Malaria: Biology and Disease

Cell

Volumn 167, Issue 3, 2016, Pages 610-624

  Cowman, Alan F ^a,b   Healer, Julie ^a   Marapana, Danushka ^a,b   Marsh, Kevin ^c  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; ARTEMISININ; MALARIA VACCINE; RECOMBINANT VACCINE; RTS,S-AS01 VACCINE;

ADAPTIVE IMMUNITY; BIOLOGY; CELL ACTIVATION; CELL INVASION; CLINICAL FEATURE; DISEASE SEVERITY; DISEASE TRANSMISSION; DRUG MECHANISM; ENDOTHELIUM CELL; ERYTHROCYTE; HEPATITIS; HOST CELL; HUMAN; IMMUNE EVASION; INFECTION CONTROL; MALARIA; MALARIA FALCIPARUM; MICROANGIOPATHY; NONHUMAN; OBSTRUCTION; PARASITE TRANSMISSION; PATHOGENESIS; PLASMODIUM VIVAX MALARIA; PREGNANCY; PRIORITY JOURNAL; REVIEW; ANIMAL; COMMUNICABLE DISEASE CONTROL; DISEASE ERADICATION; DRUG RESISTANCE; GLOBAL HEALTH; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; IMMUNOLOGY; LIFE CYCLE STAGE; LIVER; MALARIA, FALCIPARUM; MEROZOITE; MOSQUITO; PARASITOLOGY; PLASMODIUM FALCIPARUM; PROCEDURES; SPOROZOITE; TRANSMISSION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIMALARIALS; COMMUNICABLE DISEASE CONTROL; CULICIDAE; DISEASE ERADICATION; DRUG RESISTANCE; ERYTHROCYTES; GLOBAL HEALTH; HOST-PARASITE INTERACTIONS; HUMANS; LIFE CYCLE STAGES; LIVER; MALARIA VACCINES; MALARIA, FALCIPARUM; MEROZOITES; PLASMODIUM FALCIPARUM; SPOROZOITES; VACCINES, SYNTHETIC;

EID: 84994000411     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.07.055     Document Type: Review

References (98)

1. Ahmed, M.A., Cox-Singh, J., Plasmodium knowlesi - an emerging pathogen. ISBT Sci. Ser. 10 1 (2015), 134–140.
2. Ariey, F., Witkowski, B., Amaratunga, C., Beghain, J., Langlois, A.C., Khim, N., Kim, S., Duru, V., Bouchier, C., Ma, L., et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505 (2014), 50–55.
3. Ashley, E.A., Recht, J., White, N.J., Primaquine: the risks and the benefits. Malar. J., 13, 2014, 418.
4. Ataíde, R., Mayor, A., Rogerson, S.J., Malaria, primigravidae, and antibodies: knowledge gained and future perspectives. Trends Parasitol. 30 (2014), 85–94.
5. Baird, J.K., Evidence and implications of mortality associated with acute Plasmodium vivax malaria. Clin. Microbiol. Rev. 26 (2013), 36–57.
6. Baragaña, B., Hallyburton, I., Lee, M.C., Norcross, N.R., Grimaldi, R., Otto, T.D., Proto, W.R., Blagborough, A.M., Meister, S., Wirjanata, G., et al. A novel multiple-stage antimalarial agent that inhibits protein synthesis. Nature 522 (2015), 315–320.
7. Besteiro, S., Dubremetz, J.F., Lebrun, M., The moving junction of apicomplexan parasites: a key structure for invasion. Cell. Microbiol. 13 (2011), 797–805.
8. Bhanot, P., Schauer, K., Coppens, I., Nussenzweig, V., A surface phospholipase is involved in the migration of plasmodium sporozoites through cells. J. Biol. Chem. 280 (2005), 6752–6760.
9. Boddey, J.A., Cowman, A.F., Plasmodium nesting: remaking the erythrocyte from the inside out. Annu. Rev. Microbiol. 67 (2013), 243–269.
10. Bull, P.C., Lowe, B.S., Kortok, M., Molyneux, C.S., Newbold, C.I., Marsh, K., Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med. 4 (1998), 358–360.
