Abstract
Malaria parasites of the genus Plasmodium are transmitted from host to host by mosquitoes. Sexual reproduction occurs in the blood meal and the resultant motile zygote, the ookinete, migrates through the midgut epithelium and transforms to an oocyst under the basal lamina. After sporogony, sporozoites are released into the mosquito haemocoel and invade the salivary gland before injection when next the mosquito feeds on a host. Interactions between parasite and vector occur at all stages of the establishment and development of the parasite and some of these result in the death of parasite and host cells by apoptosis. Infection-induced programmed cell death occurs in patches of follicular epithelial cells in the ovary, resulting in follicle resorption and thus a reduction in egg production. We argue that fecundity reduction will result in a change in resource partitioning that may benefit the parasite. Apoptosis also occurs in cells of the midgut epithelium that have been invaded by the parasite and are subsequently expelled into the midgut. In addition, the parasite itself dies by a process of programmed cell death (PCD) in the lumen of the midgut before invasion has occurred. Caspase-like activity has been detected in the cytoplasm of the ookinetes, despite the absence of genes homologous to caspases in the genome of this, or any, unicellular eukaryote. The putative involvement of other cysteine proteases in ancient apoptotic pathways is discussed. Potential signal pathways for induction of apoptosis in the host and parasite are reviewed and we consider the evidence that nitric oxide may play a role in this induction. Finally, we consider the hypothesis that death of some parasites in the midgut will limit infection and thus prevent vector death before the parasites have developed into mature sporozoites.
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References
Abraham EG, Islam S, Srinivasan P, Ghosh AK, Valenzuela JG, Ribeiro JM, Kafatos FC, Dimopoulos G, Jacobs-Lorena M (2004) Analysis of the Plasmodium and Anopheles transcriptional repertoire during ookinete development and midgut invasion. J Biol Chem 279:5573–5580
Abraham EG, Jacobs-Lorena M (2004) Mosquito midgut barriers to malaria parasite development. Insect Biochem Mol Biol 34:667–671
Ahmed AM, Maingon R, Romans P, Hurd H (2001) Effects of malaria infection on vitellogenesis in Anopheles gambiae during two gonotrophic cycles. Insect Mol Biol 10:347–356
Ahmed AM, Maingon RD, Taylor PJ, Hurd H (1999) The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae. Invertebr Reprod Dev 36:217–222
Aikawa M, Yoshida N, Nussenzweig RS, Nussenzweig V (1981) The protective antigen of malarial sporozoites (Plasmodium berghei) is a differentiation antigen. J Immunol 126:2484–2495
Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, Sinden RE (2003) The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol 33:933–943
Al-Olayan EM, Beetsma AL, Butcher GA, Sinden RE, Hurd H (2002a) Complete development of mosquito phases of the malaria parasite in vitro. Science 295:677–679
Al-Olayan EM, Williams GT, Hurd H (2002b) Apoptosis in the malaria protozoan, Plasmodium berghei: A possible mechanism for limiting intensity of infection in the mosquito. Int J Parasitol 32:1133–1143
Ameisen JC, Idziorek T, Billautmulot O, Loyens M, Tissier JP, Potentier A, Ouaissi A (1995) Apoptosis in a unicellular eukaryote (Trypanosoma cruzi)—implications for the evolutionary origin and role of programmed cell-death in the control of cell-proliferation, differentiation and survival. Cell Death Differ 2:285–300
Arai M, Billker O, Morris HR, Panico M, Delcroix M, Dixon D, Ley SV, Sinden RE (2001) Both mosquito-derived xanthurenic acid and a host blood-derived factor regulate gametogenesis of Plasmodium in the midgut of the mosquito. Mol Biochem Parasitol 116:17–24
Aravind L, Dixit VM, Koonin EV (2001) Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 291:1279–1284
Arnoult D, Akarid K, Grodet A, Petit PX, Estaquier J, Ameisen JC (2002a) On the evolution of programmed cell death: apoptosis of the unicellular eukaryote Leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ 9:65–81
Arnoult D, Parone P, Martinou JC, Antonsson B, Estaquier J, Ameisen JC (2002b) Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159:923–929
