014) Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci Transl Med 6: 244re245.
79. Kafsack, B.F., Rovira-Graells, N., Clark, T.G., Bancells, C., Crowley, V.M., Campino, S.G., etal. (2014) A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 507: 248-252.
80. Kan, A., Tan, Y.H., Angrisano, F., Hanssen, E., Rogers, K.L., Whitehead, L., etal. (2014) Quantitative analysis of Plasmodium ookinete motion in three-dimensions suggests a critical role for cell shape in the biomechanics of malaria parasite gliding motility. Cell Microbiol 16: 734-750.
81. Kawamoto, F. (1993) Ionic regulation and signal transduction system involved in the induction of gametogenesis in malaria parasites. Ann N Y Acad Sci 707: 431-434.
82. Kawamoto, F., Kido, N., Hanaichi, T., Djamgoz, M.B.A., and Sinden, R.E. (1992) Gamete development in Plasmodium berghei regulated by ionic exchange mechanisms. Parasitol Res 78: 277-284.
83. 2+/calmodulin-dependent and cGMP-dependent pathways in gametogenesis of a rodent malaria parasite, Plasmodium berghei. Eur J Cell Biol 60: 101-107.
84. Khan, S.M., Franke-Fayard, B., Mair, G.R., Lasonder, E., Janse, C.J., Mann, M., and Waters, A.P. (2005) Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121: 675-687.
85. Krotoski, W.A., Omar, M.S., and Jumper, J.R. (1974) Immunofluorescent staining of plasmodial oocysts in the mosquito. J Parasitol 60: 344-347.
86. Kumar, N., and Carter, R. (1984) Biosynthesis of the target antigens of antibodies blocking transmission of Plasmodium falciparum. Mol Biochem Parasitol 13: 333-342.
87. Lal, K., Delves, M.J., Bromley, E., Wastling, J.M., Tomley, F.M., and Sinden, R.E. (2009) Plasmodium male development gene-1 (mdv-1) is important for female sexual development and identifies a polarised plasma membrane during zygote development. Int J Parasitol 39: 755-761.
88. Lamour, S., Straschil, U., Saric, J., and Delves, M. (2014) Changes in metabolic phenotypes of Plasmodium falciparum in vitro cultures during gametocyte development. Malar J 13: 468.
89. Lanfrancotti, A., Bertuccini, L., Silvestrini, F., and Alano, P. (2007) Plasmodium falciparum: mRNA co-expression and protein co-localisation of two gene products upregulated in early gametocytes. Exp Parasitol 116: 497-503.
90. Laveran, M.A. (1881). De la nature parasitaire des accidents de l'impaludisme. Comptes Rendues de la Societe de Biologie Paris 93, 627-630.
91. Li, J., Gutell, R.R., Damberger, S.H., Wirtz, R.A., Kissinger, J.C., Rogers, M.J., etal. (1997) Regulation and trafficking of three distinct 18 S ribosomal RNAs during development of the malaria parasite. J Mol Biol 269: 203-213.
92. Liu, Y., Tewari, R., Ning, J., Blagborough, A., Garbom, S., Pei, J., etal. (2008) The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 22: 1051-1068.
93. McCallum, W.G. (1897) On the flagellated form of the malarial parasite. Lancet 2: 1240-1241.
94. McRobert, L., Taylor, C.J., Deng, W., Fivelman, Q.L., Cummings, R.M., Polley, S.D., etal. (2008) Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLoS Biol 6: e139.
95. Mair, G., Braks, J.A.M., Garver, L.S., Wiegant, J.C.A.G., Hall, N., Dirks, R.W., etal. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313: 667669.
96. Mair, G.R., Lasonder, E., Garver, L.S., Franke-Fayard, B.M., Carret, C.K., Wiegant, J.C., etal. (2010) Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog 6: e1000767.
97. Margos, G., Navarette, S., Butcher, G., Davies, A., Willers, C., Sinden, R.E., and Lachmann, P.J. (2001) Interaction between host complement and mosquito-midgut-stage Plasmodium berghei. Infect Immun 69: 5064-5071.
