892
Views
19
CrossRef citations to date
0
Altmetric
Review

What do we know about the role of regulatory B cells (Breg) during the course of infection of two major parasitic diseases, malaria and leishmaniasis?

, , , , &

References

  • Lund FE. Cytokine-producing B lymphocytes-key regulators of immunity. Curr Opin Immunol. 2008;20(3):332–338.10.1016/j.coi.2008.03.003
  • Welner RS, Pelayo R, Kincade PW. Evolving views on the genealogy of B cells. Nat Rev Immunol. 2008;8(2):95–106.10.1038/nri2234
  • Borhis G, Richard Y. Subversion of the B-cell compartment during parasitic, bacterial, and viral infections. BMC Immunol. 2015;16(15):1–10.
  • DiLillo DJ, Hamaguchi Y, Ueda Y, et al. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol. 2008;180(1):361–371.10.4049/jimmunol.180.1.361
  • LeBien TW, Tedder TF. B lymphocytes: how they develop and function. Blood. 2008;112(5):1570–1580.10.1182/blood-2008-02-078071
  • Han J, Sun L, Fan X, et al. Role of regulatory B cells in neuroimmunologic disorders. J Neurosci Res. 2016;94(8):693–701.10.1002/jnr.v94.8
  • Liu Y, Wu Y, Ramarathinam L, et al Gene-targeted B-deficient mice reveal a critical role for B cells in the CD4 T cell response. Int Immunol. 1995;7(8):1353-1362.10.1093/intimm/7.8.1353
  • Tedder TF. B10 cells: a functionally defined regulatory B cell subset. J Immunol. 2015;194(4):1395–1401.10.4049/jimmunol.1401329
  • Harris DP, Haynes L, Sayles PC, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol. 2000;1(6):475–482.10.1038/82717
  • Shlomchik MJ, Craft JE, Mamula MJ. From T to B and back again: positive feedback in systemic autoimmune disease. Nat Rev Immunol. 2001;1(2):147–153.10.1038/35100573
  • Katz SI, Parker D, Turk JL. B-cell suppression of delayed hypersensitivity reactions. Nature. 1974;251:550–551.10.1038/251550a0
  • Neta R, Salvin SB. Specific suppression of delayed hypersensitivity: the possible presence of a suppressor B cell in the regulation of delayed hypersensitivity. J Immunol. 1974;113(6):1716–1725.
  • Fillatreau S, Sweenie CH, McGeachy MJ, et al. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3(10):944–950.10.1038/ni833
  • Mizoguchi A, Mizoguchi E, Takedatsu H, et al. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity. 2002;16(2):219–230.10.1016/S1074-7613(02)00274-1
  • Mauri C, Gray D, Mushtaq N, et al. Prevention of arthritis by interleukin 10–producing B cells. J Exp Med. 2003;197(4):489–501.10.1084/jem.20021293
  • Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42(4):607–612.10.1016/j.immuni.2015.04.005
  • Yanaba K, Bouaziz JD, Haas KM, et al. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28(5):639–650.10.1016/j.immuni.2008.03.017
  • DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann NY Acad Sci. 2010;1183(2010):38–57.10.1111/j.1749-6632.2009.05137.x
  • Wei B, Velazquez P, Turovskaya O, et al. 2005. Mesenteric B cells centrally inhibit CD4+ T cell colitis through interaction with regulatory T cell subsets. Proc Natl Acad Sci USA. 2005;102(6):2010-2015.10.1073/pnas.0409449102
  • Gray M, Miles K, Salter D, et al. Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc Natl Acad Sci USA. 2007;104(35):14080–14085.10.1073/pnas.0700326104
  • Mauri C, Blair PA. Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol. 2010;6(11):636–643.10.1038/nrrheum.2010.140
  • Mauri C, Bosma A. Immune regulatory function of B cells. Annu Rev Immunol. 2012;30:221–241.10.1146/annurev-immunol-020711-074934
