Plasmodium falciparum gametocyte transit through the cutaneous microvasculature: A new target for malaria transmission blocking vaccines?

References

• Murray CJ, Rosenfeld LC, Lim SS, Andrew KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012; 379:413-31; PMID:22305225; http://dx.doi.org/10.1016/S0140-6736(12)60034-8
   PubMed Web of Science ®Google Scholar
• World Health Organization. World Malaria Report 2014.
   Google Scholar
• Hay SI, Okiro EA, Gething PW, Patil AP, Tatem AJ, Guerra CA, Snow RW. Estimating the global clinical burden of Plasmodium falciparum malaria in 2007. PLoS Med 2010; 7:e1000290; PMID:20563310; http://dx.doi.org/10.1371/journal.pmed.1000290
   PubMed Web of Science ®Google Scholar
• Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM, et al. A research agenda to underpin malaria eradication. PLoS Med 2011; 8:e1000406; PMID:21311579; http://dx.doi.org/10.1371/journal.pmed.1000406
   PubMed Web of Science ®Google Scholar
• Nunes JK, Woods C, Carter T, Raphael T, Morin MJ, Diallo D, Leboulleux D, Jain S, Loucq C, Kaslow DC, et al. Development of a transmission-blocking malaria vaccine: progress, challenges, and the path forward. Vaccine 2014; 32:5531-9; PMID:25077422; http://dx.doi.org/10.1016/j.vaccine.2014.07.030
   PubMed Web of Science ®Google Scholar
• Roberts L, Enserink M. Malaria. Did they really say eradication? Science 2007; 318:1544-5; PMID:18063766; http://dx.doi.org/10.1126/science.318.5856.1544
   PubMed Web of Science ®Google Scholar
• Malaria Vaccine Funders Group. Malaria Vaccine Technology Roadmap; 2013. Available at: http://www.who.int/immunization/topics/malaria/vaccine_roadmap/TRM_update_nov13.pdf?ua=1
   Google Scholar
• Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, Patil AP, Tatem AJ, Howes RE, Myers MF, et al. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PloS Negl Trop Dis 2012; 6:e1814; PMID:22970336; http://dx.doi.org/10.1371/journal.pntd.0001814
   PubMed Web of Science ®Google Scholar
• Baton LA, Ranford-Cartwright LC. Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. Trends Parasitol 2005; 21:573-80; PMID:16236552; http://dx.doi.org/10.1016/j.pt.2005.09.012
   PubMed Web of Science ®Google Scholar
• Motard A, Landau I, Nussler A, Grau G, Baccam D, Mazier D, Targett GA. The role of reactive nitrogen intermediates in modulation of gametocyte infectivity of rodent malaria parasites. Parasite Immunol 1993; 15:21-6; PMID:8433851; http://dx.doi.org/10.1111/j.1365-3024.1993.tb00568.x
   PubMed Web of Science ®Google Scholar
• Puta C, Manyando C. Enhanced gametocyte production in Fansidar-treated Plasmodium falciparum malaria patients: implications for malaria transmission control programmes. Trop Med Int Health 1997; 2:227-9; PMID:9491100; http://dx.doi.org/10.1046/j.1365-3156.1997.d01-267.x
   PubMed Web of Science ®Google Scholar
• Alano P. Plasmodium falciparum gametocytes: still many secrets of a hidden life. Mol Microbiol 2007; 66:291-302; PMID:17784927; http://dx.doi.org/10.1111/j.1365-2958.2007.05904.x
   PubMed Web of Science ®Google Scholar
• Smalley ME, Brown J. Plasmodium falciparum gametocytogenesis stimulated by lymphocytes and serum from infected Gambian children. Trans R Soc Trop Med Hyg 1981; 75:316-7; PMID:7029805; http://dx.doi.org/10.1016/0035-9203(81)90348-5
   PubMed Web of Science ®Google Scholar
• Babiker HA, Schneider P, Reece SE. Gametocytes: insights gained during a decade of molecular monitoring. Trends Parasitol 2008; 24:525-30; PMID:18801702; http://dx.doi.org/10.1016/j.pt.2008.08.001
   PubMed Web of Science ®Google Scholar
• Schneweis S, Maier WA, Seitz HM. Haemolysis of infected erythrocytes-a trigger for formation of Plasmodium falciparum gametocytes? Parasitol Res 1991; 77:458-60; PMID:1891456; http://dx.doi.org/10.1007/BF00931646
   PubMed Web of Science ®Google Scholar
• Sokha CS, Trape JF, Robert V. Gametocytemia in Senegalese children with uncomplicated falciparum malaria treated with chloroquine, amodiaquine or sulfadoxine + pyrimethamine. Parasite 2001; 8:243-50; PMID:11584755; http://dx.doi.org/10.1051/parasite/2001083243
