IgG antibodies to endothelial protein C receptor-binding cysteine-rich interdomain region domains of Plasmodium falciparum erythrocyte membrane protein 1 are acquired early in life in individuals exposed to malaria

Infection and Immunity

Volumn 83, Issue 8, 2015, Pages 3096-3103

  Turner, Louise ^a,b   Lavstsen, Thomas ^a,b   Mmbando, Bruno P ^c   Wang, Christian W ^a,b   Magistrado, Pamela A ^a,b,c,d   Vestergaard, Lasse S ^a,b,e   Ishengoma, Deus S ^c   Minja, Daniel T R ^c   Lusingu, John P ^a,b,c   Theander, Thor G ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b University of Copenhagen   (Denmark)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e WORLD HEALTH ORGANIZATION   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL PROTEIN C RECEPTOR; ERYTHROCYTE MEMBRANE PROTEIN 1; IMMUNOGLOBULIN G ANTIBODY; CELL SURFACE RECEPTOR; ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; IMMUNOGLOBULIN G; LEUKOCYTE ANTIGEN; PROCR PROTEIN, HUMAN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ADOLESCENT; ADULT; AGE DISTRIBUTION; AMINO TERMINAL SEQUENCE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CHILD; CONTROLLED STUDY; CYSTEINE RICH INTERDOMAIN REGION; DISEASE SEVERITY; ENDEMIC DISEASE; HUMAN; INFANT; MALARIA; NEWBORN; NONHUMAN; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SCHOOL CHILD; TANZANIA; CHEMISTRY; FEMALE; GENETICS; IMMUNOLOGY; MALARIA FALCIPARUM; MALE; MIDDLE AGED; PARASITOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIBODIES, PROTOZOAN; ANTIGENS, CD; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMMUNOGLOBULIN G; MALARIA, FALCIPARUM; MALE; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; RECEPTORS, CELL SURFACE; TANZANIA; YOUNG ADULT;

EID: 84937791498     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00271-15     Document Type: Article

References (52)

1. Macdonald G. 1957. The epidemiology and control of malaria. Oxford University Press, London, United Kingdom.
2. Bruce-Chwatt LJ. 1963. A longitudinal survey of natural malaria infection in a group of West African adults. I West Afr Med J 12:141-173.
3. Trape JF, Rogier C, Konate L, Diagne N, Bouganali H, Canque B, Legros F, Badji A, Ndiaye G, Ndiaye P, Brahimi K, Faye O, Druilhe P, Pereira Da Silva L. 1994. The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg 51:123-137.
4. Giha HA, Rosthoj S, Dodoo D, Hviid L, Satti GM, Scheike T, Arnot DE, Theander TG. 2000. The epidemiology of febrile malaria episodes in an area of unstable and seasonal transmission. Trans R Soc Trop Med Hyg 94:645-651. http://dx.doi.org/10.1016/S0035-9203(00)90218-9.
5. 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. http://dx.doi.org/10.1186/1475-2875-3-26.
6. Dodoo D, Staalsoe T, Giha H, Kurtzhals JA, Akanmori BD, Koram K, Dunyo S, Nkrumah FK, Hviid L, Theander TG. 2001. Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infect Immun 69:3713-3718. http://dx.doi.org/10.1128/IAI.69.6.3713-3718.2001.
7. Cohen S, Mc GI, Carrington S. 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192:733-737. http://dx.doi.org/10.1038/192733a0.
8. Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, Chantavanich P, Foucault C, Chongsuphajaisiddhi T, Druilhe P. 1991. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg 45:297-308.
9. Marsh K, Howard RJ. 1986. Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science 231:150-153. http://dx.doi.org/10.1126/science.2417315.
10. Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM. 1989. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg 83:293-303. http://dx.doi.org/10.1016/0035-9203(89)90478-1.
11. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K. 1998. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med 4:358-360. http://dx.doi .org/10.1038/nm0398-358.