11. Chan, J.A., Howell, K.B., Reiling, L., Ataide, R., Mackintosh, C.L., Fowkes, F.J., Petter, M., Chesson, J.M., Langer, C., Warimwe, G.M., et al. Targets of antibodies against Plasmodium falciparum-infected erythrocytes in malaria immunity. J. Clin. Invest. 122 (2012), 3227–3238.
12. Chan, J.A., Fowkes, F.J., Beeson, J.G., Surface antigens of Plasmodium falciparum-infected erythrocytes as immune targets and malaria vaccine candidates. Cell. Mol. Life Sci. 71 (2014), 3633–3657.
13. Chen, L., Lopaticki, S., Riglar, D.T., Dekiwadia, C., Uboldi, A.D., Tham, W.H., O'Neill, M.T., Richard, D., Baum, J., Ralph, S.A., Cowman, A.F., An EGF-like protein forms a complex with PfRh5 and is required for invasion of human erythrocytes by Plasmodium falciparum. PLoS Pathog., 7, 2011, e1002199.
14. Church, J., Maitland, K., Invasive bacterial co-infection in African children with Plasmodium falciparum malaria: a systematic review. BMC Med., 12, 2014, 31.
15. Cohen, J., Nussenzweig, V., Nussenzweig, R., Vekemans, J., Leach, A., From the circumsporozoite protein to the RTS, S/AS candidate vaccine. Hum. Vaccin. 6 (2010), 90–96.
16. Cohen, S., McGREGOR, I.A., Carrington, S., Gamma-globulin and acquired immunity to human malaria. Nature 192 (1961), 733–737.
17. Collins, C.R., Hackett, F., Strath, M., Penzo, M., Withers-Martinez, C., Baker, D.A., Blackman, M.J., Malaria parasite cGMP-dependent protein kinase regulates blood stage merozoite secretory organelle discharge and egress. PLoS Pathog., 9, 2013, e1003344.
18. Collins, W.E., Jeffery, G.M., A retrospective examination of sporozoite- and trophozoite-induced infections with Plasmodium falciparum: development of parasitologic and clinical immunity during primary infection. Am. J. Trop. Med. Hyg. 61 (1999), 4–19.
19. Coppi, A., Tewari, R., Bishop, J.R., Bennett, B.L., Lawrence, R., Esko, J.D., Billker, O., Sinnis, P., Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe 2 (2007), 316–327.
20. Crosnier, C., Bustamante, L.Y., Bartholdson, S.J., Bei, A.K., Theron, M., Uchikawa, M., Mboup, S., Ndir, O., Kwiatkowski, D.P., Duraisingh, M.T., et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480 (2011), 534–537.
21. Cunnington, A.J., Walther, M., Riley, E.M., Piecing together the puzzle of severe malaria. Sci. Transl. Med., 5, 2013, 211ps218.
22. Das, S., Hertrich, N., Perrin, A.J., Withers-Martinez, C., Collins, C.R., Jones, M.L., Watermeyer, J.M., Fobes, E.T., Martin, S.R., Saibil, H.R., et al. Processing of Plasmodium falciparum merozoite surface protein MSP1 activates a spectrin-binding function enabling parasite egress from RBCs. Cell Host Microbe 18 (2015), 433–444.
23. Dondorp, A.M., Ince, C., Charunwatthana, P., Hanson, J., van Kuijen, A., Faiz, M.A., Rahman, M.R., Hasan, M., Bin Yunus, E., Ghose, A., et al. Direct in vivo assessment of microcirculatory dysfunction in severe falciparum malaria. J. Infect. Dis. 197 (2008), 79–84.
24. Dondorp, A.M., Nosten, F., Yi, P., Das, D., Phyo, A.P., Tarning, J., Lwin, K.M., Ariey, F., Hanpithakpong, W., Lee, S.J., et al. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 361 (2009), 455–467.
25. Douglas, A.D., Baldeviano, G.C., Lucas, C.M., Lugo-Roman, L.A., Crosnier, C., Bartholdson, S.J., Diouf, A., Miura, K., Lambert, L.E., Ventocilla, J.A., et al. A PfRH5-based vaccine is efficacious against heterologous strain blood-stage Plasmodium falciparum infection in aotus monkeys. Cell Host Microbe 17 (2015), 130–139.
26. Dvorin, J.D., Martyn, D.C., Patel, S.D., Grimley, J.S., Collins, C.R., Hopp, C.S., Bright, A.T., Westenberger, S., Winzeler, E., Blackman, M.J., et al. A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science 328 (2010), 910–912.
