Immune Escape Mechanisms are Plasmodium's Secret Weapons Foiling the Success of Potent and Persistently Efficacious Malaria Vaccines

Clinical Immunology

Volumn 161, Issue 2, 2015, Pages 136-143

  Farooq, Fouzia ^a   Bergmann Leitner, Elke S ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

Immune editing; Immune escape; Malaria; Vaccine

Indexed keywords

ANTIBODY; MALARIA VACCINE;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; HOST PARASITE INTERACTION; HUMAN; IMMUNE EVASION; IMMUNE RESPONSE; INNATE IMMUNITY; MOLECULAR MIMICRY; NONHUMAN; PARASITE DEVELOPMENT; PHAGOCYTOSIS; PLASMODIUM; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; TROPISM; ANIMAL; IMMUNE SYSTEM; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY;

ANIMALS; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; IMMUNITY; MALARIA VACCINES; PLASMODIUM;

EID: 84942515337     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.08.015     Document Type: Review

References (69)

1. Clyde D.F. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am. J. Trop. Med. Hyg. 1975, 24:397-401.
2. Rieckmann K.H., Beaudoin R.L., Cassells J.S., Sell K.W. Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull. World Health Organ. 1979, 57:261-265.
3. Alonso P.L., Sacarlal J., Aponte J.J., Leach A., Macete E., Milman J.B., Mandomando I., Spiessens B., Guinovart C., Espasa M., Bassat Q., Aide P., Ofori-Anyinam O., Navia M.M., Corachan S., Ceuppens M., Dubois M.C., Demoitie M.A., Dubovsky F., Menendez C., Tornieporth N., Ballou W.R., Thompson R., Cohen J. Efficacy of the RTS,S/ASO2A vaccine against Plasmodium falciparum infection and disease in young African children: randomized controlled trial. Lancet 2004, 364:1411-1420.
4. Stoute J.A., Slaoui M., Heppner D.G., Momin P., Kester K.E., Desmons P., Wellde B.T., Garcon N., Krzych U., Marchand M. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group. N. Engl. J. Med. 1997, 336:86-91.
5. Madeiros M.M., da Silva H.B., Reis A.S., Barboza R., Thompson J., D'Imperio Lima M.R., Marinho C.R.F., Tadokoro C.E. Liver accumulation of Plasmodium chabaudi-infected red blood cells and modulation of regulatory T cell and dendritic cell responses. PLoS One 2013, 8.
6. Tachado S.D., Gerold P., McConville M.J., Baldwin T., Quilici D., Schwarz R., Schofield L. Glycosylphospatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by protein tyrosine kinase-dependent and protein kinase C-dependent signaling pathways. J. Immunol. 1996, 156:1897-1907.
7. Erdman L., Finney C.A.M., Liles W.C., Kain K.C. Inflammatory pathways in malaria infection: TLRs share the stage with other components of the innate immunity. Mol. Biochem. Parasitol. 2008, 162:105-111.
8. Love M.S., Millholand M.G., Mishra S., Kulkami S., Freeman K.B., Pan W., Kavash R.W., Costanzo M.J., Jo H., Daly T.M., Williams D.R., Kowalska M.A., Bergman L.W., Poncz M., DeGrado W.F., Sinnis P., Scott R.W., Greenbaum D.C. Platelet factor 4 activity against P.falciparum and its translation to nonpeptidic mimics as antimalarials. Cell Host Microbe 2012, 12:815-823.
9. + T cells to sporozoite-induced protection against malaria. Immunology 1993, 80:1-5.
10. Bergmann-Leitner E.S., Scheiblhofer S., Weiss R., Duncan E.H., Leitner W.W., Chen D., Angov E., Khan F., Williams J.L., Winter D.B., Thalhamer J., Lyon J.A., Tsokos G.C. C3d binding to the circumsporozoite protein carboxy-terminus deviates immunity against malaria. Int. Immunol. 2005, 17:245-255.
11. Regules J.A., Cummings J.F., Ockenhouse C. The RTS,S vaccine candidate for malaria. Expert Rev. Vaccines 2011, 10:589-599.
12. Bergmann-Leitner E., Li Q., Caridha D., O'Neil M.T., Ockenhouse C., Hickman M., Angov E. Protective immune mechanisms against pre-erythrocytic forms of Plasmodium berghei depend on the target antigen. Trials Vaccinol. 2014, 3:e4-e6.
