Regulatory issues in immunity to liver and blood-stage malaria

Current Opinion in Immunology

Volumn 42, Issue , 2016, Pages 91-97

  Van Braeckel Budimir, Natalija ^a   Kurup, Samarchith P ^a   Harty, John T ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA; MALARIA VACCINE;

ANTIGEN PRESENTATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE COURSE; ERYTHROCYTE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; LIVER; MALARIA; MALARIA FALCIPARUM; NONHUMAN; PLASMODIUM BERGHEI INFECTION; PLASMODIUM CHABAUDI INFECTION; PLASMODIUM YOELII; REVIEW; SPOROZOITE; ANIMAL; BLOOD; IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LIFE CYCLE STAGE; PARASITOLOGY; PLASMODIUM; T LYMPHOCYTE; VACCINATION;

ANIMALS; BLOOD; HUMANS; IMMUNITY; IMMUNOLOGIC MEMORY; IMMUNOMODULATION; LIFE CYCLE STAGES; LIVER; MALARIA; MALARIA VACCINES; PLASMODIUM; T-LYMPHOCYTES; VACCINATION;

EID: 84975469195     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.06.008     Document Type: Review

References (65)

1. Hill A.V. Pre-erythrocytic malaria vaccines: towards greater efficacy. Nat Rev Immunol 2006, 6:21-32.
2. Butler N.S., Vaughan A.M., Harty J.T., Kappe S.H. Whole parasite vaccination approaches for prevention of malaria infection. Trends Immunol 2012, 33:247-254.
3. Nussenzweig R.S., Vanderberg J., Most H., Orton C. Protective immunity produced by the injection of X-irradiated sporozoites of Plasmodium berghei. Nature 1967, 216:160-162.
4. 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.
5. 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. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 2013, 341:1359-1365.
6. Schofield L., Villaquiran J., Ferreira A., Schellekens H., Nussenzweig R., Nussenzweig V. Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 1987, 330:664-666.
7. Weiss W.R., Sedegah M., Beaudoin R.L., Miller L.H., Good M.F. CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc Natl Acad Sci U S A 1988, 85:573-576.
8. Schmidt N.W., Butler N.S., Badovinac V.P., Harty J.T. Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS Pathog 2010, 6:e1000998.
9. Seguin M.C., Klotz F.W., Schneider I., Weir J.P., Goodbary M., Slayter M., Raney J.J., Aniagolu J.U., Green S.J. Induction of nitric oxide synthase protects against malaria in mice exposed to irradiated Plasmodium berghei infected mosquitoes: involvement of interferon gamma and CD8+ T cells. J Exp Med 1994, 180:353-358.
10. Cockburn I.A., Amino R., Kelemen R.K., Kuo S.C., Tse S.W., Radtke A., Mac-Daniel L., Ganusov V.V., Zavala F., Menard R. In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc Natl Acad Sci U S A 2013, 110:9090-9095.
11. Tran T.M., Li S., Doumbo S., Doumtabe D., Huang C.Y., Dia S., Bathily A., Sangala J., Kone Y., Traore A., et al. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis 2013, 57:40-47.
12. Overstreet M.G., Cockburn I.A., Chen Y.C., Zavala F. Protective CD8 T cells against Plasmodium liver stages: immunobiology of an 'unnatural' immune response. Immunol Rev 2008, 225:272-283.
13. Brasseur P., Agrapart M., Ballet J.J., Druilhe P., Warrell M.J., Tharavanij S. Impaired cell-mediated immunity in Plasmodium falciparum-infected patients with high-parasitemia and cerebral malaria. Clin Immunol Immunopathol 1983, 27:38-50.
14. Doolan D.L., Khamboonruang C., Beck H.P., Houghten R.A., Good M.F. Cytotoxic T lymphocyte (CTL) low-responsiveness to the Plasmodium falciparum circumsporozoite protein in naturally-exposed endemic populations: analysis of human CTL response to most known variants. Int Immunol 1993, 5:37-46.
15. Plebanski M., Aidoo M., Whittle H.C., Hill A.V. Precursor frequency analysis of cytotoxic T lymphocytes to pre-erythrocytic antigens of Plasmodium falciparum in West Africa. J Immunol 1997, 158:2849-2855.
