Age-related differences in naturally acquired T cell memory to Plasmodium falciparum Merozoite Surface Protein 1

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Chelimo, Kiprotich ^a,c   Embury, Paula B ^b   Odada Sumba, Peter ^a   Vulule, John ^a   Ofulla, Ayub V ^c   Long, Carole ^d   Kazura, James W ^b   Moormann, Ann M ^b,e  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASENO UNIVERSITY   (Kenya)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45RA ANTIGEN; GAMMA INTERFERON; L SELECTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEROZOITE SURFACE PROTEIN 1;

ADOLESCENT; ADULT; AGE DISTRIBUTION; ANTIBODY TITER; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHILD; CONTROLLED STUDY; EFFECTOR CELL; ENZYME LINKED IMMUNOSPOT ASSAY; ERYTHROCYTE COUNT; FLOW CYTOMETRY; GRANULOCYTE; HUMAN; HUMAN CELL; IMMUNOLOGICAL MEMORY; LEUKOCYTE COUNT; LYMPHOCYTE COUNT; MALARIA FALCIPARUM; MEMORY T LYMPHOCYTE; MEROZOITE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; SCHOOL CHILD; T LYMPHOCYTE SUBPOPULATION; AGE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOLOGY; INFANT; KENYA; MALE; METABOLISM; MONONUCLEAR CELL;

ANIMALIA; PLASMODIUM FALCIPARUM;

ADOLESCENT; ADULT; AGE FACTORS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; INFANT; INTERFERON-GAMMA; KENYA; LEUKOCYTES, MONONUCLEAR; MALE; MEROZOITE SURFACE PROTEIN 1; PLASMODIUM FALCIPARUM; T-LYMPHOCYTE SUBSETS; YOUNG ADULT;

EID: 80052859770     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024852     Document Type: Article

References (59)

