Pregnancy and malaria exposure are associated with changes in the B cell pool and in plasma eotaxin levels

Journal of Immunology

Volumn 193, Issue 6, 2014, Pages 2971-2983

  Requena, Pilar ^a,j   Campo, Joseph J ^a   Umbers, Alexandra J ^b   Ome, Maria ^c   Wangnapi, Regina ^c   Barrios, Diana ^a   Robinson, Leanne J ^c,d   Samol, Paula ^c   Rosanas Urgell, Anna ^c,i   Ubillos, Itziar ^a   Mayor, Alfredo ^a   López, Marta ^e   De Lazzari, Elisa ^a   Arévalo Herrera, Myriam ^f   Fernández Becerra, Carmen ^a   Del Portillo, Hernando ^a,g   Chitnis, Chetan E ^h   Siba, Peter M ^c   Bardají, Azucena ^a   Mueller, Ivo ^d   Rogerson, Stephen ^b   Menéndez, Clara ^a   Dobaño, Carlota ^a   more..

^a HOSPITAL CLÍNIC   (Spain)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^f Caucaseco Scientific Research Center   (Colombia)

^g INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^h INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

ⁱ INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^j LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD19 ANTIGEN; CD27 ANTIGEN; CD38 ANTIGEN; CD71 ANTIGEN; CHEMOKINE RECEPTOR CCR3; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; MACROPHAGE MIGRATION INHIBITION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; SCATTER FACTOR; TUMOR NECROSIS FACTOR; VASCULOTROPIN; CCL11 PROTEIN, HUMAN; CCR3 PROTEIN, HUMAN; IL8 PROTEIN, HUMAN; IMMUNOGLOBULIN D; INTERLEUKIN 8; PARASITE ANTIGEN; PROTOZOON ANTIBODY;

ADULT; ARTICLE; B LYMPHOCYTE; CELL COUNT; CELL POPULATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE ASSOCIATION; FEMALE; GESTATIONAL AGE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOGLOBULIN BLOOD LEVEL; MALARIA; MALARIA FALCIPARUM; MEMORY CELL; PAPUA NEW GUINEA; PHENOTYPE; PREGNANCY; RADIATION EXPOSURE; SPAIN; BIOSYNTHESIS; BLOOD; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE COUNT; PARASITOLOGY; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX;

ADULT; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; B-LYMPHOCYTE SUBSETS; CHEMOKINE CCL11; FEMALE; HUMANS; IMMUNOGLOBULIN D; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; INTERLEUKIN-8; LYMPHOCYTE COUNT; MALARIA; PAPUA NEW GUINEA; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PREGNANCY; RECEPTORS, CCR3; SPAIN;

EID: 84907087675     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401037     Document Type: Article

References (62)