27. Felgner, P.L., Roestenberg, M., Liang, L., Hung, C., Jain, A., Pablo, J., Nakajima-Sasaki, R., Molina, D., Teelen, K., Hermsen, C.C., Sauerwein, R., Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci Rep, 3, 2013, 3549.
28. Fowkes, F.J., Richards, J.S., Simpson, J.A., Beeson, J.G., The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med., 7, 2010, e1000218.
29. Gamo, F.J., Sanz, L.M., Vidal, J., de Cozar, C., Alvarez, E., Lavandera, J.L., Vanderwall, D.E., Green, D.V., Kumar, V., Hasan, S., et al. Thousands of chemical starting points for antimalarial lead identification. Nature 465 (2010), 305–310.
30. Gao, X., Gunalan, K., Yap, S.S., Preiser, P.R., Triggers of key calcium signals during erythrocyte invasion by Plasmodium falciparum. Nat. Commun., 4, 2013, 2862.
31. Gómez-Pérez, G.P., van Bruggen, R., Grobusch, M.P., Dobaño, C., Plasmodium falciparum malaria and invasive bacterial co-infection in young African children: the dysfunctional spleen hypothesis. Malar. J., 13, 2014, 335.
32. Greenwood, B., Doumbo, O.K., Implementation of the malaria candidate vaccine RTS,S/AS01. Lancet 387 (2016), 318–319.
33. Grüring, C., Heiber, A., Kruse, F., Flemming, S., Franci, G., Colombo, S.F., Fasana, E., Schoeler, H., Borgese, N., Stunnenberg, H.G., et al. Uncovering common principles in protein export of malaria parasites. Cell Host Microbe 12 (2012), 717–729.
34. Hanson, J., Lee, S.J., Hossain, M.A., Anstey, N.M., Charunwatthana, P., Maude, R.J., Kingston, H.W., Mishra, S.K., Mohanty, S., Plewes, K., et al. Microvascular obstruction and endothelial activation are independently associated with the clinical manifestations of severe falciparum malaria in adults: an observational study. BMC Med., 13, 2015, 122.
35. Hendriksen, I.C., White, L.J., Veenemans, J., Mtove, G., Woodrow, C., Amos, B., Saiwaew, S., Gesase, S., Nadjm, B., Silamut, K., et al. Defining falciparum-malaria-attributable severe febrile illness in moderate-to-high transmission settings on the basis of plasma PfHRP2 concentration. J. Infect. Dis. 207 (2013), 351–361.
36. Herrera, R., Anderson, C., Kumar, K., Molina-Cruz, A., Nguyen, V., Burkhardt, M., Reiter, K., Shimp, R. Jr., Howard, R.F., Srinivasan, P., et al. Reversible conformational change in the Plasmodium falciparum circumsporozoite protein masks its adhesion domains. Infect. Immun. 83 (2015), 3771–3780.
37. Holder, A.A., Proteins on the surface of the malaria parasite and cell invasion. Parasitology 108 (1994), S5–S18.
38. Hviid, L., Jensen, A.T., PfEMP1 - a parasite protein family of key importance in Plasmodium falciparum malaria immunity and pathogenesis. Adv. Parasitol. 88 (2015), 51–84.
39. Ishino, T., Yano, K., Chinzei, Y., Yuda, M., Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol., 2, 2004, E4.
40. Jiménez-Díaz, M.B., Ebert, D., Salinas, Y., Pradhan, A., Lehane, A.M., Myrand-Lapierre, M.E., O'Loughlin, K.G., Shackleford, D.M., Justino de Almeida, M., Carrillo, A.K., et al. (+)-SJ733, a clinical candidate for malaria that acts through ATP4 to induce rapid host-mediated clearance of Plasmodium. Proc. Natl. Acad. Sci. USA 111 (2014), E5455–E5462.
41. Joice, R., Nilsson, S.K., Montgomery, J., Dankwa, S., Egan, E., Morahan, B., Seydel, K.B., Bertuccini, L., Alano, P., Williamson, K.C., et al. Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci. Transl. Med., 6, 2014, 244re245.
42. Kafsack, B.F., Rovira-Graells, N., Clark, T.G., Bancells, C., Crowley, V.M., Campino, S.G., Williams, A.E., Drought, L.G., Kwiatkowski, D.P., Baker, D.A., et al. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 507 (2014), 248–252.