1. Hogh B, (1996) Clinical and parasitological studies on immunity to Plasmodium falciparum malaria in children. Scand J Infect Dis Suppl 102 pp. 1-53.
2. Taylor-Robinson AW, (2002) A model of development of acquired immunity to malaria in humans living under endemic conditions. Med Hypotheses 58: 148-156.
3. Artavanis-Tsakonas K, Tongren JE, Riley EM, (2003) The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol 133: 145-152.
4. Leri O, Perinelli P, Losi T, Mastropasqua M, Peri C, et al. (1997) [Malaria: recent immunological acquisitions and therapeutic prospects]. Clin Ter 148: 655-665.
5. Cohen S, Mc GI, Carrington S, (1961) Gamma-globulin and acquired immunity to human malaria. Nature 192: 733-737.
6. Langhorne J, Ndungu FM, Sponaas AM, Marsh K, (2008) Immunity to malaria: more questions than answers. Nat Immunol 9: 725-732.
7. Pombo DJ, Lawrence G, Hirunpetcharat C, Rzepczyk C, Bryden M, et al. (2002) Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 360: 610-617.
8. Edstein MD, Kotecka BM, Anderson KL, Pombo DJ, Kyle DE, et al. (2005) Lengthy antimalarial activity of atovaquone in human plasma following atovaquone-proguanil administration. Antimicrob Agents Chemother 49: 4421-4422.
9. Egan A, Waterfall M, Pinder M, Holder A, Riley E, (1997) Characterization of human T- and B-cell epitopes in the C terminus of Plasmodium falciparum merozoite surface protein 1: evidence for poor T-cell recognition of polypeptides with numerous disulfide bonds. Infect Immun 65: 3024-3031.
10. Garraud O, Diouf A, Holm I, Perraut R, Longacre S, (1999) Immune responses to Plasmodium falciparum-merozoite surface protein 1 (MSP1) antigen, II. Induction of parasite-specific immunoglobulin G in unsensitized human B cells after in vitro T-cell priming with MSP119. Immunology 97: 497-505.
11. Schluns KS, Lefrancois L, (2003) Cytokine control of memory T-cell development and survival. Nat Rev Immunol 3: 269-279.
12. Chattopadhyay PK, Hogerkorp CM, Roederer M, (2008) A chromatic explosion: the development and future of multiparameter flow cytometry. Immunology 125: 441-449.
13. Huaman MC, Martin LB, Malkin E, Narum DL, Miller LH, et al. (2008) Ex vivo cytokine and memory T cell responses to the 42-kDa fragment of Plasmodium falciparum merozoite surface protein-1 in vaccinated volunteers. J Immunol 180: 1451-1461.
14. Lee EA, Palmer DR, Flanagan KL, Reece WH, Odhiambo K, et al. (2002) Induction of T helper type 1 and 2 responses to 19-kilodalton merozoite surface protein 1 in vaccinated healthy volunteers and adults naturally exposed to malaria. Infect Immun 70: 1417-1421.
15. Sakai T, Hisaeda H, Nakano Y, Zhang M, Takashima M, et al. (2003) Gene gun-based co-immunization of merozoite surface protein-1 cDNA with IL-12 expression plasmid confers protection against lethal Plasmodium yoelii in A/J mice. Vaccine 21: 1432-1444.
16. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A, (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
17. Huaman MC, Mullen GE, Long CA, Mahanty S, (2009) Plasmodium falciparum apical membrane antigen 1 vaccine elicits multifunctional CD4 cytokine-producing and memory T cells. Vaccine 27: 5239-5246.
18. Erkeller-Yuksel FM, Deneys V, Yuksel B, Hannet I, Hulstaert F, et al. (1992) Age-related changes in human blood lymphocyte subpopulations. J Pediatr 120: 216-222.
19. Hulstaert F, Hannet I, Deneys V, Munhyeshuli V, Reichert T, et al. (1994) Age-related changes in human blood lymphocyte subpopulations. II. Varying kinetics of percentage and absolute count measurements. Clin Immunol Immunopathol 70: 152-158.
20. Sinigaglia F, Guttinger M, Kilgus J, Doran DM, Matile H, et al. (1988) A malaria T-cell epitope recognized in association with most mouse and human MHC class II molecules. Nature 336: 778-780.
21. Lundie RJ, de Koning-Ward TF, Davey GM, Nie CQ, Hansen DS, et al. (2008) Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells. Proc Natl Acad Sci U S A 105: 14509-14514.
22. Wilson NS, Behrens GM, Lundie RJ, Smith CM, Waithman J, et al. (2006) Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat Immunol 7: 165-172.
23. Todryk SM, Bejon P, Mwangi T, Plebanski M, Urban B, et al. (2008) Correlation of memory T cell responses against TRAP with protection from clinical malaria, and CD4 CD25 high T cells with susceptibility in Kenyans. PLoS One 3: e2027.
24. Todryk SM, Walther M, Bejon P, Hutchings C, Thompson FM, et al. (2009) Multiple functions of human T cells generated by experimental malaria challenge. Eur J Immunol 39: 3042-3051.
25. Podoba JE, Stevenson MM, (1991) CD4+ and CD8+ T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS. Infect Immun 59: 51-58.
26. Horowitz A, Newman KC, Evans JH, Korbel DS, Davis DM, et al. (2010) Cross-talk between T cells and NK cells generates rapid effector responses to Plasmodium falciparum-infected erythrocytes. J Immunol 184: 6043-6052.
27. McCall MB, Roestenberg M, Ploemen I, Teirlinck A, Hopman J, et al. (2010) Memory-like IFN-gamma response by NK cells following malaria infection reveals the crucial role of T cells in NK cell activation by P. falciparum. Eur J Immunol 40: 3472-3477.
28. Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, et al. (2009) Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog 5: e1000364.
29. Franklin BS, Parroche P, Ataide MA, Lauw F, Ropert C, et al. (2009) Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci U S A 106: 5789-5794.
30. Malhotra I, Wamachi AN, Mungai PL, Mzungu E, Koech D, et al. (2008) Fine specificity of neonatal lymphocytes to an abundant malaria blood-stage antigen: epitope mapping of Plasmodium falciparum MSP1(33). J Immunol 180: 3383-3390.