12. Giha HA, Staalsoe T, Dodoo D, Roper C, Satti GM, Arnot DE, Hviid L, Theander TG. 2000. Antibodies to variable Plasmodium falciparuminfected erythrocyte surface antigens are associated with protection from novel malaria infections. Immunol Lett 71:117-126. http://dx.doi.org/10.1016/S0165-2478(99)00173-X.
13. Lusingu JP, Jensen AT, Vestergaard LS, Minja DT, Dalgaard MB, Gesase S, Mmbando BP, Kitua AY, Lemnge MM, Cavanagh D, Hviid L, Theander TG. 2006. Levels of plasma immunoglobulin G with specificity against the cysteine-rich interdomain regions of a semiconserved Plasmodium falciparum erythrocyte membrane protein 1, VAR4, predict protection against malarial anemia and febrile episodes. Infect Immun 74:2867-2875. http://dx.doi.org/10.1128/IAI.74.5.2867-2875.2006.
14. Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG. 2003. Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2:27. http://dx.doi.org /10.1186/1475-2875-2-27.
15. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T. 2010. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. PLoS Comput Biol 6:e1000933. http://dx.doi.org/10.1371/journal.pcbi.1000933.
16. Leech JH, Barnwell JW, Miller LH, Howard RJ. 1984. Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J Exp Med 159:1567-1575. http://dx.doi .org/10.1084/jem.159.6.1567.
17. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Taraschi TF, Howard RJ. 1995. Cloning the Plasmodium falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82:77-87. http://dx.doi.org/10.1016/0092-8674(95)90054-3.
18. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101-110. http://dx.doi.org/10.1016/0092-8674(95)90056-X.
19. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82:89-100. http://dx .doi.org/10.1016/0092-8674(95)90055-1.
20. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511. http://dx .doi.org/10.1038/nature01097.
21. Nielsen MA, Staalsoe T, Kurtzhals JA, Goka BQ, Dodoo D, Alifrangis M, Theander TG, Akanmori BD, Hviid L. 2002. Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity. J Immunol 168:3444-3450. http://dx.doi.org/10.4049/jimmunol.168.7.3444.
22. Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C. 1999. Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med 5:340-343. http://dx.doi.org/10.1038/6560.
23. Goncalves BP, Huang CY, Morrison R, Holte S, Kabyemela E, Prevots DR, Fried M, Duffy PE. 2014. Parasite burden and severity of malaria in Tanzanian children. N Engl J Med 370:1799-1808. http://dx.doi.org/10.1056/NEJMoa1303944.
24. Lavstsen T, Turner L, Saguti F, Magistrado P, Rask TS, Jespersen JS, Wang CW, Berger SS, Baraka V, Marquard AM, Seguin-Orlando A, Willerslev E, Gilbert MT, Lusingu J, Theander TG. 2012. Plasmodium falciparum erythrocyte membrane protein 1 domain cassettes 8 and 13 are associated with severe malaria in children. Proc Natl Acad Sci U S A 109:E1791-E1800. http://dx.doi.org/10.1073/pnas.1120455109.
25. Avril M, Brazier AJ, Melcher M, Sampath S, Smith JD. 2013. DC8 and DC13 var genes associated with severe malaria bind avidly to diverse endothelial cells. PLoS Pathog 9:e1003430. http://dx.doi.org/10.1371/journal.ppat.1003430.
26. Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC, Andisi C, Bull PC, Mok S, Gupta AP, Wang CW, Turner L, Arman M, Raza A, Bozdech Z, Rowe JA. 2012. A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. Proc Natl Acad Sci U S A 109:E1772-E1781. http://dx.doi.org/10.1073/pnas .1120461109.
27. Bertin GI, Lavstsen T, Guillonneau F, Doritchamou J, Wang CW, Jespersen JS, Ezimegnon S, Fievet N, Alao MJ, Lalya F, Massougbodji A, Ndam NT, Theander TG, Deloron P. 2013. Expression of the domain cassette 8 Plasmodium falciparum erythrocyte membrane protein 1 is associated with cerebral malaria in Benin. PLoS One 8:e68368. http://dx.doi .org/10.1371/journal.pone.0068368.
