Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Otsyula N, Angov E, Bergmann-Leitner E, Koech M, Khan F, Bennett J, Otieno L, Cummings J, Andagalu B, Tosh D, Waitumbi J, Richie N, Shi M, Miller L, Otieno W, Otieno GA, Ware L, House B, Godeaux O, Dubois MC, Ogutu B, Ballou WR, Soisson L, Diggs C, Cohen J, Polhemus M, Heppner DG Jr, Ockenhouse CF, Spring MD, 2013. Results from tandem Phase 1 studies evaluating the safety, reactogenicity and immunogenicity of the vaccine candidate antigen Plasmodium falciparum FVO merozoite surface protein-1 (MSP142) administered intramuscularly with adjuvant system AS01. Malar J 12: 29.
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Dent AE, Chelimo K, Sumba PO, Spring MD, Crabb BS, Moormann AM, Tisch DJ, Kazura JW, 2009. Temporal stability of naturally acquired immunity to merozoite surface protein-1 in Kenyan adults. Malar J 8: 162.
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Flanagan KL, Mwangi T, Plebanski M, Odhiambo K, Ross A, Sheu E, Kortok M, Lowe B, Marsh K, Hill AV, 2003. Ex vivo interferon-gamma immune response to thrombospondin-related adhesive protein in coastal Kenyans: longevity and risk of Plasmodium falciparum infection. Am J Trop Med Hyg 68: 421–430.
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Moormann AM, John CC, Sumba PO, Tisch D, Embury P, Kazura JW, 2006. Stability of interferon-gamma and interleukin-10 responses to Plasmodium falciparum liver stage antigen-1 and thrombospondin-related adhesive protein in residents of a malaria holoendemic area. Am J Trop Med Hyg 74: 585–590.
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Moormann AM, Sumba PO, Chelimo K, Fang H, Tisch DJ, Dent AE, John CC, Long CA, Vulule J, Kazura JW, 2013. Humoral and cellular immunity to Plasmodium falciparum merozoite surface protein 1 and protection from infection with blood-stage parasites. J Infect Dis 208: 149–158.
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Wipasa J, Okell L, Sakkhachornphop S, Suphavilai C, Chawansuntati K, Liewsaree W, Hafalla JC, Riley EM, 2011. Short-lived IFN-gamma effector responses, but long-lived IL-10 memory responses, to malaria in an area of low malaria endemicity. PLoS Pathog 7: e1001281.
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Holder AA, 2009. The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria. Parasitology 136: 1445–1456.
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Pusic KM, Hashimoto CN, Lehrer A, Aniya C, Clements DE, Hui GS, 2011. T cell epitope regions of the P. falciparum MSP1-33 critically influence immune responses and in vitro efficacy of MSP1-42 vaccines. PLoS One 6: e24782.
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22.
Moormann AM, Chelimo K, Sumba OP, Lutzke ML, Ploutz-Snyder R, Newton D, Kazura J, Rochford R, 2005. Exposure to holoendemic malaria results in elevated Epstein-Barr virus loads in children. J Infect Dis 191: 1233–1238.
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ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: cross-sectional survey. Am J Trop Med Hyg 68: 100–107.
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Snider CJ, Cole SR, Chelimo K, Sumba PO, Macdonald PD, John CC, Meshnick SR, Moormann AM, 2012. Recurrent Plasmodium falciparum malaria infections in Kenyan children diminish T-cell immunity to Epstein-Barr virus lytic but not latent antigens. PLoS One 7: e31753.
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Piriou E, Kimmel R, Chelimo K, Middeldorp JM, Odada PS, Ploutz-Snyder R, Moormann AM, Rochford R, 2009. Serological evidence for long-term Epstein-Barr virus reactivation in children living in a holoendemic malaria region of Kenya. J Med Virol 81: 1088–1093.
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Singh S, Miura K, Zhou H, Muratova O, Keegan B, Miles A, Martin LB, Saul AJ, Miller LH, Long CA, 2006. Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infect Immun 74: 4573–4580.