98. Marques, S.R., Ramakrishnan, C., Carzaniga, R., Blagborough, A.M., Delves, M.J., Talman, A.M., and Sinden, R.E. (2015) An essential role of the basal body protein SAS-6 in Plasmodium male gamete development and malaria transmission. Cell Microbiol 17: 191-206.
99. Mehlhorn, H., Peters, W., and Haberkorn, A. (1980) The formation of kinetes and oocyst in Plasmodium gallinaceum (Haemosporidia) and considerations on phylogenetic relationships between Haemosporidia, Piroplasmida and other Coccidia. Protistologica 16: 135-154.
100. Miura, K., Takashima, E., Deng, B., Tullo, G., Diouf, A., Moretz, S.E., etal. (2013) Functional comparison of Plasmodium falciparum transmission-blocking vaccine candidates by the standard membrane-feeding assay. Infect Immun 81: 4377-4382.
101. Molina-Cruz, A., DeJong, R.J., Charles, B., Gupta, L., Kumar, S., Jaramillo-Guttierrez, G., and Barillas-Mury, C. (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem 283: 3217-3223.
102. Molina-Cruz, A., Garver, L.S., Alabaster, A., Bangiolo, L., Haile, A., Winikor, J., etal. (2013) The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340: 984-987.
103. Mons, B., Janse, C.J., Boorsma, E.G., and Van der Kay, H.J. (1985) Synchronized erythrocytic schizogony and gametocytogenesis of Plasmodium berghei in vivo and in vitro. Parasitology 91: 423-430.
104. Moon, R.W., Taylor, C.J., Bex, C., Schepers, R., Goulding, D., Janse, C.J., etal. (2009) A cyclic GMP signalling module that regulates gliding motility in a malaria parasite. PLoS Pathog 5: e1000599.
105. Morahan, B., and Garcia-Bustos, J. (2014) Kinase signalling in Plasmodium sexual stages and interventions to stop malaria transmission. Mol Biochem Parasitol 193: 23-32.
106. Moreira, L.A., Ito, J., Ghosh, A., Devenport, M., Zieler, H., Abraham, E.G., etal. (2002) Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 277: 40839-40843.
107. Mori, T., Hirai, M., Kuroiwa, T., and Miyagishima, S.Y. (2010) The functional domain of GCS1-based gamete fusion resides in the amino terminus in plant and parasite species. PLoS ONE 5: e15957.
108. Motard, A., Baccam, D., and Landau, I. (1990) Temporary loss of Plasmodium gametocytes infectivity during schizogony. Ann Parasitol Hum Comp 65: 218-220.
109. Muirhead-Thomson, R.C. (1957) The malarial infectivity of an African village population to mosquitoes (Anopheles gambiae). Am J Trop Med Hyg 6: 971-979.
110. Muirhead-Thomson, R.C., and Mercier, E.C. (1952a) Factors in malaria transmission by Anopheles albimanus in Jamaica. Part I. Ann Trop Med Parasitol 46: 103-116.
111. Muirhead-Thomson, R.C., and Mercier, E.C. (1952b) Factors in Malaria transmission by Anopheles albimanus in Jamaica. Part II. Ann Trop Med Parasitol 46: 201-213.
112. Muller, H.M., Crampton, J.M., Della Torre, A., Sinden, R.E., and Crisanti, A. (1993) Members of a trypsin gene family in Anopheles gambiae are induced in the gut by bloodmeal. EMBO J 12: 2891-2900.
113. Naotunne, T.D., Karunaweera, N.D., Mendis, K.N., and Carter, R. (1993) Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78: 555-562.
114. Nijhout, M.M., and Carter, R. (1978) Gamete development in malarial parasites: bicarbonate-dependent stimulation by pH in vitro. Parasitology 76: 39-53.
115. Okamoto, N., Spurck, T.P., Goodman, C.D., and McFadden, G.I. (2008) Apicoplast and mitochondrion in gametocytogenesis of Plasmodium falciparum. Eukaryot Cell 8: 128-132.
116. Olivieri, A., Bertuccini, L., Deligianni, E., Franke-Fayard, B., Curra, C., Siden-Kiamos, I., etal. (2014) Distinct properties of the egress-related osmiophilic bodies in male and female gametocytes of the rodent malaria parasite Plasmodium berghei. Cell Microbiol. doi:10.1111/cmi.12370.