28. Turner L, Lavstsen T, Berger SS, Wang CW, Petersen JE, Avril M, Brazier AJ, Freeth J, Jespersen JS, Nielsen MA, Magistrado P, Lusingu J, Smith JD, Higgins MK, Theander TG. 2013. Severe malaria is associated with parasite binding to endothelial protein C receptor. Nature 498:502-505. http://dx.doi.org/10.1038/nature12216.
29. Lau CK, Turner L, Jespersen JS, Lowe ED, Petersen B, Wang CW, Petersen JE, Lusingu J, Theander TG, Lavstsen T, Higgins MK. 2015. Structural conservation despite huge sequence diversity allows EPCR binding by the PfEMP1 family implicated in severe childhood malaria. Cell Host Microbe 17:118 -129. http://dx.doi.org/10.1016/j.chom .2014.11.007.
30. Robinson BA, Welch TL, Smith JD. 2003. Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analyzed across a parasite genome. Mol Microbiol 47:1265-1278. http://dx.doi.org/10.1046/j.1365-2958.2003.03378.x.
31. Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, Theander TG, Nkya WM, Lemnge MM, Riley EM. 2005. Altitudedependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis 191:1589-1598. http://dx.doi .org/10.1086/429669.
32. Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, Lusingu JP. 2010. A progressive declining in the burden of malaria in north-eastern Tanzania. Malar J 9:216. http://dx.doi.org/10.1186/1475-2875-9-216.
33. Cham GK, Kurtis J, Lusingu J, Theander TG, Jensen AT, Turner L. 2008. A semi-automated multiplex high-throughput assay for measuring IgG antibodies against Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) domains in small volumes of plasma. Malar J 7:108. http://dx.doi.org/10.1186/1475-2875-7-108.
34. Smith JD, Rowe JA, Higgins MK, Lavstsen T. 2013. Malaria's deadly grip: cytoadhesion of Plasmodium falciparum-infected erythrocytes. Cell Microbiol 15:1976-1983. http://dx.doi.org/10.1111/cmi.12183.
35. Berger SS, Turner L, Wang CW, Petersen JE, Kraft M, Lusingu JP, Mmbando B, Marquard AM, Bengtsson DB, Hviid L, Nielsen MA, Theander TG, Lavstsen T. 2013. Plasmodium falciparum expressing domain cassette 5 type PfEMP1 (DC5-PfEMP1) bind PECAM1. PLoS One 8:e69117. http://dx.doi.org/10.1371/journal.pone.0069117.
36. Clausen TM, Christoffersen S, Dahlback M, Langkilde AE, Jensen KE, Resende M, Agerbaek MO, Andersen D, Berisha B, Ditlev SB, Pinto VV, Nielsen MA, Theander TG, Larsen S, Salanti A. 2012. Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J Biol Chem 287:23332-23345. http://dx.doi.org/10.1074/jbc.M112.348839.
37. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, Wahlgren M. 1990. Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336:1457-1460. http://dx.doi .org/10.1016/0140-6736(90)93174-N.
38. Fried M, Duffy PE. 1998. Maternal malaria and parasite adhesion. J Mol Med (Berl) 76:162-171. http://dx.doi.org/10.1007/s001090050205.
39. Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, Magistrado P, Jensen AT, Lavstsen T, Ofori MF, Marsh K, Hviid L, Theander TG. 2004. Evidence for the involvement of VAR2CSA in pregnancyassociated malaria. J Exp Med 200:1197-1203. http://dx.doi.org/10.1084/jem.20041579.
40. Vigan-Womas I, Lokossou A, Guillotte M, Juillerat A, Bentley G, Garcia A, Mercereau-Puijalon O, Migot-Nabias F. 2010. The humoral response to Plasmodium falciparum VarO rosetting variant and its association with protection against malaria in Beninese children. Malar J 9:267. http://dx .doi.org/10.1186/1475-2875-9-267.
41. Bengtsson A, Joergensen L, Rask TS, Olsen RW, Andersen MA, Turner L, Theander TG, Hviid L, Higgins MK, Craig A, Brown A, Jensen AT. 2013. A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesioninhibitory antibodies. J Immunol 190:240-249. http://dx.doi.org/10.4049/jimmunol.1202578.