16. Chattopadhyay R., Conteh S., Li M., James E.R., Epstein J.E., Hoffman S.L. The Effects of radiation on the safety and protective efficacy of an attenuated Plasmodium yoelii sporozoite malaria vaccine. Vaccine 2009, 27:3675-3680.
17. Freitas do Rosario A.P., Muxel S.M., Rodriguez-Malaga S.M., Sardinha L.R., Zago C.A., Castillo-Mendez S.I., Alvarez J.M., D'Imperio Lima M.R. Gradual decline in malaria-specific memory T cell responses leads to failure to maintain long-term protective immunity to Plasmodium chabaudi AS despite persistence of B cell memory and circulating antibody. J Immunol 2008, 181:8344-8355.
18. Horne-Debets J.M., Faleiro R., Karunarathne D.S., Liu X.Q., Lineburg K.E., Poh C.M., Grotenbreg G.M., Hill G.R., MacDonald K.P., Good M.F., et al. PD-1 dependent exhaustion of CD8+ T cells drives chronic malaria. Cell Rep 2013, 5:1204-1213.
19. Ocana-Morgner C., Mota M.M., Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 2003, 197:143-151.
20. White C.E., Villarino N.F., Sloan S.S., Ganusov V.V., Schmidt N.W. Plasmodium suppresses expansion of T cell responses to heterologous infections. J Immunol 2015, 194:697-708.
21. Wilson N.S., Behrens G.M., Lundie R.J., Smith C.M., Waithman J., Young L., Forehan S.P., Mount A., Steptoe R.J., Shortman K.D., et al. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat Immunol 2006, 7:165-172.
22. Hafalla J.C., Claser C., Couper K.N., Grau G.E., Renia L., de Souza J.B., Riley E.M. The CTLA-4 and PD-1/PD-L1 inhibitory pathways independently regulate host resistance to Plasmodium-induced acute immune pathology. PLoS Pathog 2012, 8:e1002504.
23. Illingworth J., Butler N.S., Roetynck S., Mwacharo J., Pierce S.K., Bejon P., Crompton P.D., Marsh K., Ndungu F.M. Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J Immunol 2013, 190:1038-1047.
24. Costa P.A., Leoratti F.M., Figueiredo M.M., Tada M.S., Pereira D.B., Junqueira C., Soares I.S., Barber D.L., Gazzinelli R.T., Antonelli L.R. Induction of inhibitory receptors on T cells during Plasmodium vivax malaria impairs cytokine production. J Infect Dis 2015, 212:1999-2010.
25. Nitcheu J., Bonduelle O., Combadiere C., Tefit M., Seilhean D., Mazier D., Combadiere B. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol 2003, 170:2221-2228.
26. Belnoue E., Kayibanda M., Vigario A.M., Deschemin J.C., van Rooijen N., Viguier M., Snounou G., Renia L. On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria. J Immunol 2002, 169:6369-6375.
27. Storm J., Craig A.G. Pathogenesis of cerebral malaria - inflammation and cytoadherence. Front Cell Infect Microbiol 2014, 4:100.
28. Nie C.Q., Bernard N.J., Schofield L., Hansen D.S. CD4+ CD25+ regulatory T cells suppress CD4+ T-cell function and inhibit the development of Plasmodium berghei-specific TH1 responses involved in cerebral malaria pathogenesis. Infect Immun 2007, 75:2275-2282.
29. Kossodo S., Monso C., Juillard P., Velu T., Goldman M., Grau G.E. Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology 1997, 91:536-540.
30. Walther M., Tongren J.E., Andrews L., Korbel D., King E., Fletcher H., Andersen R.F., Bejon P., Thompson F., Dunachie S.J., et al. Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 2005, 23:287-296.
31. Torcia M.G., Santarlasci V., Cosmi L., Clemente A., Maggi L., Mangano V.D., Verra F., Bancone G., Nebie I., Sirima B.S., et al. Functional deficit of T regulatory cells in Fulani, an ethnic group with low susceptibility to Plasmodium falciparum malaria. Proc Natl Acad Sci U S A 2008, 105:646-651.
32. Perez-Mazliah D., Langhorne J. CD4 T-cell subsets in malaria: TH1/TH2 revisited. Front Immunol 2014, 5:671.
