Insect-malaria parasites interactions: The salivary gland

Insect Biochemistry and Molecular Biology

Volumn 34, Issue 7, 2004, Pages 615-624

  Rodriguez, Mario H ^a   Hernández Hernández, Fidel De La C ^b  

^a Ctro Invest Sobre Enferm I   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Malaria; Mosquito; Proteins; Salivary glands; Sporozoites

Indexed keywords

AEDES; ANIMAL; CONFERENCE PAPER; HOST PARASITE INTERACTION; MOSQUITO; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLASMODIUM; SALIVARY GLAND;

AEDES; ANIMALS; CULICIDAE; HOST-PARASITE RELATIONS; PLASMODIUM; SALIVARY GLANDS;

ANOPHELES GAMBIAE; INSECTA; PLASMODIUM FALCIPARUM; VERTEBRATA;

EID: 3142623161     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2004.03.014     Document Type: Conference Paper

References (112)

1. Adams J., Sim B., Dolan S., Fang X., Kaslow D., Miller L. A family of erythrocyte binding proteins of malaria parasites. Proc. Natl. Acad. Sci. (USA). 89:1992;7085-7089
2. Aikawa M., Miller L.H., Johnson J., Rabbege J. Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. J. Cell Biol. 77:1978;72-82
3. Al-Olayan E.M., Beetsma A.L., Butcher G.A., Sinden R.E., Hurd H. Complete development of mosquito phases of the malaria parasite in vitro. Science. 295:2002;677-679
4. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:1997;3389-3402
5. Arcà B., Lombardo F., Lanfrancotti A., Spanos L., Veneri M., Louis C., Coluzzi M. A cluster of four D7-related genes is expressed in the salivary glands of the African malaria vector Anopheles gambiae. Insect Mol. Biol. 11:2002;47-55
6. Ball G.H., Chao J. Infectivity to canaries of sporozoites of Plasmodium relictum developing in vitro. J. Parasitol. 47:1961;787-790
7. Barreau C., Touray M., Pimenta P.F., Miller L.H., Vernick K.D. Plasmodium gallinaceum: sporozoite invasion of Aedes aegypti salivary glands is inhibited by antigland antibodies and by lectins. Exp. Parasitol. 81:1995;332-343
8. Beerntsen B.T., Champagne D.E., Coleman J.L., Campos Y.A., James A.A. Characterization of the Sialokinin I gene encoding the salivary vasodilator of the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 8:1999;459-468
9. Beier J.C. Malaria sporozoites: survival, transmission and disease control. Parasitol. Today. 9:1993;210-215
10. Blackman M., Bannister L. Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Mol. Biochem. Parasitol. 117:2001;11-25
11. Brennan J., Kent M., Dhar R., Fulioka H., Kumar N. Anopheles gambiae salivary gland proteins as putative targets for blocking transmission of malaria parasites. Proc. Natl. Acad. Sci. (USA). 97:2000;13859-13864
12. Brown P., Gill A.C., Nugent G., Mc Vey J.H., Tomleya F. Domains of invasion organelle proteins from apicomplexan parasites are homologous with the Apple domains of blood coagulation factor XI and plasma pre-kallikrein and are members of the PAN module superfamily. FEBS Lett. 497:2001;31-38
13. Bumstead J., Tomley F. Induction of secretion and surface capping of microneme proteins in Eimeria tenella. Mol. Biochem. Parasitol. 110:2000;311-321
14. Calvo E., de Bianchi A.G., James A.A., Marinotti O. The major acid soluble proteins of adult female Anopheles darlingii salivary glands include a member of the D-7 related family of proteins. Insect Biochem. Mol. Biol. 32:2002;1419-1427
15. Carruthers V. Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitol. Int. 48:1999;1-10