42. Adams Y, Kuhnrae P, Higgins MK, Ghumra A, Rowe JA. 2014. Rosetting Plasmodium falciparum-infected erythrocytes bind to human brain microvascular endothelial cells in vitro, demonstrating a dual adhesion phenotype mediated by distinct P. falciparum erythrocyte membrane protein 1 domains. Infect Immun 82:949-959. http://dx.doi.org/10.1128/IAI .01233-13.
43. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M. 1998. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 17:5418-5426. http://dx.doi.org/10.1093/emboj/17.18.5418.
44. Joergensen L, Bengtsson DC, Bengtsson A, Ronander E, Berger SS, Turner L, Dalgaard MB, Cham GK, Victor ME, Lavstsen T, Theander TG, Arnot DE, Jensen AT. 2010. Surface coexpression of two different PfEMP1 antigens on single Plasmodium falciparum-infected erythrocytes facilitates binding to ICAM1 and PECAM1. PLoS Pathog 6:e1001083. http://dx.doi.org/10.1371/journal.ppat.1001083.
45. Jiang L, Mu J, Zhang Q, Ni T, Srinivasan P, Rayavara K, Yang W, Turner L, Lavstsen T, Theander TG, Peng W, Wei G, Jing Q, Wakabayashi Y, Bansal A, Luo Y, Ribeiro JM, Scherf A, Aravind L, Zhu J, Zhao K, Miller LH. 2013. PfSET vs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499:223-227. http://dx.doi.org/10.1038/nature12361.
46. Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, Lavstsen T. 2009. The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int 58:478-480. http://dx.doi.org/10.1016/j.parint.2009.07.004.
47. Turner L, Wang CW, Lavstsen T, Mwakalinga SB, Sauerwein RW, Hermsen CC, Theander TG. 2011. Antibodies against PfEMP1, RIFIN, MSP3, and GLURP are acquired during controlled Plasmodium falciparum malaria infections in naive volunteers. PLoS One 6:e29025. http://dx .doi.org/10.1371/journal.pone.0029025.
48. Cham GK, Turner L, Lusingu J, Vestergaard L, Mmbando BP, Kurtis JD, Jensen AT, Salanti A, Lavstsen T, Theander TG. 2009. Sequential, ordered acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 domains. J Immunol 183:3356-3363. http://dx.doi .org/10.4049/jimmunol.0901331.
49. Cham GK, Turner L, Kurtis JD, Mutabingwa T, Fried M, Jensen AT, Lavstsen T, Hviid L, Duffy PE, Theander TG. 2010. Hierarchical, domain type-specific acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 in Tanzanian children. Infect Immun 78:4653-4659. http://dx.doi.org/10.1128/IAI.00593-10.
50. Ghumra A, Semblat JP, Ataide R, Kifude C, Adams Y, Claessens A, Anong DN, Bull PC, Fennell C, Arman M, Amambua-Ngwa A, Walther M, Conway DJ, Kassambara L, Doumbo OK, Raza A, Rowe JA. 2012. Induction of strain-transcending antibodies against group A PfEMP1 surface antigens from virulent malaria parasites. PLoS Pathog 8:e1002665. http://dx.doi.org/10.1371/journal.ppat.1002665.
51. Goncalves BP, Fried M, Duffy PE. 2014. Parasite burden and severity of malaria in Tanzanian children. N Engl J Med 371:482. http://dx.doi.org /10.1056/NEJMc1406607.
52. Mayor A, Rovira-Vallbona E, Srivastava A, Sharma SK, Pati SS, Puyol L, Quinto L, Bassat Q, Machevo S, Mandomando I, Chauhan VS, Alonso PL, Chitnis CE. 2009. Functional and immunological characterization of a Duffy binding-like alpha domain from Plasmodium falciparum erythrocyte membrane protein 1 that mediates rosetting. Infect Immun 77:3857-3863. http://dx.doi.org/10.1128/IAI.00049-09.