Endogenously-Produced Hyaluronan and Its Potential to Regulate the Development of Peritoneal Adhesions
Language English Country Switzerland Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Review
PubMed
35053193
PubMed Central
PMC8773905
DOI
10.3390/biom12010045
PII: biom12010045
Knihovny.cz E-resources
- Keywords
- fibrosis, hyaluronan, inflammation, mesothelial cell, mesothelial-to-mesenchymal transition, metabolism, peritoneal adhesion,
- MeSH
- Epithelium MeSH
- Fibroblasts physiology MeSH
- Hyaluronic Acid * metabolism MeSH
- Myofibroblasts metabolism MeSH
- Peritoneum * metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- Hyaluronic Acid * MeSH
Formation of peritoneal adhesions (PA) is one of the major complications following intra-abdominal surgery. It is primarily caused by activation of the mesothelial layer and underlying tissues in the peritoneal membrane resulting in the transition of mesothelial cells (MCs) and fibroblasts to a pro-fibrotic phenotype. Pro-fibrotic transition of MCs-mesothelial-to-mesenchymal transition (MMT), and fibroblasts activation to myofibroblasts are interconnected to changes in cellular metabolism and culminate in the deposition of extracellular matrix (ECM) in the form of fibrotic tissue between injured sides in the abdominal cavity. However, ECM is not only a mechanical scaffold of the newly synthetized tissue but reciprocally affects fibrosis development. Hyaluronan (HA), an important component of ECM, is a non-sulfated glycosaminoglycan consisting of N-acetyl-D-glucosamine (GlcNAc) and D-glucuronic acid (GlcUA) that can affect the majority of processes involved in PA formation. This review considers the role of endogenously produced HA in the context of different fibrosis-related pathologies and its overlap in the development of PA.
Contipro a s Dolní Dobrouč 401 561 02 Dolní Dobrouč Czech Republic
Institute of Biophysics Academy of Sciences of the Czech Republic 612 65 Brno Czech Republic
Institute of Experimental Biology Faculty of Science Masaryk University 611 37 Brno Czech Republic
International Clinical Research Center St Anne's University Hospital 656 91 Brno Czech Republic
See more in PubMed
Brochhausen C., Schmitt V.H., Planck C.N., Rajab T.K., Hollemann D., Tapprich C., Kramer B., Wallwiener C., Hierlemann H., Zehbe R., et al. Current strategies and future perspectives for intraperitoneal adhesion prevention. J. Gastrointest Surg. 2012;16:1256–1274. doi: 10.1007/s11605-011-1819-9. PubMed DOI
Canis M., Botchorishvili R., Bourdel N., Gremeau A.S., Curinier S., Rabischong B. Pelvic adhesions and fertility: Where are we in 2018? J. Visc. Surg. 2018;155((Suppl. 1)):S11–S15. doi: 10.1016/j.jviscsurg.2018.02.004. PubMed DOI
Koninckx P.R., Gomel V., Ussia A., Adamyan L. Role of the peritoneal cavity in the prevention of postoperative adhesions, pain, and fatigue. Fertil. Steril. 2016;106:998–1010. doi: 10.1016/j.fertnstert.2016.08.012. PubMed DOI
Herrick S.E., Wilm B. Post-Surgical Peritoneal Scarring and Key Molecular Mechanisms. Biomolecules. 2021;11:692. doi: 10.3390/biom11050692. PubMed DOI PMC
Zwicky S.N., Stroka D., Zindel J. Sterile Injury Repair and Adhesion Formation at Serosal Surfaces. Front. Immunol. 2021;12:684967. doi: 10.3389/fimmu.2021.684967. PubMed DOI PMC
Capella-Monsonis H., Kearns S., Kelly J., Zeugolis D.I. Battling adhesions: From understanding to prevention. BMC Biomed. Eng. 2019;1:5. doi: 10.1186/s42490-019-0005-0. PubMed DOI PMC
