Research progress on the immunopathological mechanism of Schistosoma japonicum egg-induced granuloma

doi:10.12140/j.issn.1000-7423.2019.06.018

Abstract

Abstract:

After infection with Schistosoma japonicum, mature female adult worms lay eggs which deposit in the liver, intestinal wall, and other tissues of the infected mammalian host, which induces predominant Th2 immune responses and causes egg granuloma and fibrosis. It has been reported that neutrophils, macrophages, eosinophils, natural killer cells, B cells (including regulatory B cells), T cells (including Th1, Th2, and Th17 cells), Treg cells, hepatic stellate cells, and hepatocytes are involved in this process. In this paper, we reviewed the cell types involved in the egg granulomatous response of S. japonicum and their possible mechanisms in order to provide a helpful reference for related researchers in this field.

Key words: Schistosoma japonicum, Egg granuloma, Immune response, Pathological mechanism

CLC Number:

R383.24

Yu-jun SUN, Zhao-qi LI, Fang-li LV. Research progress on the immunopathological mechanism of Schistosoma japonicum egg-induced granuloma[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2019, 37(6): 713-717.

Figures/Tables 1

References 48

[1]	Chuah C, Jones MK, Burke ML, et al. Cellular and chemokine-mediated regulation in schistosome-induced hepatic pathology[J]. Trends Parasitol, 2014, 30(3): 141-150.
[2]	Elbaz T, Esmat G.Hepatic and intestinal schistosomiasis: review[J]. J Adv Res, 2013, 4(5): 445-452.
[3]	Chuah C, Jones MK, Burke ML, et al. Defining a pro-inflammatory neutrophil phenotype in response to schistosome eggs[J]. Cell Microbiol, 2014, 16(11): 1666-1677.
[4]	Keshari RS, Jyoti A, Dubey M, et al. Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition[J]. PLoS One, 2012, 7(10): e48111.
[5]	de Buck M, Gouwy M, Proost P, et al. Identification and characterization of MIP-1α/CCL3 isoform 2 from bovine serum as a potent monocyte/dendritic cell chemoattractant[J]. Biochem Pharmacol, 2013, 85(6): 789-797.
[6]	Cheung R, Malik M, Ravyn V, et al. An arrestin-dependent multi-kinase signaling complex mediates MIP-1beta/CCL4 signaling and chemotaxis of primary human macrophages[J]. J Leukoc Biol, 2009, 86(4): 833-845.
[7]	Charmoy M, Brunner-Agten S, Aebischer D, et al. Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice[J]. PLoS Pathog, 2010, 6(2): e1000755.
[8]	de Filippo K, Dudeck A, Hasenberg M, et al. Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation[J]. Blood, 2013, 121(24): 4930-4937.
[9]	Bonville CA, Percopo CM, Dyer KD, et al. Interferon-γ coordinates CCL3-mediated neutrophil recruitment in vivo[J]. BMC Immunol, 2009, 10: 14.
[10]	Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria[J]. Science, 2004, 303(5663): 1532-1535.
[11]	Urban CF, Reichard U, Brinkmann V, et al. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms[J]. Cell Microbiol, 2006, 8(4): 668-676.
[12]	Guimarães-Costa AB, Nascimento MT, Froment GS, et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps[J]. Proc Natl Acad Sci USA, 2009, 106(16): 6748-6753.
[13]	Yousefi S, Simon D, Simon HU.Eosinophil extracellular DNA traps: molecular mechanisms and potential roles in disease[J]. Curr Opin Immunol, 2012, 24(6): 736-739.
[14]	Dudeck A, Köberle M, Goldmann O, et al. Mast cells as protectors of health[J]. J Allergy Clin Immunol, 2019, 144(4): S4-S18.
[15]	Wong KW, Jacobs WR Jr.Mycobacterium tuberculosis exploits human interferon γ to stimulate macrophage extracellular trap formation and necrosis[J]. J Infect Dis, 2013, 208(1): 109-119.
[16]	Keshari RS, Jyoti A, Kumar S, et al. Neutrophil extracellular traps contain mitochondrial as well as nuclear DNA and exhibit inflammatory potential[J]. Cytometry A, 2012, 81(3): 238-247.
[17]	Chuah C, Jones MK, Burke ML, et al. Spatial and temporal transcriptomics of Schistosoma japonicum-induced hepatic granuloma formation reveals novel roles for neutrophils[J]. J Leukoc Biol, 2013, 94(2): 353-365.
[18]	Shen J, Lai DH, Wilson RA, et al. Nitric oxide blocks the development of the human parasite Schistosoma japonicum[J]. Proc Natl Acad Sci USA, 2017, 114(38): 10214-10219.
[19]	Peng H, Zhang Q, Li X, et al. IL-33 Contributes to Schistosoma japonicum-induced hepatic pathology through induction of M2 macrophages[J]. Sci Rep, 2016, 6: 29844.
[20]	Tang H, Liang YB, Chen ZB, et al. Soluble egg antigen activates M2 macrophages via the STAT6 and PI3K pathways, and Schistosoma japonicum alternatively activates macrophage polarization to improve the survival rate of septic mice[J]. J Cell Biochem, 2017, 118(12): 4230-4239.