31. Jackola DR, Ruger JK, Miller RA, (1994) Age-associated changes in human T cell phenotype and function. Aging (Milano) 6: 25-34.
32. Spring MD, Chelimo K, Tisch DJ, Sumba PO, Rochford R, et al. (2010) Allele specificity of gamma interferon responses to the carboxyl-terminal region of Plasmodium falciparum merozoite surface protein 1 by Kenyan adults with naturally acquired immunity to malaria. Infect Immun 78: 4431-4441.
33. Saule P, Trauet J, Dutriez V, Lekeux V, Dessaint JP, et al. (2006) Accumulation of memory T cells from childhood to old age: central and effector memory cells in CD4(+) versus effector memory and terminally differentiated memory cells in CD8(+) compartment. Mech Ageing Dev 127: 274-281.
34. Luty AJ, Lell B, Schmidt-Ott R, Lehman LG, Luckner D, et al. (1999) Interferon-gamma responses are associated with resistance to reinfection with Plasmodium falciparum in young African children. J Infect Dis 179: 980-988.
35. Taylor-Robinson AW, Phillips RS, (1992) Functional characterization of protective CD4+ T-cell clones reactive to the murine malaria parasite Plasmodium chabaudi. Immunology 77: 99-105.
36. Kern DE, Grabstein KH, Okuno K, Schreiber RD, Greenberg PD, (1989) Identification of a unique T cell-derived lymphokine that primes macrophages for tumor cytotoxicity. J Immunol 143: 4308-4316.
37. Moormann AM, (2009) How might infant and paediatric immune responses influence malaria vaccine efficacy? Parasite Immunol 31: 547-559.
38. Riley EM, Morris-Jones S, Blackman MJ, Greenwood BM, Holder AA, (1993) A longitudinal study of naturally acquired cellular and humoral immune responses to a merozoite surface protein (MSP1) of Plasmodium falciparum in an area of seasonal malaria transmission. Parasite Immunol 15: 513-524.
39. Winkler S, Willheim M, Baier K, Schmid D, Aichelburg A, et al. (1999) Frequency of cytokine-producing T cells in patients of different age groups with Plasmodium falciparum malaria. J Infect Dis 179: 209-216.
40. Achtman AH, Bull PC, Stephens R, Langhorne J, (2005) Longevity of the immune response and memory to blood-stage malaria infection. Curr Top Microbiol Immunol 297: 71-102.
41. Baird JK, (1998) Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. Ann Trop Med Parasitol 92: 367-390.
42. Bouchaud O, Cot M, Kony S, Durand R, Schiemann R, et al. (2005) Do African immigrants living in France have long-term malarial immunity? Am J Trop Med Hyg 72: 21-25.
43. Deloron P, Chougnet C, (1992) Is immunity to malaria really short-lived? Parasitol Today 8: 375-378.
44. Siegrist CA, (2007) The challenges of vaccine responses in early life: selected examples. J Comp Pathol 137 (Suppl 1): S4-9.
45. Willems F, Vollstedt S, Suter M, (2009) Phenotype and function of neonatal DC. Eur J Immunol 39: 26-35.
46. Wang L, Crouch L, Richie TL, Nhan DH, Coppel RL, (2003) Naturally acquired antibody responses to the components of the Plasmodium falciparum merozoite surface protein 1 complex. Parasite Immunol 25: 403-412.
47. Woehlbier U, Epp C, Kauth CW, Lutz R, Long CA, et al. (2006) Analysis of antibodies directed against merozoite surface protein 1 of the human malaria parasite Plasmodium falciparum. Infect Immun 74: 1313-1322.
48. Yazdani SS, Mukherjee P, Chauhan VS, Chitnis CE, (2006) Immune responses to asexual blood-stages of malaria parasites. Curr Mol Med 6: 187-203.
49. Corran P, Coleman P, Riley E, Drakeley C, (2007) Serology: a robust indicator of malaria transmission intensity? Trends Parasitol 23: 575-582.
50. Esser MT, Marchese RD, Kierstead LS, Tussey LG, Wang F, et al. (2003) Memory T cells and vaccines. Vaccine 21: 419-430.
51. Tsuji T, Nibu R, Iwai K, Kanegane H, Yachie A, et al. (1994) Efficient induction of immunoglobulin production in neonatal naive B cells by memory CD4+ T cell subset expressing homing receptor L-selectin. J Immunol 152: 4417-4424.
52. Jangpatarapongsa K, Sirichaisinthop J, Sattabongkot J, Cui L, Montgomery SM, et al. (2006) Memory T cells protect against Plasmodium vivax infection. Microbes Infect 8: 680-686.
53. Precopio ML, Betts MR, Parrino J, Price DA, Gostick E, et al. (2007) Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8(+) T cell responses. J Exp Med 204: 1405-1416.
54. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, et al. (1994) Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg 50: 529-536.
55. Schwarz NG, Adegnika AA, Breitling LP, Gabor J, Agnandji ST, et al. (2008) Placental malaria increases malaria risk in the first 30 months of life. Clin Infect Dis 47: 1017-1025.
56. Singh S, Kennedy MC, Long CA, Saul AJ, Miller LH, et al. (2003) Biochemical and immunological characterization of bacterially expressed and refolded Plasmodium falciparum 42-kilodalton C-terminal merozoite surface protein 1. Infect Immun 71: 6766-6774.
57. Udhayakumar V, Anyona D, Kariuki S, Shi YP, Bloland PB, et al. (1995) Identification of T and B cell epitopes recognized by humans in the C-terminal 42-kDa domain of the Plasmodium falciparum merozoite surface protein (MSP)-1. J Immunol 154: 6022-6030.
58. Miyakoda M, Kimura D, Yuda M, Chinzei Y, Shibata Y, et al. (2008) Malaria-specific and nonspecific activation of CD8+ T cells during blood stage of Plasmodium berghei infection. J Immunol 181: 1420-1428.
59. Noland GS, Hendel-Paterson B, Min XM, Moormann AM, Vulule JM, et al. (2008) Low prevalence of antibodies to preerythrocytic but not blood-stage Plasmodium falciparum antigens in an area of unstable malaria transmission compared to prevalence in an area of stable malaria transmission. Infect Immun 76: 5721-5728.