13. Bergmann-Leitner E.S., Duncan E.H., Angov E. MSP-1p42-specific antibodies affect growth and development of intra-erythrocytic parasites of Plasmodium falciparum. Malar. J. 2009, 8:183.
14. Bergmann-Leitner E., Duncan E.H., Angov E. The impact of immune responses on the erythrocytic stages of Plasmodium and the implication for vaccine development. Malaria Parasites 2012, Intech - Open Access Publisher, Rijeka, Croatia. O. Okwa (Ed.).
15. Druilhe P., Perignon J.L. Mechanisms of defense against P. falciparum asexual blood stages in humans. Immunol. Lett. 1994, 41:115-120.
16. Doolan D.L., Hoffman S.L. The complexity of protective immunity against liver-stage malaria. J. Immunol. 2000, 165:1453-1462.
17. Coppi A., Pinzon-Ortiz C., Hutter C., Sinnis P. The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. J. Exp. Med. 2005, 201:27-33.
18. Stewart M.J., Vanderberg J.P. Malaria sporozoites release circumsporozoite protein from their apical end and translocate it along their surface. J. Protozool. 1991, 38:411-421.
19. Bergmann-Leitner E.S., Mease R.M., De La Vega P., Savranskaya T., Polhemus M., Ockenhouse C., Angov E. Immunization with pre-erythrocytic antigen CelTOS from Plasmodium falciparum elicits cross-species protection against heterologous challenge with Plasmodium berghei. PLoS One 2010, 5.
20. Mota M.M., Pradel G., Vanderberg J.P., Hafalla J.C., Frevert U., Nussenzweig R.S., Nussenzweig V., Rodriguez A. Migration fo Plasmodium sporozoites through cells before infection. Science 2001, 291:141-144.
21. Kawamoto Y., Winger L.A., Hong K., Matsuoka H., Chinzei Y., Kawamoto F., Kamimura K., Arakawa R., Sinden R.E., Miyama A. Plasmodium berghei: sporozoites are sensitive to human serum but not susceptible host serum. Exp. Parasitol. 1992, 75:361-368.
22. Margos G., Navarette S., Butcher G., Davies A., Willers C., Sinden R.E., Lachmann P.J. Interaction between host complement and mosquito-midgut-stage Plasmodium berghei. Infect. Immun. 2001, 69:5064-5071.
23. Giribaldi G., Ulliers D., Mannu F., Arese P., Turini F. Growth of Plasmodium falciparum induces stage-dependent haemichrome formation, oxidate aggregation of band 3, membrane deposition of complement and antibodies, and phagocytosis of parasitized erythrocytes. Br. J. Haematol. 2001, 113:492-499.
24. Stanley H.A., Mayes J.T., Cooper N.R., Reese R.T. Complement activation by the surface of Plasmodium falciparum infected erythrocytes. Mol. Immunol. 1984, 21:145-150.
25. Bergmann-Leitner E.S., Leitner W.W., Tsokos G.C. Complement 3d: From molecular adjuvant to target of immune escape mechanisms. Clin. Immunol. 2006, 121:177-185.
26. Rowe J.A., Moulds J.M., Newbold C.I., Miller L.H. P.falciparum rosetting mediated by a parasite-variant erythrocyte membran protein and complement receptor-1. Nature 1997, 388:292-295.
27. Kirchgatter K., Del Portillo H.A. Clinical and molecular aspects of severe malaria. An. Acad. Bras. Cienc. 2005, 77:455-475.
28. Liehl P., Mota M.M. Innate recognition of malaria parasites by mammalian hosts. Int. J. Parasitol. 2012, 42f:557-566.
29. Graewe S., Rankin K.E., Lehmann C., Deschermeier C., Hecht L., Froehlke U., Stanway R.R., Heussler V. Hostile takeover by Plasmodium: reorganization of parasite and host cell membranes during liver stage egress. PLoS Pathog. 2011, 7.
30. Singh A.P., Buscaglia C.A., Levay A., Nussenzweig R.S., Walker J.R., Winzeler E.A., Fuji H., Fontoura B.M., Nussenzweig V. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 2007, 131:492.
31. Bergmann-Leitner E.S., Leitner W.W., Duncan E.H., Savranskaya T., Angov E. Molecular adjuvants for malaria DNA vaccines based on the modulation of host-cell apoptosis. Vaccine 2009, 27:5700-5708.
32. Frevert U., Galinski M.R., Hugel F.U., Allon N., Schreier H., Smulevitch S., Shakibaei M., Claviio P. Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. EMBO J. 1998, 17:3816-3826.