43. Kaushansky, A., Douglass, A.N., Arang, N., Vigdorovich, V., Dambrauskas, N., Kain, H.S., Austin, L.S., Sather, D.N., Kappe, S.H., Malaria parasites target the hepatocyte receptor EphA2 for successful host infection. Science 350 (2015), 1089–1092.
44. Khunrae, P., Dahlbäck, M., Nielsen, M.A., Andersen, G., Ditlev, S.B., Resende, M., Pinto, V.V., Theander, T.G., Higgins, M.K., Salanti, A., Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J. Mol. Biol. 397 (2010), 826–834.
45. Kuhen, K.L., Chatterjee, A.K., Rottmann, M., Gagaring, K., Borboa, R., Buenviaje, J., Chen, Z., Francek, C., Wu, T., Nagle, A., et al. KAF156 is an antimalarial clinical candidate with potential for use in prophylaxis, treatment, and prevention of disease transmission. Antimicrob. Agents Chemother. 58 (2014), 5060–5067.
46. Kwiatkowski, D., Hill, A.V.S., Sambou, I., Twumasi, P., Castracane, J., Manogue, K.R., Cerami, A., Brewster, D.R., Greenwood, B.M., TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336 (1990), 1201–1204.
47. Lacerda, M.V., Fragoso, S.C., Alecrim, M.G., Alexandre, M.A., Magalhães, B.M., Siqueira, A.M., Ferreira, L.C., Araújo, J.R., Mourão, M.P., Ferrer, M., et al. Postmortem characterization of patients with clinical diagnosis of Plasmodium vivax malaria: to what extent does this parasite kill?. Clin. Infect. Dis. 55 (2012), e67–e74.
48. Langhorne, J., Ndungu, F.M., Sponaas, A.M., Marsh, K., Immunity to malaria: more questions than answers. Nat. Immunol. 9 (2008), 725–732.
49. Lin, C.S., Uboldi, A.D., Epp, C., Bujard, H., Tsuboi, T., Czabotar, P.E., Cowman, A.F., Multiple Plasmodium falciparum merozoite surface protein 1 complexes mediate merozoite binding to human erythrocytes. J. Biol. Chem. 291 (2016), 7703–7715.
50. Llanos-Cuentas, A., Lacerda, M.V., Rueangweerayut, R., Krudsood, S., Gupta, S.K., Kochar, S.K., Arthur, P., Chuenchom, N., Möhrle, J.J., Duparc, S., et al. Tafenoquine plus chloroquine for the treatment and relapse prevention of Plasmodium vivax malaria (DETECTIVE): a multicentre, double-blind, randomised, phase 2b dose-selection study. Lancet 383 (2014), 1049–1058.
51. Luxemburger, C., Ricci, F., Nosten, F., Raimond, D., Bathet, S., White, N.J., The epidemiology of severe malaria in an area of low transmission in Thailand. Trans. R. Soc. Trop. Med. Hyg. 91 (1997), 256–262.
52. Mantel, P.Y., Hoang, A.N., Goldowitz, I., Potashnikova, D., Hamza, B., Vorobjev, I., Ghiran, I., Toner, M., Irimia, D., Ivanov, A.R., et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 13 (2013), 521–534.
53. March, S., Ng, S., Velmurugan, S., Galstian, A., Shan, J., Logan, D.J., Carpenter, A.E., Thomas, D., Sim, B.K., Mota, M.M., et al. A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. Cell Host Microbe 14 (2013), 104–115.
54. Marsh, K., Forster, D., Waruiru, C., Mwangi, I., Winstanley, M., Marsh, V., Newton, C., Winstanley, P., Warn, P., Peshu, N., et al. Indicators of life-threatening malaria in African children. N. Engl. J. Med. 332 (1995), 1399–1404.
55. Mbengue, A., Bhattacharjee, S., Pandharkar, T., Liu, H., Estiu, G., Stahelin, R.V., Rizk, S.S., Njimoh, D.L., Ryan, Y., Chotivanich, K., et al. A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria. Nature 520 (2015), 683–687.
56. McLean, A.R., Ataide, R., Simpson, J.A., Beeson, J.G., Fowkes, F.J., Malaria and immunity during pregnancy and postpartum: a tale of two species. Parasitology 142 (2015), 999–1015.