Manou D., Caon I., Bouris P., Triantaphyllidou I.E., Giaroni C., Passi A., Karamanos N.K., Vigetti D., Theocharis A.D. The Complex Interplay Between Extracellular Matrix and Cells in Tissues. Methods Mol. Biol. 2019;1952:1–20. doi: 10.1007/978-1-4939-9133-4_1. PubMed DOI
Frantz C., Stewart K.M., Weaver V.M. The extracellular matrix at a glance. J. Cell Sci. 2010;123:4195–4200. doi: 10.1242/jcs.023820. PubMed DOI PMC
Bonnans C., Chou J., Werb Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 2014;15:786–801. doi: 10.1038/nrm3904. PubMed DOI PMC
Bulow R.D., Boor P. Extracellular Matrix in Kidney Fibrosis: More Than Just a Scaffold. J. Histochem. Cytochem. 2019;67:643–661. doi: 10.1369/0022155419849388. PubMed DOI PMC
Parker M.W., Rossi D., Peterson M., Smith K., Sikstrom K., White E.S., Connett J.E., Henke C.A., Larsson O., Bitterman P.B. Fibrotic extracellular matrix activates a profibrotic positive feedback loop. J. Clin. Investig. 2014;124:1622–1635. doi: 10.1172/JCI71386. PubMed DOI PMC
Ricard-Blum S. The collagen family. Cold Spring Harb. Perspect. Biol. 2011;3:a004978. doi: 10.1101/cshperspect.a004978. PubMed DOI PMC
Villesen I.F., Daniels S.J., Leeming D.J., Karsdal M.A., Nielsen M.J. Review article: The signalling and functional role of the extracellular matrix in the development of liver fibrosis. Aliment Pharm. 2020;52:85–97. doi: 10.1111/apt.15773. PubMed DOI
Chen K.B., Chen J., Jin X.L., Huang Y., Su Q.M., Chen L. Exosome-mediated peritoneal dissemination in gastric cancer and its clinical applications. Biomed. Rep. 2018;8:503–509. doi: 10.3892/br.2018.1088. PubMed DOI PMC
Herrera J., Henke C.A., Bitterman P.B. Extracellular matrix as a driver of progressive fibrosis. J. Clin. Investig. 2018;128:45–53. doi: 10.1172/JCI93557. PubMed DOI PMC
Theocharis A.D., Skandalis S.S., Gialeli C., Karamanos N.K. Extracellular matrix structure. Adv. Drug Deliv. Rev. 2016;97:4–27. doi: 10.1016/j.addr.2015.11.001. PubMed DOI
Vigetti D., Karousou E., Viola M., Deleonibus S., De Luca G., Passi A. Hyaluronan: Biosynthesis and signaling. Biochim. Biophys. Acta. 2014;1840:2452–2459. doi: 10.1016/j.bbagen.2014.02.001. PubMed DOI
Litwiniuk M., Krejner A., Speyrer M.S., Gauto A.R., Grzela T. Hyaluronic Acid in Inflammation and Tissue Regeneration. Wounds A Compend. Clin. Res. Pract. 2016;28:78–88. PubMed
Itano N., Sawai T., Yoshida M., Lenas P., Yamada Y., Imagawa M., Shinomura T., Hamaguchi M., Yoshida Y., Ohnuki Y., et al. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem. 1999;274:25085–25092. doi: 10.1074/jbc.274.35.25085. PubMed DOI
Vigetti D., Viola M., Karousou E., De Luca G., Passi A. Metabolic control of hyaluronan synthases. Matrix Biol. J. Int. Soc. Matrix Biol. 2014;35:8–13. doi: 10.1016/j.matbio.2013.10.002. PubMed DOI
Heldin P., Lin C.Y., Kolliopoulos C., Chen Y.H., Skandalis S.S. Regulation of hyaluronan biosynthesis and clinical impact of excessive hyaluronan production. Matrix Biol. J. Int. Soc. Matrix Biol. 2019;78-79:100–117. doi: 10.1016/j.matbio.2018.01.017. PubMed DOI
Garantziotis S., Savani R.C. Hyaluronan biology: A complex balancing act of structure, function, location and context. Matrix Biol. J. Int. Soc. Matrix. Biol. 2019;78-79:1–10. doi: 10.1016/j.matbio.2019.02.002. PubMed DOI PMC
Kaul A., Singampalli K.L., Parikh U.M., Yu L., Keswani S.G., Wang X. Hyaluronan, a double-edged sword in kidney diseases. Pediatric Nephrol. 2021 doi: 10.1007/s00467-021-05113-9. PubMed DOI PMC
Erickson M., Stern R. Chain gangs: New aspects of hyaluronan metabolism. Biochem. Res. Int. 2012;2012:893947. doi: 10.1155/2012/893947. PubMed DOI PMC
