调节性B细胞调控寄生虫感染的研究进展

doi:10.16431/j.cnki.1671-7236.2024.02.035

Abstract

Abstract: Parasitic diseases are infectious diseases that are widespread throughout the world and pose a serious threat to human and animal health.Parasites activate the body’s immune system when they invade the host.The host fights the parasitic infection through innate and acquired immune responses and protects itself from an excessive immune response through a variety of regulatory mechanisms.Regulatory B cells (Bregs) are a subset of B cells with immunosuppressive functions during parasitic infections.They have been more extensively studied in autoimmune diseases, cancer and allergic reactions.Currently, an increasing number of studies have shown that parasitic infections can induce the production of Bregs, and that Bregs can inhibit the inflammatory response by secreting the anti-inflammatory cytokine interleukin-10 (IL-10), thus reducing the damage of parasitic infections to the host.However, the signaling pathways and activation mechanisms of Breg proliferation are still unclear and require further investigation.In this review, the author briefly described the different types of Bregs and their phenotypes, and summarized the immunomodulatory roles of Bregs during Plasmodium, Schistosoma, Leishmania, Toxoplasma and Trypanosoma infections, with the aim of providing new insights into parasite treatment and prevention strategies.

Key words: parasites; immunomodulation; regulatory B cells

CLC Number:

S855.9⁺9

FENG Anni, LI Qilong, ZHANG Yiwei, SANG Xiaoyu, CHEN Ran, FENG Ying, JIANG Ning. Research Progress on Regulation of Parasitic Infections by Regulatory B Cells[J]. China Animal Husbandry and Veterinary Medicine, 2024, 51(2): 790-798.