33. Dups J.N., Pepper M., Cockburn I.A. Antibody and B cell responses to Plasmodium sporozoites. Front Microbiol 2014, 5:625.
34. Crompton P.D., Moebius J., Portugal S., Waisberg M., Hart G., Garver L.S., Miller L.H., Barillas-Mury C., Pierce S.K. Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annu Rev Immunol 2014, 32:157-187.
35. Jagannathan P., Eccles-James I., Bowen K., Nankya F., Auma A., Wamala S., Ebusu C., Muhindo M.K., Arinaitwe E., Briggs J., et al. IFNgamma/IL-10 co-producing cells dominate the CD4 response to malaria in highly exposed children. PLoS Pathog 2014, 10:e1003864.
36. Su Z., Stevenson M.M. Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect Immun 2000, 68:4399-4406.
37. McCoy M.E., Golden H.E., Doll T.A., Yang Y., Kaba S.A., Zou X., Gerbasi V.R., Burkhard P., Lanar D.E. Mechanisms of protective immune responses induced by the Plasmodium falciparum circumsporozoite protein-based, self-assembling protein nanoparticle vaccine. Malar J 2013, 12:136.
38. Gitau E.N., Tuju J., Karanja H., Stevenson L., Requena P., Kimani E., Olotu A., Kimani D., Marsh K., Bull P., et al. CD4+ T cell responses to the Plasmodium falciparum erythrocyte membrane protein 1 in children with mild malaria. J Immunol 2014, 192:1753-1761.
39. Keswani T., Bhattacharyya A. Differential role of T regulatory and Th17 in Swiss mice infected with Plasmodium berghei ANKA and Plasmodium yoelii. Exp Parasitol 2014, 141:82-92.
40. Ishida H., Matsuzaki-Moriya C., Imai T., Yanagisawa K., Nojima Y., Suzue K., Hirai M., Iwakura Y., Yoshimura A., Hamano S., et al. Development of experimental cerebral malaria is independent of IL-23 and IL-17. Biochem Biophys Res Commun 2010, 402:790-795.
41. Koch O., Rockett K., Jallow M., Pinder M., Sisay-Joof F., Kwiatkowski D. Investigation of malaria susceptibility determinants in the IFNG/IL26/IL22 genomic region. Genes Immun 2005, 6:312-318.
42. Kimura D., Miyakoda M., Kimura K., Honma K., Hara H., Yoshida H., Yui K. Interleukin-27-producing CD4(+) T cells regulate protective immunity during malaria parasite infection. Immunity 2016, 44:672-682.
43. Hansen D.S., Schofield L. Natural regulatory T cells in malaria: host or parasite allies?. PLoS Pathog 2010, 6:e1000771.
44. Torres K.J., Villasis E., Bendezu J., Chauca J., Vinetz J.M., Gamboa D. Relationship of regulatory T cells to Plasmodium falciparum malaria symptomatology in a hypoendemic region. Malar J 2014, 13:108.
45. Roetynck S., Olotu A., Simam J., Marsh K., Stockinger B., Urban B., Langhorne J. Phenotypic and functional profiling of CD4 T cell compartment in distinct populations of healthy adults with different antigenic exposure. PLOS ONE 2013, 8:e55195.
46. Finney O.C., Riley E.M., Walther M. Regulatory T cells in malaria - friend or foe?. Trends Immunol 2010, 31:63-70.
47. Hisaeda H., Maekawa Y., Iwakawa D., Okada H., Himeno K., Kishihara K., Tsukumo S., Yasutomo K. Escape of malaria parasites from host immunity requires CD4+CD25+ regulatory T cells. Nat Med 2004, 10:29-30.
48. Amante F.H., Stanley A.C., Randall L.M., Zhou Y., Haque A., McSweeney K., Waters A.P., Janse C.J., Good M.F., Hill G.R., et al. A role for natural regulatory T cells in the pathogenesis of experimental cerebral malaria. Am J Pathol 2007, 171:548-559.
49. Randall L.M., Amante F.H., McSweeney K.A., Zhou Y., Stanley A.C., Haque A., Jones M.K., Hill G.R., Boyle G.M., Engwerda C.R. Common strategies to prevent and modulate experimental cerebral malaria in mouse strains with different susceptibilities. Infect Immun 2008, 76:3312-3320.