57. McNamara, C.W., Lee, M.C., Lim, C.S., Lim, S.H., Roland, J., Nagle, A., Simon, O., Yeung, B.K., Chatterjee, A.K., McCormack, S.L., et al. Targeting Plasmodium PI(4)K to eliminate malaria. Nature 504 (2013), 248–253.
58. Mikolajczak, S.A., Vaughan, A.M., Kangwanrangsan, N., Roobsoong, W., Fishbaugher, M., Yimamnuaychok, N., Rezakhani, N., Lakshmanan, V., Singh, N., Kaushansky, A., et al. Plasmodium vivax liver stage development and hypnozoite persistence in human liver-chimeric mice. Cell Host Microbe 17 (2015), 526–535.
59. Miotto, O., Amato, R., Ashley, E.A., MacInnis, B., Almagro-Garcia, J., Amaratunga, C., Lim, P., Mead, D., Oyola, S.O., Dhorda, M., et al. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat. Genet. 47 (2015), 226–234.
60. Mok, S., Ashley, E.A., Ferreira, P.E., Zhu, L., Lin, Z., Yeo, T., Chotivanich, K., Imwong, M., Pukrittayakamee, S., Dhorda, M., et al. Drug resistance. Population transcriptomics of human malaria parasites reveals the mechanism of artemisinin resistance. Science 347 (2015), 431–435.
61. Moxon, C.A., Wassmer, S.C., Milner, D.A. Jr., Chisala, N.V., Taylor, T.E., Seydel, K.B., Molyneux, M.E., Faragher, B., Esmon, C.T., Downey, C., et al. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood 122 (2013), 842–851.
62. Naing, C., Whittaker, M.A., Nyunt Wai, V., Mak, J.W., Is Plasmodium vivax malaria a severe malaria?: a systematic review and meta-analysis. PLoS Negl. Trop. Dis., 8, 2014, e3071.
63. Ndungu, F.M., Olotu, A., Mwacharo, J., Nyonda, M., Apfeld, J., Mramba, L.K., Fegan, G.W., Bejon, P., Marsh, K., Memory B cells are a more reliable archive for historical antimalarial responses than plasma antibodies in no-longer exposed children. Proc. Natl. Acad. Sci. USA 109 (2012), 8247–8252.
64. Nunes-Silva, S., Dechavanne, S., Moussiliou, A., Pstrąg, N., Semblat, J.P., Gangnard, S., Tuikue-Ndam, N., Deloron, P., Chêne, A., Gamain, B., Beninese children with cerebral malaria do not develop humoral immunity against the IT4-VAR19-DC8 PfEMP1 variant linked to EPCR and brain endothelial binding. Malar. J., 14, 2015, 493.
65. Osier, F.H., Mackinnon, M.J., Crosnier, C., Fegan, G., Kamuyu, G., Wanaguru, M., Ogada, E., McDade, B., Rayner, J.C., Wright, G.J., et al. New antigens for a multicomponent blood-stage malaria vaccine. Sci. Transl. Med., 6, 2014, 247ra102.
66. Paul, A.S., Saha, S., Engelberg, K., Jiang, R.H., Coleman, B.I., Kosber, A.L., Chen, C.T., Ganter, M., Espy, N., Gilberger, T.W., et al. Parasite calcineurin regulates host cell recognition and attachment by apicomplexans. Cell Host Microbe 18 (2015), 49–60.
67. Rahimi, B.A., Thakkinstian, A., White, N.J., Sirivichayakul, C., Dondorp, A.M., Chokejindachai, W., Severe vivax malaria: a systematic review and meta-analysis of clinical studies since 1900. Malar. J., 13, 2014, 481.
68. Reddy, K.S., Amlabu, E., Pandey, A.K., Mitra, P., Chauhan, V.S., Gaur, D., Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. Proc. Natl. Acad. Sci. USA 112 (2015), 1179–1184.
69. Regev-Rudzki, N., Wilson, D.W., Carvalho, T.G., Sisquella, X., Coleman, B.M., Rug, M., Bursac, D., Angrisano, F., Gee, M., Hill, A.F., et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153 (2013), 1120–1133.