Arrighi RB, Hurd H (2002) The role of Plasmodium berghei ookinete proteins in binding to basal lamina components and transformation into oocysts. Int J Parasitol 32:91–98
Bai P, Bakondi E, Szabo E, Gergely P, Szabo C, Virag L (2001) Partial protection by poly(ADP-ribose) polymerase inhibitors from nitroxyl-induced cytotoxicity in thymocytes. Free Radic Biol Med 31:1616–1623
Barillas-Mury C, Wizel B, Han YS (2000) Mosquito immune responses and malaria transmission: lessons from insect model systems and implications for vertebrate innate immunity and vaccine development. Insect Biochem Mol Biol 30:429–442
Baton LA, Ranford-Cartwright LC (2004) Plasmodium falciparum ookinete invasion of the midgut epithelium of Anopheles stephensi is consistent with the Time Bomb model. Parasitology (in press)
Billingsley PF, Lehane MJ (eds) (1996) The Insect Midgut. Chapman and Hall
Billingsley PF, Rudin W (1992) The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species. J Parasitol 78:430–440
Billingsley PF, Sinden RE (1997) Determinants of malaria-mosquito specificity. Parasitol Today 13:297–301
Billker O, Dechamps S, Tewari R, Wenig G, Franke-Fayard B, Brinkmann V (2004) Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117:503–514
Billker O, Shaw MK, Margos G, Sinden RE (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
Blanco ARA, Paez A, Gerold P, Dearsly AL, Margos G, Schwartz RT, Barker G, Rodriguez MC, Sinden RE (1999) The biosynthesis and post-translational modification of Pbs21, an ookinete-surface protein of Plasmodium berghei. Mol Biochem Parasitol 98:163–173
Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, Levashina EA (2002) Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep 3:852–856
Brockhaus F, Brune B (1999) Overexpression of CuZn superoxide dismutase protects RAW 264.7 macrophages against nitric oxide cytotoxicity. Biochem J 338:295–303
Buszczak M, Cooley L (2000) Eggs to die for: cell death during Drosophila oogenesis. Cell Death Differ 7:1071–1074
Cao Y-M, Tsuboi T, Torii M (1998) Nitric oxide inhibits the development of Plasmodium yoelii gametocytes into gametes. Parasitol Int 47:157–166
Carwardine SL, Hurd H (1997) Effects of Plasmodium yoelii nigeriensis infection on Anopheles stephensi egg development and resorption. Med Vet Entomol 11:265–269
Cavaliere V, Taddei C, Gargiulo G (1998) Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster. Dev Genes Evol 208:106–112
Chao S, Nagoshi RN (1999) Induction of apoptosis in the germline and follicle layer of Drosophila egg chambers. Mech Dev 88:159–172
Chose O, Sarde CO, Gerbod D, Viscogliosi E, Roseto A (2003) Programmed cell death in parasitic protozoans that lack mitochondria. Trends Parasitol 19:559–564
Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffmann JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Muller HM, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, von Mering C, Xu J, Zheng L, Bork P, Kafatos FC (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298:159–165
Clements AN, Boocock MR (1984) Ovarian development in mosquitoes: stages of growth and arrest and follicular resorption. Physiol Entomol 9:1–8
Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC, Gwadz RW (1986) Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234:607–610
Colombatti A, Bonaldo P, Dolian R (1993) Type A molecules: interacting domains found in several non-fibrillar collagens and in other extracellular matrix proteins. Matrix 13:297–306
Cruz MA, Yuan H, Lee JR, Wise RJ, Handin RI (1995) Interaction of the von Wille-brand factor (vWF) with collagen. J Biol Chem 270:10822–10827
Das M, Mukherjee SB, Shaha C (2001) Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J Cell Sci 114:2461–2469
Deponte M, Becker K (2004b) Plasmodium falciparum—do killers commit suicide? Trends Parasitol 20:165–169
Dessens JT, Beetsma AL, Dimopoulos G, Wengenlik K, Crisanti A, Kafatos F, Sinden RE (1999) CTRP is essential for mosquito infection by malaria ookinetes. EMBO J 18:6221–6227
Dessens JT, Siden-Kiamos I, Mendoza J, Mahairaki V, Khater E, Vlachou D, Xu XI, Kafatos FC, Louis C, Dimopoulos G, Sinden RE (2003) SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 49:319–329
Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, Kafatos FC (2002) Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA 99:8814–8819
Dimopoulos G, Muller HM, Levashina EA, Kafatos FC (2001) Innate immune defense against malaria infection in the mosquito. Curr Opin Immunol 13:79–88
Dimopoulos G, Seeley D, Wolf A, Kafatos FC (1998) Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J 17:6115–6123
Ferguson HM, Read AF (2002) Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol 18:256–261
Foley K, Cooley L (1998) Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency. Development 125:1075–1082
Frohlich KU, Madeo F (2000) Apoptosis in yeast—a monocellular organism exhibits altruistic behaviour. FEBS Lett 473:6–9
Gad AM, Maier WA, Piekarski G (1979) Pathology of Anopheles stephensi after infection with Plasmodium berghei berghei. II. Changes in amino acid contents. Z Parasitenkd 60:263–276
Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498–511
Ghosh A, Edwards MJ, Jacobs-Lorena M (2000) The journey of the malaria parasite in the mosquito: hopes for the new century. Parasitol Today 16:196–201
Han YS, Barillas-Mury C (2002) Implications of Time Bomb model of ookinete invasion of midgut cells. Insect Biochem Mol Biol 32:1311–1316
Han YS, Thompson J, Kafatos FC, Barillas-Mury C (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J 19:6030–6040
Harada M, Owhashi M, Suguri S, Kumatori A, Nakamura M, Kanbara H, Matsuoka H, Ishii A (2001) Superoxide-dependent and-independent pathways are involved in the transmission blocking of malaria. Parasitol Res 87:605–608
Harvey NL, Daish T, Mills K, Dorstyn L, Quinn LM, Read SH, Richardson H, Kumar S (2001) Characterization of the Drosophila caspase, DAMM. J Biol Chem 276:25342–25350
Hogg JC, Hurd H (1995) Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111:555–562
Hogg JC, Hurd H (1997) The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s. l. In north east Tanzania. Parasitology 114:325–331
Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O’Brochta DA, Pfannkoch C, Qi R, Regier A, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser M, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149
Hopwood JA, Ahmed AM, Polwart A, Williams GT, Hurd H (2001) Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. J Exp Biol 204:2773–2780
Hurd H (1990) Physiological and behavioral interactions between parasites and invertebrate hosts. Adv Parasitol 29:271–318
Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17:363–368
Hurd H (2003) Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol 48:141–161
Janse CJ, Waters AP (2002) The Plasmodium berghei research model of malaria. http://www.lumc.nl/1040/research/malaria/model.html
Kappe SH, Buscaglia CA, Bergman LW, Coppens I, Nussenzweig V (2004) Apicomplexan gliding motility and host cell invasion: overhauling the motor model. Trends Parasitol 20:13–16
Koella JC (1999) An evolutionary view of the interactions between anopheline mosquitoes and malaria parasites. Microbes Infect 1:303–308
Kumar S, Christophides GK, Cantera R, Charles B, Han YS, Meister S, Dimopoulos G, Kafatos FC, Barillas-Mury C (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci USA 100:14139–14144
Langer RC, Hayward RE, Tsuboi T, Tachibana M, Torii M, Vinetz JM (2001) Micronemal transport of Plasmodium ookinete chitinases to the electron-dense area of the apical complex for extracellular secretion. Infect Immun 68:6461–6465
Lanz-Mendoza H, Hernandez-Martinez S, Ku-Lopez M, Rodriguez Mdel C, Herrera-Ortiz A, Rodriguez MH (2002) Superoxide anion in Anopheles albimanus hemolymph and midgut is toxic to Plasmodium berghei ookinetes. J Parasitol 88:702–706
Lee JO, Rieu P, Arnaout MA, Liddington R (1995) Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11 lb/CD18). Cell 80:631–638
Lee N, Bertholet S, Debrabant A, Muller J, Duncan R, Nakhasi HL (2002) Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death Differ 9:53–64
Limviroj W, Yano K, Yuda M, Ando K, Chinzei Y (2002) Immuno-electron microscopic observations of Plasmodium berghei CTRP localisation in the midgut of the vector mosquito Anopheles stenphensi. J Parasitol 88:664–672