  • Evans JG, Chavez-Rueda KA, Eddaoudi A, et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol. 2007;178(12):7868–7878.10.4049/jimmunol.178.12.7868
  • Blair PA, Chavez-Rueda KA, Evans JG, et al. Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol. 2009;182(6):3492–3502.10.4049/jimmunol.0803052
  • Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10–competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117(2):530–541.10.1182/blood-2010-07-294249
  • Khoder A, Sarvaria A, Alsuliman A, et al. Regulatory B cells are enriched within the IgM memory and transitional subsets in healthy donors but are deficient in chronic GVHD. Blood. 2014;124(13):2034–2045.10.1182/blood-2014-04-571125
  • Blair PA, Noreña LY, Flores-Borja F, et al. CD19+CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32(1):129–140.10.1016/j.immuni.2009.11.009
  • Flores-Borja F, Bosma A, Ng D, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med. 2013;5(173):173ra23.10.1126/scitranslmed.3005407
  • Xiao S, Brooks CR, Zhu C, et al. Defect in regulatory B-cell function and development of systemic autoimmunity in T-cell Ig mucin 1 (Tim-1) mucin domain-mutant mice. Proc Natl Acad Sci USA. 2012;109(30):12105–12110.10.1073/pnas.1120914109
  • Matsumoto M, Baba A, Yokota T, et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity. 2014;41(6):1040–1051.10.1016/j.immuni.2014.10.016
  • Shen P, Roch T, Lampropoulou V, et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature. 2014;507(7492):366–370.10.1038/nature12979
  • O’garra A, Chang R, Go N, et al. Ly‐1 B (B‐1) cells are the main source of B cell‐derived interleukin 10. Eur J Immunol. 1992;22(3):711–717.10.1002/(ISSN)1521-4141
  • Mizoguchi A, Mizoguchi E, Smith RN, et al. Suppressive role of B cells in chronic colitis of T cell receptor α mutant mice. J Exp Med. 1997;186(10):1749–1756.10.1084/jem.186.10.1749
  • Mauri C, Menon M. The expanding family of regulatory B cells. Int Immunol. 2003;27(10):479–486.
  • Mizoguchi A, Bhan AK. A case for regulatory B cells. J Immunol. 2006;176(2):705–710.10.4049/jimmunol.176.2.705
  • Saraiva M, O’Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol. 2010;10(3):170–181.10.1038/nri2711
  • Douglas RS, Woo EY, Capocasale RJ, et al. Altered response to and production of TGF-beta by B cells from autoimmune NZB mice. Cell. Immunol. 1997;179:126–137.10.1006/cimm.1997.1149
  • Wang RX, Yu CR, Dambuza IM, et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med. 2014;20(6):633–641.10.1038/nm.3554
  • Egwuagu CE, Yu CR. Interleukin 35-producing B cells (I35-Breg): a new mediator of regulatory B-cell functions in CNS autoimmune diseases. Crit Rev Immunol. 2015;35(1):49–57.10.1615/CritRevImmunol.v35.i1
  • Natarajan P, Singh A, McNamara JT, et al. Regulatory B cells from hilar lymph nodes of tolerant mice in a murine model of allergic airway disease are CD5+, express TGF-beta, and co-localize with CD4+Foxp3+ T cells. Mucosal Immunol. 2012;5(6):691–701.10.1038/mi.2012.42
  • Yang M, Sun L, Wang S, et al. Novel function of B cell-activating factor in the induction of IL-10–Producing regulatory B cells. J Immunol. 2010;184(7):3321–3325.10.4049/jimmunol.0902551
  • Cepok S, Rosche B, Grummel V, et al. Short-lived plasma blasts are the main B cell effector subset during the course of multiple sclerosis. Brain. 2005;128:1667–1676.10.1093/brain/awh486
  • Krumbholz M, Theil D, Derfuss T, et al. BAFF is produced by astrocytes and up-regulated in multiple sclerosis lesions and primary central nervous system lymphoma. J Exp Med. 2005;201(2):195–200.