70. Riglar, D.T., Richard, D., Wilson, D.W., Boyle, M.J., Dekiwadia, C., Turnbull, L., Angrisano, F., Marapana, D.S., Rogers, K.L., Whitchurch, C.B., et al. Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9 (2011), 9–20.
71. Riley, E.M., Stewart, V.A., Immune mechanisms in malaria: new insights in vaccine development. Nat. Med. 19 (2013), 168–178.
72. Risco-Castillo, V., Topçu, S., Marinach, C., Manzoni, G., Bigorgne, A.E., Briquet, S., Baudin, X., Lebrun, M., Dubremetz, J.F., Silvie, O., Malaria sporozoites traverse host cells within transient vacuoles. Cell Host Microbe 18 (2015), 593–603.
73. Rodrigues, C.D., Hannus, M., Prudêncio, M., Martin, C., Gonçalves, L.A., Portugal, S., Epiphanio, S., Akinc, A., Hadwiger, P., Jahn-Hofmann, K., et al. Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4 (2008), 271–282.
74. Scott, J.A., Berkley, J.A., Mwangi, I., Ochola, L., Uyoga, S., Macharia, A., Ndila, C., Lowe, B.S., Mwarumba, S., Bauni, E., et al. Relation between falciparum malaria and bacteraemia in Kenyan children: a population-based, case-control study and a longitudinal study. Lancet 378 (2011), 1316–1323.
75. Seder, R.A., Chang, L.J., Enama, M.E., Zephir, K.L., Sarwar, U.N., Gordon, I.J., Holman, L.A., James, E.R., Billingsley, P.F., Gunasekera, A., et al., VRC 312 Study Team. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341 (2013), 1359–1365.
76. Singh, S., Alam, M.M., Pal-Bhowmick, I., Brzostowski, J.A., Chitnis, C.E., Distinct external signals trigger sequential release of apical organelles during erythrocyte invasion by malaria parasites. PLoS Pathog., 6, 2010, e1000746.
77. Smith, J.D., Rowe, J.A., Higgins, M.K., Lavstsen, T., Malaria's deadly grip: cytoadhesion of Plasmodium falciparum-infected erythrocytes. Cell. Microbiol. 15 (2013), 1976–1983.
78. Snow, R.W., Omumbo, J.A., Lowe, B., Molyneux, C.S., Obiero, J.O., Palmer, A., Weber, M.W., Pinder, M., Nahlen, B., Obonyo, C., et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349 (1997), 1650–1654.
79. Spangenberg, T., Burrows, J.N., Kowalczyk, P., McDonald, S., Wells, T.N., Willis, P., The open access malaria box: a drug discovery catalyst for neglected diseases. PLoS ONE, 8, 2013, e62906.
80. Spillman, N.J., Allen, R.J., McNamara, C.W., Yeung, B.K., Winzeler, E.A., Diagana, T.T., Kirk, K., Na(+) regulation in the malaria parasite Plasmodium falciparum involves the cation ATPase PfATP4 and is a target of the spiroindolone antimalarials. Cell Host Microbe 13 (2013), 227–237.
81. Spring, M., Murphy, J., Nielsen, R., Dowler, M., Bennett, J.W., Zarling, S., Williams, J., de la Vega, P., Ware, L., Komisar, J., et al. First-in-human evaluation of genetically attenuated Plasmodium falciparum sporozoites administered by bite of Anopheles mosquitoes to adult volunteers. Vaccine 31 (2013), 4975–4983.
82. Straimer, J., Gnädig, N.F., Witkowski, B., Amaratunga, C., Duru, V., Ramadani, A.P., Dacheux, M., Khim, N., Zhang, L., Lam, S., et al. Drug resistance. K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates. Science 347 (2015), 428–431.
83. Sturm, A., Amino, R., van de Sand, C., Regen, T., Retzlaff, S., Rennenberg, A., Krueger, A., Pollok, J.M., Menard, R., Heussler, V.T., Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313 (2006), 1287–1290.
84. Tavares, J., Formaglio, P., Thiberge, S., Mordelet, E., Van Rooijen, N., Medvinsky, A., Ménard, R., Amino, R., Role of host cell traversal by the malaria sporozoite during liver infection. J. Exp. Med. 210 (2013), 905–915.
85. Taylor, T.E., Molyneux, M.E., The pathogenesis of pediatric cerebral malaria: eye exams, autopsies, and neuroimaging. Ann. N Y Acad. Sci. 1342 (2015), 44–52.