117. Opitz, C., and Soldati, D. (2002) 'The glideosom': a dynamic complex powering gliding motion and host cell invasion by Toxoplasma gondii. Mol Microbiol 45: 597-604.
118. Osta, M.A., Christophides, G.K., and Kafatos, F.C. (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030-2032.
119. Pakpour, N., Corby-Harris, V., Green, G.P., Smithers, H.M., Cheung, K.W., Riehle, M.A., and Luckhart, S. (2012) Ingested human insulin inhibits the mosquito NF-ΚB-dependent immune response to Plasmodium falciparum. Infect Immun 80: 2141-2149.
120. Pakpour, N., Camp, L., Smithers, H.M., Wang, B., Tu, Z., Nadler, S.A., and Luckhart, S. (2013) Protein kinase C-dependent signaling controls the midgut epithelial barrier to malaria parasite infection in anopheline mosquitoes. PLoS ONE 8: e76535.
121. Paton, M.G., Barker, G.C., Matsuoka, H., Ramesar, J., Janse, C.J., Waters, A.P., and Sinden, R.E. (1993) Structure and expression of a conserved and post-transcriptionally regulated gene encoding a surface protein of the sexual stages from malaria parasite Plasmodium berghei. Mol Biochem Parasitol 59: 263-275.
122. Peatey, C.L., Watson, J.A., Trenholme, K.R., Brown, C.L., Nielson, L., Guenther, M., etal. (2013) Enhanced gametocyte formation in erythrocyte progenitor cells: a site-specific adaptation by Plasmodium falciparum. J Infect Dis 208: 1170-1174.
123. Philip, N., Vaikkinen, H.J., Tetley, L., and Waters, A.P. (2012) A unique kelch domain phosphatase in Plasmodium regulates ookinete morphology, motility and invasion. PLoS ONE 7: e44617.
124. Ponnudurai, T., Lensen, A.H.W., and Meuwissen, J.H.E.T. (1983) An automated large-scale culture system of Plasmodium falciparum using tangential flow filtration for medium change. Parasitology 87: 439-445.
125. Ponzi, M., Siden-Kiamos, I., Bertuccinin, L., Curra, C., Kroeze, H., Camarda, G., etal. (2009) Egress of Plasmodium berghei gametes from their host erythrocyte is mediated by MDV-1/PEG3 protein. Cell Microbiol 11: 1272-1288.
126. Povelones, M., Upton, L.M., Sala, K.A., and Christophides, G.K. (2011) Structure-function analysis of the Anopheles gambiae LRIM1/APL1C complex and its interaction with complement C3-like protein TEP1. PLoS Pathog 7: e1002023.
127. Raibaud, A., Lupetti, P., Paul, R.E.L., Mercati, D., Brey, P.T., Sinden, R.E., etal. (2001) Cryofracture electron microscopy of the ookinete pellicle of Plasmodium gallinaceum reveals the existence of novel pores in the alveolar membranes. J Struct Biol 135: 47-57.
128. Raine, J.D., Ecker, A., Mendoza, J., Tewari, R., Stanway, R.R., and Sinden, R.E. (2007) Female inheritance of malarial lap genes is essential for mosquito transmission. PLoS Pathog 3: e30.
129. Ramakrishnan, C., Dessens, J.T., Armson, R., Pinto, S.B., Talman, A.M., Blagborough, A.M., and Sinden, R.E. (2011) Vital functions of the malarial ookinete protein, CTRP, reside in the A domains. Int J Parasitol 41: 1029-1039.
130. Ranfordcartwright, L.C., Balfe, P., Carter, R., and Walliker, D. (1991) Genetic hybrids of Plasmodium falciparum identified by amplification of genomic DNA from single oocysts. Mol Biochem Parasitol 49: 239-244.
131. Reininger, L., Billker, O., Tewari, R., Mukhopadhyay, A., Fennell, C., Dorin-Semblat, D., etal. (2005) A nima-related protein kinase is essential for completion of the sexual cycle of malaria parasites. J Biol Chem 280: 31957-31964.
132. Reininger, L., Tewari, R., Fennell, C., Holland, Z., Goldring, D., Ranford-Cartwright, L., etal. (2009) An essential role for the Plasmodium nek-2 nima-related protein kinase in the sexual development of malaria parasites. J Biol Chem 284: 20858-20868.