  • Hartung HP, Kieseier BC. Atacicept: targeting B cells in multiple sclerosis. Ther Adv Neurol Disord. 2010;3(4):205–216.10.1177/1756285610371146
  • Magliozzi R, Howell O, Vora A, et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain. 2007;130(4):1089–1104.
  • Ramanujam M, Davidson A. BAFF blockade for systemic lupus erythematosus: will the promise be fulfilled? Immunol Rev. 2008;223:156–174.10.1111/imr.2008.223.issue-1
  • Gross JA, Dillon SR, Mudri S, et al. TACI-Ig neutralizes molecules critical for B cell development and autoimmune disease impaired B cell maturation in mice lacking BLyS. Immunity. 2001;15:289–302.
  • Wei F, Chang Y, Wei W. The role of BAFF in the progression of rheumatoid arthritis. Cytokine. 2015;76(2):537–544.10.1016/j.cyto.2015.07.014
  • Jamin C, Morva A, Lemoine S, et al. Regulatory B lymphocytes in humans: a potential role in autoimmunity. Arthritis Rheum. 2008;58(7):1900–1906.10.1002/art.v58:7
  • Noh G, Lee JH. Regulatory B cells and allergic diseases. Allergy Asthma Immunol Res. 2011;3(3):168–177.10.4168/aair.2011.3.3.168
  • Berthelot JM, Jamin C, Amrouche K, et al. Regulatory B cells play a key role in immune system balance. Joint Bone Spine. 2013;80(1):18–22.10.1016/j.jbspin.2012.04.010
  • Mauri C, Ehrenstein MR. The ‘short’ history of regulatory B cells. Trends Immunol. 2008;29(1):34–40.10.1016/j.it.2007.10.004
  • Sato S, Steeber DA, Tedder TF. The CD19 signal transduction molecule is a response regulator of B-lymphocyte differentiation. Proc Natl Acad Sci USA. 1995;92:11558–11562.10.1073/pnas.92.25.11558
  • Ma K, Li J, Fang Y, et al. Roles of B cell-intrinsic TLR signals in systemic lupus erythematosus. Int J Mol Sci. 2015;16(6):13084–13105.10.3390/ijms160613084
  • Barr TA, Brown S, Ryan G, et al. TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur J Immunol. 2007;37(11):3040–3053.10.1002/(ISSN)1521-4141
  • Chiron D, Bekeredjian-Ding I, Pellat-Deceunynck C, et al. Toll-like receptors: lessons to learn from normal and malignant human B cells. Blood. 2008;112(6):2205–2213.10.1182/blood-2008-02-140673
  • Connolly DJ, O’Neill LA. New developments in Toll-like receptor targeted therapeutics. Curr Opin Pharmacol. 2012;12(4):510–518.10.1016/j.coph.2012.06.002
  • Klinker MW, Lundy SK. Multiple mechanisms of immune suppression by B lymphocytes. Mol Med. 2012;18(1):123.