86. Tham, W.-H., Healer, J., Cowman, A.F., Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Trends Parasitol. 28 (2012), 23–30.
87. Tham, W.H., Lim, N.T., Weiss, G.E., Lopaticki, S., Ansell, B.R., Bird, M., Lucet, I., Dorin-Semblat, D., Doerig, C., Gilson, P.R., et al. Plasmodium falciparum adhesins play an essential role in signalling and activation of invasion into human erythrocytes. PLoS Pathog., 11, 2015, e1005343.
88. Theisen, M., Roeffen, W., Singh, S.K., Andersen, G., Amoah, L., van de Vegte-Bolmer, M., Arens, T., Tiendrebeogo, R.W., Jones, S., Bousema, T., et al. A multi-stage malaria vaccine candidate targeting both transmission and asexual parasite life-cycle stages. Vaccine 32 (2014), 2623–2630.
89. Turner, L., Lavstsen, T., Berger, S.S., Wang, C.W., Petersen, J.E., Avril, M., Brazier, A.J., Freeth, J., Jespersen, J.S., Nielsen, M.A., et al. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498 (2013), 502–505.
90. Vaidya, A.B., Morrisey, J.M., Zhang, Z., Das, S., Daly, T.M., Otto, T.D., Spillman, N.J., Wyvratt, M., Siegl, P., Marfurt, J., et al. Pyrazoleamide compounds are potent antimalarials that target Na+ homeostasis in intraerythrocytic Plasmodium falciparum. Nat. Commun., 5, 2014, 5521.
91. van Eijk, A.M., Ayisi, J.G., Ter Kuile, F.O., Slutsker, L., Shi, Y.P., Udhayakumar, V., Otieno, J.A., Kager, P.A., Lal, R.B., Steketee, R.W., Nahlen, B.L., HIV, malaria, and infant anemia as risk factors for postneonatal infant mortality among HIV-seropositive women in Kisumu, Kenya. J. Infect. Dis. 196 (2007), 30–37.
92. Vaughan, A.M., Mikolajczak, S.A., Wilson, E.M., Grompe, M., Kaushansky, A., Camargo, N., Bial, J., Ploss, A., Kappe, S.H., Complete Plasmodium falciparum liver-stage development in liver-chimeric mice. J. Clin. Invest. 122 (2012), 3618–3628.
93. Volz, J., Yap, A., Sisquella, X., Thompson, J.K., Lim, N.T.Y., Whitehead, L.W., Chen, L., Lampe, M., Tham, W.-T., Wilson, D., et al. The essential invasion complex PfRh5/PfRipr/CyRPA is linked to injection of calcium into human erythrocytes by merozoites during invasion. Cell Host Microbe 20 (2016), 60–71.
94. Wassmer, S.C., Taylor, T.E., Rathod, P.K., Mishra, S.K., Mohanty, S., Arevalo-Herrera, M., Duraisingh, M.T., Smith, J.D., Investigating the pathogenesis of severe malaria: a multidisciplinary and cross-geographical approach. Am. J. Trop. Med. Hyg. 93 (2015), 42–56.
95. Weiss, G.E., Gilson, P.R., Taechalertpaisarn, T., Tham, W.H., de Jong, N.W., Harvey, K.L., Fowkes, F.J., Barlow, P.N., Rayner, J.C., Wright, G.J., et al. Revealing the sequence and resulting cellular morphology of receptor-ligand interactions during Plasmodium falciparum invasion of erythrocytes. PLoS Pathog., 11, 2015, e1004670.
96. WHO (2015). The World Malaria Report http://wwwwhoint/malaria/publications/world-malaria-report-2015/report/en/ ISBN 978 92 4 156515 8.
97. Wu, Y., Sinden, R.E., Churcher, T.S., Tsuboi, T., Yusibov, V., Development of malaria transmission-blocking vaccines: from concept to product. Adv. Parasitol. 89 (2015), 109–152.
98. Yeo, T.W., Lampah, D.A., Kenangalem, E., Tjitra, E., Weinberg, J.B., Granger, D.L., Price, R.N., Anstey, N.M., Decreased endothelial nitric oxide bioavailability, impaired microvascular function, and increased tissue oxygen consumption in children with falciparum malaria. J. Infect. Dis. 210 (2014), 1627–1632.