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Longevity of Genotype-Specific Immune Responses to Plasmodium falciparum Merozoite Surface Protein 1 in Kenyan Children from Regions of Different Malaria Transmission Intensity
Natalie M. Bowman
Natalie M. Bowman
Division of Infectious Diseases, University of North Carolina, School of Medicine, Chapel Hill, North Carolina.
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Jonathan J. Juliano
Jonathan J. Juliano
Division of Infectious Diseases, University of North Carolina, School of Medicine, Chapel Hill, North Carolina.
Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.
Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina.
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Cynthia J. Snider
Cynthia J. Snider
Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.
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Oksana Kharabora
Oksana Kharabora
Division of Infectious Diseases, University of North Carolina, School of Medicine, Chapel Hill, North Carolina.
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Steven R. Meshnick
Steven R. Meshnick
Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.
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John Vulule
John Vulule
Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya.
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Chandy C. John
Chandy C. John
Ryan White Center for Pediatric Infectious Disease and Global Health, Indiana University, Indianapolis, Indiana.
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Ann M. Moormann
Ann M. Moormann
Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, Massachusetts.
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Naturally acquired immunity to Plasmodium falciparum presents a changing landscape as malaria control programs and vaccine initiatives are implemented. Determining which immunologic indicators remain surrogates of past infection, as opposed to mediators of protection, led us to compare stability of immune responses across regions with divergent malaria transmission intensities. A repeat cross-sectional study of Kenyan children from a malaria-holoendemic area and an epidemic-prone area was used to examine longitudinal antibody and interferon-gamma (IFN-γ) responses to the 3D7 and FVO variants of merozoite surface protein 1 (MSP1). Antibodies to MSP1 were common in both study populations and did not significantly wane over a 21-month time period. IFN-γ responses were less frequent and rapidly disappeared in children after a prolonged period of no malaria transmission. Antibody and IFN-γ responses rarely correlated with each other; however, MSP1-specific IFN-γ response correlated with lack of concurrent P. falciparum parasitemia of the same genotype, though only statistically significantly in the malaria-holoendemic region (odds ratio = 0.31, 95% confidence interval = 0.12–0.84). This study affirms that antimalarial antibodies are informative for evaluation of history of malaria exposure within individuals, whereas cell-mediated immunity, though short lived under natural exposure conditions, might provide an assessment of recent infection and protection from parasitemia.
Author Notes
Financial support: Natalie Bowman was supported by K23 AI113197-01, a Burroughs Wellcome Trust/American Society of Tropical Medicine and Hygiene, and Ruth Kirchner NRSA T32 grant AI715134-13. This work was partially supported by National Institutes of Health grants CTSA UL1RR025747, R01 AI089819, R01 AI43906, and K08 AI51565 (Ann M. Moormann), R01 CA134051 (Ann M. Moormann).
Authors' addresses: Natalie M. Bowman, Jonathan J. Juliano, and Oksana Kharabora, Division of Infectious Diseases, University of North Carolina, School of Medicine, Chapel Hill, NC, E-mails: natalie_bowman@med.unc.edu, jonathan_juliano@med.unc.edu, and oxsana.k@gmail.com. Cynthia J. Snider and Steven R. Meshnick, Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, E-mails: cjsnider@hotmail.com and meshnick@email.unc.edu. John Vulule, Biomedical Sciences, Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya, E-mail: jvulule@gmail.com. Chandy C. John, Ryan White Center for Pediatric Infectious Disease and Global Health, Indiana University, Indianapolis, IN, E-mail: chjohn@iu.edu. Ann M. Moormann, University of Massachusetts Medical School, Worcester, MA, E-mail: ann.moormann@umassmed.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2014. World Malaria Report. Geneva, Switzerland: World Health Organization.
-
2.
Moonen B, Cohen JM, Snow RW, Slutsker L, Drakeley C, Smith DL, Abeyasinghe RR, Rodriguez MH, Maharaj R, Tanner M, Targett G, 2010. Operational strategies to achieve and maintain malaria elimination. Lancet 376: 1592–1603.
-
3.
Riley EM, Stewart VA, 2013. Immune mechanisms in malaria: new insights in vaccine development. Nat Med 19: 168–178.
-
4.
Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J, GeoSentinel Surveillance Network, 2006. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 43: 1185–1193.