16. Champagne D.E., Ribeiro J.M. Sialokinin I and II: vasodilatory tachykinins from the yellow fever mosquito Aedes aegypti. Proc. Natl. Acad. Sci. (USA). 91:1994;138-142
17. Champagne D.E., Smartt C.T., Ribeiro J.M., James A.A. The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5′-nucleotidase family. Proc. Natl. Acad. Sci. (USA). 92:1995;694-698
18. Chaudhuri A., Zbizezna V., Johnson C., Nichols M., Rubinstein P., Marsh W., Pogo A. Purification and characterization of an erythrocyte membrane protein complex Duffy blood group antigenicity. Possible receptors for Plasmodium vivax and Plasmodium knowlesi malaria parasites. J. Biol. Chem. 23:1989;13770-13774
19. Christophers S.R. Aedes aegypti: The Yellow Fever Mosquito. 1960;Cambridge University Press
20. Clements A.N. Biology of Mosquitoes: Development, Nutrition and Reproduction. 1992;Chapman & Hall, London
21. Daher V.R., Krettli A.U. Infectivity of Plasmodium gallinaceum sporozoites from oocysts. J. Protozool. 27:1980;440-442
22. de Lara Capurro M., Coleman J., Beerntsen B.T., Myles K.M., Olson K.E., Rocha E., Krettli A.U., James A.A. Virus-expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am. J. Trop. Med. Hyg. 62:2000;427-433
23. Donahue C., Carruthers V., Gilk S., Ward G. The Toxoplasma homolog of Plasmodium apical membrane antigen-1 (AMA-1) is a microneme protein secreted in response to elevated intracellular calcium levels. Mol. Biochem. Parasitol. 111:2000;15-30
24. Edwards J.F., Higgs S., Beaty B.J. Mosquito feeding-induced enhancement of cache valley virus (Bunyaviridae) infection in mice. J. Med. Entomol. 35:1998;261-265
25. Foster W.A. Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol. 40:1995;443-474
26. Francischetti I.M., Valenzuela J.G., Ribeiro J.M. Anophelin: kinetics and mechanism of thrombin inhibition. Biochemistry. 38:1999;16678-16685
27. Frevert U., Sinnis P., Esko J.D., Nussenzweig V. Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei sporozoite invasion in vitro. Mol. Biochem. Parasitol. 76:1996;257-266
28. Gantt S., Persson C., Rose K., Birkett A.J., Abagyan R., Nussenzweig V. Antibodies against TRAP do not inhibit Plasmodium sporozoite infectivity in vivo. Infect. Immun. 68:2000;3667-3673
29. Gosh A.K., Ribolla P.E., Jacobs-Lorena M. Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display library. Proc. Natl. Acad. Sci. (USA). 98:2001;13278-13281
30. Gilberger T.W., Thompson J.K., Reed M.B., Good R.T., Cowman A.E. The cytoplasmic domain of the Plasmodium falciparum ligand EBA-175 is essential for invasion but not protein trafficking. J. Cell Biol. 162:2003;317-327
31. Girma J.P., Meyer D., Verweij C.L., Pannekoek H., Sixma J.J. Structure-function relationship of human von Willebrand factor. Blood. 70:1987;605-611
32. Golenda C.F., Starkweather W.H., Wirtz R.A. The distribution of circumsporozoite protein (CS) in Anopheles stephensi mosquitoes infected with Plasmodium falciparum malaria. J. Histochem. Cytochem. 38:1990;475-481
33. Healer J., Crawford S., Ralph S., McFadden G., Cowman A. Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infect. Immun. 70:2002;5751-5758
34. Holiday-Hanson M.L., Yuval B., Washino R.K. Energetics and sugar-feeding of field-collected anopheline females. J. Vector Ecol. 22:1997;83-89
