Hyaluronan and versican in the control of human T-lymphocyte adhesion and migration

Matrix Biology

Volumn 31, Issue 2, 2012, Pages 90-100

  Evanko, Stephen P ^a   Potter Perigo, Susan ^a   Bollyky, Paul L ^a   Nepom, Gerald T ^a   Wight, Thomas N ^a  

^a BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

Hyaluronan; Inflammation; Lymphocyte; Migration; Myofibroblast; Versican

Indexed keywords

ANTIBODY; COLLAGEN GEL; HYALURONIC ACID; HYALURONIDASE; VERSICAN;

ARTICLE; CELL ADHESION; CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; CELL TRANSPORT; CHEMICAL COMPOSITION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; LUNG FIBROBLAST; LYMPHOCYTE MIGRATION; MYOFIBROBLAST; PRIORITY JOURNAL; SOLID STATE; SYNOVIOCYTE; T LYMPHOCYTE;

ANTIGENS, CD44; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN; EXTRACELLULAR MATRIX; FIBROBLASTS; FLUORESCEIN-5-ISOTHIOCYANATE; HUMANS; HYALURONIC ACID; HYALURONOGLUCOSAMINIDASE; INFLAMMATION; LUNG; LYMPHOCYTE ACTIVATION; POLY I-C; PROTEIN BINDING; TIME-LAPSE IMAGING; VERSICANS;

EID: 84857033876     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2011.10.004     Document Type: Article

References (49)