-
5.
Pavli A, Maltezou HC, 2010. Malaria and travellers visiting friends and relatives. Travel Med Infect Dis 8: 161–168.
-
6.
Cohen S, Mc GI, Carrington S, 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192: 733–737.
-
7.
Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, Oloo AJ, Hawley W, Lal A, Nahlen B, Campbell CC, 1999. Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission II. Descriptive epidemiology of malaria infection and disease among children. Am J Trop Med Hyg 60: 641–648.
-
8.
Marsh K, Kinyanjui S, 2006. Immune effector mechanisms in malaria. Parasite Immunol 28: 51–60.
-
9.
Fowkes FJ, Richards JS, Simpson JA, Beeson JG, 2010. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Med 7: e1000218.
-
10.
Otsyula N, Angov E, Bergmann-Leitner E, Koech M, Khan F, Bennett J, Otieno L, Cummings J, Andagalu B, Tosh D, Waitumbi J, Richie N, Shi M, Miller L, Otieno W, Otieno GA, Ware L, House B, Godeaux O, Dubois MC, Ogutu B, Ballou WR, Soisson L, Diggs C, Cohen J, Polhemus M, Heppner DG Jr, Ockenhouse CF, Spring MD, 2013. Results from tandem Phase 1 studies evaluating the safety, reactogenicity and immunogenicity of the vaccine candidate antigen Plasmodium falciparum FVO merozoite surface protein-1 (MSP142) administered intramuscularly with adjuvant system AS01. Malar J 12: 29.
-
11.
Dent AE, Chelimo K, Sumba PO, Spring MD, Crabb BS, Moormann AM, Tisch DJ, Kazura JW, 2009. Temporal stability of naturally acquired immunity to merozoite surface protein-1 in Kenyan adults. Malar J 8: 162.
-
12.
Flanagan KL, Mwangi T, Plebanski M, Odhiambo K, Ross A, Sheu E, Kortok M, Lowe B, Marsh K, Hill AV, 2003. Ex vivo interferon-gamma immune response to thrombospondin-related adhesive protein in coastal Kenyans: longevity and risk of Plasmodium falciparum infection. Am J Trop Med Hyg 68: 421–430.
-
13.
Moormann AM, John CC, Sumba PO, Tisch D, Embury P, Kazura JW, 2006. Stability of interferon-gamma and interleukin-10 responses to Plasmodium falciparum liver stage antigen-1 and thrombospondin-related adhesive protein in residents of a malaria holoendemic area. Am J Trop Med Hyg 74: 585–590.
-
14.
Moormann AM, Sumba PO, Chelimo K, Fang H, Tisch DJ, Dent AE, John CC, Long CA, Vulule J, Kazura JW, 2013. Humoral and cellular immunity to Plasmodium falciparum merozoite surface protein 1 and protection from infection with blood-stage parasites. J Infect Dis 208: 149–158.
-
15.
Wipasa J, Okell L, Sakkhachornphop S, Suphavilai C, Chawansuntati K, Liewsaree W, Hafalla JC, Riley EM, 2011. Short-lived IFN-gamma effector responses, but long-lived IL-10 memory responses, to malaria in an area of low malaria endemicity. PLoS Pathog 7: e1001281.
-
16.
Udhayakumar V, Anyona D, Kariuki S, Shi YP, Bloland PB, Branch OH, Weiss W, Nahlen BL, Kaslow DC, Lal AA, 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.
-
17.
Blackman MJ, Ling IT, Nicholls SC, Holder AA, 1991. Proteolytic processing of the Plasmodium falciparum merozoite surface protein-1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Mol Biochem Parasitol 49: 29–33.
-
18.
Holder AA, Lockyer MJ, Odink KG, Sandhu JS, Riveros-Moreno V, Nicholls SC, Hillman Y, Davey LS, Tizard ML, Schwarz RT, Robert RF, 1985. Primary structure of the precursor to the three major surface antigens of Plasmodium falciparum merozoites. Nature 317: 270–273.
-
19.