35. Isawa H., Yuda M., Orito Y., Chinzei Y. A mosquito salivary protein inhibits activation of the plasma contact system by binding to factor XII and high molecular weight kininogen. J. Biol. Chem. 277:2002;27651-27658
36. James A.A. Molecular and biochemical analyses of the salivary glands of vector mosquitoes. Bull. Inst. Pasteur. 92:1994;133-150
37. James A.A., Rossignol P.A. Mosquito salivary glands. Parasitological and molecular aspects. Parasitol. Today. 7:1991;267-271
38. James A.A., Blackmer K., Marinotti O., Ghosn C.R., Racioppi J.V. Isolation and characterization of the gene expressing the major salivary gland protein of the female mosquito, Aedes aegypti. Mol. Biochem. Parasitol. 44:1991;245-253
39. Janzen H.G., Wright K.A. The salivary glands of Aedes aegypti (L.): an electron microscope study. Can. J. Zool. 49:1971;1343-1350
40. Jeffery C.J. Moonlighting proteins: old proteins learning new tricks. Trends Genet. 19:2003;415-417
41. Jewett T.J., Sibley L.D. Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol. Cell. 11:2003;885-894
42. Jonas A. Lecithin cholesterol acyltransferase. Biochem. Biophys. Acta. 1529:2000;245-256
43. Joy D., Feng X., Mu J., Furuya T., Chotivanich K., Kretti A., Ho M., Wang A., White N., Suh E., Beerli P., Su X. Early origin and recent expansion of Plasmodium falciparum. Science. 300:2003;318-321
44. Kappe S., Bruderer T., Gantt S., Fujioka H., Nussenzweig V., Ménard R. Conservation of a gliding motility and cell invasion machinery in Apicomplexan parasites. J. Cell Biol. 147:1999;937-943
45. Kariu T., Yuda M., Yano K., Chinzei Y. MAEBL is essential for malarial sporozoite infection of the mosquito salivary gland. J. Exp. Med. 195:2002;1317-1323
46. Klotz F.W., Hadley T.J., Aikawa M., Leech J., Howard R.J., Miller L.H. A 60-kDa Plasmodium falciparum protein at the moving junction formed between merozoite and erythrocyte during invasion. Mol. Biochem. Parasitol. 36:1989;177-185
47. Lanfrancotti A., Lombardo F., Santolamazza F., Veneri M., Castrignano T., Coluzzi M., Arcà B. Novel cDNAs encoding salivary proteins from the malaria vector Anopheles gambiae. FEBS Lett. 517:2002;67-71
48. Langer R.C., Hayward R.E., Tsuboi T., Tachibana M., Torii M., Vinetz J.M. Micronemal transport of Plasmodium ookinete chitinases to the electron-dense area of the apical complex for extracellular secretion. Infect. Immun. 68:2000;6461-6465
49. Lawler J., Hynes R.O. The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J. Cell Biol. 103:1986;1635-1648
50. Lehane M.J. The Biology of Blood Sucking Insects. 1991;Harper Collins Academic, London
51. Maier W.A., Becker-Feldman H., Seitz H.M. Pathology of malaria infected mosquitoes. Parasitol. Today. 3:1987;216-218
52. Marinotti O., James A.A., Ribeiro J.M.C. Diet and salivation in female Aedes aegypti mosquitoes. J. Insect Physiol. 36:1990;545-548
53. Marinotti O., deBrito M., Moreira C.K. Apyrase and alphaglucosidase in the salivary glands of Aedes albopictus. Comp. Biochem. Physiol. Ser. B. 113:1996;675-679
54. Matuschewski K., Nunes A.C., Nussenzweig V., Robert Ménard R. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 21:2002a;1597-1606
55. Matuschewski K., Ross J., Brown S.M., Kaiser K., Nussenzweig V., Kappe S.H.I. Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J. Biol. Chem. 277:2002b;41948-41953
