1921
Volume 93, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Large scale antibody responses in malaria remains unexplored in the endemic setting. Protein microarray analysis of asexual-stage was used to identify antigens recognized in sera from residents of hypoendemic Peruvian Amazon. Over 24 months, of 106 participants, 91 had two symptomatic malaria episodes, 11 had three episodes, 3 had four episodes, and 1 had five episodes. relapse was distinguished from reinfection by a merozoite surface protein-3α restriction fragment length polymorphism polymerase chain reaction (MSP3α PCR-RFLP) assay. Notably, reinfection subjects did not have higher reactivity to the entire set of recognized blood-stage antigens than relapse subjects, regardless of the number of malaria episodes. The most highly recognized proteins were MSP 4, 7, 8, and 10 (PVX_003775, PVX_082650, PVX_097625, and PVX_114145); sexual-stage antigen s16 (PVX_000930); early transcribed membrane protein (PVX_090230); tryptophan-rich antigen (Pv-fam-a) (PVX_092995); apical merozoite antigen 1 (PVX_092275); and proteins of unknown function (PVX_081830, PVX_117680, PVX_118705, PVX_121935, PVX_097730, PVX_110935, PVX_115450, and PVX_082475). Genes encoding reactive proteins exhibited a significant enrichment of non-synonymous nucleotide variation, an observation suggesting immune selection. These data identify candidates for seroepidemiological tools to support malaria elimination efforts in -endemic regions.

Loading

Article metrics loading...

The graphs shown below represent data from March 2017
/content/journals/10.4269/ajtmh.15-0232
2015-10-07
2019-03-20
Loading full text...

Full text loading...

/deliver/fulltext/14761645/93/4/801.html?itemId=/content/journals/10.4269/ajtmh.15-0232&mimeType=html&fmt=ahah

