TSG6 hyaluronan matrix remodeling dampens the inflammatory response during colitis

Matrix Biology - Tập 121 - Trang 149-166 - 2023
Nansy Albtoush1,2, Kimberly A. Queisser1,2, Ash Zawerton2, Mark E. Lauer3, Ellen J. Beswick4, Aaron C Petrey1,5,6,2
1University of Utah Molecular Medicine Program, Salt Lake City, Utah, 84112
2Lerner Research Institute, Department of Inflammation & Immunity, Cleveland Clinic, Cleveland, OH 44195, USA
3Lerner Research Institute, Department of Biomedical Engineering, Cleveland Clinic, Cleveland, OH 44195, USA
4Division of Gastroenterology, Department of Internal Medicine, University of Kentucky, Lexington, KY, United States
5Department of Pathology, Division of Microbiology & Immunology, University of Utah School of Medicine, Salt Lake City, Utah, 84132, USA
6Division of Gastroenterology, Department of Internal Medicine, University of Utah, Salt Lake City, Utah, USA

Tài liệu tham khảo

Gerdin, 1991, Localisation of hyaluronan in the human intestinal wall, Gut, 32, 760, 10.1136/gut.32.7.760 Weigel, 1997, Hyaluronan synthases, J Biol Chem, 272, 13997, 10.1074/jbc.272.22.13997 Day, 2019, TSG-6: A multifunctional protein with anti-inflammatory and tissue-protective properties, Matrix Biol, 78-79, 60, 10.1016/j.matbio.2018.01.011 Milner, 2003, TSG-6: a multifunctional protein associated with inflammation, J Cell Sci, 116, 1863, 10.1242/jcs.00407 Sivakumar, 2018, Midgut Laterality Is Driven by Hyaluronan on the Right, Dev Cell, 46, 533, 10.1016/j.devcel.2018.08.002 Hamm, 2008, Frequent expression loss of Inter-alpha-trypsin inhibitor heavy chain (ITIH) genes in multiple human solid tumors: a systematic expression analysis, BMC Cancer, 8, 25, 10.1186/1471-2407-8-25 Yingsung, 2003, Molecular heterogeneity of the SHAP-hyaluronan complex. Isolation and characterization of the complex in synovial fluid from patients with rheumatoid arthritis, The Journal of biological chemistry, 278, 32710, 10.1074/jbc.M303658200 Zhuo, 2006, SHAP potentiates the CD44-mediated leukocyte adhesion to the hyaluronan substratum, J Biol Chem, 281, 20303, 10.1074/jbc.M506703200 Lauer, 2015, Hyaluronan and Its Heavy Chain Modification in Asthma Severity and Experimental Asthma Exacerbation, J Biol Chem, 290, 23124, 10.1074/jbc.M115.663823 Swaidani, 2013, TSG-6 protein is crucial for the development of pulmonary hyaluronan deposition, eosinophilia, and airway hyperresponsiveness in a murine model of asthma, J Biol Chem, 288, 412, 10.1074/jbc.M112.389874 Zhang, 2012, Constitutive expression of inter-alpha-inhibitor (IalphaI) family proteins and tumor necrosis factor-stimulated gene-6 (TSG-6) by human amniotic membrane epithelial and stromal cells supporting formation of the heavy chain-hyaluronan (HC-HA) complex, J Biol Chem, 287, 12433, 10.1074/jbc.M112.342873 Zhuo, 2004, Inter-alpha-trypsin inhibitor, a covalent protein-glycosaminoglycan-protein complex, The Journal of biological chemistry, 279, 38079, 10.1074/jbc.R300039200 Day, 2005, Hyaluronan cross-linking: a protective mechanism in inflammation?, Trends in immunology, 26, 637, 10.1016/j.it.2005.09.009 de La Motte, 1999, Mononuclear leukocytes preferentially bind via CD44 to hyaluronan on human intestinal mucosal smooth muscle cells after virus infection or treatment with poly(I.C), J Biol Chem, 274, 30747, 10.1074/jbc.274.43.30747 de la Motte, 2003, Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid:polycytidylic acid: inter-alpha-trypsin inhibitor is crucial to structure and function, Am J Pathol, 163, 121, 10.1016/S0002-9440(10)63636-X Kessler, 2008, Hyaluronan (HA) deposition precedes and promotes leukocyte recruitment in intestinal inflammation, Clin Transl Sci, 1, 57, 10.1111/j.1752-8062.2008.00025.x