133. Reininger, L., Garcia, M., Tomlins, A., Muller, S., and Doerig, C. (2012) The Plasmodium falciparum, Nima-related kinase Pfnek-4: a marker for asexual parasites committed to sexual differentiation. Malar J 11: 250.
134. Rijpma, S., van den Heuvel, J., van der Velden, M., Sauerwein, R., Russel, F., and Koenderink, J. (2014) Atovaquone and quinine anti-malarials inhibit ATP binding cassette transporter activity. Malar J 13: 359.
135. Rodrigues, F.G., Santos, M.N., de Carvalho, T.X.T., Rocha, B.C., Riehle, M.A., Pimenta, P.F.P., etal. (2008) Expression of a mutated phospholipase A2 in transgenic Aedes fluviatilis mosquitoes impacts Plasmodium gallinaceum development. Insect Mol Biol 17: 175-183.
136. Rodriguez, M.C., Margos, G., Compton, H., Ku, M., Lanz, H., Rodríguez, M.H., and Sinden, R.E. (2002) Plasmodium berghei: routine production of pure gametocytes, extracellular gametes, zygotes, and ookinetes. Exp Parasitol 101: 73-76.
137. Roller, N.R., and Desser, S.S. (1973) The effect of temperature, age and density of gametocytes, and changes in gas composition on exflagellation of Leucocytozoon simondi. Can J Zool 51: 577-587.
138. Rosales-Ronquillo, M.C., and Silverman, P.H. (1974) In vitro ookinete development of the rodent malarial parasite, Plasmodium berghei. J Parasitol 60: 819-824.
139. Ross, R. (1897) On some peculiar pigmented cells found in two mosquitoes fed on malarial blood. Br Med J 18: 1786-1788.
140. Rossignol, P.A., Ribeiro, J.M.C., Jungery, M., Turell, M.J., Spielman, A., and Bailey, C.L. (1985) Enhanced mosquito blood-finding success on parasitaemic hosts: evidence for vector-parasite mutualism. Proc Nat Acadf Sci U S A 82: 7725-7727.
141. Ruecker, A., Mathias, D.K., Straschil, U., Churcher, T.S., Dinglasan, R.R., Leroy, D., etal. (2014) A male and female gametocyte functional viability assay to identify biologically relevant malaria transmission-blocking drugs. Antimicrob Agents Chemother 58: 7292-7302.
142. Sauerwein, R.W. (2007) Malaria transmission-blocking vaccines: the bonus of effective malaria control. Microbes Infect 9: 792-795.
143. van Schaijk, B.C.L., van Dijk, M.R., van de Vegte-Bolmer, M., van Gemert, G.J., van Dooren, M.W., Eksi, S., etal. (2006) Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol Biochem Parasitol 149: 216-222.
144. Sebastian, S., Brochet, M., Collins, M.-Á., Schwach, F., Jones, M.-Á., Goulding, D., etal. (2012) A Plasmodium calcium-dependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe 12: 9-19.
145. Shahabuddin, M. (2002) Do Plasmodium ookinetes invade a specific cell type in the mosquito midgut? Trends Parasitol 18: 157-161.
146. Shahabuddin, M., and Kaslow, D.C. (1994a). Biology of the development of Plasmodium in the mosquito midgut: a molecular and cellular view. Bull l'Institut Pasteur 92: 119-132.
147. Shahabuddin, M., and Kaslow, D.C. (1994b) Plasmodium: parasite chitinase and its role in malaria transmission. Exp Parasitol 79: 85-88.
148. Shahabuddin, M., Toyoshima, T., Aikawa, M., and Kaslow, D.C. (1993) Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. Proc Natl Acad Sci U S A 90: 4266-4270.
149. Shahabuddin, M., Kaidoh, T., Aikawa, M., and Kaslow, D.C. (1995) Plasmodium gallinaceum: mosquito peritrophic matrix and the parasite-vector compatibility. Exp Parasitol 81: 386-393.
150. Shao, L., Devenport, M., and Jacobs-Lorena, M. (2001) The peritrophic matrix of hematophagous insects. Arch Insect Biochem Physiol 47: 119-125.