1. Bollyky P.L., Falk B.A., Long S.A., Preisinger A., Braun K.R., Wu R.P., Evanko S.P., Buckner J.H., Wight T.N., Nepom G.T. CD44 costimulation promotes FoxP3+ regulatory T cell persistence and function via production of IL-2, IL-10, and TGF-beta. J. Immunol. 2009, 183:2232-2241.
2. Bollyky P.L., Falk B.A., Wu R.P., Buckner J.H., Wight T.N., Nepom G.T. Intact extracellular matrix and the maintenance of immune tolerance: high molecular weight hyaluronan promotes persistence of induced CD4+CD25+ regulatory T cells. J. Leukoc. Biol. 2009, 86:567-572.
3. Bollyky P.L., Lord J.D., Masewicz S.A., Evanko S.P., Buckner J.H., Wight T.N., Nepom G.T. Cutting edge: high molecular weight hyaluronan promotes the suppressive effects of CD4+CD25+ regulatory T cells. J. Immunol. 2007, 179:744-747.
4. Bollyky, P.L., Wu, R.P., Falk, B.A., Lord, J.D., Long, S.A., Preisinger, A., Teng, B., Holt, G.E., Standifer, N.E., Braun, K.R., Xie, C.F., Samuels, P.L., Vernon, R.B., Gebe, J.A., Wight, T.N., Nepom, G.T., 2011. ECM components guide IL-10 producing regulatory T-cell (TR1) induction from effector memory T-cell precursors. Proc. Natl. Acad. Sci. U. S. A. 108, 7938-7943.
5. Brewton R.G., Mayne R. Mammalian vitreous humor contains networks of hyaluronan molecules: electron microscopic analysis using the hyaluronan-binding region (G1) of aggrecan and link protein. Exp. Cell Res. 1992, 198:237-249.
6. Day A.J., de la Motte C.A. Hyaluronan cross-linking: a protective mechanism in inflammation?. Trends Immunol. 2005, 26:637-643.
7. De la Motte C.A., Hascall V.C., Calabro A., Yen-Lieberman B., Strong S.A. 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. 1999, 274:30747-30755.
8. Denucci C.C., Mitchell J.S., Shimizu Y. Integrin function in T-cell homing to lymphoid and nonlymphoid sites: getting there and staying there. Crit. Rev. Immunol. 2009, 29:87-109.
9. Dours-Zimmermann M.T., Maurer K., Rauch U., Stoffel W., Fassler R., Zimmermann D.R. Versican V2 assembles the extracellular matrix surrounding the nodes of ranvier in the CNS. J. Neurosci. 2009, 29:7731-7742.
10. Dutt S., Kleber M., Matasci M., Sommer L., Zimmermann D.R. Versican V0 and V1 guide migratory neural crest cells. J. Biol. Chem. 2006, 281:12123-12131.
11. Ernst H., Zanin M.K.B., Everman D., Hoffman S. Receptor-mediated adhesive and anti-adhesive functions of chondroitin sulfate proteoglycan preparations from embryonic chicken brain. J. Cell Sci. 1995, 108:3807-3816.
12. Evanko S.P., Angello J.C., Wight T.N. Formation of hyaluronan and versican rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 1999, 19:1004-1013.
13. Evanko S.P., Potter-Perigo S., Johnson P.Y., Wight T.N. Organization of hyaluronan and versican in the extracellular matrix of human fibroblasts treated with the viral mimetic poly I:C. J. Histochem. Cytochem. 2009, 57:1041-1060.
14. Evanko S.P., Tammi M.I., Tammi R.H., Wight T.N. Hyaluronan-dependent pericellular matrix. Adv. Drug Deliv. Rev. 2007, 59:1351-1365.
15. Friedl P., Weigelin B. Interstitial leukocyte migration and immune function. Nat. Immunol. 2008, 9:960-969.
16. Hattori N., Carrino D.A., Lauer M.E., Vasanji A., Wylie J.D., Nelson C.M., Apte S.S. Pericellular versican regulates the fibroblast-myofibroblast transition. A role for ADAMTS5-mediated proteolysis. J. Biol. Chem. 2011, 286:34298-34310.
17. Hernandez D., Miquel-Serra L., Docampo M.J., Marco-Ramell A., Cabrera J., Fabra A., Bassols A. V3 versican isoform alters the behavior of human melanoma cells by interfering with CD44/ErbB-dependent signaling. J. Biol. Chem. 2010, 286:1475-1485.
18. Hoare K., Savani R.C., Wang C., Yang B., Turley E.A. Identification of hyaluronan binding proteins using a biotinylated hyaluronan probe. Connect. Tissue Res. 1993, 30:117-126.
19. Johnson P., Ruffell B. CD44 and its role in inflammation and inflammatory diseases. Inflamm. Allergy Drug Targets 2009, 8:208-220.
20. Kasperkovitz P.V., Timmer T.C., Smeets T.J., Verbeet N.L., Tak P.P., van Baarsen L.G., Baltus B., Huizinga T.W., Pieterman E., Fero M., Firestein G.S., van der Pouw Kraan T.C., Verweij C.L. Fibroblast-like synoviocytes derived from patients with rheumatoid arthritis show the imprint of synovial tissue heterogeneity: evidence of a link between an increased myofibroblast-like phenotype and high-inflammation synovitis. Arthritis Rheum. 2005, 52:430-441.
21. Korpos E., Wu C., Song J., Hallmann R., Sorokin L. Role of the extracellular matrix in lymphocyte migration. Cell Tissue Res. 2009, 339:47-57.
22. Kultti A., Rilla K., Tiihonen R., Spicer A.P., Tammi R.H., Tammi M.I. Hyaluronan synthesis induces microvillus-like cell surface protrusions. J. Biol. Chem. 2006, 281:15821-15828.
23. Landolt R.M., Vaughan L., Winterhalter K.H., Zimmermann D.R. Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development 1995, 121:2303-2312.