  • Yang M, Deng J, Liu Y, et al. IL-10–producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am J Pathol. 2012;180(6):2375–2385.10.1016/j.ajpath.2012.03.010
  • Lindner S, Dahlke K, Sontheimer K, et al. Interleukin 21–induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013;73(8):2468–2479.10.1158/0008-5472.CAN-12-3450
  • DiLillo DJ, Weinberg JB, Yoshizaki A, et al. Chronic lymphocytic leukemia and regulatory B cells share IL-10 competence and immunosuppressive function. Leukemia. 2013;27(1):170–182.10.1038/leu.2012.165
  • Candando KM, Lykken JM, Tedder TF. B10 cell regulation of health and disease. Immunol Rev. 2014;259(1):259–272.10.1111/imr.12176
  • Lykken JM, Candando KM, Tedder TF. Regulatory B10 cell development and function. Int Immunol. 2015;27(10):471–477.10.1093/intimm/dxv046
  • Inoue S, Leitner WW, Golding B, et al. Inhibitory effects of B cells on antitumor immunity. Cancer Res. 2006;66(15):7741–7747.10.1158/0008-5472.CAN-05-3766
  • Das A, Ellis G, Pallant C, et al. IL-10–producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J Immunol. 2012;189(8):3925–3935.10.4049/jimmunol.1103139
  • Siewe B, Stapleton JT, Martinson J, et al. Regulatory B cell frequency correlates with markers of HIV disease progression and attenuates anti-HIV CD8⁺ T cell function in vitro. J Leukoc Biol. 2013;93(5):811–818.10.1189/jlb.0912436
  • Liu J, Zhan W, Kim CJ, et al. IL-10–producing B cells are induced early in HIV-1 infection and suppress HIV-1–specific T cell responses. PLoS One. 2014;9(2):e89236.10.1371/journal.pone.0089236
  • Majlessi L, Lo-Man R, Leclerc C. Regulatory B and T cells in infections. Microbes Infect. 2008;10(9):1030–1035.10.1016/j.micinf.2008.07.017
  • Neves P, Lampropoulou V, Calderon-Gomez E, et al. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity. 2010;33(5):777–790.10.1016/j.immuni.2010.10.016
  • Goenka R, Parent MA, Elzer PH, et al. B cell–deficient mice display markedly enhanced resistance to the intracellular bacterium Brucella abortus. J Infect Dis. 2011;203(8):1136–1146.10.1093/infdis/jiq171
  • Velupillai P, Secor WE, Horauf AM, et al. B-1 cell (CD5+B220+) outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars. J Immunol. 1997;158(1):338–344.
  • Gaubert S, Viana da Costa A, Maurage CA, et al. X–linked immunodeficiency affects the outcome of Schistosoma mansoni infection in the murine model. Parasite Immunol. 1999;21(2):89–101.10.1046/j.1365-3024.1999.00205.x
  • Mangan NE, Fallon RE, Smith P, et al. Helminth infection protects mice from anaphylaxis via IL-10–producing B cells. J Immunol. 2004;173(10):6346–6356.10.4049/jimmunol.173.10.6346
  • Amu S, Saunders SP, Kronenberg M, et al. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3–positive T regulatory cells in a murine model. J Allergy Clin Immunol. 2010;125(5):1114–1124.10.1016/j.jaci.2010.01.018
  • Van der Vlugt LE, Labuda LA, Ozir-Fazalalikhan A, et al. Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS One. 2012;7(2):e30883.10.1371/journal.pone.0030883
  • Van der Vlugt LE, Zinsou JF, Ozir-Fazalalikhan A, et al. Interleukin 10 (IL-10) –producing CD1dhi regulatory B cells from Schistosoma haematobium–infected individuals induce IL-10–positive T cells and suppress effector T-cell cytokines. J Infect Dis. 2014;210(8):1207–1216.10.1093/infdis/jiu257
  • Velupillai P, Harn DA. Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome–infected mice: a mechanism for regulation of CD4+ T–cell subsets. Proc Natl Acad Sci USA. 1994;91(1):18–22.10.1073/pnas.91.1.18
  • Ronet C, Hauyon-La Torre Y, Revaz-Breton M, et al. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J Immunol. 2010;184(2):886–894.10.4049/jimmunol.0901114
  • Bankoti R, Gupta K, Levchenko A, et al. Marginal zone B cells regulate antigen-specific T cell responses during infection. J Immunol. 2012;188(8):3961–3971.10.4049/jimmunol.1102880
  • Bao LQ, Huy NT, Kikuchi M, et al. CD19(+) B cells confer protection against experimental cerebral malaria in semi-immune rodent model. PLoS One. 2013;8(5):e64836.10.1371/journal.pone.0064836
  • Liu Y, Chen Y, Li Z, et al. Role of IL-10–producing regulatory B cells in control of cerebral malaria in Plasmodium berghei infected mice. Eur J Immunol. 2013;43(11):2907–2918.10.1002/eji.v43.11
  • Andreani G, Ouellet M, Menasria R, et al. Leishmania infantum amastigotes trigger a subpopulation of human B cells with an immunoregulatory phenotype. PLoS Negl Trop Dis. 2015;9(2):e0003543.10.1371/journal.pntd.0003543
  • Jeong YI, Hong SH, Choa SH, et al. Induction of IL-10–producing regulatory B cells following Toxoplasma gondii infection is important to the cyst formation. Biochem Biophys Rep. 2016;2016(7):91–97.