[21]	Zhu JF, Xu ZP, Chen XJ, et al. Parasitic antigens alter macrophage polarization during Schistosoma japonicum infection in mice[J]. Parasit Vectors, 2014, 7: 122.
[22]	Ramachandran P, Iredale JP.Macrophages: central regulators of hepatic fibrogenesis and fibrosis resolution[J]. J Hepatol, 2012, 56(6): 1417-1419.
[23]	Schulte W, Bernhagen J, Bucala R.Cytokines in sepsis: potent immunoregulators and potential therapeutic targets: an updated view[J]. Mediators Inflamm, 2013, 2013: 165974.
[24]	Shaker Y, Samy N, Ashour E.Hepatobiliary schistosomiasis[J]. J Clin Transl Hepatol, 2014, 2(3): 212-216.
[25]	Li L, Cha HF, Yu XX, et al. The characteristics of NK cells in Schistosoma japonicum-infected mouse spleens[J]. Parasitol Res, 2015, 114(12): 4371-4379.
[26]	Chen DH, Xie HY, Luo XP, et al. Roles of Th17 cells in pulmonary granulomas induced by Schistosoma japonicum in C57BL/6 mice[J]. Cell Immunol, 2013, 285(1-2): 149-157.
[27]	Zhan TZ, Zhang TT, Wang YY, et al. Dynamics of Th9 cells and their potential role in immunopathogenesis of murine schistosomiasis[J]. Parasit Vectors, 2017, 10(1): 305.
[28]	Hou X, Yu FZ, Man SQ, et al. Negative regulation of Schistosoma japonicum egg-induced liver fibrosis by natural killer cells[J]. PLoS Negl Trop Dis, 2012, 6(1): e1456.
[29]	王晓玲, 胡媛, 曹建平. 自然杀伤细胞及其受体与血吸虫病肝纤维化[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(5): 504-509.
[30]	Ji F, Liu ZJ, Cao JP, et al. B cell response is required for granuloma formation in the early infection of Schistosoma japonicum[J]. PLoS One, 2008, 3(3): e1724.
[31]	Noh G, Lee JH.Regulatory B cells and allergic diseases[J]. Allergy Asthma Immunol Res, 2011, 3(3): 168-177.
[32]	Berthelot JM, Jamin C, Amrouche K, et al. Regulatory B cells play a key role in immune system balance[J]. Joint Bone Spine, 2013, 80(1): 18-22.
[33]	Tian F, Hu XL, Xian KW, et al. B10 cells induced by Schistosoma japonicum soluble egg antigens modulated regulatory T cells and cytokine production of T cells[J]. Parasitol Res, 2015, 114(10): 3827-3834.
[34]	Xu XY, Wen XY,Chi Y, et al. Activation-induced T helper cell death contributes to Th1/Th2 polarization following murine Schistosoma japonicum infection[J]. J Biomed Biotechnol, 2010, 202397.
[35]	Zhang YX, Huang DK, Gao WD, et al. Lack of IL-17 signaling decreases liver fibrosis in murine schistosomiasis japonica[J]. Int Immunol, 2015, 27(7): 317-325.
[36]	Meng FL, Wang K, Aoyama T, et al. Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice[J]. Gastroenterology, 2012, 143(3): 765-776.
[37]	方会龙, 陈福春, 江超, 等. IL-17在日本血吸虫虫卵肉芽肿中的作用[J]. 湘南学院学报(医学版), 2018, 20(2): 13-15.
[38]	Louahed J, Zhou Y, Maloy WL, et al. Interleukin 9 promotes influx and local maturation of eosinophils[J]. Blood, 2001, 97(4): 1035-1042.
[39]	Dugas B, Renauld JC, Pène J, et al. Interleukin-9 potentiates the interleukin-4-induced immunoglobulin (IgG, IgM and IgE) production by normal human B lymphocytes[J]. Eur J Immunol, 1993, 23(7): 1687-1692.
[40]	Zhou Y, Sonobe Y, Akahori T, et al. IL-9 promotes Th17cell migration into the central nervous system via CC chemokine ligand-20 produced by astrocytes[J]. J Immunol, 2011, 186(7): 4415-4421.
[41]	Chen XJ, Yang XW, Li Y, et al. Follicular helper T cells promote liver pathology in mice during Schistosoma japonicum infection[J]. PLoS Pathog, 2014, 10(5): e1004097.
[42]	Good-Jacobson KL, Szumilas CG, Chen LP, et al. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells[J]. Nat Immunol, 2010, 11(6): 535-542.
[43]	Glatman ZA, Taylor JJ, King IL, et al. T follicular helper cells differentiate from Th2 cells in response to helminth antigens[J]. J Exp Med, 2009, 206(5): 991-999.
[44]	Lüthje K, Kallies A, Shimohakamada Y, et al. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse[J]. Nat Immunol, 2012, 13(5): 491-498.
[45]	Anthony BJ, Ramm GA, McManus DP. Role of resident liver cells in the pathogenesis of schistosomiasis[J]. Trends Parasitol, 2012, 28(12): 572-579.
[46]	刘欣, 齐永芬, 鱼艳荣. 血吸虫病肝纤维化中可溶性虫卵抗原对肝星状细胞的作用[J]. 中国寄生虫学与寄生虫病杂志, 2019, 37(2): 218-222.
[47]	Anthony BJ, James KR, Gobert GN, et al. Schistosoma japonicum eggs induce a proinflammatory, anti-fibrogenic phenotype in hepatic stellate cells[J]. PLoS One, 2013, 8(6): e68479.
[48]	Wang Q, Chou X, Guan F, et al. Enhanced wnt signalling in hepatocytes is associated with Schistosoma japonicum infection and contributes to liver fibrosis[J]. Sci Rep, 2017, 7(1): 230.