151. Shiao, S.H., Whitten, M.M.A., Zachary, D., HoffmannJ, A., and Levashina, E.A. (2006) Fz2 and Cdc42 mediate melanization and actin polymerization but are dispensable for Plasmodium killing in the mosquito midgut. PLoS Pathog 2: 1152-1164.
152. Shrinet, J., Nandal, U.K., Adak, T., Bhatnagar, R.K., and Sunil, S. (2014) Inference of the oxidative stress network in Anopheles stephensi upon Plasmodium infection. PLoS ONE 9: e114461.
153. Siden-Kiamos, I., and Louis, C. (2008) Intracellular calcium levels in the Plasmodium berghei ookinete. Parasitology 135: 1355-1362.
154. Silvestrini, F., Bozdech, Z., Lanfrancotti, A., Di Guilio, E., Bultrini, E., Picci, L., etal. (2005) Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol Biochem Parasitol 143: 100-110.
155. Simon, N., Lasonder, E., Scheuermayer, M., Kuehn, A., Tews, S., Fischer, R., etal. (2013) Malaria parasites co-opt human factor H to prevent complement-mediated lysis in the mosquito midgut. Cell Host Microbe 13: 29-41.
156. Sinden, R.E. (1982) Gametocytogenesis of Plasmodium falciparum in vitro: ultrastructural observations on the lethal action of chloroquine. Ann Trop Med Parasitol 76: 15-23.
157. Sinden, R.E. (1985) Gametocytogenesis in Plasmodium spp., and observations on the meiotic division. Ann Soc Belg Med Trop 65: 21-33.
158. Sinden, R.E. (1991) Mitosis and meiosis in malarial parasites. Acta Leiden 60: 19-27.
159. Sinden, R.E., and Croll, N.A. (1975) Cytology and kinetics of microgametogenesis and fertilization of Plasmodium yoelii nigeriensis. Parasitology 70: 53-65.
160. Sinden, R.E., and Garnham, P.C.C. (1973) A comparative study of the ultrastructure of Plasmodium sporozoites within the oocyst and salivary glands, with particular reference to the incidence of the micropore. Trans R Soc Trop Med Hyg 67: 631-637.
161. Sinden, R.E., and Hartley, R.H. (1985) Identification of the meiotic division of malarial parasites. J Protozool 32: 742-744.
162. Sinden, R.E., and Smalley, M.E. (1979) Gametocytogenesis of Plasmodium falciparum in vitro: the cell cycle. Parasitology 79: 277-296.
163. Sinden, R.E., Canning, E.U., and Spain, B. (1976) Gametogenesis and fertilization in Plasmodium yoelii nigeriensis: a transmission electron microscope study. Proc R Soc 193: 55-76.
164. Sinden, R.E., Canning, E.U., Bray, R.S., and Smalley, M.E. (1978) Gametocyte and gamete development in Plasmodium falciparum. Proc R Soc Lond B 201: 375-399.
165. Sinden, R.E., Ponnudurai, T., Smits, M.A., Simm, A.M., and Meuwissen, J.H.E.T. (1984) Gametocytogenesis of Plasmodium falciparum in vitro: a simple technique for the routine culture of pure capacitated gametocytes en masse. Parasitology 88: 239-247.
166. Sinden, R.E., Hartley, R., and Winger, L. (1985) The development of Plasmodium ookinetes in vitro: an ultra-structural study including a description of the meiotic division. Parasitology 91: 227-244.
167. Sinden, R.E., Suhrbier, A., Davies, C., Fleck, S., Hodivala, K., and Nicholas, J.C. (1990) The development and routine application of high-density exoerythrocytic-stage cultures of Plasmodium berghei. Bull World Health Organ 68: 115-125.
168. Sinden, R.E., Talman, A., Marques, S.R., Wass, M.N., and Sternberg, M.J.E. (2010) The flagellum in malarial parasites. Curr Opin Microbiol 13: 491-500.
169. Sinha, A., Hughes, K.R., Modrzynska, K.K., Otto, T.D., Pfander, C., Dickens, N.J., etal. (2014) A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 507: 253-257.