56. McCutchan T.F., Kissinger J.C., Touray M.G., Rogers M.J., Li J., Sullivan M., Braga E.M., Krettli A.U., Miller L.H. Comparison of circumsporozoite proteins from avian and mammalian malarias: biological and phylogenetic implications. Proc. Natl. Acad. Sci. (USA). 93:1996;11889-11894
57. Meis J.F., Wismans P.G., Jap P.H.K., Lensen A.H., Ponnudurai T. A scanning electron microscopic study of the sporogonic development of Plasmodium falciparum in Anopheles stephensi. Acta Trop. 50:1992;227-236
58. Ménard R. The journey of the malaria sporozoite through its hosts: two parasite proteins lead the way. Microbes Infect. 2:2000;633-642
59. Ménard R., Sultan A.A., Cortex C., Altszuler R., Van Dijk M.R., Janse C.J., Waters A.P., Nussenzweig R.S., Nussenzweig V. Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature. 385:1997;336-340
60. Michon P., Stevens J., Kaneko O., Adams J. Evolutionary relationships of conserved cysteine-rich motifs in adhesive molecules of malaria parasites. Mol. Biol. Evol. 19:2002;1128-1142
61. Miller L.H., Aikawa M., Johnson J.G., Shiroishi T. Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J. Exp. Med. 149:1979;172-184
62. Montero-Solis C., Gonzalez-Ceron L., Rodriguez M.H., Cirerol B.E., Zamudio F., Posan L.D., James A.A., Hernandez-Hernandez F.C. Identification and characterization of gp65, a salivary-gland-specific molecules expressed in the malaria vector Anopheles albimanus. Insect Mol. Biol. 13:2004;155-164
63. Moran P., Caras I.W. Requirements for glycosylphosphatidylinositol attachment are similar but not identical in mammalian cells and parasitic protozoa. J. Cell Biol. 125:1994;333-343
64. Nguyen T.V., Fujiokas H., Kang A.S., Rogers W.O., Fidock D.A., James A.A. Stage-dependent localization of a novel gene product of the malaria parasite, Plasmodium falciparum. J. Biol. Chem. 276:2001;26724-26731
65. Nussenzweig R.S., Chen D. The antibody response to sporozoites of simian and human parasites: its stage and species specificity and strain cross-reactivity. Bull. WHO. 50:1974;293-297
66. Orlandi P., Klotz F., Haynes J. A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha2-3)Gal sequences of glycophorin A. J. Cell Biol. 116:1992;901-909
67. Orr C.W.M., Hudson A., West A.S. The salivary glands of Aedes aegypti: histological-histochemical studies. Can. J. Zool. 39:1961;265-272
68. Osorio J.E., Godsey M.S., Defoliart G.R., Yuill T.M. La Crosse viremias in white-tailed deer and chipmunks exposed by injection or mosquito bite. Am. J. Trop. Med. Hyg. 54:1996;338-342
69. Perrone J.B., DeMaio J., Spielman A. Regions of mosquito salivary glands distinguished by surface lectin-binding characteristics. Insect Biochem. 16:1986;313-318
70. Peterson D.S., Miller L.H., Wellems T.E. Isolation of multiple sequences from the Plasmodium falciparum genome that encode conserved domains homologous to those in erythrocyte-binding proteins. Proc. Natl. Acad. Sci. (USA). 92:1995;7100-7104
71. Pimenta P.F., Touray M., Miller L. The journey of malaria sporozoites in the mosquito salivary gland. J. Euk. Microbiol. 41:1994;608-624
72. Posthuma G., Meis F.G.M., Verhave J.P., Hollingdale M.R., Ponnudurai T., Meuwissen J.H., Geuze H.J. Localization of circumsporozoite protein of the malaria parasite Plasmodium falciparum during sporogony in Anopheles stephensi midguts using immunoelectron-microscopy of ultrathin cryosections. Eur. J. Cell Biol. 46:1988;18-24
73. Ribeiro J.M. Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect. Agents Dis. 4:1995;143-152