Petrey, 2016, Thrombin Cleavage of Inter-alpha-inhibitor Heavy Chain 1 Regulates Leukocyte Binding to an Inflammatory Hyaluronan Matrix, J Biol Chem, 291, 24324, 10.1074/jbc.M116.755660 Petrey, 2019, Platelet hyaluronidase-2 regulates the early stages of inflammatory disease in colitis, Blood, 134, 765, 10.1182/blood.2018893594 Fiocchi, 1997, Intestinal inflammation: a complex interplay of immune and nonimmune cell interactions, The American journal of physiology, 273, G769 Ouyang, 2005, The emergence of inflammatory bowel disease in the Asian Pacific region, Curr Opin Gastroenterol, 21, 408 Vermeire, 2012, Towards a novel molecular classification of IBD, Dig Dis, 30, 425, 10.1159/000338147 Vermeire, 2012, Classification of inflammatory bowel disease: the old and the new, Curr Opin Gastroenterol, 28, 321, 10.1097/MOG.0b013e328354be1e Ananthakrishnan, 2015, Epidemiology and risk factors for IBD, Nat Rev Gastroenterol Hepatol, 12, 205, 10.1038/nrgastro.2015.34 Jostins, 2012, Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease, Nature, 491, 119, 10.1038/nature11582 de Souza, 2016, Immunopathogenesis of IBD: current state of the art, Nat Rev Gastroenterol Hepatol, 13, 13, 10.1038/nrgastro.2015.186 Shimshoni, 2015, ECM remodelling in IBD: innocent bystander or partner in crime? The emerging role of extracellular molecular events in sustaining intestinal inflammation, Gut, 64, 367, 10.1136/gutjnl-2014-308048 Mukhopadhyay, 2004, Specificity of the tumor necrosis factor-induced protein 6-mediated heavy chain transfer from inter-alpha-trypsin inhibitor to hyaluronan: implications for the assembly of the cumulus extracellular matrix, The Journal of biological chemistry, 279, 11119, 10.1074/jbc.M313471200 Rugg, 2005, Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan, The Journal of biological chemistry, 280, 25674, 10.1074/jbc.M501332200 Termeer, 2002, Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4, J Exp Med, 195, 99, 10.1084/jem.20001858 Hundhausen, 2021, Endothelial hyaluronan synthase 3 aggravates acute colitis in an experimental model of inflammatory bowel disease, Matrix Biol, 102, 20, 10.1016/j.matbio.2021.08.001 Yamaguchi, 2017, Serum-Derived Hyaluronan-Associated Protein Is a Novel Biomarker for Inflammatory Bowel Diseases, Digestion, 95, 146, 10.1159/000456071 de la Motte, 2009, Platelet-derived hyaluronidase 2 cleaves hyaluronan into fragments that trigger monocyte-mediated production of proinflammatory cytokines, Am J Pathol, 174, 2254, 10.2353/ajpath.2009.080831 Perse, 2012, Dextran sodium sulphate colitis mouse model: traps and tricks, J Biomed Biotechnol, 2012, 10.1155/2012/718617 Meshkibaf, 2016, Protective role of G-CSF in dextran sulfate sodium-induced acute colitis through generating gut-homing macrophages, Cytokine, 78, 69, 10.1016/j.cyto.2015.11.025 Li, 2014, IL-10 modulates DSS-induced colitis through a macrophage-ROS-NO axis, Mucosal Immunol, 7, 869, 10.1038/mi.2013.103 Beck-Schimmer, 1998, Hyaluronan induces monocyte chemoattractant protein-1 expression in renal tubular epithelial cells, J Am Soc Nephrol, 9, 2283, 10.1681/ASN.V9122283 Hodge-Dufour, 1997, Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages, J Immunol, 159, 2492, 10.4049/jimmunol.159.5.2492 Webber, 2009, Hyaluronan orchestrates transforming growth factor-beta1-dependent maintenance of myofibroblast phenotype, J Biol Chem, 284, 9083, 10.1074/jbc.M806989200 Mukhopadhyay, 2001, Two distinct populations of tumor necrosis factor-stimulated gene-6 protein in the extracellular matrix of expanded mouse cumulus cell-oocyte complexes, Arch Biochem Biophys, 394, 173, 10.1006/abbi.2001.2552 Briggs, 2015, Metal Ion-dependent Heavy Chain Transfer Activity of TSG-6 Mediates