50. Cambos M., Belanger B., Jacques A., Roulet A., Scorza T. Natural regulatory (CD4+CD25+FOXP+) T cells control the production of pro-inflammatory cytokines during Plasmodium chabaudi adami infection and do not contribute to immune evasion. Int J Parasitol 2008, 38:229-238.
51. Couper K.N., Blount D.G., Wilson M.S., Hafalla J.C., Belkaid Y., Kamanaka M., Flavell R.A., de Souza J.B., Riley E.M. IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog 2008, 4:e1000004.
52. Vigario A.M., Gorgette O., Dujardin H.C., Cruz T., Cazenave P.A., Six A., Bandeira A., Pied S. Regulatory CD4+CD25+ Foxp3+ T cells expand during experimental Plasmodium infection but do not prevent cerebral malaria. Int J Parasitol 2007, 37:963-973.
53. Steeg C., Adler G., Sparwasser T., Fleischer B., Jacobs T. Limited role of CD4+Foxp3+ regulatory T cells in the control of experimental cerebral malaria. J Immunol 2009, 183:7014-7022.
54. Walther M., Jeffries D., Finney O.C., Njie M., Ebonyi A., Deininger S., Lawrence E., Ngwa-Amambua A., Jayasooriya S., Cheeseman I.H., et al. Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog 2009, 5:e1000364.
55. Minigo G., Woodberry T., Piera K.A., Salwati E., Tjitra E., Kenangalem E., Price R.N., Engwerda C.R., Anstey N.M., Plebanski M. Parasite-dependent expansion of TNF receptor II-positive regulatory T cells with enhanced suppressive activity in adults with severe malaria. PLoS Pathog 2009, 5:e1000402.
56. Jangpatarapongsa K., Chootong P., Sattabongkot J., Chotivanich K., Sirichaisinthop J., Tungpradabkul S., Hisaeda H., Troye-Blomberg M., Cui L., Udomsangpetch R. Plasmodium vivax parasites alter the balance of myeloid and plasmacytoid dendritic cells and the induction of regulatory T cells. Eur J Immunol 2008, 38:2697-2705.
57. Villarino N.F., LeCleir G.R., Denny J.E., Dearth S.P., Harding C.L., Sloan S.S., Gribble J.L., Campagna S.R., Wilhelm S.W., Schmidt N.W. Composition of the gut microbiota modulates the severity of malaria. Proc Natl Acad Sci U S A 2016, 113:2235-2240.
58. Abel S., Luckheide N., Westendorf A.M., Geffers R., Roers A., Muller W., Sparwasser T., Matuschewski K., Buer J., Hansen W. Strong impact of CD4+ Foxp3+ regulatory T cells and limited effect of T cell-derived IL-10 on pathogen clearance during Plasmodium yoelii infection. J Immunol 2012, 188:5467-5477.
59. Sakaguchi S., Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T. Regulatory T cells: how do they suppress immune responses?. Int Immunol 2009, 21:1105-1111.
60. Penaloza-MacMaster P., Kamphorst A.O., Wieland A., Araki K., Iyer S.S., West E.E., O'Mara L., Yang S., Konieczny B.T., Sharpe A.H., et al. Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection. J Exp Med 2014, 211:1905-1918.
61. Camisaschi C., Casati C., Rini F., Perego M., De Filippo A., Triebel F., Parmiani G., Belli F., Rivoltini L., Castelli C. LAG-3 expression defines a subset of CD4(+)CD25(high)Foxp3(+) regulatory T cells that are expanded at tumor sites. J Immunol 2010, 184:6545-6551.
62. 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 clears established blood-stage Plasmodium infection. Nat Immunol 2012, 13:188-195.
63. Jacobs T., Graefe S.E., Niknafs S., Gaworski I., Fleischer B. Murine malaria is exacerbated by CTLA-4 blockade. J Immunol 2002, 169:2323-2329.
64. Schlotmann T., Waase I., Julch C., Klauenberg U., Muller-Myhsok B., Dietrich M., Fleischer B., Broker B.M. CD4 alphabeta T lymphocytes express high levels of the T lymphocyte antigen CTLA-4 (CD152) in acute malaria. J Infect Dis 2000, 182:367-370.
65. Haque A., Best S.E., Amante F.H., Mustafah S., Desbarrieres L., de Labastida F., Sparwasser T., Hill G.R., Engwerda C.R. CD4+ natural regulatory T cells prevent experimental cerebral malaria via CTLA-4 when expanded in vivo. PLoS Pathog 2010, 6. e1001221.