1. WHO. 2011. Global estimates of malaria cases and deaths 2000- 2009. In World Malaria Report 2011. World Health Organization, Geneva, Switzerland. p. 73-75
2. Pierce, S. K., and L. H. Miller. 2009. World Malaria Day 2009: what malaria knows about the immune system that immunologists still do not. J. Immunol. 182: 5171-5177
3. Greenwood, B. M., A. M. Greenwood, R. W. Snow, P. Byass, S. Bennett, and A. B. Hatib-N'Jie. 1989. The effects of malaria chemoprophylaxis given by traditional birth attendants on the course and outcome of pregnancy. Trans. R. Soc. Trop. Med. Hyg. 83: 589-594
4. Brabin, B. 19 91. An assessment of low birthweight risk in primiparae as an indicator of malaria control in pregnancy. Int. J. Epidemiol. 20: 276-283
5. Menendez, C., J. Ordi, M. R. Ismail, P. J. Ventura, J. J. Aponte, E. Kahigwa, F. Font, and P. L. Alonso. 2000. The impact of placental malaria on gestational age and birth weight. J. Infect. Dis. 181: 1740-1745
6. Granja, A. C., F. Machungo, A. Gomes, S. Bergström, and B. Brabin. 1998. Malaria-related maternal mortality in urban Mozambique. Ann. Trop. Med. Parasitol. 92: 257-263
7. Romagosa, C., J. Ordi, F. Saute, L. Quintó, F. Machungo, M. R. Ismail, C. Carrilho, N. Osman, P. L. Alonso, and C. Menendez. 2007. Seasonal variations in maternal mortality in Maputo, Mozambique: the role of malaria. Trop. Med. Int. Health 12: 62-67
8. Bardají , A., B. Sigauque, S. Sanz, M. Maixenchs, J. Ordi, J. J. Aponte, S. Mabunda, P. L. Alonso, and C. Menéndez. 2011. Impact of malaria at the end of pregnancy on infant mortality and morbidity. J. Infec t. Dis. 203: 691-699
9. Mathad, J. S., and A. Gupta. 2012. Tuberculosis in pregnant and postpartum women: epidemiology, management, and research gaps. Clin. Infect. Dis. 55: 1532-1549
10. Rasmussen, S. A., D. J. Jamieson, and T. M. Uyeki. 2012. Effects of influenza on pregnant women and infants. Am. J. Obstet. Gynecol. 207:S3-S8
11. Salanti, A., M. Dahlbä ck, L. Turn er, M. A. Nielsen, L. Barfod, P. Magistrado, A. T. Jensen, T. Lavstsen, M. F. Ofori, K. Marsh, et al. 2004. Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J. Exp. Med. 200: 119 7-1203
12. Mayor, A., E. Rovira-Vallbona, S. Machevo, Q. Bassat, R. Aguilar, L. Quintó, A. Jiménez, B. Sigauque, C. Doban? o, S. Kumar, et al. 2011. Parity and placental infection affect antibody responses against Plasmodium falciparum during pregnancy. Infect. Immun. 79: 1654-1659
13. O'Neil-Dunne, I., R. N. Achur, S. T . Agbor-Enoh, M. Valiyaveettil, R. S. Naik, C. F. Ockenhouse, A. Zhou, R. Megnekou, R. Leke, D. W. Taylor, and D. C. Gowda. 2001. Gravidity-dependent production of antibodies that inhibit binding of Plasmodium falci parum-infected erythrocytes to placental chondroitin sulfate proteoglycan during pregnancy. Infect. Immun. 69: 7487-7492
14. Ricke, C. H., T. Staalsoe, K. Koram, B. D. Akanmori, E. M. Riley, T. G. T heander, and L. Hviid. 2000. Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparuminfected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A. J. I mmunol. 165: 3309-3316
15. Ibitokou, S., M. Oesterholt, L. Brutus, S. Borgella, C. Agbowaï, S. Ezinmègnon, J. Lusingu, C. Schmiegelow, A. Massougbodji, P. Deloron, et al. 2012. Peripheral blood cell signatures of Plasmodium falciparum infection during pregnancy. PLoS One 7: e49621
16. Ampomah, P., L. Stevenson, M. F. Ofori, L. Barfod, and L. Hviid. 2014. Kinetics of B cell responses to Pla smodium falciparum erythrocyte membrane protein 1 in Ghanaian women naturally exposed to malaria parasites. J. Immunol. 192: 5236-5244