74. Ribeiro J.M. Blood-feeding in mosquitoes: probing time and salivary gland anti-haemostatic activities in representatives of three genera (Aedes, Anopheles, Culex). Med. Vet. Entomol. 14:2000;142-148
75. Ribeiro J.M., Francischetti I.M.B. Role of arthropod saliva in blood feeding sialome and post-sialome perspectives. Annu. Rev. Entomol. 48:2003;73-88
76. Ribeiro J.M., Nussenzweig R.H. The salivary catechol oxidase/peroxidase activities of the mosquito Anopheles albimanus. J. Exp. Biol. 179:1993;273-287
77. Ribeiro J.M., Sarkis J.J., Rossignol P.A., Spielman A. Salivary apyrase of Aedes aegypti: characterization and secretory fate. Comp. Biochem. Physiol. Ser. B. 79:1984;81-86
78. Ribeiro J.M., Charlab R., Valenzuela J.G. The salivary adenosine deaminase activity of the mosquitoes Culex quinquefasciatus and Aedes aegypti. J. Exp. Biol. 204:2001;2001-2010
79. Robson K.J., Hall J.R., Jennings M.W., Harris T.J., Marsh K., Newbold C.I., Tate V.E., Weatherhall D.J. A highly conserved amino-acid sequence in trombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature. 335:1988;79-82
80. Rogers W.O., Hedstrom R.C., Hoffman S.L. Characterization of Plasmodium falciparum sporozoite surface protein 2. Proc. Natl. Acad. Sci. (USA). 2:1992;9176-9180
81. Rosenberg R. Inability of Plasmodium knowlesi sporozoites to invade Anopheles freeborni salivary glands. Am. J. Trop. Med. Hyg. 34:1985;687-691
82. Rossignol P.A., Lueders A.M. Bacteriolytic factor in the salivary glands of Aedes aegypti. Comp. Biochem. Physiol. 83B:1986;819-822
83. Rossignol P.A., Ribeiro J.M., Spielman A. Increased intradermal probing time in sporozoite-infected mosquitoes. Am. J. Trop. Med. Hyg. 33:1984;17-20
84. Sam-Yellowe T.Y., Del Rio R.A., Fujioka H., Aikawa M., Yang J.C., Yakubu Z. Isolation of merozoite rhoptries, identification of novel rhoptry-associated proteins from Plasmodium yoelii, P. chabaudi, P. berghei, and conserved interspecies reactivity of organelles and proteins with P. falciparum rhoptry-specific antibodies. Exp. Parasitol. 89:1998;271-284
85. Schneider I. Cultivation in vitro of Plasmodium gallinaceum oocysts. Exp. Parasitol. 22:1968;178-186
86. Shahabuddin M., Toyoshima T., Aikawa M., Kaslow D.C. Transmission- blocking activity of a chitinase inhibitor activation of malaria parasite chitinase by mosquito protease. Proc. Natl. Acad. Sci. (USA). 90:1993;4266-4270
87. Sidjanski S.P., Vanderberg J.P., Sinnis P. Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol. Biochem. Parasitol. 90:1997;33-41
88. Sinai A., Joiner K. The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J. Cell Biol. 154:2001;95-108
89. Sinden R.E. Cell biology. Killick Kendrick R., Peters W.A. Rodent Malaria. 1978;85-186 Academic Press, New York
90. Sinden R.E. The cell biology of sexual development in Plasmodium. Parasitology. 86:1983;7-28
91. Sinden R.E. The biology of Plasmodium in the mosquito. Experientia. 40:1984;1330-1343
92. Stark K.R., James A.A. A factor Xa-directed anticoagulant from the salivary glands of the yellow fever mosquito Aedes aegypti. Exp. Parasitol. 81:1995;321-331
93. Stark K.R., James A.A. Salivary gland anticoagulants in Culicine and Anopheline mosquitoes (Diptera: Culicidae). J. Med. Entomol. 33:1996;645-650
94. Stark K.R., James A.A. Isolation and characterization of the gene encoding a novel factor Xa-directed anticoagulant from the yellow fever mosquito, Aedes aegypti. J. Biol. Chem. 273:1998;20802-20890