33. Ma J., Trop S., Baer S., Rakhmanaliev E., Arany Z., Dumoulin P., Zhang H., Romano J., Coppens I., Levitsky V., Levitskaya J. Dynamics of the major histocompatibility complex class I processing and presentation pathway in the course of malaria parasite development in human hepatocytes: implications for vaccine development. PLoS One 2013, 8.
34. 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 2006, 313:1287-1290.
35. Leitner W.W., Krzych U. Plasmodium falciparum malaria blood stge parasites preferentially inhibit macrophages with high phagocytic activity. Parasite Immunol. 1997, 19:103-110.
36. Awandare G.A., Hittner J.B., Kremsner P.G., Ochiel D.O., Keller C.C., Weinberg J.B., Clark I.A., Perkins D.J. Decreased circulating macrophage migration inhibitory factor (MIF) protein and blood mononuclear cell MIF transcripts in children with Plasmodium falciparum malaria. Clin. Immunol. 2006, 119:219-225.
37. Urban B.C., Ferguson D.J., Pain A., Willcox N., Plebanski M., Austyn J.M., Roberts D.J. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 1999, 400:73-77.
38. Preiser P.R., Jarra W., Capiod T., Snounou G. A rhoptry-protein-associated mechanism of cloncal phenotypic variation in rodent malaria. Nature 1999, 398:618-622.
39. Ramasamy R. Molecular basis for evasion of host immunity and pathogenesis in malaria. Biochim. Biophys. Acta 1998, 1406:10-27.
40. Berkowitz A.L., Thakur K.T. Acute inflammatory demyelinating polyradiculoneuropathy following malaria. J. Clin. Neurosci. 2014, 21:704-706.
41. Johnson A.S., Delisca G., Booth G.S. Warm autoimmune hemolytic anemia secondary to Plasmodium ovale infectionL a case report and review of the literature. Transfus. Apher. Sci. 2013, 49:571-573.
42. Zambrano-Villa S., Rosales-Borias D., Carrero J.C., Ortiz-Ortiz L. How protozoan parasites evade the immune response. Trends Parasitol. 2002, 18:272-278.
43. Hommel M. Modulation of host cell receptors: a mechanism for the survival of malaria parasites. Parasitology 1997, 115:S45-S55.
44. Grau G.E., Behr C. T cells and malaria: is Th1 cell activation a prerquisite for pathology?. Res. Immunol. 1994, 145:4410445.
45. Lee E.A., Flanagan K.L., Minigo G., Reece W.H., Bailey R., Pinder M., Hill A., Plebanski M. Dimorphic Plasmodium falciparum merozoite surface protein-1 epitopes turn off memory T cells and interfere with T cell priming. Eur. J. Immunol. 2006, 36:1168-1178.
46. Plebanski M., Lee E.A., Hill A. Immune evasion in malaria; altered peptide ligands of the circumsporozoite protein. Parasitology 1997, 115:S55-S66.
47. Ferrandiz E., Cazenave P.-A., Pied S., Six A. Su.43. Compartmentalized Modifications of the Peripheral T-Cell Repertoire Are Associated to Experimental Cerebral Malaria. Clin. Immunol. 2006, 119:S174. (Supplement).
48. Holder A.A., Guevara Patino J.A., Uthaipibull C., Syed S.E., Ling I.T., Scott-Finnigan T., Blackman M.J. Merozoite surface protein 1, immune evasion, and vaccines against asexual blood stage malaria. Parassitologia 1999, 41:409-414.
49. + T cell cycle arrest during priming as a consequence of dendritic cell interaction wiht plasmodium-infected red cells. J. Immunol. 2005, 175:3525-3533.
50. Xu H., Wipasa J., Yan H., Zeng M., Makobongo M.O., Finkelman F.D., Kelso A., Good M.F. The mechanism and significance of deletion of parasite-specific CD4(+) T cells in malaria infection. J. Exp. Med. 2002, 195:881-892.
51. Ansari N.A., Saluja S., Salotra P. Elevated levels of interferon-γ, interleukin-10, and interleukin-6 during active disease in Indian kala azar. Clin. Immunol. 2006, 119:339-345.
52. Jason J., Archibald L.K., Nwanyanwu O.C., Bell M., Buchanan I., Larned J., Kazembe P.N., Dobbie H., Parekh B., Byrd M.G., Eick A., Han A., Jarvis W.R. Cytokines and Malaria Parasitemia. Clin. Immunol. 2001, 100:208-218.