Stern R. Hyaluronan catabolism: A new metabolic pathway. Eur. J. Cell Biol. 2004;83:317–325. doi: 10.1078/0171-9335-00392. PubMed DOI
Yamaguchi Y., Yamamoto H., Tobisawa Y., Irie F. TMEM2: A missing link in hyaluronan catabolism identified? Matrix Biol. J. Int. Soc. Matrix Biol. 2019;78–79:139–146. doi: 10.1016/j.matbio.2018.03.020. PubMed DOI PMC
Tobisawa Y., Fujita N., Yamamoto H., Ohyama C., Irie F., Yamaguchi Y. The cell surface hyaluronidase TMEM2 is essential for systemic hyaluronan catabolism and turnover. J. Biol. Chem. 2021;297:101281. doi: 10.1016/j.jbc.2021.101281. PubMed DOI PMC
Yamazaki K., Fukuda K., Matsukawa M., Hara F., Yoshida K., Akagi M., Munakata H., Hamanishi C. Reactive oxygen species depolymerize hyaluronan: Involvement of the hydroxyl radical. Pathophysiology. 2003;9:215–220. doi: 10.1016/S0928-4680(03)00024-5. PubMed DOI
Avenoso A., Bruschetta G., D’Ascola A., Scuruchi M., Mandraffino G., Gullace R., Saitta A., Campo S., Campo G.M. Hyaluronan fragments produced during tissue injury: A signal amplifying the inflammatory response. Arch. Biochem. Biophys. 2019;663:228–238. doi: 10.1016/j.abb.2019.01.015. PubMed DOI
Albano G.D., Bonanno A., Cavalieri L., Ingrassia E., Di Sano C., Siena L., Riccobono L., Gagliardo R., Profita M. Effect of High, Medium, and Low Molecular Weight Hyaluronan on Inflammation and Oxidative Stress in an In Vitro Model of Human Nasal Epithelial Cells. Mediat. Inflamm. 2016;2016:8727289. doi: 10.1155/2016/8727289. PubMed DOI PMC
Yung S., Chan T.M. Hyaluronan--regulator and initiator of peritoneal inflammation and remodeling. Int. J. Artif. Organs. 2007;30:477–483. doi: 10.1177/039139880703000605. PubMed DOI
Dong Y., Arif A., Olsson M., Cali V., Hardman B., Dosanjh M., Lauer M., Midura R.J., Hascall V.C., Brown K.L., et al. Endotoxin free hyaluronan and hyaluronan fragments do not stimulate TNF-alpha, interleukin-12 or upregulate co-stimulatory molecules in dendritic cells or macrophages. Sci. Rep. 2016;6:36928. doi: 10.1038/srep36928. PubMed DOI PMC
Safrankova B., Hermannova M., Nesporova K., Velebny V., Kubala L. Absence of differences among low, middle, and high molecular weight hyaluronan in activating murine immune cells in vitro. Int. J. Biol. Macromol. 2018;107:1–8. doi: 10.1016/j.ijbiomac.2017.08.131. PubMed DOI
Scott J.E., Cummings C., Brass A., Chen Y. Secondary and tertiary structures of hyaluronan in aqueous solution, investigated by rotary shadowing-electron microscopy and computer simulation. Hyaluronan is a very efficient network-forming polymer. Biochem. J. 1991;274 Pt 3:699–705. doi: 10.1042/bj2740699. PubMed DOI PMC
Harris E.N., Baker E. Role of the Hyaluronan Receptor, Stabilin-2/HARE, in Health and Disease. Int. J. Mol. Sci. 2020;21:3504. doi: 10.3390/ijms21103504. PubMed DOI PMC
de la Motte C.A. Hyaluronan in intestinal homeostasis and inflammation: Implications for fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 2011;301:G945–G949. doi: 10.1152/ajpgi.00063.2011. PubMed DOI PMC
Wilson R.B. Hypoxia, cytokines and stromal recruitment: Parallels between pathophysiology of encapsulating peritoneal sclerosis, endometriosis and peritoneal metastasis. Pleura Peritoneum. 2018;3:20180103. doi: 10.1515/pp-2018-0103. PubMed DOI PMC
Banerji S., Wright A.J., Noble M., Mahoney D.J., Campbell I.D., Day A.J., Jackson D.G. Structures of the Cd44-hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction. Nat. Struct. Mol. Biol. 2007;14:234–239. doi: 10.1038/nsmb1201. PubMed DOI