   PubMed Web of Science ®Google Scholar
• Buckling A, Ranford-Cartwright LC, Miles A, Read AF. Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology 1999; 118:339-46; PMID:10340323; http://dx.doi.org/10.1017/S0031182099003960
   PubMed Web of Science ®Google Scholar
• Kafsack BF, Rovira-Graells N, Clark TG, Bancells C, Crowley VM, Campino SG, Williams AE, Drought LG, Kwiatkowski DP, Baker DA, et al. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 2014; 131:248-52; http://dx.doi.org/10.1038/nature12920
   Web of Science ®Google Scholar
• Sinha A, Hughes KR, Modrzynska KK, Otto TD, Pfander C, Dickens NJ, Religa AA, Bushell E, Graham AL, Cameron R, et al. A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 2014; 13:253-7; http://dx.doi.org/10.1038/nature12970
   Web of Science ®Google Scholar
• Bruce MC, Alano P, Duthrie S, Carter R. Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology 1990; 100:191-200; PMID:2189114; http://dx.doi.org/10.1017/S0031182000061199
   PubMed Web of Science ®Google Scholar
• Hawking F, Wilson ME, Gammage K. Evidence for cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Trans R Soc Trop Med Hyg 1971; 65:549-59; PMID:5003557; http://dx.doi.org/10.1016/0035-9203(71)90036-8
   PubMed Web of Science ®Google Scholar
• Thomson JG, Robertson A. The structure and development of Plasmodium falciparum gametocytes in the internal organs and peripheral circulation. Trans R Soc Trop Med Hyg 1935; 29:31-40; http://dx.doi.org/10.1016/S0035-9203(35)90015-3
   Google Scholar
• Farfour E, Charlotte F, Settegrana C, Miyara M, Buffet P. The extravascular compartment of the bone marrow: A niche for Plasmodium falciparum gametocyte maturation? Malar J 2012; 11:285; PMID:22905863; http://dx.doi.org/10.1186/1475-2875-11-285
   PubMed Web of Science ®Google Scholar
• Joice R, Nilsson SK, Montgomery J, Dankwa S, Egan E, Morahan B, Seydel KB, Bertuccini L, Alano P, Williamson KC, et al. Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci Transl Med 2014; 6:244re5; PMID:25009232; http://dx.doi.org/10.1126/scitranslmed.3008882
   PubMed Web of Science ®Google Scholar
• Smalley ME, Abdalla S, Brown J. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans R Soc Trop Med Hyg 1981; 75:103-5; PMID:7022784; http://dx.doi.org/10.1016/0035-9203(81)90019-5
   PubMed Web of Science ®Google Scholar
• Tibúrcio M, Sauerwein R, Lavazec C, Alano P. Erythrocyte remodeling by Plasmodium falciparum gametocytes in the human host interplay. Trends Parasitol 2015; 31:270-8; PMID:25824624; http://dx.doi.org/10.1016/j.pt.2015.02.006
   PubMed Web of Science ®Google Scholar
• Tibúrico M, Niang M, Deplaine G, Perrot S, Bischoff E, Ndour PA, Silvestrini F, Khattab A, Milon G, David PH, et al. A switch in infected erythrocyte deformability at the maturation and blood circulation of Plasmodium falciparum transmission stages. Blood 2012; 119:e172-80; PMID:22517905; http://dx.doi.org/10.1182/blood-2012-03-414557
   PubMedGoogle Scholar
• Aingaran M, Zhang R, Law SK, Peng Z, Undisz A, Meyer E, Diez-Silva M, Burke TA, Spielmann T, Lim CT, et al. Host cell deformability is linked to transmission in the human malaria parasite Plasmodium falciparum. Cell Microbiol 2012; 14:983-93; PMID:22417683; http://dx.doi.org/10.1111/j.1462-5822.2012.01786.x
   PubMed Web of Science ®Google Scholar
• Mohandas N, Chasis JA. Red blood cell deformability, membrane material properties and shape: regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol 1993; 30:171-92; PMID:8211222
   PubMed Web of Science ®Google Scholar
• Beeson JG, Reeder JC, Rogerson SJ, Brown GV. Parasite adhesion and immune evasion in placental malaria. Trends Parasitol 2001; 17:331-7; PMID:11423376; http://dx.doi.org/10.1016/S1471-4922(01)01917-1
   PubMed Web of Science ®Google Scholar
• Bhattacharjee S, van Ooij C, Balu B, Adams JH, Haldar K. Maurer's clefts of Plasmodium falciparum are secretory organelles that concentrate virulence protein reporters for delivery to the host erythrocyte. Blood 2008; 111:2418-26; PMID:18057226; http://dx.doi.org/10.1182/blood-2007-09-115279