17. Caraux, A., B. Klein, B. Paiva, C. Bret, A. Schmitz, G. M. Fuhler, N. A. Bos, H. E. Johnsen, A. Orfao, and M. Perez-Andres, Myeloma Stem Cell Network. 2010. Circulating human B and plasma cells: age-associated changes in counts and detailed characterization of circulating normal CD1382 and CD138+ plasma cells. Haematologica 95: 1016-1020.
18. Morbach H.,E.M. Eichhorn,J. G. Liese,H. J, Girschick, 2010. Reference values forBcell subpopulations from infancy to adulthood. Clin.Exp. Immunol, 162, 271-279.
19. Fecteau, J. F., G. Cô té, and S. Néron. 2006. A new memory CD27-IgG+ B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J. Immunol. 177: 3728-3736
20. Moir, S., J. Ho, A. Malaspina, W. Wang, A. C. DiPoto, M. A. O'Shea, G. Roby, S. Kottilil, J. Arthos, M. A. Proschan, et al. 2008. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIVinfected viremic individuals. J. Exp. Med. 205: 1797-1805.
21. Weiss, G. E., P. D. Crompton, S. Li, L. A. Walsh, S. Moir, B. Traore, K. Kayentao, A. Ongoiba, O. K. Doumbo, and S. K. Pierce. 2009. Atypical memory B cells are greatly expanded in individ uals living in a malaria-endemic area. J. Immunol. 183: 2176-2182
22. Weiss, G. E., E. H. Clark, S. Li, B. Traore, K. Kayentao, A. Ongoiba, J. N. Hernandez, O. K. Doumbo, S. K. Pierce, O. H. Branch, and P. D. Crompton. 2011. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS One 6: e15983
23. Illingworth, J., N. S. Butler, S. Roetynck, J. Mwacharo, S. K. Pierce, P. Bejon, P. D. Crompton, K. Marsh, and F. M. Ndungu. 2013. Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J. Immunol. 190: 1038-1047
24. Scholzen, A., A. C. Teirlinck, E. M. Bijker, M. Roestenberg, C. C. Hermsen, S. L. Hoffman, and R. W. Sauerwein. 2014. BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection. J. Immunol. 192: 3719-3729
25. Portugal, S., D. Doumtabe, B. Traore, L. H. Miller, M. Troye-Blomberg, O. K. Doumbo, A. Dolo, S. K. Pierce, and P. D. Crompton. 2012. B cell analysis of ethnic groups in Mali with differential susceptibility to malaria. Malar. J. 11: 162
26. Muelle nbeck, M. F., B. Ueberheide, B. Amulic, A. Epp, D. Fenyo, C. E. Busse, M. Esen, M. Theisen, B. Mordmüller, and H. Wardemann. 2013. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing an tibodies. J. Exp. Med. 210: 389-399
27. Wipasa, J., C. Suphavilai, L. C. Okell, J. Cook, P. H. Corran, K. Thaikla, W. Liewsaree, E. M. Riley, and J. C. R. Hafalla. 2010. Long-l ived antibody and B cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathog. 6: e1000770
28. Ndungu, F. M., A. Olotu, J. Mwacharo, M. Nyonda, J. Apfeld, L. K. Mramba, G. W. Fegan, P. Bejon, and K. Marsh. 2012. Memory B cells are a more reliable archive for historical antimalarial responses than plasma antibodies in no-longer exposed children. Proc. Natl. Acad. Sci. USA 109: 8247-8252
29. Asito, A. S., E. Piriou, W. G. Z. O. Jura, C. Ouma, P. S. Odada, S. Ogola, N. Fiore, and R. Rochford. 2011. Suppression of circulating IgD+CD27+ memory B cells in infants living in a malaria-endemic region of Kenya. Malar. J. 10: 362
30. Kruetzmann, S., M. M. Rosado, H.Weber, U. Germing, O. Tournilhac, H.-H. Peter, R. Berner, A. Peters, T. Boehm, A. Plebani, et al. 2003. Human immunoglobulinM memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J. Exp. Med. 197: 939-945
31. Muzzio, D., A. C. Zenclussen, and F. Jensen. 2013. The role of B cells in pregnancy: the good and the bad. Am. J. Reprod. Immunol. 69: 408-412
32. Rijken, M. J., R. McGready, M. E. Boel, R. Poespoprodjo, N. Singh, D. Syafruddin, S. Rogerson, and F. Nosten. 2012. Malaria in pregnancy in the Asia-Pacific region. Lancet Infect. Dis. 12: 75-88
33. Sanz, I., C. Wei, F. E.-H. Lee, and J. Anolik. 2008. Phenotypic and functional heterogeneity of human memory B cells. Semin. Immunol. 20: 67-82