Wolny P.M., Banerji S., Gounou C., Brisson A.R., Day A.J., Jackson D.G., Richter R.P. Analysis of CD44-hyaluronan interactions in an artificial membrane system: Insights into the distinct binding properties of high and low molecular weight hyaluronan. J. Biol. Chem. 2010;285:30170–30180. doi: 10.1074/jbc.M110.137562. PubMed DOI PMC
Yang C., Cao M., Liu H., He Y., Xu J., Du Y., Liu Y., Wang W., Cui L., Hu J., et al. The high and low molecular weight forms of hyaluronan have distinct effects on CD44 clustering. J. Biol. Chem. 2012;287:43094–43107. doi: 10.1074/jbc.M112.349209. PubMed DOI PMC
Kim S.J., Owen S.C. Hyaluronic acid binding to CD44S is indiscriminate of molecular weight. Biochim. Biophys. Acta-Biomembr. 2020;1862:183348. doi: 10.1016/j.bbamem.2020.183348. PubMed DOI
Sunabori T., Koike M., Asari A., Oonuki Y., Uchiyama Y. Suppression of Ischemia-Induced Hippocampal Pyramidal Neuron Death by Hyaluronan Tetrasaccharide through Inhibition of Toll-Like Receptor 2 Signaling Pathway. Am. J. Pathol. 2016;186:2143–2151. doi: 10.1016/j.ajpath.2016.03.016. PubMed DOI
Rugg M.S., Willis A.C., Mukhopadhyay D., Hascall V.C., Fries E., Fulop C., Milner C.M., Day A.J. Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J. Biol. Chem. 2005;280:25674–25686. doi: 10.1074/jbc.M501332200. PubMed DOI
Lesley J., Gal I., Mahoney D.J., Cordell M.R., Rugg M.S., Hyman R., Day A.J., Mikecz K. TSG-6 modulates the interaction between hyaluronan and cell surface CD44. J. Biol. Chem. 2004;279:25745–25754. doi: 10.1074/jbc.M313319200. PubMed DOI
Fulop C., Szanto S., Mukhopadhyay D., Bardos T., Kamath R.V., Rugg M.S., Day A.J., Salustri A., Hascall V.C., Glant T.T., et al. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development. 2003;130:2253–2261. doi: 10.1242/dev.00422. PubMed DOI
Fasanello D.C., Su J., Deng S., Yin R., Colville M.J., Berenson J.M., Kelly C.M., Freer H., Rollins A., Wagner B., et al. Hyaluronic acid synthesis, degradation, and crosslinking in equine osteoarthritis: TNF-alpha-TSG-6-mediated HC-HA formation. Arthritis Res. 2021;23:218. doi: 10.1186/s13075-021-02588-7. PubMed DOI PMC
Ni K., Gill A., Tseng V., Mikosz A.M., Koike K., Beatman E.L., Xu C.Y., Cao D., Gally F., Mould K.J., et al. Rapid clearance of heavy chain-modified hyaluronan during resolving acute lung injury. Respir. Res. 2018;19:107. doi: 10.1186/s12931-018-0812-1. PubMed DOI PMC
Bogdani M., Johnson P.Y., Potter-Perigo S., Nagy N., Day A.J., Bollyky P.L., Wight T.N. Hyaluronan and hyaluronan-binding proteins accumulate in both human type 1 diabetic islets and lymphoid tissues and associate with inflammatory cells in insulitis. Diabetes. 2014;63:2727–2743. doi: 10.2337/db13-1658. PubMed DOI PMC
Mutoji K.N., Sun M., Nash A., Puri S., Hascall V., Coulson-Thomas V.J. Anti-inflammatory protein TNFalpha-stimulated gene-6 (TSG-6) reduces inflammatory response after brain injury in mice. BMC Immunol. 2021;22:52. doi: 10.1186/s12865-021-00443-7. PubMed DOI PMC
Kang I., Chang M.Y., Wight T.N., Frevert C.W. Proteoglycans as Immunomodulators of the Innate Immune Response to Lung Infection. J. Histochem. Cytochem. Off. J. Histochem. Soc. 2018;66:241–259. doi: 10.1369/0022155417751880. PubMed DOI PMC
Gill S., Wight T.N., Frevert C.W. Proteoglycans: Key regulators of pulmonary inflammation and the innate immune response to lung infection. Anat. Rec. 2010;293:968–981. doi: 10.1002/ar.21094. PubMed DOI PMC