  • Schaut RG, Lamb IM, Toepp AJ, et al. Regulatory IgDhi B cells suppress T cell function via IL-10 and PD-L1 during progressive visceral leishmaniasis. J. Immunol. 2016;196(10):4100–4109.10.4049/jimmunol.1502678
  • Tate EW, Bell AS, Rackham MD, et al. N-Myristoyltransferase as a potential drug target in malaria and leishmaniasis. Parasitology. 2014;141(1):37–49.10.1017/S0031182013000450
  • World Health Organization (WHO) [Internet]. World Malaria Report 2015; 2015 [updated 2016 April 20]. Avaliable from: http://www.rbm.who.int.
  • Schofield L, Grau GE. Immunological processes in malaria pathogenesis. Nat Rev Immunol. 2005;5:722–735.10.1038/nri1686
  • Riley EM, Couper KN, Helmby H, et al. Neuropathogenesis of human and murine malaria. Trends Parasitol. 2010;26(6):277–278.10.1016/j.pt.2010.03.002
  • Clark IA, Budd AC, Alleva LM, et al. Human malarial disease: a consequence of inflammatory cytokine release. Malar J. 2006;5(1):1.
  • Haque A, Best SE, Ammerdorffer A, et al. Type I interferons suppress CD4+ T-cell–dependent parasite control during blood–stage Plasmodium infection. Eur J Immunol. 2011;41(9):2688–2698.10.1002/eji.201141539
  • Asito AS, Moormann AM, Kiprotich C, et al. Alterations on peripheral B cell subsets following an acute uncomplicated clinical malaria infection in children. Malar J. 2008;7(1):1–8.
  • Nduati E, Gwela A, Karanja H, et al. The plasma concentration of the B cell activating factor is increased in children with acute malaria. J Infect Dis. 2011;204(6):962–970.10.1093/infdis/jir438
  • Scholzen A, Teirlinck AC, Bijker EM, et al. BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection. J Immunol. 2014;192(8):3719–3729.10.4049/jimmunol.1302960
  • Scholzen A, Sauerwein RW. How malaria modulates memory: activation and dysregulation of B cells in Plasmodium infection. Trends Parasitol. 2013;29(5):252–262.10.1016/j.pt.2013.03.002
  • Borhis G, Richard Y. Subversion of the B-cell compartment during parasitic, bacterial, and viral infections. BMC Immunol. 2015;16(1):1–10.
  • Rest JR. Cerebral malaria in inbred mice. I. A new model and its pathology. Trans R Soc Trop Med Hyg. 1982;76(3):410–415.10.1016/0035-9203(82)90203-6
  • Good MF, Xu H, Wykes M, et al. Development and regulation of cell–mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu Rev Immunol. 2005;23:69–99.10.1146/annurev.immunol.23.021704.115638
  • Amante FH, Haque A, Stanley AC, et al. Immune–mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J Immunol. 2010;185(6):3632–3642.10.4049/jimmunol.1000944
  • Fillatreau S, Gray D, Anderton SM. Not always the bad guys: B cells as regulators of autoimmune pathology. Nat Rev Immunol. 2008;8(5):391–397.
  • Margry B, Kersemakers SC, Hoek A, et al. Activated peritoneal cavity B-1a cells possess regulatory B cell properties. PLoS One. 2014;9(2):e88869.10.1371/journal.pone.0088869
  • Bismuth G, Gary-Gouy H. Signaling functions of the CD5 molecule. Curr Trends Immunol. 1998;1:79–87.