References

[1] TORGERSON P R.One world health:Socioeconomic burden and parasitic disease control priorities[J].Veterinary Parasitology,2013,195:223-232.
[2] MIZOGUCHI A,MIZOGUCHI E,TAKEDATSU H,et al.Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation[J].Immunity,2002,16:219-230.
[3] CATALÁN D,MANSILLA M A,FERRIER A,et al.Immunosuppressive mechanisms of regulatory B cells[J]. Frontiers in Immunology,2021,12:611795.
[4] EGWUAGU C E,YU C R.Interleukin 35-producing B cells (i35-Breg):A new mediator of regulatory B-cell functions in CNS autoimmune diseases[J].Critical Review in Immunology,2015,35:49-57.
[5] CHERUKURI A,MOHIB K,ROTHSTEIN D M.Regulatory B cells:TIM-1,transplant tolerance,and rejection[J].Immunological Reviews,2021,299:31-44.
[6] MAURI C,BOSMA A.Immune regulatory function of B cells.[J].Annual Review of Immunology,2021,30:221-241.
[7] BOONPIYATHAD T,SATITSUKSANOA P,AKDIS M,et al.IL-10 producing T and B cells in allergy[J].Seminars in Immunology,2019,44:101326.
[8] MICHAUD D,STEWARD C R,MIRLEKAR B,et al.Regulatory B cells in cancer[J].Immunological Reviews,2021,299:74-92.
[9] MINCIULLO P L,CASCIO A,DAVID A,et al.Anaphylaxis caused by helminths:Review of the literature[J].European Review for Medical and Pharmacological Sciences,2012,16:1512-1518.
[10] ALLEN J E,SUTHERLAND T E.Host protective roles of type 2 immunity:Parasite killing and tissue repair,flip sides of the same coin[J]. Seminars in Immunology,2014,26:329-340.
[11] 谢静,黄海斌,赵权,等.调节性B细胞在寄生虫感染中的免疫调节作用[J].中国病原生物学杂志,2019,14(4):482-484. XIE J,HUANG H B,ZHAO Q,et al.The role of regulatory B cells in immunity during a parasite infection[J].Journal of Pathogen Biology,2019,14(4):482-484.(in Chinese)
[12] MENGMENG Z,JIACUI S,SHANSHAN D,et al.Serum IL-35 levels are associated with activity and progression of sarcoidosis[J]. Frontiers in Immunology,2020,11:977.
[13] JANSEN K,CEVHERTAS L,MA S,et al.Regulatory B cells,A to Z[J].Allergy,2021,76:2699-2715.
[14] MATSUMOTO M,BABA A,YOKOTA T,et al.Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation[J].Immunity,2014,41:1040-1051.
[15] ROSSER E C,MAURI C.Regulatory B cells:Origin,phenotype,and function[J].Immunity,2015,42:607-612.
[16] OLEINIKA K,MAURI C,SALAMA A D.Effector and regulatory B cells in immune-mediated kidney disease[J]. Nature Reviews Nephrology,2019,15:11-26.
[17] ROSSER E C,OLEINIKA K,TONON S,et al.Regulatory B cells are induced by gut microbiota-driven interleukin-1β and interleukin-6 production[J].Nature Medicine,2014,20:1334-1339.
[18] YOSHIZAKI A,MIYAGAKI T,DILILLO D J,et al.Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions[J].Nature,2012,491:264-268.
[19] WORLD HEALTH ORGANIZATION.World malaria report 2020:20 years of global progress and challenges[R].Geneva:World Health Organization,2020.
[20] 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].The Journal of Infectious Diseases,2011,204:962-970.
[21] ASITO A S,MOORMANN A M,KIPROTICH C,et al.Alterations on peripheral B cell subsets following an acute uncomplicated clinical malaria infection in children[J]. Malaria Journal,2008,7:238.
[22] SCHOLZEN A,TEIRLINCK A C,BIJKER E M,et al.BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection[J]. Journal of Immunology,2014,192:3719-3729.
[23] 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]. Journal of Immunology,2010,184:3321-3325.
[24] SCHOLZEN A,SAUERWEIN R W.How malaria modulates memory:Activation and dysregulation of B cells in Plasmodium infection[J].Trends in Parasitology,2013,29:252-262.
[25] BORHIS G,RICHARD Y.Subversion of the B-cell compartment during parasitic,bacterial,and viral infections[J]. BMC Immunology,2015,16:15.
[26] BAO L Q,HUY N T,KIKUCHI M,et al.CD19⁺ B cells confer protection against experimental cerebral malaria in semi-immune rodent model[J].PLoS One,2013,8:e64836.
[27] 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[J].European Journal of Immunology, 2013,43:2907-2918.
[28] REST J R.Cerebral malaria in inbred mice.Ⅰ.A new model and its pathology[J].Transactions of the Royal Society of Tropical Medicine and Hygiene,1982,76:410-415.
[29] SCHOFIELD L,GRAU G E.Immunological processes in malaria pathogenesis[J].Nature Reviews Immunology,2005,5:722-735.
[30] AMANTE F H,HAQUE A,STANLEY A C,et al.Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria[J]. Journal of Immunology,2010,185:3632-3642.
[31] HAN X,YANG J,ZHANG Y,et al.Potential role for regulatory B cells as a major source of interleukin-10 in spleen from Plasmodium chabaudi-infected mice[J].Infection and Immunity,2018,86:e00016-18.
[32] KALKAL M,CHAUHAN R,THAKUR R S,et al.IL-10 producing regulatory B cells mediated protection against murine malaria pathogenesis[J].Biology (Basel),2022,11:669.
[33] CHITSULO L,LOVERDE P,ENGELS D.Schistosomiasis[J].Nature Reviews Microbiology,2004,2:12-13.
[34] GAUBERT S,VIANA DA COSTA A,MAURAGE C A,et al.X-linked immunodeficiency affects the outcome of Schistosoma mansoni infection in the murine model[J].Parasite Immunology,1999,21:89-101.
[35] VELUPILLAI P,SECOR W E,HORAUF A M,et al.B-1 cell (CD5⁺B220⁺) outgrowth in murine schistosomiasis is genetically restricted and is largely due to activation by polylactosamine sugars[J].Journal of Immunology,1997,158:338-344.
[36] VELUPILLAI P,HARN D A.Oligosaccharide-specific induction of interleukin 10 production by B220⁺ cells from schistosome-infected mice:A mechanism for regulation of CD4⁺ T-cell subsets[J].Proceedings of the National Academy of Sciences of the United States of America,1994,91:18-22.