Tang M., Diao J., Gu H., Khatri I., Zhao J., Cattral M.S. Toll-like Receptor 2 Activation Promotes Tumor Dendritic Cell Dysfunction by Regulating IL-6 and IL-10 Receptor Signaling. Cell Rep. 2015;13:2851–2864. doi: 10.1016/j.celrep.2015.11.053. PubMed DOI
Albeiroti S., Soroosh A., de la Motte C.A. Hyaluronan’s Role in Fibrosis: A Pathogenic Factor or a Passive Player? Biomed. Res. Int. 2015;2015:790203. doi: 10.1155/2015/790203. PubMed DOI PMC
Sullivan W.J., Mullen P.J., Schmid E.W., Flores A., Momcilovic M., Sharpley M.S., Jelinek D., Whiteley A.E., Maxwell M.B., Wilde B.R., et al. Extracellular Matrix Remodeling Regulates Glucose Metabolism through TXNIP Destabilization. Cell. 2018;175:117–132.e121. doi: 10.1016/j.cell.2018.08.017. PubMed DOI PMC
Si M., Wang Q., Li Y., Lin H., Luo D., Zhao W., Dou X., Liu J., Zhang H., Huang Y., et al. Inhibition of hyperglycolysis in mesothelial cells prevents peritoneal fibrosis. Sci. Transl. Med. 2019;11 doi: 10.1126/scitranslmed.aav5341. PubMed DOI
Zhao X., Psarianos P., Ghoraie L.S., Yip K., Goldstein D., Gilbert R., Witterick I., Pang H., Hussain A., Lee J.H., et al. Metabolic regulation of dermal fibroblasts contributes to skin extracellular matrix homeostasis and fibrosis. Nat. Metab. 2019;1:147–157. doi: 10.1038/s42255-018-0008-5. PubMed DOI
Chanmee T., Ontong P., Izumikawa T., Higashide M., Mochizuki N., Chokchaitaweesuk C., Khansai M., Nakajima K., Kakizaki I., Kongtawelert P., et al. Hyaluronan Production Regulates Metabolic and Cancer Stem-like Properties of Breast Cancer Cells via Hexosamine Biosynthetic Pathway-coupled HIF-1 Signaling. J. Biol. Chem. 2016;291:24105–24120. doi: 10.1074/jbc.M116.751263. PubMed DOI PMC
Grandoch M., Flogel U., Virtue S., Maier J.K., Jelenik T., Kohlmorgen C., Feldmann K., Ostendorf Y., Castaneda T.R., Zhou Z., et al. 4-Methylumbelliferone improves the thermogenic capacity of brown adipose tissue. Nat. Metab. 2019;1:546–559. doi: 10.1038/s42255-019-0055-6. PubMed DOI PMC
Tammi M.I., Oikari S., Pasonen-Seppanen S., Rilla K., Auvinen P., Tammi R.H. Activated hyaluronan metabolism in the tumor matrix—Causes and consequences. Matrix Biol. J. Int. Soc. Matrix Biol. 2019;78-79:147–164. doi: 10.1016/j.matbio.2018.04.012. PubMed DOI
Tsitrina A.A., Krasylov I.V., Maltsev D.I., Andreichenko I.N., Moskvina V.S., Ivankov D.N., Bulgakova E.V., Nesterchuk M., Shashkovskaya V., Dashenkova N.O., et al. Inhibition of hyaluronan secretion by novel coumarin compounds and chitin synthesis inhibitors. Glycobiology. 2021;31:959–974. doi: 10.1093/glycob/cwab038. PubMed DOI PMC
Tsuchiya S., Ohashi Y., Ishizuka S., Ishiguro N., O’Rourke D.P., Knudson C.B., Knudson W. Suppression of murine osteoarthritis by 4-methylumbelliferone. J. Orthop. Res. 2020;38:1122–1131. doi: 10.1002/jor.24541. PubMed DOI PMC
Terabe K., Ohashi Y., Tsuchiya S., Ishizuka S., Knudson C.B., Knudson W. Chondroprotective effects of 4-methylumbelliferone and hyaluronan synthase-2 overexpression involve changes in chondrocyte energy metabolism. J. Biol. Chem. 2019;294:17799–17817. doi: 10.1074/jbc.RA119.009556. PubMed DOI PMC
Andreichenko I.N., Tsitrina A.A., Fokin A.V., Gabdulkhakova A.I., Maltsev D.I., Perelman G.S., Bulgakova E.V., Kulikov A.M., Mikaelyan A.S., Kotelevtsev Y.V. 4-methylumbelliferone Prevents Liver Fibrosis by Affecting Hyaluronan Deposition, FSTL1 Expression and Cell Localization. Int. J. Mol. Sci. 2019;20:6301. doi: 10.3390/ijms20246301. PubMed DOI PMC