53. Ong'echa J.M., Remo A.M., Kristoff J., Hittner J.B., Were T., Ouma C., Otieno R.O., Vulule J.M., Keller C.C., Awandare G.A., Perkins D.J. Increased circulating interleukin (IL)-23 in children with malarial anemia: In vivo and in vitro relationship with co-regulatory cytokines IL-12 and IL-10. Clin. Immunol. 2008, 126:211-221.
54. Wenisch C., Varijanonta S., Looareesuwan S., Graninger W., Pichler R., Wernsdorfer W. Soluble Intercellular Adhesion Molecule-1 (ICAM-1), Endothelial Leukocyte Adhesion Molecule-1 (ELAM-1), and Tumor Necrosis Factor Receptor (55 kDa TNF-R) in Patients with Acute Plasmodium falciparum Malaria. Clin. Immunol. Immunopathol. 1994, 71:344-348.
55. + regulatory T cells, dendritic cells, and circulating cytokines in uncomplicated malaria: do different parasite species elicit similar host responses?. Infect. Immun. 2010, 78:4763-4772.
56. + regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 2005, 23:287-296.
57. + regulatory T cells. Nat. Med. 2004, 10.
58. Hisaeda H., Tetsutani K., Imai T., Moriya C., Tu L., Hamano S., Duan X., Chou B., Ishida H., Aramaki A., Shen J., Ishii K.J., Coban C., Akira S., Takeda K., Yasutomo K., Torii M., Himeno K. Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J. Immunol. 2008, 180:2496-2503.
59. Chizzolini C., Nicholson J.K.A., Geinoz A., Olsen-Rasmussen M.A., Schrijvers D. In vivo decreased expression of CD25 (p55 chain of IL-2 receptor) on CD3+ T cells correlates with low in vitro responsiveness to Plasmodium falciparum antigen in subjects living in a malaria endemic area. Clin. Immunol. Immunopathol. 1991, 60:209-219.
60. Butler N.S., Moebius J., Pewe L.L., Traore B., Doumbo O.K., Tygrett L.T., Waldschmidt T.J., Crompton P.D., Harty J.T. Therapeutic blockade of PD-L1 and LAG-3 rapidly clreas established blood-stage Plasmodium infection. Nat. Immunol. 2011, 13:188-195.
61. Jeurissen A., Ceuppens J.L., Bossuyt X. T lymphocyte dependence of the antibody response to "T lymphocyte independent type 2" antigens. Immunology 2004, 111:1-7.
62. Achtman A.H., Bull P.C., Stephens R., Langhorne J. Longevity of the immune response and memory to blood stage malaria infection. Curr. Top. Microbiol. Immunol. 2005, 297:71-102.
63. Stephens R., Langhorne J. Effector memory Th1 CD4 T cells are maintained in a mouse model of chronic malaria. PLoS Pathog. 2010, 6.
64. Behet M.C., Foquet L., van Gernert G.J., Bijker E.M., Meuleman P., Leroux-Roels G., Hermsen C.C., Scholzen A., Sauerwein R.W. Sporozoite immunization of human volunteers under chemoprophylaxis induces functional antibodies against pre-erythrocytic stages of Plasmodium falciparum. Malar. J. 2014, 13.
65. Bijker E.M., Teirlinck A.C., Schats R., van Gernert G.J., van de Vegte-Bolmer M., van Lieshout L., IntHout J., Hermsen C.C., Scholzen A., Visser L.G., Sauerwein R.W. Cytotoxic markers associate with protection against malaria in human volunteers immunized with Plasmodium falciparum sporozoites. J. Infect. Dis. 2014, 210:1605-1610.
66. + T cell responses and protection against Plasmodium falciparum infections. PLoS One 2013, 8.
67. Bejon P., White M.T., Olotu A., Bojang K., Lusingu J.P.A., Salim N., Otsyula N.N., Agnandji S.T., Asante K.P., Owusu-Agyei S., Abdulla S., Ghani A.C. Efficacy of RTS,S malaria vaccines: individual-participant pooled analysis of phase 2 data. Lancet 2013, 13:319-327.
68. Plotkin S.A. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 2010, 17:1055-1065.
69. Roestenberg M., Teirlinck A.C., McCall M.B., Teelen K., Makamdop K.M., Wiersma J., Arens T., Beckers P., van Gernert G.J., van de Vegte-Bolmer M., van der Vren A.J., Luty A.J., Hermsen C.C., Sauerwein R.W. Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 2011, 377:1770-1776.