   PubMed Web of Science ®Google Scholar
• Marti M, Good RT, Rug M, Knuepfer E, Cowman AF. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 2004; 306:1930-3; PMID:15591202; http://dx.doi.org/10.1126/science.1102452
   PubMed Web of Science ®Google Scholar
• Hiller NL, Bhattacharjee S, van Ooij C, et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004; 306:1934-7; PMID:15591203; http://dx.doi.org/10.1126/science.1102737
   PubMed Web of Science ®Google Scholar
• Cooke BM, Mohandas N, Coppel RL. Malaria and the red blood cell membrane. Semin Hematol 2004; 41:173-88; PMID:15071793; http://dx.doi.org/10.1053/j.seminhematol.2004.01.004
   PubMed Web of Science ®Google Scholar
• Glenister FK, Coppel RL, Cowman AL, Mohandas N, Cooke BM. Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood 2002; 99:1060-3; PMID:11807013; http://dx.doi.org/10.1182/blood.V99.3.1060
   PubMed Web of Science ®Google Scholar
• Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, Wickham ME, Brown GV, Coppel RL, Cowman AF. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 1997; 89:287-96; PMID:9108483; http://dx.doi.org/10.1016/S0092-8674(00)80207-X
   PubMed Web of Science ®Google Scholar
• Waller KL, Nunomura W, An X, Cooke BM, Mohandas N, Coppel RL. Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 2003; 102:1911-4; PMID:12730097; http://dx.doi.org/10.1182/blood-2002-11-3513
   PubMed Web of Science ®Google Scholar
• Glenister RK, Fernandez KM, Kats LM, Hanssen E, Mohandas N, Coppel RL, Cooke BM. Functional alteration of red blood cells by a megadalton protein of Plasmodium falciparum. Blood 2009; 113:919-28; PMID:18832660; http://dx.doi.org/10.1182/blood-2008-05-157735
   PubMed Web of Science ®Google Scholar
• Hayward RE, Tiwari B, Piper KP, Baruch DI, Day KP. Virulence and transmission success of the malarial parasite Plasmodium falciparum. Proc Natl Acad Sci USA 1999; 96:4563-8; PMID:10200302; http://dx.doi.org/10.1073/pnas.96.8.4563
   PubMed Web of Science ®Google Scholar
• Day KP, Hayward RE, Smith D, Culvenor JG. CD36-dependent adhesion and knob expression of the transmission stages of Plasmodium falciparum is stage specific. Mol Biochem Parasitol 1998; 93:167-77; PMID:9662702; http://dx.doi.org/10.1016/S0166-6851(98)00040-1
   PubMed Web of Science ®Google Scholar
• Rogers NJ, Daramola O, Targett GA, Hall BS. CD36 and intercellular adhesion molecule 1 mediate adhesion of developing Plasmodium falciparum gametocytes. Infect Immun 1996; 64:1480-3; PMID:8606124
   PubMed Web of Science ®Google Scholar
• Silvestrini F, Tibúrcio M, Bertuccini L, Alano P. Differential adhesive properties of sequestered asexual and sexual stages of Plasmodium falciparum on human endothelial cells are tissue independent. PloS One 2012; 7:e31567; PMID:22363675; http://dx.doi.org/10.1371/journal.pone.0031567
   PubMed Web of Science ®Google Scholar
• Ramdani G, Naissant B, Thompson E, Breil F, Lorthiois A, Dupuy F, Cummings R, Duffier Y, Corbett Y, Mercereau-Puijalon O, et al. cAMP-signalling regulates gametocyte-infected erythrocyte deformability required for malaria parasite transmission. PloS Pathog 2015; 11:e1004815; PMID:25951195; http://dx.doi.org/10.1371/journal.ppat.1004815
   PubMedGoogle Scholar
• Dixon MW, Dearnley MK, Hanssen E, Gilberger T, Tilley L. Shape-shifting gametocytes: how and why does P. falciparum go banana-shaped? Trends Parasitol 2012; 28:471-8; PMID:22939181; http://dx.doi.org/10.1016/j.pt.2012.07.007
   PubMed Web of Science ®Google Scholar
• Sinden RE. Gametocytogenesis of Plasmodium falciparum in vitro: ultrastructural observations on the lethal action of chloroquine. Ann Trop Med Parasitol 1982; 76:15-23; PMID:7044323; http://dx.doi.org/10.1080/00034983.1982.11687500
   PubMed Web of Science ®Google Scholar
• Braverman IM. Ultrastructure and organization of the cutaneous microvasculature in normal and pathologic states. J Invest Dermatol 1989; 93:2S-9S; PMID:2666519; http://dx.doi.org/10.1111/1523-1747.ep12580893
   PubMed Web of Science ®Google Scholar