24. Lesley J., Howes N., Perschl A., Hyman R. Hyaluronan binding function of CD44 is transiently activated on T cells during an in vivo immune response. J. Exp. Med. 1994, 180:383-387.
25. Majors A.K., Austin R.C., de la Motte C.A., Pyeritz R.E., Hascall V.C., Kessler S.P., Sen G., Strong S.A. Endoplasmic reticulum stress induces hyaluronan deposition and leukocyte adhesion. J. Biol. Chem. 2003, 278:47223-47231.
26. 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.
27. Morgelin M., Paulsson M., Heinegard D., Aebi U., Engel J. Evidence of a defined spatial arrangement of hyaluronate in the central filament of cartilage proteoglycan aggregates. Biochem. J. 1995, 307:595-601.
28. Mow V.C., Mak A.F., Lai W.M., Rosenberg L.C., Tang L.H. Viscoelastic properties of proteoglycan subunits and aggregates in varying solution concentrations. J. Biomech. 1984, 17:325-338.
29. Mrass P., Kinjyo I., Ng L.G., Reiner S.L., Pure E., Weninger W. CD44 mediates successful interstitial navigation by killer T cells and enables efficient antitumor immunity. Immunity 2008, 29:971-985.
30. Noble P.W. Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol. 2002, 21:25-29.
31. Olin K.L., Potter-Perigo S., Barrett P.H., Wight T.N., Chait A. Lipoprotein lipase enhances the binding of native and oxidized low density lipoproteins to versican and biglycan synthesized by cultured arterial smooth muscle cells. J. Biol. Chem. 1999, 274:34629-34636.
32. Olin K.L., Potter-Perigo S., Barrett P.H., Wight T.N., Chait A. Biglycan, a vascular proteoglycan, binds differently to HDL2 and HDL3: role of apoE. Arterioscler. Thromb. Vasc. Biol. 2001, 21:129-135.
33. Potter-Perigo S., Johnson P.Y., Evanko S.P., Chan C.K., Braun K.R., Wilkinson T.S., Altman L.C., Wight T.N. Polyinosine-polycytidylic acid stimulates versican accumulation in the extracellular matrix promoting monocyte adhesion. Am. J. Respir. Cell Mol. Biol. 2010, 43:109-120.
34. Raghu G., Chen Y.Y., Rusch V., Rabinovitch P.S. Differential proliferation of fibroblasts cultured from normal and fibrotic human lungs. Am. Rev. Respir. Dis. 1988, 138:703-708.
35. Ruffell B., Johnson P. Hyaluronan induces cell death in activated T cells through CD44. J. Immunol. 2008, 181:7044-7054.
36. Selbi W., de la Motte C.A., Hascall V.C., Day A.J., Bowen T., Phillips A.O. Characterization of hyaluronan cable structure and function in renal proximal tubular epithelial cells. Kidney Int. 2006, 70:1287-1295.
37. Sorokin L. The impact of the extracellular matrix on inflammation. Nat. Rev. Immunol. 2010, 10:712-723.
38. Sugiura H., Ichikawa T., Koarai A., Yanagisawa S., Minakata Y., Matsunaga K., Hirano T., Akamatsu K., Ichinose M. Activation of Toll-like receptor 3 augments myofibroblast differentiation. Am. J. Respir. Cell Mol. Biol. 2009, 40:654-662.
39. Sugiyama K., Komada Y., Deguchi T., Zhang X.L., Azuma E., Ido M., Yamamoto H., Sakurai M. CD3-mediated T cell activation is inhibited by anti-CD44 monoclonal antibodies directed to the hyaluronan-binding region. Immunol. Invest. 1999, 28:185-200.
40. Toole B.P. Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 2004, 4:528-539.
41. Underhill C.B., Nguyen H., Shizari M., Culty M. CD44 positive macrophages take up hyaluronan during lung development. Dev. Biol. 1993, 155:324-336.
42. Wang A., Hascall V.C. Hyaluronan structures synthesized by rat mesangial cells in response to hyperglycemia induce monocyte adhesion. J. Biol. Chem. 2004, 279:10279-10285.
43. Webber J., Jenkins R.H., Meran S., Phillips A., Steadman R. Modulation of TGFbeta1-dependent myofibroblast differentiation by hyaluronan. Am. J. Pathol. 2009, 175:148-160.
44. Westergren-Thorsson G., Larsen K., Nihlberg K., Andersson-Sjoland A., Hallgren O., Marko-Varga G., Bjermer L. Pathological airway remodelling in inflammation. Clin. Respir. J. 2010, 4(Suppl 1):1-8.
45. Wilson E.H., Harris T.H., Mrass P., John B., Tait E.D., Wu G.F., Pepper M., Wherry E.J., Dzierzinski F., Roos D., Haydon P.G., Laufer T.M., Weninger W., Hunter C.A. Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 2009, 30:300-311.
46. Wolf K., Muller R., Borgmann S., Brocker E.B., Friedl P. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 2003, 102:3262-3269.
47. Yamagata M., Kimata K. Repression of a malignant cell-substratum adhesion phenotype by inhibiting the production of the anti-adhesive proteoglycan, PG-M/versican. J. Cell Sci. 1994, 107:2581-2590.
48. Yamagata M., Saga S., Kato M., Bernfield M., Kimata K. Selective distributions of proteoglycans and their ligands in pericellular matrix of cultured fibroblasts. Implications for their roles in cell-substratum adhesion. J. Cell Sci. 1993, 106:55-65.
49. Yamagata M., Suzuki S., Akiyama S., Yamada K., Kimata K. Regulation of cell-substrate adhesion by proteoglycans immobilized on extracellular substrates. J. Biol. Chem. 1989, 264:8012-8018.