34. Mazumdar, S., S. Sachdeva, V. S. Chauhan, and S. S. Yazdani. 2010. Identification of cultivation condition to prod uce correctly folded form of a malaria vaccine based on Plasmodium falciparum merozoite surface protein-1 in Escherichia coli. Bioprocess Biosyst. Eng. 33: 719-730
35. Kocken, C. H. M., C. Withers-Martinez, M. A. Dubbeld, A. van der Wel, F. Hackett, A. Valderrama, M. J. Blackman, and A.W. Thomas. 2002. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodi es that inhibit erythrocyte invasion. Infect. Immun. 70: 4471-4476
36. Pandey, K. C., S. Singh, P. Pattnaik, C. R. Pillai, U. Pillai, A. Lynn, S. K. Jain, and C. E. Chitnis. 2002. Bacterially expressed and refolded receptor binding domain of Plasmodium falciparum EBA-175 elicits invasion inhibitory antibodies. Mol. Biochem. Parasitol. 123: 23-33
37. Mayor, A., U. Kumar, A. Bardají, P. Gupta, A. Jiménez, A. Hamad, B. Sigaúque, B. Singh, L. Quintó , S. Kumar, et al. 2013. Improved pregnancy outcomes in women exposed to malaria with high antibody levels against Plasmodi um falciparum. J. Infect. Dis. 207: 1664-1674
38. Valderrama-Aguirre, A., G. Quintero, A. Gómez, A. Castellanos, Y. Pérez, F. Méndez, M. Arévalo-Herrera, and S. Herrera. 2005. Ant igenicity, immunogenicity, and protective efficacy of Plasmodium vivax MSP1 PV200l: a potential malaria vaccine subunit. Am. J. Trop. Med. Hyg. 73: 16-24
39. Devi, Y. S., P. Mukherjee, S. S. Yazdani, A. R. Shakri, S. Mazumdar, S. Pandey, C. E. Chitnis, and V. S. Chauhan. 2007. Immunogenicity of Plasmodium vivax combination subunit vaccine formulated with human compatible adjuvants in mice. Vaccine 25: 5166-5174.
40. Herrera S.,A. Bonelo,B.L. Perlaza,A. Z. Valencia,C. Cifuentes,S. Hurtado,G. Quintero,J. A. López,G. Corradin,M. Arévalo-Herrera, 2004, Use of long synthetic peptides to stud y the antigenicity and immunogenicity of the Plasmodium vivax circumsporozoite protein. Int. J. Parasitol, 34, 1535-1546.
41. Rui, E., C. Fernandez-Becerra, S. Takeo, S. Sanz, M. V. Lacerda, T. Tsuboi, and H. A. del Portillo. 2011. Plasmodium vivax: comparison of immunogenicity among proteins expressed in the cell-free systems of Escherichia coli and wheat germ by suspension array assays. Malar. J. 10: 192
42. Singh, S., K. Pandey, R. Chattopadhayay, S. S. Yazdani, A. Lynn, A. Bharadwaj, A. Ranjan, and C. Chitnis. 2001. Biochemical, biophysical, and functional characterization of bacterially expressed and refolded receptor binding domain of Plasmodium vivax duffy-binding protein. J. Biol. Chem. 276: 17111-17116
43. Bernabeu, M., F. J. Lopez, M. Ferrer, L. Martin-Jaular, A. Razaname, G. Corradin, A. G. Maier, H. A. Del Portillo, and C. Fernandez-Becerra. 2012. Functional analysis of Plasmodium vivax VIR proteins reveals different subcellular localizations and cytoadherence to the ICAM-1 endothelial receptor. Cell. Microbiol. 14: 386-400
44. Castellanos, M. E., A. Bardají, M. Menegon, A. Mayor, M. Desai, C. Severini, C. Menéndez, and N. Padilla. 2012. Plasmodium vivax congenital malaria in an area of very low endemicity in Guatemala: imp lications for clinical and epidemiological surveillance in a malaria elimination context. Malar. J. 11: 411
45. Rosanas-Urgell, A., D. Mueller, I. Betuela, C. Barnadas, J. Iga, P. A. Zimmerman, H. A. del Portillo, P. Siba, I. Mueller, and I. Felger. 2010. Comparison of diagnostic methods for the detection and quantification of the four sympatric Plasmodium species in field samples from Papua New Guinea. Malar. J. 9: 361
46. Lanzavecchia, A. 1985. Antigen-specific interaction between T and B cells. Nature 314: 537-539