Luckhart S, Crampton AL, Zamora R, Lieber MJ, Dos Santos PC, Peterson TML, Emmith N, Lim J, Wink DA, Vodovotz Y (2003) Mammalian transforming growth factor betal activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infect Immun 71:3000–3009
Luckhart S, Vodovotz Y, Cui L, Rosenberg R (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci USA 95:5700–5705
Mack SR, Samuels S, Vanderberg JP (1979) Hemolymph of Anopheles stephensi from uninfected and Plasmodium berghei-infected mosquitoes: 2. Free amino acids. FEBS Lett 430:59–63
Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Frohlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
Moreira ME, Del Portillo HA, Milder RV, Balanco JM, Barcinski MA (1996) Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis. J Cell Physiol 167:305–313
Motard A, Landau I, Nussler A, Grau G, Baccam D, Mazier D, Targett GA (1993) The role of reactive nitrogen intermediates in modulation of gametocyte infectivity of rodent malaria parasites. Parasite Immunol 15:21–26
Mottram JC, Helms MJ, Coombs GH, Sajid M (2003) Clan CD cysteine peptidases of parasitic protozoa. Trends Parasitol 19:182–187
Murphy MP (1999) Nitric oxide and cell death. Biochim Biophys Acta 1411:401–414
Myung JM, Marshall P, Sinnis P (2004) The Plasmodium circumsporozoite protein is involved in mosquito salivary gland invasion by sporozoites. Mol Biochem Parasitol 133:53–59
Naotunne TS, Karunaweera ND, Mendis KN, 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
Ojcius DM, Perfettini JL, Bonnin A, Laurent F (1999) Caspase-dependent apoptosis during infection with Cryptosporidium parvum. Microbes Infect 1:1163–1168
Paul REL, Brey PT, Robert V (2002) Plasmodium sex determination and transmission to mosquitoes. Trends Parasitol 18:32–37
Piacenza L, Peluffo G, Radi R (2001) L-Arginine-dependent suppression of apoptosis in Trypanosoma cruzi: contribution of the nitric oxide and polyamine pathways. Proc Natl Acad Sci USA 98:7301–7306
Picot S, Burnod J, Bracchi V, Chumpitazi BF, Ambroise-Thomas P (1997) Apoptosis related to chloroquine sensitivity of the human malaria parasite Plasmodium falciparum. Trans R Soc Trop Med Hyg 91:590–591
Potocnjak P, Yoshida N, Nussenzweig RS, Nussenzweig N (1980) Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med 151:1504–1513
Rozman-Pungercar J, Kopitar-Jerala N, Bogyo M, Turk D, Vasiljeva O, Stefe I, Vandenabeele P, Bromme D, Puizdar V, Fonovic M, Trstenjak-Prebanda M, Dolenc I, Turk V, Turk B (2003) Inhibition of papain-like cysteine proteases and legumain by caspase-specific inhibitors: when reaction mechanism is more important than specificity. Cell Death Differ 10:881–888
Sandoval M, Ronzio RA, Muanza DN, Clark DA, Miller MJ (1997) Peroxynitrite-induced apoptosis in epithelial (T84) and macrophage (RAW 264.7) cell lines: effect of legume-derived polyphenols (phytolens). Nitric Oxide 1:476–483
Selzer PM, Pingel S, Hsieh I, Ugele B, Chan VJ, Engel JC, Bogyo M, Russell DG, Sakanari JA, McKerrow JH (1999) Cysteine protease inhibitors as chemotherapy: lessons from a parasite target. Proc Natl Acad Sci USA 96:11015–11022
Shahabuddin M, Pimenta PFP (1998) Plasmodium gallinaceum preferentially invades vesicular ATPase-expressing cells in Aedes aegypti midgut. Proc Natl Acad Sci USA 95:3385–3389
Shahabuddin M, Toyoshima T, Aikawa M, Kaslow DC (1993) Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinases by mosquito protease. Proc Natl Acad Sci USA 90:4266–4270
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Tree 11:317–321
Sidén-Kiamos I, Vlachou D, Margos G, Beetsma AL, Waters AP, Sinden RE, Louis C (2000) Distinct roles for Pbs21 and Pbs25 in the in vitro ookinete to oocyst transformation of Plasmodium berghei. J Cell Sci 113:3419–3426
Sidjanski SP, Vanderberg JP, Sinnis P (1997) Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol Biochem Parasitol 90:33–41
Simonetti AB (1996) The biology of malarial parasite in the mosquito—a review. Mem I Oswaldo Cruz 97:519–541
Simonetti AB, Billingsley PF, Winger LA, Sinden RE (1993) Kinetics of expression of two major Plasmodium berghei antigens in the mosquito vector, Anopheles stephensi. Jf Eukaryotic Microbiol 40:569–576
Sinden RE (1978) Cell biology. In: Killick Kendrick R, Peters W (eds) Rodent Malaria. Academic Press, London, pp 85–168