95. Sterling C.R., Aikawa M., Vanderberg J.P. The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi. An electron microscope study. J. Parasitol. 59:1973;593-605
96. Stewart M.J., Vanderberg J.P. Malaria sporozoites release circumsporozoite protein from their apical end and translocate it along their surface. J. Protozool. 38:1991;411-421
97. Sultan A.A., Thathy V., Frevert U., Frevert U., Robson K.J., Crisanti A., Nussenzweig V., Nussenzweig R.S., Ménard R. TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell. 90:1997;511-522
98. Suwan N., Wilkinson M.C., Crampton J.M., Bates P.A. Expression of D7 and D7-related proteins in the salivary glands of human malaria mosquitoes Anopheles stephensi. Insect Mol. Biol. 11:2002;223-232
99. Tabor C.W., Tabor H. Polyamines. Annu. Rev. Biochem. 53:1984;749-790
100. Tewari R., Spaccapelo R., Bistoni F., Holder A.A., Crisanti A. Function of region I and II adhesive motifs of Plasmodium falciparum circumsporozoite protein in sporozoite motility and infectivity. J. Biol. Chem. 277:2002;47613-47618
101. Touray M.G., Warburg A., Laughinghouse A., Krettli A.U., Miller L.H. Developmentally regulated infectivity of malaria sporozoites for mosquito salivary glands and the vertebrate host. J. Exp. Med. 175:1992;1607-1612
102. Touray M.G., Seeley D.C. Jr., Miller L.H. Plasmodium gallinaceum: differential lysis of two developmental stages of malaria sporozoites by the alternative pathway of complement. Exp. Parasitol. 78:1994;294-301
103. Valenzuela J.G., Pham V.M., Garfield M.K., Francischetti I.M., Ribeiro J.M.C. To ward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 32:2002;1101-1122
104. Vanderberg J.P. Studies on the motility of Plasmodium sporozoites. J. Protozool. 21:1974;527-537
105. Vanderberg J.P. Development of infectivity by the Plasmodium berghei sporozoite. J. Parasitol. 61:1975;43-50
106. Vanderberg J.P., Rhodin J., Yoeli M. Electron microscopic and histochemical studies of sporozoite formation in Plasmodium berghei. J. Protozool. 14:1967;82-103
107. Vanderberg J.P., Nussenzweig R.S., Sanabria Y., Nawrot R., Most H. Stage specificity of anti-sporozoite anti-bodies in rodent malaria and its relationship to protective immunity. Proc. Helminthol. Soc. Wash. 39:1972;514-525
108. Vaughan J.A., Noden B.H., Beier J.C. Population dynamics of Plasmodium falciparum sporogony in laboratory-infected Anopheles gambiae. J. Parasitol. 78:1992;716-724
109. Wengelnik K., Spaccapelo R., Naitza S., Robson K.J., Janse C.J., Bistoni F., Waters A.P., Crisanti A. The A-domain and the thrombospondin-related motif of Plasmodium falciparum TRAP are implicated in the invasion process of mosquito salivary glands. EMBO J. 18:1999;5195-5204
110. Wikel S.K., Rachamandra R.N., Bergman D.K. Arthropod modulation of host immune responses. Wikel S.K. The Immunology of Host-Ectoparasitic Arthropod Relationships. 1996;107-130 CAB International, Wallingford
111. Wright K.A. The anatomy of the salivary glands of Anopheles stephensi. Liston. Can. J. Zool. 47:1969;579-588
112. Yuda M., Yano K., Tsuboi K., Torii M., Chinzei M. von Willebrand factor A domain-related protein, a novel microneme protein of the malaria ookinete highly conserved throughout Plasmodium parasites. Mol. Biochem. Parasitol. 116:2001;65-72