Assembly of the Cumulus-Oocyte Matrix, J Biol Chem, 290, 28708, 10.1074/jbc.M115.669838 Salustri, 2004, PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization, Development, 131, 1577, 10.1242/dev.01056 Nagyeri, 2011, TSG-6 protein, a negative regulator of inflammatory arthritis, forms a ternary complex with murine mast cell tryptases and heparin, J Biol Chem, 286, 23559, 10.1074/jbc.M111.222026 Lauer, 2013, Irreversible heavy chain transfer to hyaluronan oligosaccharides by tumor necrosis factor-stimulated gene-6, J Biol Chem, 288, 205, 10.1074/jbc.M112.403998 He, 2013, Immobilized heavy chain-hyaluronic acid polarizes lipopolysaccharide-activated macrophages toward M2 phenotype, J Biol Chem, 288, 25792, 10.1074/jbc.M113.479584 Sala, 2015, Mesenchymal Stem Cells Reduce Colitis in Mice via Release of TSG6, Independently of Their Localization to the Intestine, Gastroenterology, 149, 163, 10.1053/j.gastro.2015.03.013 Song, 2018, TSG-6 released from intraperitoneally injected canine adipose tissue-derived mesenchymal stem cells ameliorate inflammatory bowel disease by inducing M2 macrophage switch in mice, Stem Cell Res Ther, 9, 91, 10.1186/s13287-018-0841-1 Song, 2017, TSG-6 Secreted by Human Adipose Tissue-derived Mesenchymal Stem Cells Ameliorates DSS-induced colitis by Inducing M2 Macrophage Polarization in Mice, Sci Rep, 7, 5187, 10.1038/s41598-017-04766-7 Zhang, 2021, Inflammatory cytokines-stimulated human muscle stem cells ameliorate ulcerative colitis via the IDO-TSG6 axis, Stem Cell Res Ther, 12, 50, 10.1186/s13287-020-02118-3 Mittal, 2016, TNFalpha-stimulated gene-6 (TSG6) activates macrophage phenotype transition to prevent inflammatory lung injury, Proc Natl Acad Sci U S A, 113, E8151, 10.1073/pnas.1614935113 He, 2009, Biochemical characterization and function of complexes formed by hyaluronan and the heavy chains of inter-alpha-inhibitor (HC*HA) purified from extracts of human amniotic membrane, J Biol Chem, 284, 20136, 10.1074/jbc.M109.021881 Krausgruber, 2011, IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses, Nat Immunol, 12, 231, 10.1038/ni.1990 Paun, 2008, Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response, J Biol Chem, 283, 14295, 10.1074/jbc.M800501200 Corbin, 2020, IRF5 guides monocytes toward an inflammatory CD11c(+) macrophage phenotype and promotes intestinal inflammation, Sci Immunol, 5, 10.1126/sciimmunol.aax6085 Lee, 1990, Isolation and characterization of eight tumor necrosis factor-induced gene sequences from human fibroblasts, Mol Cell Biol, 10, 1982 Lee, 1992, A novel secretory tumor necrosis factor-inducible protein (TSG-6) is a member of the family of hyaluronate binding proteins, closely related to the adhesion receptor CD44, J Cell Biol, 116, 545, 10.1083/jcb.116.2.545 Szanto, 2004, Enhanced neutrophil extravasation and rapid progression of proteoglycan-induced arthritis in TSG-6-knockout mice, Arthritis Rheum, 50, 3012, 10.1002/art.20655 Mindrescu, 2002, Reduced susceptibility to collagen-induced arthritis in DBA/1J mice expressing the TSG-6 transgene, Arthritis Rheum, 46, 2453, 10.1002/art.10503 Sammarco, 2019, Hyaluronan Accelerates Intestinal Mucosal Healing through Interaction with TSG-6, Cells, 8, 10.3390/cells8091074 Zhang, 2017, Tumor necrosis factor alpha-stimulated gene-6 (TSG-6) inhibits the inflammatory response by inhibiting the activation of P38 and JNK signaling pathway and decreases the restenosis of vein grafts in rats, Heart Vessels, 32, 1536, 10.1007/s00380-017-1059-3 Tuo, 2012, Anti-inflammatory recombinant TSG-6 stabilizes the progression of focal retinal degeneration in a murine model, J Neuroinflammation, 9, 59, 10.1186/1742-2094-9-59 Mindrescu, 2000, Amelioration of collagen-induced