  • Carsetti R, Rosado MM, Wardmann H. Peripheral development of B cells in mouse and man. Immunol Rev. 2004;197:179–191.10.1111/imr.2004.197.issue-1
  • Lee J, Kuchen S, Fischer R, et al. Identification and characterization of a human CD5+ pre-naive B cell population. J Immunol. 2009;182 (7):4116-4126.10.4049/jimmunol.0803391
  • Griffin DO, Holodick NE, Rothstein TL. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+CD27+CD43+CD70-. J Exp Med. 2011;208(1):67–80.10.1084/jem.20101499
  • Dalloul A. CD5: a safeguard against autoimmunity and a shield for cancer cells. Autoimmun Rev. 2009;8(4):349–353.10.1016/j.autrev.2008.11.007
  • Gary-Gouy H, Sainz-Perez A, Marteau JB, et al. Natural phosphorylation of CD5 in chronic lymphocytic leukemia B cells and analysis of CD5-regulated genes in a B cell line suggest a role for CD5 in malignant phenotype. J Immunol. 2007;179(7):4335–4344.10.4049/jimmunol.179.7.4335
  • Maseda D, Candando KM, Smith SH, et al 2013. Peritoneal cavity regulatory B cells (B10 cells) modulate IFN-γ+ CD4+ T cell numbers during colitis development in mice. J Immunol. 2013;191(5):2780-2795.10.4049/jimmunol.1300649
  • Jeong YI, Hong SH, Cho SH, et al. Induction of IL-10–producing CD1dhighCD5+ regulatory B cells following Babesia microti-infection. PLoS One. 2012;7(10):e46553.10.1371/journal.pone.0046553
  • Sakkas H, Gartzonika C, Levidiotou S. Laboratory diagnosis of human visceral leishmaniasis. J Vector Borne Dis. 2016;53(1):8–16.
  • World Health Organization (WHO) [Internet] [updated 2017 March 09]. Available from: http://www.who.int/leishmaniasis/en/.
  • Chappuis F, Sundar S, Hailu A, et al. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol. 2007;5(11):873–882.
  • Stanley AC, Engwerda CR. Balancing immunity and pathology in visceral leishmaniasis. Immunol Cell Biol. 2007;85(2):138–147.10.1038/sj.icb7100011
  • Reithinger R, Dujardin JC, Louzir H, et al. Cutaneous leishmaniasis. Lancet Infect Dis. 2007;7(9):581–596.10.1016/S1473-3099(07)70209-8
  • Silveira FT, Lainson R, De Castro Gomes CM, et al. Immunopathogenic competences of Leishmania (V.) braziliensis and L. (L.) amazonensis in American cutaneous leishmaniasis. Parasite Immunol. 2009;31(8):423–431.10.1111/pim.2009.31.issue-8
  • Amezcua Vesely MC, Bermejo DA, Montes CL, et al. B-cell response during protozoan parasite infections. J Parasitol Res. 2012;2012:362131.
  • Kumar R, Nylén S. Immunobiology of visceral leishmaniasis. Front Immunol. 2012;3(251):1–10.
  • Nylén S, Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol. 2007;28(9):378–384.10.1016/j.it.2007.07.004
  • Wanasen N, Xin L, Soong L. Pathogenic role of B cells and antibodies in murine Leishmania amazonensis infection. Int J Parasitol. 2008;38(3–4):417–429.10.1016/j.ijpara.2007.08.010
  • Deak E, Jayakumar A, Cho KW, et al. Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation. Eur J Immunol. 2010;40(5):1355–1368.10.1002/eji.200939455
  • Rodrigues V, Cordeiro-da-Silva A, Laforge M, et al. Regulation of immunity during visceral Leishmania infection. Parasit Vectors. 2016;9(118):1–13.