• Braverman IM, Keh-Yen A. Ultrastructure of the human dermal microcirculation: III. The vessels in the mid- and lower dermis and subcutaneous fat. J Invest Dermatol 1981; 77:297-304; PMID:7264363; http://dx.doi.org/10.1111/1523-1747.ep12482470
   PubMed Web of Science ®Google Scholar
• Braverman IM, Yen A. Ultrastructure of the human dermal microcirculation: II. The capillary loops of the dermal papillae. J Invest Dermatol 1977; 68:44-52; PMID:830769; http://dx.doi.org/10.1111/1523-1747.ep12485165
   PubMed Web of Science ®Google Scholar
• Yen A, Braverman IM. Ultrastructure of the human dermal microcirculation: the horizontal plexus of the papillary dermis. J Invest Dermatol 1976; 66:131-42; PMID:1249441; http://dx.doi.org/10.1111/1523-1747.ep12481678
   PubMed Web of Science ®Google Scholar
• Histology Guide, Faculty of Biological Sciences, University of Leeds. Available at http://www.histology.leeds.ac.uk/skin/skin_layers.php
   Google Scholar
• Gordon RM, Lumsden WHR. A study of the behavior of the mouth-parts of mosquitoes when taking up blood from living tissue; together with some observations on the ingestion of microfilariae. Ann Trop Med Parasit 1939; 33:259-78; http://dx.doi.org/10.1080/00034983.1939.11685071
   Google Scholar
• Robinson GG. The mouthparts and their function in the female mosquito, Anopheles maculipennis. Parasitology 1939; 31:212-42; http://dx.doi.org/10.1017/S0031182000012774
   Google Scholar
• Swaminathan VS. Mechanics of a Mosquito Bite (Thesis submitted to the North Carolina State University, Raleigh NC). 2006.
   Google Scholar
• Clements AN. “The biology of mosquitoes” Volume 1. Chapman and Hall.
   Google Scholar
• Choumet V, Attout T, Chartier L, Khun J, et al. Visualizing non infectious and infectious Anopheles gambiae blood feedings in naïve and saliva-immunized mice. PLoS One 2012; 7:e50464; PMID:23272060; http://dx.doi.org/10.1371/journal.pone.0050464
   PubMed Web of Science ®Google Scholar
• Gautret P, Miltgen F, Gantier JC, Chabaud AG, Landau I. Enhanced gametocyte formation by Plasmodium chabaudi in immature erythrocytes: pattern of production, sequestration, and infectivity to mosquitoes. J Parasitol 1996; 82:900-6; PMID:8973397; http://dx.doi.org/10.2307/3284196
   PubMed Web of Science ®Google Scholar
• Landau I, Chabaud A. Parasitic pattern of rodent Plasmodium in blood from mouse tail and from Anopheles blood meal. Parassitologia 2002; 44:111-5; PMID:12404818
   PubMedGoogle Scholar
• Chardome M, Janssen PJ. Enquête sur l'incidence malarienne par la method dermique dans la regionde Lubilash (Congo Belge). Ann Soc Belge Med Trop 1952; 32:209-11; PMID:12976890
   PubMedGoogle Scholar
• Pichon G, Awono-Ambene HP, Robert V. High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host. Parasitology 2000; 121:115-20; PMID:11085230; http://dx.doi.org/10.1017/S0031182099006277
   PubMed Web of Science ®Google Scholar
• Magesa SM, Mdira YK, Akida JA, Bygbjerg IC, Jakobsen PH. Observations on the periodicity of Plasmodium falciparum gametocytes in natural human infections. Acta Trop 2000; 76:239-46; PMID:10974164; http://dx.doi.org/10.1016/S0001-706X(00)00110-8
   PubMed Web of Science ®Google Scholar
• Prausnitz MR. Microneedles for transdermal drug delivery. Adv Drug Deliv Rev 2004; 56:581-7; PMID:15019747; http://dx.doi.org/10.1016/j.addr.2003.10.023
   PubMed Web of Science ®Google Scholar
• Jarolim P, Palek J, Amato D, Hassan K, Sapak P, Nurse GT, Rubin HL, Zhai S, Sahr KE, Liu SC. Deletion in erythrocyte band 3 gene in malaria-resistant Southeast Asian ovalocytosis. Proc Natl Acad Sci USA 1991; 88:11022-6; PMID:1722314; http://dx.doi.org/10.1073/pnas.88.24.11022
   PubMed Web of Science ®Google Scholar
• Mohandas N, Lie-Injo LE, Friedman M, Mak JW. Rigid membranes of Malayan Ovalocytes: A likely genetic barrier against malaria. Blood 1984; 63:1385-92; PMID:6722355
   PubMed Web of Science ®Google Scholar
• Landau I, Miltgen F, Boulard Y, Chabaud AG, Baccam D. Etudes sur les gamétocytes des Plasmodium du groupe “vivax:” Morphologie, évolution, prise par les Anophèles et infectivité des microgamétocytes de Plasmodium yoelii. Annales de Parasitologie Humaine et Comparée 1979; 54:145-61.