[37] MANGAN N E,FALLON R E,SMITH P,et al.Helminth infection protects mice from anaphylaxis via IL-10-producing B cells[J].Journal of Immunology,2004,173:6346-6356.
[38] AMU S,SAUNDERS S P,KRONENBERG M,et al.Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model[J].Journal of Allergy and Clinical Immunology,2010,125:1114-1124.
[39] VAN DER VLUGT L E,ZINSOU J F,OZIR-FAZALALIKHAN A,et al.Interleukin 10(IL-10)-producing CD1d^hi regulatory B cells from Schistosoma haematobium-infected individuals induce IL-10-positive T cells and suppress effector T-cell cytokines[J].The Journal of Infectious Diseases,2014,210:1207-1216.
[40] VAN DER VLUGT L E,LABUDA L A,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[J].PLoS One,2012,7:e30883.
[41] HAEBERLEIN S,OBIEGLO K,OZIR-FAZALALIKHAN A,et al.Schistosome egg antigens,including the glycoprotein IPSE/alpha-1,trigger the development of regulatory B cells[J]. PLoS Pathogens,2017,13:e1006539.
[42] TIAN F,HU X,XIAN K,et al.B10 cells induced by Schistosoma japonicum soluble egg antigens modulated regulatory T cells and cytokine production of T cells[J].Parasitology Research,2015,114:3827-3834.
[43] XIAO J,GUAN F,SUN L,et al.B cells induced by Schistosoma japonicum infection display diverse regulatory phenotypes and modulate CD4⁺ T cell response[J].Parasites&Vectors,2020,13:147.
[44] KAYE P,SCOTT P.Leishmaniasis:Complexity at the host-pathogen interface[J].Nature Reviews Microbiology,2011,9:604-615.
[45] SAURABH S.Leishmaniasis[J].Lancet,2019,393:871.
[46] CHAPPUIS F,SUNDAR S,HAILU A,et al.Visceral leishmaniasis:What are the needs for diagnosis,treatment and control?[J]. Nature Reviews Microbiology,2007,5:873-882.
[47] 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].Journal of Immunology,2010,184:886-894.
[48] SCHAUT R G,LAMB I M,TOEPP A J,et al.Regulatory IgD^hi B cells suppress T cell function via IL-10 and PD-L1 during progressive visceral leishmaniasis[J].Journal of Immunology, 2016,196:4100-4109.
[49] ANDREANI G,OUELLET M,MENASRIA R,et al.Leishmania infantum amastigotes trigger a subpopulation of human B cells with an immunoregulatory phenotype[J].PLoS Neglected Tropical Diseases,2015,9:e0003543.
[50] YANABA K,BOUAZIZ J D,HAAS K M,et al.A regulatory B cell subset with a unique CD1d^hiCD5⁺ phenotype controls T cell-dependent inflammatory responses[J].Immunity,2008,28:639-650.
[51] BANKOTI R,GUPTA K,LEVCHENKO A,et al.Marginal zone B cells regulate antigen-specific T cell responses during infection[J]. Journal of Immunology,2012,188:3961-3671.
[52] RANATUNGA D,HEDRICH C M,WANG F,et al.A human IL10 BAC transgene reveals tissue-specific control of IL-10 expression and alters disease outcome[J].Proceedings of the National Academy of Sciences of the United States of America,2009,106:17123-17128.
[53] GONZAGA W F,XAVIER V,VIVANCO B C,et al.B-1 cells contribute to susceptibility in experimental infection with Leishmania(Leishmania)chagasi[J].Parasitology,2015,142:1506-1515.
[54] NYLÉN S,SACKS D.Interleukin-10 and the pathogenesis of human visceral leishmaniasis[J].Trends in Immunology,2007,28:378-384.
[55] MURRAY H W.Interleukin 10 receptor blockade--pentavalent antimony treatment in experimental visceral leishmaniasis[J].Acta Tropica,2005,93:295-301.
[56] FALEIRO R J,KUMAR R,HAFNER L M,et al.Immune regulation during chronic visceral leishmaniasis[J]. PLoS Neglected Tropical Diseases,2014,8:e2914.
[57] GOLLOB K J,VIANA A G,DUTRA W O.Immunoregulation in human American leishmaniasis:Balancing pathology and protection[J]. Parasite Immunology,2014,36:367-376.
[58] KOCHANOWSKY J A,KOSHY A A. Toxoplasma gondii[J].Current Biology,2018,28:R770-r1.
[59] ELMORE S A,JONES J L,CONRAD P A,et al.Toxoplasma gondii:Epidemiology,feline clinical aspects,and prevention[J]. Trends in Parasitology,2010,26:190-196.
[60] SUZUKI Y,ORELLANA M A,SCHREIBER R D,et al.Interferon-gamma:The major mediator of resistance against Toxoplasma gondii[J]. Science,1988,240:516-518.
[61] JEONG Y I,HONG S H,CHO S H,et al.Toxoplasma gondii infection suppresses house dust mite extract-induced atopic dermatitis in NC/Nga mice[J]. Allergy Asthma&Immunology Research,2015,7:557-564.
[62] JEONG Y I,HONG S H,CHO S H,et al.Induction of IL-10-producing regulatory B cells following Toxoplasma gondii infection is important to the cyst formation[J].Biochemistry and Biophysics Reports,2016,7:91-97.
[63] BERN C.Chagas'disease[J].The New England Journal of Medicine,2015,373:456-466.
[64] PÉREZ-MOLINA J A,MOLINA I.Chagas disease[J].Lancet,2018,391:82-94.
[65] GIRARD M C,ACEVEDO G R,OSSOWSKI M S,et al.Ex vivo characterization of Breg cells in patients with chronic Chagas disease[J]. Scientific Reports,2021,11:5511.
[66] GIRARD M C,OSSOWSKI M S,MUÑOZ-CALDERÓN A,et al.Trypanosoma cruzi induces regulatory B cell alterations in patients with chronic Chagas disease[J].Frontiers in Cellular and Infection Microbiology,2021,11:723549.
[67] JEONG Y I,HONG S H,CHO S H,et al.Induction of IL-10-producing CD1d^highCD5⁺ regulatory B cells following Babesia microti-infection[J].PLoS One,2012,7:e46553.
[68] MAJLESSI L,LO-MAN R,LECLERC C.Regulatory B and T cells in infections[J].Microbes and Infection,2008,10:1030-1035.

Research Progress on Regulation of Parasitic Infections by Regulatory B Cells

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