References

  1. White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM, , 2014. Malaria. Lancet 383: 723735. [Google Scholar]
  2. Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RG, , 2013. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet 382: 900911. [Google Scholar]
  3. Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA, , 2009. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555566. [Google Scholar]
  4. Alonso PL, Brown G, Arevalo-Herrera M, Binka F, Chitnis C, Collins F, Doumbo OK, Greenwood B, Hall BF, Levine MM, Mendis K, Newman RD, Plowe CV, Rodriguez MH, Sinden R, Slutsker L, Tanner M, , 2011. A research agenda to underpin malaria eradication. PLoS Med 8: e1000406. [Google Scholar]
  5. Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, Patil AP, Tatem AJ, Howes RE, Myers MF, George DB, Horby P, Wertheim HF, Price RN, Mueller I, Baird JK, Hay SI, , 2012. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis 6: e1814. [Google Scholar]
  6. Feachem RG, Phillips AA, Hwang J, Cotter C, Wielgosz B, Greenwood BM, Sabot O, Rodriguez MH, Abeyasinghe RR, Ghebreyesus TA, Snow RW, , 2010. Shrinking the malaria map: progress and prospects. Lancet 376: 15661578. [Google Scholar]
  7. Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, McCarthy J, Vallely A, Drakeley C, , 2010. Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J 9: 169. [Google Scholar]
  8. Tongol-Rivera P, Kano S, Miguel E, Tongol P, Suzuki M, , 1993. Application of seroepidemiology in identification of local foci in a malarious community in Palawan, The Philippines. Am J Trop Med Hyg 49: 608612. [Google Scholar]
  9. Hamlin KL, Moss DM, Priest JW, Roberts J, Kubofcik J, Gass K, Streit TG, Nutman TB, Eberhard ML, Lammie PJ, , 2012. Longitudinal monitoring of the development of antifilarial antibodies and acquisition of Wuchereria bancrofti in a highly endemic area of Haiti. PLoS Negl Trop Dis 6: e1941. [Google Scholar]
  10. Joseph H, Maiava F, Naseri T, Silva U, Lammie P, Melrose W, , 2011. Epidemiological assessment of continuing transmission of lymphatic filariasis in Samoa. Ann Trop Med Parasitol 105: 567578. [Google Scholar]
  11. Noordin R, Muhi J, Md Idris Z, Arifin N, Kiyu A, , 2012. Duration of detection of anti-BmR1 IgG4 antibodies after mass-drug administration (MDA) in Sarawak, Malaysia. Trop Biomed 29: 191196. [Google Scholar]
  12. Nuti M, Ferrari JD, Au AC, , 1982. Seroepidemiology of Bancroftian filariasis in the Seychelles Islands. Tropenmed Parasitol 33: 2527. [Google Scholar]
  13. Steel C, Kubofcik J, Ottesen EA, Nutman TB, , 2012. Antibody to the filarial antigen Wb123 reflects reduced transmission and decreased exposure in children born following single mass drug administration (MDA). PLoS Negl Trop Dis 6: e1940. [Google Scholar]
  14. Tisch DJ, Bockarie MJ, Dimber Z, Kiniboro B, Tarongka N, Hazlett FE, Kastens W, Alpers MP, Kazura JW, , 2008. Mass drug administration trial to eliminate lymphatic filariasis in Papua New Guinea: changes in microfilaremia, filarial antigen, and Bm14 antibody after cessation. Am J Trop Med Hyg 78: 289293. [Google Scholar]
  15. Arnold BF, Priest JW, Hamlin KL, Moss DM, Colford JM, Jr Lammie PJ, , 2014. Serological measures of malaria transmission in Haiti: comparison of longitudinal and cross-sectional methods. PLoS One 9: e93684. [Google Scholar]
  16. Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, Lemmens K, Theisen M, Soares IS, D'Alessandro U, Coosemans M, Erhart A, , 2012. Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J 11: 86. [Google Scholar]
  17. De Carvalho ME, Ferreira MU, De Souza MR, Ninomia RT, Matos GF, Camargo LM, Ferreira CS, , 1992. Malaria seroepidemiology: comparison between indirect fluorescent antibody test and enzyme immunoassay using bloodspot eluates. Mem Inst Oswaldo Cruz 87: 205208. [Google Scholar]
  18. 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. [Google Scholar]
  19. Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, Masika P, Mosha J, Bousema T, Shekalaghe S, Cook J, Corran P, Ghani A, Riley EM, Drakeley C, , 2009. Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS One 4: e6083. [Google Scholar]
  20. Warren M, Collins WE, Jeffery GM, Skinner JC, , 1983. The seroepidemiology of malaria in middle America. V. Antibody responses in an indicator population from an endemic area with attack phase antimalaria activities. Am J Trop Med Hyg 32: 12091215. [Google Scholar]
  21. Lu F, Li J, Wang B, Cheng Y, Kong DH, Cui L, Ha KS, Sattabongkot J, Tsuboi T, Han ET, , 2014. Profiling the humoral immune responses to Plasmodium vivax infection and identification of candidate immunogenic rhoptry-associated membrane antigen (RAMA). J Proteomics 102C: 6682. [Google Scholar]
  22. Finney OC, Danziger SA, Molina DM, Vignali M, Takagi A, Ji M, Stanisic DI, Siba PM, Liang X, Aitchison JD, Mueller I, Gardner MJ, Wang R, , 2014. Predicting antidisease immunity using proteome arrays and sera from children naturally exposed to malaria. Mol Cell Proteomics 13: 26462660. [Google Scholar]