   PubMed Web of Science ®Google Scholar
• Sutherland CJ. Surface antigens of Plasmodium falciparum gametocytes – A new class of transmission-blocking vaccine targets? Mol Biochem Parasitol 2009; 166:93-8; PMID:19450726; http://dx.doi.org/10.1016/j.molbiopara.2009.03.007
   PubMed Web of Science ®Google Scholar
• Williamson KC. Pfs230: from malaria transmission-blocking vaccine candidate toward function. Parasite Immunol 2003; 25:351-9; PMID:14521577; http://dx.doi.org/10.1046/j.1365-3024.2003.00643.x
   PubMed Web of Science ®Google Scholar
• Jones S, Grignard L, Nebie I, Chilongola J, Dodoo D, Sauerwein R, Theisen M, Roeffen W, Singh SK, Singh RK, et al. Naturally acquired antibody responses to recombinant Pfs230 and Pfs48/45 transmission blocking vaccine candidates. J Infect 2015; 71:117-27; PMID:25869538; http://dx.doi.org/10.1016/j.jinf.2015.03.007
   PubMed Web of Science ®Google Scholar
• Singh SK, Roeffen W, Andersen G, Bousema T, Christiansen M, Sauerwein R, Theisen M. A plasmodium falciparum 48/45 single epitope R0.6C subunit protein elicits high levels of transmission blocking antibodies. Vaccine 2015; 33:1981-6; PMID:25728318; http://dx.doi.org/10.1016/j.vaccine.2015.02.040
   PubMed Web of Science ®Google Scholar
• Ouédraogo AL, Roeffen W, Luty AJ, de Vlas SJ, Nebie I, Ilboudo-Sanogo E, Cuzin-Ouattara N, Teleen K, Tiono AB, Sirima SB, et al. Naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs48/45 and Pfs230 in an area of seasonal transmission. Infect Immun 2011; 79:4957-64; http://dx.doi.org/10.1128/IAI.05288-11
   PubMed Web of Science ®Google Scholar
• Kumar R, Ray PC, Datta D, Bansal GP, Angov E, Kumar N. Nanovaccines for malaria using Plasmodium falciparum antigen Pfs25 attached to gold nanoparticles. Vaccine 2015; 33:5064-71; PMID:26299750; http://dx.doi.org/10.1016/j.vaccine.2015.08.025
   PubMed Web of Science ®Google Scholar
• Kumar R, Angov E, Kumar N. Potent malaria transmission-blocking antibody responses elicited by Plasmodium falciparum Pfs25 expressed in Escherichia coli after successful protein refolding. Infect Immun 2014; 82:1453-9; PMID:24421036; http://dx.doi.org/10.1128/IAI.01438-13
   PubMed Web of Science ®Google Scholar
• Wu Y, Ellis RD, Shaffer D, Fontes E, Malkin EM, Mahanty S, Fay MP, Narum D, Rausch K, Miles AP, et al. Phase 1 trial of malaria transmission blocking vaccine candidate Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS One 2008; 3:e2636; PMID:18612426; http://dx.doi.org/10.1371/journal.pone.0002636
   PubMed Web of Science ®Google Scholar
• Nacher M. Does the shape of Plasmodium falciparum gametocytes have a function? Med Hypotheses 2004; 62:618-9; PMID:15050117; http://dx.doi.org/10.1016/j.mehy.2003.11.011
   PubMed Web of Science ®Google Scholar