47. Hou, P., E. Araujo, T. Zhao, M. Zhang, D. Massenburg, M. Veselits, C. Doyle, A. R. Dinner, and M. R. Clark. 2006. B cell antigen receptor signaling and internalizati on are mutually exclusive events. PLoS Biol. 4: e200
48. Courtney, A. H., N. R. Bennett, D. B. Zwick, J. Hudon, and L. L. Kiessling. 2014. Synthetic antigens reveal dynamics of BCR endocytosis during inhibitory signaling. ACS Chem. Biol. 9: 202-210
49. Country Progress Report Papua New Guinea reporting period January 2010- December 2011. In Global AIDS Report 2012. Papua New Guinea National AIDS Coun cil Secretariat. Port Moresby, Papua New Guinea. p. 25-26
50. Kline, K., J. S. McCarthy, M. Pearson, A. Loukas, and P. J. Hotez. 2013. Neglected tropical diseases of Oceania: review of their prevalence, dis tribution, and opportunities for control. PLoS Negl. Trop. Dis. 7: e1755
51. Sohn, H.W., P. D. Krueger, R. S. Davis, and S. K. Pierce. 2011. FcRL4 acts as an adaptive to innate molecular switch dampening BCR signaling and enhancing TLR signaling. Blood 118: 6332-6341
52. Yeo, L., H. Lom, M. Juarez, M. Snow, C. D. Buckley, A. Filer, K. Raza, and D. Scheel-Toellner. 2014. Expression of FcR L4 defines a pro-inflammatory, RANKL-producing B cell subset in rheumatoid arthritis. Ann. Rheum. Dis. DOI: 10.1136/annrheumdis-2013-204116
53. Radbruch, A., G. Muehlinghaus, E. O. Luger, A. Inamine, K. G. C. Smith, T. Dörner, and F. Hiepe. 2006. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat. Rev. Immunol. 6: 741-750
54. Petroff, M. G. 2011. Review: fetal antigens-identity, origins, and influences on the maternal immune system. Placenta 32: S176-S181
55. Wahlgren, M., K. Berzins, P. Perlmann, and A. Björkman. 1983. Characterization of the humoral immune res ponse in Plasmodium falciparum malaria. I. Estimation of antibodies to P. falciparum or human erythrocytes by means of microELISA. Clin. Exp. Immunol. 54: 127-134
56. Hart, M., A. Steel, S. A. Clark, G. Moyle, M. Nelson, D. C. Henderson, R. Wilson, F. Gotch, B. Gazzard, and P. Kelleher. 2007. Loss of discrete memory B cell subsets is associated with impaired immunization responses in HIV-1 infection and may be a risk facto r for invasive pneumococcal disease. J. Immunol. 178: 8212-8220
57. Shi, Y., T. Yamazaki, Y. Okubo, Y. Uehara, K. Sugane, and K. Agematsu. 2005. Regulation of aged humoral immune defense against pneumococcal bacteria by IgM memory B cell. J. Immunol. 175: 3262-3267
58. Cunnington, A. J., and E. M. Riley. 2010. Suppression of vaccine responses by malaria: insignificant or overlooked? Expert Rev. Vaccines 9: 409-429
59. Jinquan, T., H. H. Jacobi, C. Jing, A. Millner, E. Sten, L. Hviid, L. Anting, L. P. Ryder, C. Glue, P. S. Skov, et al. 2003. CCR3 expression induced by IL-2 and IL-4 functioning as a deat h receptor for B cells. J. Immunol. 171: 1722-1731
60. Kraus, T. A., R. S. Sperling, S. M. Engel, Y. Lo, L. Kellerman, T. Singh, M. Loubeau, Y. Ge, J. L. Garrido, M. Rodríguez-García, and T. M. Moran. 2010. Peripheral blood cytokine profiling during pregnancy and post-partum periods. Am. J. Reprod. Immunol. 64: 411-426.
61. Li H.,Y.-H. Huang,M.-Q. Li,Y.-H. Meng,X. Chen,J. Shao,C.-L. Tang,M.-R. Du,L.-P. Jin,D.-J. Li, 2013. Trophoblasts-derived chemokine CCL24 promotes the proliferation, growth and apopt osis of decidual stromal cells in human early pregnancy. Int. J. Clin. Exp. Pathol, 6, 1028-1037.
62. Badr, G., G. Borhis, E. A. Lefevre, N. Chaoul, F. Deshayes, V. Dessirier, G. Lapree, A. Tsapis, and Y. Richard. 2008. BAFF enhances chemotaxis of primary human B cells: a particular synergy between BAFF and CXCL13 on memory B cells. Blood 111: 2744-2754