170. Sinton, J.A. (1926). Studies in malaria, with special reference to treatment. Part IV. The occurrence of sexual forms of Plasmodium falciparum in the peripheral circulation. Indian J Med Res XIII, 895-916.
171. Sinton, J.A., Baily, J.D., and Chand, D. (1926). Studies in malaria with special reference to treatment. IV. The occurrence of sexual forms of P.falciparum in the peripheral circulation. Indian J Med Res XIII, 895-902.
172. Slavic, K., Delves, M.J., Prudencio, M., Talman, A.M., Straschil, U., Derbyshire, E.T., etal. (2011) Use of a selective inhibitor to define the chemotherapeutic potential of the plasmodial hexose transporter in different stages of the parasite's life cycle. Antimicrob Agents Chemother 55: 2824-2830.
173. Smalley, M.E. (1977) Plasmodium falciparum gametocytes: the effect of chloroquine on their development. Trans R Soc Trop Med Hyg 71: 526-529.
174. Smalley, M.E., and Sinden, R.E. (1977) Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74: 1-8.
175. Smalley, M.E., Abdalla, S., and Brown, J. (1981) The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans R Soc Trop Med Hyg 75: 103-105.
176. Sologub, L., Kuehn, A., Kern, S., Przyborski, J., Schillig, R., and Pradel, G. (2011) Malaria proteases mediate inside-out egress of gametocytes from red blood cells following parasite transmission to the mosquito. Cell Microbiol 13: 897-912.
177. Stanway, R.R., Witt, T., Zobiak, B., Aepfelbacher, M., and Heussler, V.T. (2009) GFP-targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites. Biol Cell 101: 415-435.
178. Straschil, U., Talman, A.M., Ferguson, D.J., Bunting, K.A., Xu, Z., Bailes, E., etal. (2010) The Armadillo repeat protein PF16 is essential for flagellar structure and function in Plasmodium male gametes. PLoS ONE 5: e12901.
179. Suhrbier, A., Janse, C.J., Mons, B., Fleck, S.L., Nicholas, J., Davies, C.S., and Sinden, R.E. (1987). The complete development in vitro of the vertebrate stages of Plasmodium berghei. Trans R Soc Trop Med Hyg 82, 907-910.
180. Talman, A., Prieto, J., Marques, S., Ubaida-Mohien, C., Lawniczak, M., Wass, M., etal. (2014) Proteomic analysis of the Plasmodium male gamete reveals the key role for glycolysis in flagellar motility. Malar J 13: 315.
181. Talman, A.M., Lacroix, C., Marques, S.R., Blagborough, A.M., Carzaniga, R., Ménard, R., and Sinden, R.E. (2011) PbGEST mediates malaria transmission to both mosquito and vertebrate host. Mol Microbiol 82: 462-474.
182. Tao, D., Ubaida-Mohien, C., Mathias, D.K., King, J.G., Pastrana-Mena, R., Tripathi, A., etal. (2014) Sex-partitioning of the Plasmodium falciparum stage V gametocyte proteome provides insight into falciparum-specific cell biology. Mol Cell Proteomics 13: 2705-2724.
183. Targett, G., Drakeley, C., Jawara, M., von Seidlein, L., Coleman, R., Deen, J., etal. (2001) Artesunate reduces but does not prevent posttreatment transmission of Plasmodium falciparum to Anopheles gambiae. J Infect Dis 183: 1254-1259.
184. Templeton, T.J., Keister, D.B., Muratova, O., Procter, J.L., and Kaslow, D.C. (1998) Adherence of erythrocytes during exflagellation of Plasmodium falciparum microgametes is dependent on erythrocyte surface sialic acid and glycophorins. J Exp Med 187: 1599-1609.
185. Tewari, R., Straschil, U., Bateman, A., Bohme, U., Cherevach, I., Gong, P., etal. (2010) The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe 8: 377-387.
186. Thompson, J., and Sinden, R.E. (1994) In situ detection of Pbs21 mRNA during sexual development of Plasmodium berghei. Mol Biochem Parasitol 68: 189-196.
187. Tiburcio, M., Niang, M., Deplaine, G., Perrot, S., Bischoff, E., Ndour, P.A., etal. (2012) A switch in infected erythrocyte deformability at the maturation and blood circulation of Plasmodium falciparum transmission stages. Blood 119: e172-e180.
