Seroreactivity to a Large Panel of Field-Derived Plasmodium falciparum Apical Membrane Antigen 1 and Merozoite Surface Protein 1 Variants Reflects Seasonal and Lifetime Acquired Responses to Malaria

Jason A. Bailey Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Jason A. Bailey in
Current site
Google Scholar
PubMed Close
,
Jozelyn Pablo Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Jozelyn Pablo in
Current site
Google Scholar
PubMed Close
,
Amadou Niangaly Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Amadou Niangaly in
Current site
Google Scholar
PubMed Close
,
Mark A. Travassos Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Mark A. Travassos in
Current site
Google Scholar
PubMed Close
,
Amed Ouattara Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Amed Ouattara in
Current site
Google Scholar
PubMed Close
,
Drissa Coulibaly Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Drissa Coulibaly in
Current site
Google Scholar
PubMed Close
,
Matthew B. Laurens Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Matthew B. Laurens in
Current site
Google Scholar
PubMed Close
,
Shannon L. Takala-Harrison Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Shannon L. Takala-Harrison in
Current site
Google Scholar
PubMed Close
,
Kirsten E. Lyke Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Kirsten E. Lyke in
Current site
Google Scholar
PubMed Close
,
Jeff Skinner Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Jeff Skinner in
Current site
Google Scholar
PubMed Close
,
Andrea A. Berry Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Andrea A. Berry in
Current site
Google Scholar
PubMed Close
,
Algis Jasinskas Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Algis Jasinskas in
Current site
Google Scholar
PubMed Close
,
Rie Nakajima-Sasaki Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Rie Nakajima-Sasaki in
Current site
Google Scholar
PubMed Close
,
Bourema Kouriba Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Bourema Kouriba in
Current site
Google Scholar
PubMed Close
,
Mahamadou A. Thera Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Mahamadou A. Thera in
Current site
Google Scholar
PubMed Close
,
Philip L. Felgner Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Philip L. Felgner in
Current site
Google Scholar
PubMed Close
,
Ogobara K. Doumbo Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Ogobara K. Doumbo in
Current site
Google Scholar
PubMed Close
, and
Christopher V. Plowe Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Infectious Diseases, Department of Medicine, University of California, Irvine, California; Laboratory of Immunogenetics, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, Department of Epidemiology of Parasitic Diseases, University of Sciences, Techniques and Technology, Bamako, Mali

Search for other papers by Christopher V. Plowe in
Current site
Google Scholar
PubMed Close
DOI:
https://doi.org/10.4269/ajtmh.14-0140
Volume/Issue:
Volume 92: Issue 1
Page(s):
9–12
Restricted access
Get Permissions

Parasite antigen diversity poses an obstacle to developing an effective malaria vaccine. A protein microarray containing Plasmodium falciparum apical membrane antigen 1 (AMA1, n = 57) and merozoite surface protein 1 19-kD (MSP119, n = 10) variants prevalent at a malaria vaccine testing site in Bandiagara, Mali, was used to assess changes in seroreactivity caused by seasonal and lifetime exposure to malaria. Malian adults had significantly higher magnitude and breadth of seroreactivity to variants of both antigens than did Malian children. Seroreactivity increased over the course of the malaria season in children and adults, but the difference was more dramatic in children. These results help to validate diversity-covering protein microarrays as a promising tool for measuring the breadth of antibody responses to highly variant proteins, and demonstrate the potential of this new tool to help guide the development of malaria vaccines with strain-transcending efficacy.

Author Notes

* Address correspondence to Christopher V. Plowe, Howard Hughes Medical Institute/Center for Vaccine Development, University of Maryland School of Medicine, 685 West Baltimore Street, HSF1 480, Baltimore, MD 21201. E-mail: cplowe@medicine.umaryland.edu