Tsai J.M., Sinha R., Seita J., Fernhoff N., Christ S., Koopmans T., Krampitz G.W., McKenna K.M., Xing L., Sandholzer M., et al. Surgical adhesions in mice are derived from mesothelial cells and can be targeted by antibodies against mesothelial markers. Sci. Transl. Med. 2018;10 doi: 10.1126/scitranslmed.aan6735. PubMed DOI
Koopmans T., Rinkevich Y. Mesothelial to mesenchyme transition as a major developmental and pathological player in trunk organs and their cavities. Commun. Biol. 2018;1:170. doi: 10.1038/s42003-018-0180-x. PubMed DOI PMC
Mutsaers S.E., Prele C.M., Pengelly S., Herrick S.E. Mesothelial cells and peritoneal homeostasis. Fertil. Steril. 2016;106:1018–1024. doi: 10.1016/j.fertnstert.2016.09.005. PubMed DOI
Witowski J., Jorres A. Peritoneal cell culture: Fibroblasts. Perit. Dial. Int. 2006;26:292–299. doi: 10.1177/089686080602600302. PubMed DOI
Kawanishi K. Diverse properties of the mesothelial cells in health and disease. Pleura Peritoneum. 2016;1:79–89. doi: 10.1515/pp-2016-0009. PubMed DOI PMC
Fortin C.N., Saed G.M., Diamond M.P. Predisposing factors to post-operative adhesion development. Hum. Reprod. Update. 2015;21:536–551. doi: 10.1093/humupd/dmv021. PubMed DOI
Yung S., Coles G.A., Williams J.D., Davies M. The source and possible significance of hyaluronan in the peritoneal cavity. Kidney Int. 1994;46:527–533. doi: 10.1038/ki.1994.304. PubMed DOI
Yung S., Thomas G.J., Davies M. Induction of hyaluronan metabolism after mechanical injury of human peritoneal mesothelial cells in vitro. Kidney Int. 2000;58:1953–1962. doi: 10.1111/j.1523-1755.2000.00367.x. PubMed DOI
Tzuman Y.C., Sapoznik S., Granot D., Nevo N., Neeman M. Peritoneal adhesion and angiogenesis in ovarian carcinoma are inversely regulated by hyaluronan: The role of gonadotropins. Neoplasia. 2010;12:51–60. doi: 10.1593/neo.91272. PubMed DOI PMC
Koistinen V., Jokela T., Oikari S., Karna R., Tammi M., Rilla K. Hyaluronan-positive plasma membrane protrusions exist on mesothelial cells in vivo. Histochem. Cell Biol. 2016;145:531–544. doi: 10.1007/s00418-016-1405-z. PubMed DOI
Haslinger B., Mandl-Weber S., Sellmayer A., Sitter T. Hyaluronan fragments induce the synthesis of MCP-1 and IL-8 in cultured human peritoneal mesothelial cells. Cell Tissue Res. 2001;305:79–86. doi: 10.1007/s004410100409. PubMed DOI
Yung S., Coles G.A., Davies M. IL-1 beta, a major stimulator of hyaluronan synthesis in vitro of human peritoneal mesothelial cells: Relevance to peritonitis in CAPD. Kidney Int. 1996;50:1337–1343. doi: 10.1038/ki.1996.446. PubMed DOI
Raby A.C., Gonzalez-Mateo G.T., Williams A., Topley N., Fraser D., Lopez-Cabrera M., Labeta M.O. Targeting Toll-like receptors with soluble Toll-like receptor 2 prevents peritoneal dialysis solution-induced fibrosis. Kidney Int. 2018;94:346–362. doi: 10.1016/j.kint.2018.03.014. PubMed DOI
Shi J., Li Q., Sheng M., Zheng M., Yu M., Zhang L. The Role of TLR4 in M1 Macrophage-Induced Epithelial-Mesenchymal Transition of Peritoneal Mesothelial Cells. Cell. Physiol. Biochem. Int. J. Exp. Cell. Physiol. Biochem. Pharmacol. 2016;40:1538–1548. doi: 10.1159/000453204. PubMed DOI
Tsai J.M., Shoham M., Fernhoff N.B., George B.M., Marjon K.D., McCracken M.N., Kao K.S., Sinha R., Volkmer A.K., Miyanishi M., et al. Neutrophil and monocyte kinetics play critical roles in mouse peritoneal adhesion formation. Blood Adv. 2019;3:2713–2721. doi: 10.1182/bloodadvances.2018024026. PubMed DOI PMC