188. Trager, W., and Gill, G.S. (1992) Enhanced gametocyte formation in young erythrocytes by Plasmodium falciparum in vitro. J Protozool 39: 429-432.
189. Tran, P.N., Brown, S.H., Mitchell, T.W., Matuschewski, K., McMillan, P.J., Kirk, K., etal. (2014) A female gametocyte-specific ABC transporter plays a role in lipid metabolism in the malaria parasite. Nat Commun 5: 4773.
190. Vermeulen, A.N., Ponnudurai, T., Beckers, P.J.A., Verhave, J.P., Smits, M.A., and Meuwissen, J.H.E.T. (1985) Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission-blocking antibodies in the mosquito. J Exp Med 162: 1460-1476.
191. Vervenne, R.A., Dirks, R.W., Ramesar, J., Waters, A.P., and Janse, C.J. (1994) Differential expression in blood stages of the gene coding for the 21-kilodalton surface protein of ookinetes of Plasmodium berghei as detected by RNA in situ hybridisation. Mol Biochem Parasitol 68: 259-266.
192. Vlachou, D., Zimmermann, T., Cantera, R., Janse, C.J., Waters, A.P., and Kafatos, F.C. (2004) Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol 6: 671-685.
193. Wass, M.N., Stanway, R., Blagborough, A.M., Lal, K., Prieto, J.H., Raine, D., etal. (2012) Proteomic analysis of Plasmodium in the mosquito: progress and pitfalls. Parasitology 139: 1131-1145.
194. Waters, A.P. (1994) The ribosomal RNA genes of Plasmodium. Adv Parasitol 34: 33-79.
195. Waters, A.P., Syin, C., and McCutchan, T.F. (1989) Development regulation of stage-specific ribosome populations in plasmodium. Nature 342: 438-440.
196. Wiley, J.D., Merino, E.F., Krai, P.M., McLean, K.J., Tripathi, A.K., Vega-Rodríguez, J., etal. (2014) Isoprenoid precursor biosynthesis is the essential metabolic role of the apicoplast during gametocytogenesis in Plasmodium falciparum. Eukaryotic Cell. pii.EC.00198-00114.
197. Wilson, L.G., Carter, L.M., and Reece, S.E. (2013) High-speed holographic microscopy of malaria parasites reveals ambidextrous flagellar waveforms. Proc Natl Acad Sci U S A 110: 18769-18774.
198. Wirth, C.C., Glushakova, S., Scheuermayer, M., Repnik, U., Garg, S., Schaack, D., etal. (2014) Perforin-like protein PPLP2 permeabilizes the red blood cell membrane during egress of Plasmodium falciparum gametocytes. Cell Microbiol 16: 709-733.
199. Wong, W., Bai, X.C., Brown, A., Fernandez, I.S., Hanssen, E., Condron, M., etal. (2014) Cryo-EM structure of the Plasmodium falciparum 80S ribosome bound to the anti-protozoan drug emetine. eLife 3. doi:10.7554/elife.03080.
200. Young, J.A., Fivelman, Q.L., Blair, P.L., de la Vega, P., Le Roch, K.G., Zhou, Y., etal. (2005) The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol 143: 67-79.
201. Yuda, M., Iwanaga, S., Shigenobu, S., Mair, G.R., Janse, C.J., Waters, A.P., etal. (2009) Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol 71: 1402-1414.
202. Zhu, J.D., Waters, A.P., Appiah, A., McCutchan, T.F., Lal, A.A., and Hollingdale, M.R. (1990) Stage-specific ribosomal RNA expression switches during sporozoite invasion of hepatocytes. J Biol Chem 265: 12740-12744.
203. Zieler, H., Nawrocki, J.P., and Shahabuddin, M. (1999) Plasmodium gallinaceum ookinetes adhere specifically to the midgut epithelium of Aedes aegypti by interaction with a carbohydrate ligand. J Exp Biol 202: 485-495.
204. Zieler, H., Garon, C.F., Fischer, E.R., and Shahabuddin, M. (2000) A tubular network associated with the brush-border surface of Aedes aegypti midgut: implications for pathogen transmission by mosquitoes. J Exp Biol 203: 1599-1611.