arthritis in DBA/1J mice by recombinant TSG-6, a tumor necrosis factor/interleukin-1-inducible protein, Arthritis Rheum, 43, 2668, 10.1002/1529-0131(200012)43:12<2668::AID-ANR6>3.0.CO;2-E Abbadi, 2016, Hyaluronan Rafts on Airway Epithelial Cells, J Biol Chem, 291, 1448, 10.1074/jbc.M115.704288 Janssen, 2001, Expression of inter-alpha-trypsin inhibitor and tumor necrosis factor-stimulated gene 6 in renal proximal tubular epithelial cells, Kidney Int, 60, 126, 10.1046/j.1523-1755.2001.00779.x Kim, 2017, Hyaluronan 35kDa treatment protects mice from Citrobacter rodentium infection and induces epithelial tight junction protein ZO-1 in vivo, Matrix Biol, 62, 28, 10.1016/j.matbio.2016.11.001 Hill, 2012, Specific-sized hyaluronan fragments promote expression of human beta-defensin 2 in intestinal epithelium, J Biol Chem, 287, 30610, 10.1074/jbc.M112.356238 Kessler, 2018, Multifunctional Role of 35 Kilodalton Hyaluronan in Promoting Defense of the Intestinal Epithelium, J Histochem Cytochem, 66, 273, 10.1369/0022155417746775 Hill, 2013, Human milk hyaluronan enhances innate defense of the intestinal epithelium, J Biol Chem, 288, 29090, 10.1074/jbc.M113.468629 Kim, 2018, Layilin is critical for mediating hyaluronan 35kDa-induced intestinal epithelial tight junction protein ZO-1 in vitro and in vivo, Matrix Biol, 66, 93, 10.1016/j.matbio.2017.09.003 Petrey, 2019, Hyaluronan in inflammatory bowel disease: Cross-linking inflammation and coagulation, Matrix Biol, 78-79, 314, 10.1016/j.matbio.2018.03.011 Wei, 2020, IL-10 and IL-22 in Mucosal Immunity: Driving Protection and Pathology, Front Immunol, 11, 1315, 10.3389/fimmu.2020.01315 Koelink, 2020, Anti-TNF therapy in IBD exerts its therapeutic effect through macrophage IL-10 signalling, Gut, 69, 1053, 10.1136/gutjnl-2019-318264 Dharmasiri, 2021, Human Intestinal Macrophages Are Involved in the Pathology of Both Ulcerative Colitis and Crohn Disease, Inflamm Bowel Dis, 27, 1641, 10.1093/ibd/izab029 Soroosh, 2016, Crohn's Disease Fibroblasts Overproduce the Novel Protein KIAA1199 to Create Proinflammatory Hyaluronan Fragments, Cell Mol Gastroenterol Hepatol, 2, 358, 10.1016/j.jcmgh.2015.12.007 Kim, 2020, The Role of Hyaluronan Treatment in Intestinal Innate Host Defense, Front Immunol, 11, 569, 10.3389/fimmu.2020.00569 Zheng, 2009, Regulation of colonic epithelial repair in mice by Toll-like receptors and hyaluronic acid, Gastroenterology, 137, 2041, 10.1053/j.gastro.2009.08.055 Kessler, 2015, Hyaluronan Synthase 3 Null Mice Exhibit Decreased Intestinal Inflammation and Tissue Damage in the DSS-Induced Colitis Model, Int J Cell Biol, 2015, 10.1155/2015/745237 Kuipers, 2016, Hyaluronan synthesis is necessary for autoreactive T-cell trafficking, activation, and Th1 polarization, Proc Natl Acad Sci U S A, 113, 1339, 10.1073/pnas.1525086113 Homann, 2018, Hyaluronan synthase 3 promotes plaque inflammation and atheroprogression, Matrix Biol, 66, 67, 10.1016/j.matbio.2017.09.005 Dyer, 2014, TSG-6 inhibits neutrophil migration via direct interaction with the chemokine CXCL8, J Immunol, 192, 2177, 10.4049/jimmunol.1300194 Kieu, 2022, Kinetics of LYVE-1-positive M2-like macrophages in developing and repairing dental pulp in vivo and their pro-angiogenic activity in vitro, Sci Rep, 12, 5176, 10.1038/s41598-022-08987-3 Mahler, 1998, Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis, Am J Physiol, 274, G544 Colon, 2009, Transfer of inter-alpha-inhibitor heavy chains to hyaluronan by surface-linked hyaluronan-TSG-6 complexes, J Biol Chem, 284, 2320, 10.1074/jbc.M807183200 Petrey, 2016, Hyaluronan Depolymerization by Megakaryocyte Hyaluronidase-2 Is Required for Thrombopoiesis, Am J Pathol, 186, 2390, 10.1016/j.ajpath.2016.05.004