Dechaud H., Witz C.A., Montoya-Rodriguez I.A., Degraffenreid L.A., Schenken R.S. Mesothelial cell-associated hyaluronic acid promotes adhesion of endometrial cells to mesothelium. Fertil. Steril. 2001;76:1012–1018. doi: 10.1016/S0015-0282(01)02839-4. PubMed DOI
Rodgers A.K., Nair A., Binkley P.A., Tekmal R., Schenken R.S. Inhibition of CD44 N- and O-linked glycosylation decreases endometrial cell lines attachment to peritoneal mesothelial cells. Fertil. Steril. 2011;95:823–825. doi: 10.1016/j.fertnstert.2010.09.005. PubMed DOI PMC
Krediet R.T., Struijk D.G. Peritoneal changes in patients on long-term peritoneal dialysis. Nat. Rev. Nephrol. 2013;9:419–429. doi: 10.1038/nrneph.2013.99. PubMed DOI
Wang N., Li Q., Zhang L., Lin H., Hu J., Li D., Shi S., Cui S., Zhou J., Ji J., et al. Mesenchymal stem cells attenuate peritoneal injury through secretion of TSG-6. PLoS ONE. 2012;7:e43768. doi: 10.1371/journal.pone.0043768. PubMed DOI PMC
Kanda R., Hamada C., Kaneko K., Nakano T., Wakabayashi K., Io H., Horikoshi S., Tomino Y. Pentraxin 3 as a new biomarker of peritoneal injury in peritoneal dialysis patients. J. Artif. Organs. 2013;16:66–73. doi: 10.1007/s10047-012-0663-3. PubMed DOI
Tai Y.S., Jou I.M., Jung Y.C., Wu C.L., Shiau A.L., Chen C.Y. In vivo expression of thrombospondin-1 suppresses the formation of peritoneal adhesion in rats. World J. Gastrointest Surg. 2019;11:85–92. doi: 10.4240/wjgs.v11.i2.85. PubMed DOI PMC
Osada S., Hamada C., Shimaoka T., Kaneko K., Horikoshi S., Tomino Y. Alterations in proteoglycan components and histopathology of the peritoneum in uraemic and peritoneal dialysis (PD) patients. Nephrol. Dial. Transpl. 2009;24:3504–3512. doi: 10.1093/ndt/gfp268. PubMed DOI
Wang X., Balaji S., Steen E.H., Blum A.J., Li H., Chan C.K., Manson S.R., Lu T.C., Rae M.M., Austin P.F., et al. High-molecular weight hyaluronan attenuates tubulointerstitial scarring in kidney injury. JCI Insight. 2020;5:e136345. doi: 10.1172/jci.insight.136345. PubMed DOI PMC
Chang S.H., Yeh Y.H., Lee J.L., Hsu Y.J., Kuo C.T., Chen W.J. Transforming growth factor-beta-mediated CD44/STAT3 signaling contributes to the development of atrial fibrosis and fibrillation. Basic Res. Cardiol. 2017;112:58. doi: 10.1007/s00395-017-0647-9. PubMed DOI
Decleves A.E., Caron N., Voisin V., Legrand A., Bouby N., Kultti A., Tammi M.I., Flamion B. Synthesis and fragmentation of hyaluronan in renal ischaemia. Nephrol. Dial. Transplant. Off. Publ. Eur. Dial. Transpl. Assoc.-Eur. Ren. Assoc. 2012;27:3771–3781. doi: 10.1093/ndt/gfs098. PubMed DOI
Frangogiannis N.G. Cardiac fibrosis. Cardiovasc. Res. 2021;117:1450–1488. doi: 10.1093/cvr/cvaa324. PubMed DOI PMC
Muller J., Gorressen S., Grandoch M., Feldmann K., Kretschmer I., Lehr S., Ding Z., Schmitt J.P., Schrader J., Garbers C., et al. Interleukin-6-dependent phenotypic modulation of cardiac fibroblasts after acute myocardial infarction. Basic Res. Cardiol. 2014;109:440. doi: 10.1007/s00395-014-0440-y. PubMed DOI
Colombaro V., Decleves A.E., Jadot I., Voisin V., Giordano L., Habsch I., Nonclercq D., Flamion B., Caron N. Inhibition of hyaluronan is protective against renal ischaemia-reperfusion injury. Nephrol. Dial. Transplant. Off. Publ. Eur. Dial. Transpl. Assoc.-Eur. Ren. Assoc. 2013;28:2484–2493. doi: 10.1093/ndt/gft314. PubMed DOI
Meran S., Thomas D., Stephens P., Martin J., Bowen T., Phillips A., Steadman R. Involvement of hyaluronan in regulation of fibroblast phenotype. J. Biol. Chem. 2007;282:25687–25697. doi: 10.1074/jbc.M700773200. PubMed DOI