Sinden RE (1997) Infection of mosquitoes with rodent malaria. In: The molecular biology of insect disease vectors: a methods manual. Chapman & Hall (eds), London pp 67–91
Sinden RE, Billingsley PF (2001) Plasmodium invasion of mosquito cells: hawk or dove? Trends Parasitol 17:209–212
Sinden RE, Croll NA (1975) Cytology and kinetics of microgametogenesis and fertilization in Plasmodium yoelii nigeriensis. Parasitology 70:53–65
Skulachev VP (1996) Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxide-producing mitochondria and cell. FEBS Lett 397:7–10
Sokolova MI (1994) A redescription of the morphology of mosquito (Diptera: Culicidae) ovarioles during vitellogenesis. Bull Soc Vector Ecol 19:53–68
Soller M, Bownes M, Kubli E (1999) Control of oocyte maturation in sexually mature Drosophila females. Dev Biol 208:337–351
Srinivasan P, Abraham EG, Ghosh AK, Valenzuela J, Ribeiro JM, Dimopoulos G, Kafatos FC, Adams JH, Fujioka H, Jacobs-Lorena M (2004) Analysis of the Plasmodium and Anopheles transcriptomes during oocyst differentiation. J Biol Chem 279:5581–5587
Szabo C (2003) Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 140–141:105–112
Szallies A, Kubata BK, Duszenko M (2002) A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS Lett 517:144–150
Templeton TJ, Kaslow DC, Fidock DA (2000) Developmental arrest of the human malaria parasite Plasmodium falciparum within the mosquito midgut via CTRP gene disruption. Mol Microbiol 36:1–9
Thathy V, Fujioka H, Gantt S, Nussenzweig R, Nussenzweig V, Ménard R (2002) Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology. EMBO J 21:1586–1596
Tomas AM, Margos G, Dimopoulos G, van Lin LHM, de Koning-Ward TF, Sinha R, Lupetti P, Beetsma AL, Rodriguez MC, Karras M, Hager A, Mendoza J, Butcher GA, Kafatos F, Janse CJ, Waters AP, Sinden RE (2001) P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J 20:3975–3983
Torii M, Nakamura K, Seiber KP, Miller LH, Aikawa M (1992) Penetration of the mosquito (Aedes aegypti) midgut by ookinetes of Plasmodium gallinaceum. J Protozool 39:449–454
Tsuboi T, Kaslow DC, Gozar MM, Tachibana M, Cao YM, Torii M (1998) Sequence polymorphism in two novel Plasmodium vivax ookinete surface proteins, Pvs25 and Pvs28, that are malaria transmission-blocking vaccine candidates. Mol Med 4:772–782
Uren AG, O’Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6:961–967
Vaughan JA, Hensley L, Beier JC (1994) Sporogonic development of Plasmodium yoelii in five anopheline species. J Parasitol 80:674–681
Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M, Miller LH (1995) Plasmodium gallinaceum: a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Exp Parasitol 80:583–595
Vlachou D, Zimmermann T, Cantera R, Janse CJ, Waters AP, Kafatos FC (2004) Realtime, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol 6:671–685
Wang KK (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23:20–26
Welburn SC, Dale C, Ellis D, Beecroft R, Pearson TW (1996) Apoptosis in procyclic Trypanosoma brucei rhodesiense in vitro. Cell Death Differ 3:229–236
Welburn SC, Murphy NB (1998) Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms. Cell Death Differ 5:615–622
Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig N, Aikawa M (1981) Biosynthesis of Pb44, the protective antigen of sporozoites of Plasmodium berghei. J Exp Med. 154:1225–1236
Yuda M, Sakaida H, Chinzei Y (1999) Targeted disruption of the Plasmodium berghei CTRP gene reveals its essential role in malaria infection of the vector mosquito. J Exp Med 190:1711–1715
Yuda M, Yano K, Tsuboi T, Torii M, Chinzei Y (2001) von Willebrand Factor A domain-related protein, a novel microneme protein of the malaria ookinete highly conserved throughout the Plasmodium parasites. Mol Biochem Parasitol 116:65–72
Zieler H, Dvorak JA (2000) Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells. Proc Natl Acad Sci USA 97:11516–11521
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Hurd, H., Carter, V., Nacer, A. (2005). Interactions Between Malaria and Mosquitoes: The Role of Apoptosis in Parasite Establishment and Vector Response to Infection. In: Griffin, D.E. (eds) Role of Apoptosis in Infection. Current Topics in Microbiology and Immunology, vol 289. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-27320-4_9
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