Egan AF, Chappel JA, Burghaus PA, Morris JS, McBride JS, Holder AA, Kaslow DC, Riley EM, 1995. Serum antibodies from malaria-exposed people recognize conserved epitopes formed by the two epidermal growth factor motifs of MSP119, the carboxy-terminal fragment of the major merozoite surface protein of Plasmodium falciparum. Infect Immun 63: 456–466.
-
20.
Holder AA, 2009. The carboxy-terminus of merozoite surface protein 1: structure, specific antibodies and immunity to malaria. Parasitology 136: 1445–1456.
-
21.
Pusic KM, Hashimoto CN, Lehrer A, Aniya C, Clements DE, Hui GS, 2011. T cell epitope regions of the P. falciparum MSP1-33 critically influence immune responses and in vitro efficacy of MSP1-42 vaccines. PLoS One 6: e24782.
-
22.
Moormann AM, Chelimo K, Sumba OP, Lutzke ML, Ploutz-Snyder R, Newton D, Kazura J, Rochford R, 2005. Exposure to holoendemic malaria results in elevated Epstein-Barr virus loads in children. J Infect Dis 191: 1233–1238.
-
23.
ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: cross-sectional survey. Am J Trop Med Hyg 68: 100–107.
-
24.
Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC, 2006. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J 5: 78.
-
25.
Snider CJ, Cole SR, Chelimo K, Sumba PO, Macdonald PD, John CC, Meshnick SR, Moormann AM, 2012. Recurrent Plasmodium falciparum malaria infections in Kenyan children diminish T-cell immunity to Epstein-Barr virus lytic but not latent antigens. PLoS One 7: e31753.
-
26.
Piriou E, Kimmel R, Chelimo K, Middeldorp JM, Odada PS, Ploutz-Snyder R, Moormann AM, Rochford R, 2009. Serological evidence for long-term Epstein-Barr virus reactivation in children living in a holoendemic malaria region of Kenya. J Med Virol 81: 1088–1093.
-
27.
Singh S, Miura K, Zhou H, Muratova O, Keegan B, Miles A, Martin LB, Saul AJ, Miller LH, Long CA, 2006. Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infect Immun 74: 4573–4580.
-
28.
Spring MD, Chelimo K, Tisch DJ, Sumba PO, Rochford R, Long CA, Kazura JW, Moormann AM, 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.
-
29.
Terrientes ZI, Vergara J, Kramer K, Herrera S, Chang SP, 2005. Restricted genetic diversity of Plasmodium falciparum major merozoite surface protein 1 in isolates from Colombia. Am J Trop Med Hyg 73: 55–61.
-
30.
Badu K, Afrane YA, Larbi J, Stewart VA, Waitumbi J, Angov E, Ong'echa JM, Perkins DJ, Zhou G, Githeko A, Yan G, 2012. Marked variation in MSP-119 antibody responses to malaria in western Kenyan highlands. BMC Infect Dis 12: 50.
-
31.
Supargiyono S, Bretscher MT, Wijayanti MA, Sutanto I, Nugraheni D, Rozqie R, Kosasih AA, Sulistyawati S, Hawley WA, Lobo NF, Cook J, Drakeley CJ, 2013. Seasonal changes in the antibody responses against Plasmodium falciparum merozoite surface antigens in areas of differing malaria endemicity in Indonesia. Malar J 12: 444.
-
32.
White MT, Griffin JT, Akpogheneta O, Conway DJ, Koram KA, Riley EM, Ghani AC, 2014. Dynamics of the antibody response to Plasmodium falciparum infection in African children. J Infect Dis 210: 1115–1122.
-
33.
Sutton PL, Clark EH, Silva C, Branch OH, 2010. The Plasmodium falciparum merozoite surface protein-1 19 KD antibody response in the Peruvian Amazon predominantly targets the non-allele specific, shared sites of this antigen. Malar J 9: 3.
-
34.
Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K, 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349: 1650–1654.
-
35.
Lusingu JP, Vestergaard LS, Mmbando BP, Drakeley CJ, Jones C, Akida J, Savaeli ZX, Kitua AY, Lemnge MM, Theander TG, 2004. Malaria morbidity and immunity among residents of villages with different Plasmodium falciparum transmission intensity in north-eastern Tanzania. Malar J 3: 26.
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