Meran S., Thomas D.W., Stephens P., Enoch S., Martin J., Steadman R., Phillips A.O. Hyaluronan facilitates transforming growth factor-beta1-mediated fibroblast proliferation. J. Biol. Chem. 2008;283:6530–6545. doi: 10.1074/jbc.M704819200. PubMed DOI
Jenkins R.H., Thomas G.J., Williams J.D., Steadman R. Myofibroblastic differentiation leads to hyaluronan accumulation through reduced hyaluronan turnover. J. Biol. Chem. 2004;279:41453–41460. doi: 10.1074/jbc.M401678200. PubMed DOI
Ontong P., Prachayasittikul V. Unraveled roles of hyaluronan in severe COVID-19. EXCLI J. 2021;20:117–125. doi: 10.17179/excli2020-3215. PubMed DOI PMC
Pandey A., Kulshrestha R., Bansal S.K. Dynamic role of LMW-hyaluronan fragments and Toll-like receptors 2,4 in progression of bleomycin induced lung parenchymal injury to fibrosis. Egypt. J. Bronchol. 2021;15:1–13. doi: 10.1186/s43168-021-00073-y. DOI
Li Y., Jiang D., Liang J., Meltzer E.B., Gray A., Miura R., Wogensen L., Yamaguchi Y., Noble P.W. Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J. Exp. Med. 2011;208:1459–1471. doi: 10.1084/jem.20102510. PubMed DOI PMC
Huebener P., Abou-Khamis T., Zymek P., Bujak M., Ying X., Chatila K., Haudek S., Thakker G., Frangogiannis N.G. CD44 is critically involved in infarct healing by regulating the inflammatory and fibrotic response. J. Immunol. 2008;180:2625–2633. doi: 10.4049/jimmunol.180.4.2625. PubMed DOI
Midgley A.C., Oltean S., Hascall V., Woods E.L., Steadman R., Phillips A.O., Meran S. Nuclear hyaluronidase 2 drives alternative splicing of CD44 pre-mRNA to determine profibrotic or antifibrotic cell phenotype. Sci. Signal. 2017;10 doi: 10.1126/scisignal.aao1822. PubMed DOI
Patouraux S., Rousseau D., Bonnafous S., Lebeaupin C., Luci C., Canivet C.M., Schneck A.S., Bertola A., Saint-Paul M.C., Iannelli A., et al. CD44 is a key player in non-alcoholic steatohepatitis. J. Hepatol. 2017;67:328–338. doi: 10.1016/j.jhep.2017.03.003. PubMed DOI
Yang Y.M., Noureddin M., Liu C., Ohashi K., Kim S.Y., Ramnath D., Powell E.E., Sweet M.J., Roh Y.S., Hsin I.F., et al. Hyaluronan synthase 2-mediated hyaluronan production mediates Notch1 activation and liver fibrosis. Sci. Transl. Med. 2019;11 doi: 10.1126/scitranslmed.aat9284. PubMed DOI PMC
Zaman A., Cui Z., Foley J.P., Zhao H., Grimm P.C., Delisser H.M., Savani R.C. Expression and role of the hyaluronan receptor RHAMM in inflammation after bleomycin injury. Am. J. Respir. Cell Mol. Biol. 2005;33:447–454. doi: 10.1165/rcmb.2004-0333OC. PubMed DOI PMC
Cui Z., Liao J., Cheong N., Longoria C., Cao G., DeLisser H.M., Savani R.C. The Receptor for Hyaluronan-Mediated Motility (CD168) promotes inflammation and fibrosis after acute lung injury. Matrix Biol. J. Int. Soc. Matrix Biol. 2019;78-79:255–271. doi: 10.1016/j.matbio.2018.08.002. PubMed DOI PMC
Colombaro V., Jadot I., Decleves A.E., Voisin V., Giordano L., Habsch I., Malaisse J., Flamion B., Caron N. Lack of hyaluronidases exacerbates renal post-ischemic injury, inflammation, and fibrosis. Kidney Int. 2015;88:61–71. doi: 10.1038/ki.2015.53. PubMed DOI
Evanko S.P., Potter-Perigo S., Petty L.J., Workman G.A., Wight T.N. Hyaluronan Controls the Deposition of Fibronectin and Collagen and Modulates TGF-beta1 Induction of Lung Myofibroblasts. Matrix Biol. 2015;42:74–92. doi: 10.1016/j.matbio.2014.12.001. PubMed DOI PMC
Chen C.H., Sue Y.M., Cheng C.Y., Chen Y.C., Liu C.T., Hsu Y.H., Hwang P.A., Huang N.J., Chen T.H. Oligo-fucoidan prevents renal tubulointerstitial fibrosis by inhibiting the CD44 signal pathway. Sci. Rep. 2017;7:40183. doi: 10.1038/srep40183. PubMed DOI PMC