Authors' addresses: Jason A. Bailey, Mark A. Travassos, Amed Ouattara, Matthew B. Laurens, Shannon L. Takala-Harrison, Kirsten E. Lyke, and Christopher V. Plowe, Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, MD, E-mails: jbail006@umaryland.edu, aouattara@medicine.umaryland.edu, mlaurens@medicine.umaryland.edu, stakala@medicine.umaryland.edu, klyke@medicine.umaryland.edu, and cplowe@medicine.umaryland.edu. Jozelyn Pablo, Algis Jasinskas, Rie Nakajima-Sasaki, and Philip L. Felgner, Division of Infectious Diseases, University of California, Irvine, CA, E-mails: jozelynp@gmail.com, ajasinsk@uci.edu, and rie3@uci.edu. Amadou Niangaly, Drissa Coulibaly, and Mahamadou A. Thera, Faculty of Medicine, Malaria Research and Training Center Bamako, University of Bamako, Bamako, Mali, and Malaria Research and Training Center, Mali University of Science, Techniques, and Technology of Bamako, Bamako, Mali, E-mails: niangaly@icermali.org, coulibalyd@icermali.org, and mthera@icermali.org. Jeff Skinner, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health Rockville, MD, E-mail: skinnerj@niaid.nih.gov. Bourema Kouriba and Ogobara K. Doumbo, Malaria Research and Training Center, University of Science, Techniques, and Technology of Bamako, Bamako, Mali, E-mails: kouriba@icermali.org and okd@icermali.org.

Copyright:
© The American Society of Tropical Medicine and Hygiene 2015
Received:
07 Mar 2014
|
Accepted:
26 Jul 2014
|
Published Online:
07 Jan 2015
Cover The American Journal of Tropical Medicine and Hygiene
The American Journal of Tropical Medicine and Hygiene
Print ISSN:
0002-9637
Online ISSN:
1476-1645
  • 1.

    Ouattara A, Mu J, Takala-Harrison S, Saye R, Sagara I, Dicko A, Niangaly A, Duan J, Ellis RD, Miller LH, Su XZ, Plowe CV, Doumbo OK, 2010. Lack of allele-specific efficacy of a bivalent AMA1 malaria vaccine. Malar J 9: 175.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Takala SL, Plowe CV, 2009. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunol 31: 560–573.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Hviid L, 2005. Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop 95: 270–275.

  • 4.

    Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, Kone AK, Guindo AB, Traore K, Traore I, Kouriba B, Diallo DA, Diarra I, Daou M, Dolo A, Tolo Y, Sissoko MS, Niangaly A, Sissoko M, Takala-Harrison S, Lyke KE, Wu Y, Blackwelder WC, Godeaux O, Vekemans J, Dubois MC, Ballou WR, Cohen J, Thompson D, Dube T, Soisson L, Diggs CL, House B, Lanar DE, Dutta S, Heppner DG Jr, Plowe CV, 2011. A field trial to assess a blood-stage malaria vaccine. N Engl J Med 365: 1004–1013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Sagara I, Dicko A, Ellis RD, Fay MP, Diawara SI, Assadou MH, Sissoko MS, Kone M, Diallo AI, Saye R, Guindo MA, Kante O, Niambele MB, Miura K, Mullen GE, Pierce M, Martin LB, Dolo A, Diallo DA, Doumbo OK, Miller LH, Saul A, 2009. A randomized controlled phase 2 trial of the blood stage AMA1-C1/Alhydrogel malaria vaccine in children in Mali. Vaccine 27: 3090–3098.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Thera MA, Doumbo OK, Coulibaly D, Diallo DA, Kone AK, Guindo AB, Traore K, Dicko A, Sagara I, Sissoko MS, Baby M, Sissoko M, Diarra I, Niangaly A, Dolo A, Daou M, Diawara SI, Heppner DG, Stewart VA, Angov E, Bergmann-Leitner ES, Lanar DE, Dutta S, Soisson L, Diggs CL, Leach A, Owusu A, Dubois MC, Cohen J, Nixon JN, Gregson A, Takala SL, Lyke KE, Plowe CV, 2008. Safety and immunogenicity of an AMA-1 malaria vaccine in Malian adults: results of a phase 1 randomized control trial. PLoS One 3: e1465.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Takala SL, Coulibaly D, Thera MA, Dicko A, Smith DL, Guindo AB, Kone AK, Traore K, Ouattara A, Djimde AA, Sehdev PS, Lyke KE, Diallo DA, Doumbo OK, Plowe CV, 2007. Dynamics of polymorphism in a malaria vaccine antigen at a vaccine-testing site in Mali. PLoS One 4: e93.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, Escalante AA, Ouattara A, Traore K, Niangaly A, Djimde AA, Doumbo OK, Plowe CV, 2009. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med 2: 2ra5.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Ouattara A, Takala-Harrison S, Thera MA, Coulibaly D, Niangaly A, Saye R, Tolo Y, Dutta S, Heppner DG, Soisson L, Diggs CL, Vekemans J, Cohen J, Blackwelder WC, Dube T, Laurens MB, Doumbo OK, Plowe CV, 2013. Molecular basis of allele-specific efficacy of a blood-stage malaria vaccine: vaccine development implications. J Infect Dis 207: 511–519.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Doolan DL, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C, Randall A, Molina D, Liang X, Freilich DA, Oloo JA, Blair PL, Aguiar JC, Baldi P, Davies DH, Felgner PL, 2008. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics 8: 4680–4694.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Barry AE, Trieu A, Fowkes FJ, Pablo J, Kalantari-Dehaghi M, Jasinskas A, Tan X, Kayala MA, Tavul L, Siba PM, Day KP, Baldi P, Felgner PL, Doolan DL, 2011. The stability and complexity of antibody responses to the major surface antigen of Plasmodium falciparum are associated with age in a malaria endemic area. Mol Cell Proteomics 10: M111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Crompton PD, Kayala MA, Traore B, Kayentao K, Ongoiba A, Weiss GE, Molina DM, Burk CR, Waisberg M, Jasinskas A, Tan X, Doumbo S, Doumtabe D, Kone Y, Narum DL, Liang X, Doumbo OK, Miller LH, Doolan DL, Baldi P, Felgner PL, Pierce SK, 2010. A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proc Natl Acad Sci USA 107: 6958–6963.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Trieu A, Kayala MA, Burk C, Molina DM, Freilich DA, Richie TL, Baldi P, Felgner PL, Doolan DL, 2011. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol Cell Proteomics 10: M111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Baum E, Badu K, Molina DM, Liang X, Felgner PL, Yan G, 2013. Protein microarray analysis of antibody responses to Plasmodium falciparum in western Kenyan highland sites with different transmission levels. PLoS One 8: e82246.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Ouattara A, Takala-Harrison S, Thera MA, Coulibaly D, Niangaly A, Saye R, Tolo Y, Dutta S, Heppner DG, Soisson L, Diggs CL, Vekemans J, Cohen J, Blackwelder WC, Dube T, Laurens MB, Doumbo OK, Plowe CV, 2013. Molecular basis of allele-specific efficacy of a blood-stage malaria vaccine: vaccine development implications. J Infect Dis 207: 511–519.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Takala SL, Smith DL, Thera MA, Coulibaly D, Doumbo OK, Plowe CV, 2007. Short report: rare Plasmodium falciparum merozoite surface protein 1 19-kda (msp-1(19)) haplotypes identified in Mali using high-throughput genotyping methods. Am J Trop Med Hyg 76: 855–859.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Davies DH, Liang X, Hernandez JE, Randall A, Hirst S, Mu Y, Romero KM, Nguyen TT, Kalantari-Dehaghi M, Crotty S, Baldi P, Villarreal LP, Felgner PL, 2005. Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci USA 102: 547–552.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Thera MA, Doumbo OK, Coulibaly D, Diallo DA, Sagara I, Dicko A, Diemert DJ, Heppner DG Jr., Stewart VA, Angov E, Soisson L, Leach A, Tucker K, Lyke KE, Plowe CV, 2006. Safety and allele-specific immunogenicity in Malian adults: results of a phase I randomized trial. PLoS Clin Trials 1: e34.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Kone AK, Guindo AB, Traore K, Sissoko M, Diallo DA, Diarra I, Kouriba B, Daou M, Dolo A, Baby M, Sissoko MS, Sagara I, Niangaly A, Traore I, Olotu A, Godeaux O, Leach A, Dubois MC, Ballou WR, Cohen J, Thompson D, Dube T, Soisson L, Diggs CL, Takala SL, Lyke KE, House B, Lanar DE, Dutta S, Heppner DG, Plowe CV, 2010. Safety and immunogenicity of an AMA-1 malaria vaccine in Malian adults: results of a phase 1 randomized control trial. PLoS One 5: e9041.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Sboner A, Karpikov A, Chen G, Smith M, Mattoon D, Freeman-Cook L, Schweitzer B, Gerstein MB, 2009. Robust-linear-model normalization to reduce technical variability in functional protein microarrays. J Proteome Res 8: 5451–5464.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Vafa M, Troye-Blomberg M, Anchang J, Garcia A, Migot-Nabias F, 2008. Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malar J 7: 17.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 2056 1795 216
Full Text Views 336 17 4
PDF Downloads 102 16 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save