  23. Bozdech Z, Mok S, Hu G, Imwong M, Jaidee A, Russell B, Ginsburg H, Nosten F, Day NP, White NJ, Carlton JM, Preiser PR, , 2008. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc Natl Acad Sci USA 105: 1629016295. [Google Scholar]
  24. Westenberger SJ, McClean CM, Chattopadhyay R, Dharia NV, Carlton JM, Barnwell JW, Collins WE, Hoffman SL, Zhou Y, Vinetz JM, Winzeler EA, , 2010. A systems-based analysis of Plasmodium vivax lifecycle transcription from human to mosquito. PLoS Negl Trop Dis 4: e653. [Google Scholar]
  25. Molina DM, Finney OC, Arevalo-Herrera M, Herrera S, Felgner PL, Gardner MJ, Liang X, Wang R, , 2012. Plasmodium vivax pre-erythrocytic-stage antigen discovery: exploiting naturally acquired humoral responses. Am J Trop Med Hyg 87: 460469. [Google Scholar]
  26. 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: 46804694. [Google Scholar]
  27. 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: 69586963. [Google Scholar]
  28. Chuquiyauri R, Penataro P, Brouwer KC, Fasabi M, Calderon M, Torres S, Gilman RH, Kosek M, Vinetz JM, , 2013. Microgeographical differences of Plasmodium vivax relapse and re-infection in the Peruvian Amazon. Am J Trop Med Hyg 89: 326338. [Google Scholar]
  29. Kosek M, Yori PP, Gilman RH, Calderon M, Zimic M, Chuquiyauri R, Jeri C, Pinedo-Cancino V, Matthias MA, Llanos-Cuentas A, Vinetz JM, , 2012. High degree of Plasmodium vivax diversity in the Peruvian Amazon demonstrated by tandem repeat polymorphism analysis. Am J Trop Med Hyg 86: 580586. [Google Scholar]
  30. Roshanravan B, Kari E, Gilman RH, Cabrera L, Lee E, Metcalfe J, Calderon M, Lescano AG, Montenegro-James S, Calampa C, Vinetz JM, , 2003. Endemic malaria in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 69: 4552. [Google Scholar]
  31. Cui L, Mascorro CN, Fan Q, Rzomp KA, Khuntirat B, Zhou G, Chen H, Yan G, Sattabongkot J, , 2003. Genetic diversity and multiple infections of Plasmodium vivax malaria in western Thailand. Am J Trop Med Hyg 68: 613619. [Google Scholar]
  32. Chuquiyauri R, Paredes M, Penataro P, Torres S, Marin S, Tenorio A, Brouwer KC, Abeles S, Llanos-Cuentas A, Gilman RH, Kosek M, Vinetz JM, , 2011. Socio-demographics and the development of malaria elimination strategies in the low transmission setting. Acta Trop 121: 292302. [Google Scholar]
  33. Cui L, Mascorro CN, Fan Q, Rzomp KA, Jhuntirat B, Zhou G, Chen H, Yan G, Sattabongkot J, , 2003. Genetic diversity and multiple infections of Plasmodium vivax malaria in western Thailand. Am J Trop Med Hyg 68: 613619. [Google Scholar]
  34. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoeckert CJ, Jr Treatman C, Wang H, , 2009. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 37: D539D543. [Google Scholar]
  35. Nielsen H, Brunak S, von Heijne G, , 1999. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng 12: 39. [Google Scholar]
  36. Molina D, Finney OC, Aravelo-Herrera M, Herrera S, Felgner PL, Gardner MJ, Liang X, Wang R, , 2012. Plasmodium vivax pre-erythrocytic-stage antigen discovery: exploiting naturally acquired humoral responses. Am J Trop Med Hyg 87: 460469. [Google Scholar]
  37. Van den Eede P, Soto-Calle VE, Delgado C, Gamboa D, Grande T, Rodriguez H, Llanos-Cuentas A, Anne J, D'Alessandro U, Erhart A, , 2011. Plasmodium vivax sub-patent infections after radical treatment are common in Peruvian patients: results of a 1-year prospective cohort study. PLoS One 6: e16257. [Google Scholar]
  38. Crompton PD, Moebius J, Portugal S, Waisberg M, Hart G, Garver LS, Miller LH, Barillas C, Pierce SK, , 2014. Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annu Rev Immunol 32: 157187. [Google Scholar]
  39. Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, Nandy A, Guthmann JP, Nosten F, Carlton J, Looareesuwan S, Nair S, Sudimack D, Day NP, Anderson TJ, White NJ, , 2007. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis 195: 927933. [Google Scholar]
  40. Chen N, Auliff A, Rieckmann K, Gatton M, Cheng Q, , 2007. Relapses of Plasmodium vivax infection result from clonal hypnozoites activated at predetermined intervals. J Infect Dis 195: 934941. [Google Scholar]
  41. Perez-Leal O, Sierra AY, Barrero CA, Moncada C, Martinez P, Cortes J, Lopez Y, Salazar LM, Hoebeke J, Patarroyo MA, , 2005. Identifying and characterising the Plasmodium falciparum merozoite surface protein 10 Plasmodium vivax homologue. Biochem Biophys Res Commun 331: 11781184. [Google Scholar]
  42. Cheng Y, Wang B, Sattabongkot J, Lim CS, Tsuboi T, Han ET, , 2014. Immunogenicity and antigenicity of Plasmodium vivax merozoite surface protein 10. Parasitol Res 113: 25592568. [Google Scholar]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.15-0232
Loading
/content/journals/10.4269/ajtmh.15-0232
Loading

Data & Media loading...

Supplementary Table 1

Supplementary Table 2

  • Received : 24 Mar 2015
  • Accepted : 13 May 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error