  • Bankoti R, Stäger S. Differential regulation of the immune response in the spleen and liver of mice infected with Leishmania donovani. J Trop Med. 2012;2012:639304.
  • Schurr E, Kidane K, Yemaneberhan T, et al. Cutaneous leishmaniasis in Ethiopia: I. Lymphocyte transformation and antibody titre. Trop Med Parasitol. 1986;37(4):403–408.
  • Mengistu G, Akuffo HO, Yemane-Berhan T, et al. Serum antibody specificities to Leishmania aethiopica antigens in patients with localized and diffuse cutaneous leishmaniasis. Parasite Immunol. 1990;12(5):495–495.10.1111/pim.1990.12.issue-4-5
  • Galvao-Castro B, Sá Ferreira JA, Marzochi KF, et al. Polyclonal B cell activation, circulating immune complexes and autoimmunity in human American visceral leishmaniasis. Clin Exp Immunol. 1984;56(1):58–66.
  • Costa CH, Stewart JM, Gomes RB, et al. Asymptomatic human carriers of Leishmania chagasi. Am J Trop Med Hyg. 2002;66(4):334–7l.
  • Gidwani K, Picado A, Ostyn B, et al. Persistence of Leishmania donovani antibodies in past visceral leishmaniasis cases in India. Clin Vaccine Immunol. 2011;18(2):346–348.10.1128/CVI.00473-10
  • Hasker E, Malaviya P, Gidwani K, et al. Strong association between serological status and probability of progression to clinical visceral leishmaniasis in prospective cohort studies in India and Nepal. PLoS Negl Trop Dis. 2014;8(1):e2657.10.1371/journal.pntd.0002657
  • Soulas P, Koenig-Marrony S, Julien S, et al. A role for membrane IgD in the tolerance of pathological human rheumatoid factor B cells. Eur J Immunol. 2002;32(9):2623–2634.10.1002/1521-4141(200209)32:9<2623::AID-IMMU2623>3.0.CO;2-0
  • Maity PC, Blount A, Jumaa H, et al. B cell antigen receptors of the IgM and IgD classes are clustered in different protein islands that are altered during B cell activation. Sci Signal. 2015; 8(394):ra93.10.1126/scisignal.2005887
  • Geisberger R, Lamers M, Achatz G. The riddle of the dual expression of IgM and IgD. Immunology. 2006;118(4):429–437.
  • Ranatunga D, Hedrich CM, Wang F, et al. A human IL10 BAC transgene reveals tissue–specific control of IL-10 expression and alters disease outcome. Proc Natl Acad Sci USA. 2009;106(40):17123–17128.10.1073/pnas.0904955106
  • Gonzaga WF, Xavier V, Vivanco BC, et al. B-1 cells contribute to susceptibility in experimental infection with Leishmania (Leishmania) chagasi. Parasitology. 2015;142(12):1506–1515.10.1017/S0031182015000943
  • Murray HW. Interleukin 10 receptor blockade–pentavalent antimony treatment in experimental visceral leishmaniasis. Acta Trop. 2005;93(3):295–295.10.1016/j.actatropica.2004.11.008
  • 134. Faleiro RJ, Kumar R, Hafner LM, et al. Immune regulation during chronic visceral leishmaniasis. PLoS Negl Trop Dis. 2014;8(7):e2914.10.1371/journal.pntd.0002914
  • Gollob KJ, Viana AG, Dutra WO. Immunoregulation in human American leishmaniasis: balancing pathology and protection. Parasite Immunol. 2014;36(8):367–376.10.1111/pim.2014.36.issue-8
  • Singh OP, Sundar S. Immunotherapy and targeted therapies in treatment of visceral leishmaniasis: current status and future prospects. Front Immunol. 2014;5(296):1–9.
  • Khadem F, Uzonna JE. Immunity to visceral leishmaniasis: implications for immunotherapy. Future Microbiol. 2014;9(7):901–915.10.2217/fmb.14.43

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.