Overexpression of hyaluronan synthase 2 alters hyaluronan distribution and function in proximal tubular epithelial cells

Journal of the American Society of Nephrology

Volumn 17, Issue 6, 2006, Pages 1553-1567

  Selbi, Wisam ^a   Day, Anthony J ^b   Rugg, Marilyn S ^b   Fülöp, Csaba ^c   De La Motte, Carol A ^d   Bowen, Timothy ^a   Hascall, Vincent C ^c   Phillips, Aled O ^a  

^a CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^b MRC Immunochemistry Unit   (United Kingdom)

^c Section of Connective Tissue Biology   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; HYALURONAN SYNTHASE 2; HYALURONIC ACID; HYALURONIDASE; INTER ALPHA INHIBITOR; MESSENGER RNA; MUTANT PROTEIN; PLASMA PROTEIN; PROTEIN PRECURSOR; RECOMBINANT PROTEIN; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; COVALENT BOND; ENZYME INDUCTION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GENE; GENE OVEREXPRESSION; GLYCOSAMINOGLYCAN METABOLISM; HUMAN; HUMAN CELL; INFLAMMATION; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; KIDNEY SCAR; MOLECULAR WEIGHT; MONOCYTE; PRIORITY JOURNAL; TUMOR NECROSIS FACTOR ALPHA STIMULATED GENE 6;

EID: 33646923701     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2005080879     Document Type: Article

References (68)

1. Hansell P, Goransson V, Odlind C, Gerdin B, Hallgren R: Hyaluronan content in the kidney in different states of body hydration. Kidney Int 58: 2061-2068, 2000
2. Sibalic V, Fan X, Loffing J, Wurthrich RP: Upregulated renal tubular CD44, hyaluronan, and osteopontin in kdkd mice with interstitial nephritis. Nephrol Dial Transplant 12: 1344-1353, 1997
3. Lewington AJP, Padanilam BJ, Martin DR, Hammeramn MR: Expression of CD44 in kidney after acute ischemic injury in rats. Am J Physiol 278: R247-R254, 2000
4. Wells A, Larsson E, Hanas E, Laurent T, Hallgren R, Tufvesson G: Increased hyaluronan in acutely rejecting human kidney grafts. Transplantation 55: 1346-1349, 1993
5. Wells AF, Larsson E, Tengblad A, Fellstrom B, Tufvesson G, Klareskog L, Laurent TC: The localisation of hyaluronan in normal and rejected human kidneys. Transplantation 50: 240-243, 1990
6. Sano N, Kitazawa K, Sugisaki T: Localization and roles of CD44, hyaluronic acid and osteopontin in IgA nephropathy. Nephron 89: 416-421, 2001
7. Yang J, Liu Y: Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 159: 1465-1475, 2001
8. Tian YC, Phillips AO: Interaction between the TGF-beta type II receptor/Smad pathway and beta-catenin during TGF-beta1 mediated adherens junction disassembly. Am J Pathol 160: 1619-1628, 2002
9. Tian YC, Fraser DJ, Attisano L, Phillips AO: TGF-beta1 mediated alterations of renal proximal tubular epithelial cell phenotype. Am J Physiol 285: F130-F142, 2003
10. Evans RA, Tian YC, Steadman R, Phillips AO: TGF-beta1-mediated fibroblast-myofibroblast terminal differentiation-the role of Smad proteins. Exp Cell Res 282: 90-100, 2003
11. Grande M, Franzen A, Karlsson JO, Ericson LE, Heldin NE, Nilsson M: Transforming growth factor-beta and epideral growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes. J Cell Sci 115: 4227-4236, 2002
12. Zeisberg M, Bonner G, Maeshima Y, Colorado P, Muller GA, Strutz F, Kalluri R: Collagen composition and assembly regulates epithelial mesenchymal transdifferentiation. Am J Pathol 159: 1313-1321, 2001
13. Tian YC, Phillips AO: TGF-beta1 mediated inhibition of HK-2 cell migration. J Am Soc Nephrol 14: 631-640, 2003
14. Ito T, Williams JD, Fraser DJ, Phillips AO: Hyaluronan regulates TGF-beta1 receptor compartmentalisation. J Biol Chem 279: 25326-25332, 2004
15. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL: Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5: 410-421, 2003
16. Ito T, Williams JD, Fraser DJ, Phillips AO: Hyaluronan attenuates TGF-beta1 mediated signalling in renal proximal tubular epithelial cells. Am J Pathol 164: 1979-1988, 2004
17. Spicer AP, McDonald JA: Characterisation and molecular evolution of a vertebrate hyaluronan synthase gene family. J Biol Chem 272: 1923-1932, 1998
18. Jones SG, Jones S, Phillips AO: Regulation of renal proximal tubular epithelial cell hyaluronan generation: Implications for diabetic nephropathy. Kidney Int 59: 1739-1749, 2001
19. Evanko SP, Angello JC, Wight TN: Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19: 1004-1013, 1999
20. Cohen M, Klein E, Geiger B, Addadi L: Organization and adhesive properties of the hyaluronan pericellular coat of chondrocytes and epithelial cells. Biophys J 85: 1996-2005, 2003
21. Selbi WD, De La Motte CA, Hascall VC, Phillips AO: BMP-7 modulates HA mediated proximal tubular cell-monocyte interaction. J Am Soc Nephrol 15: 1199-1211, 2004
22. Zhang XL, Selbi WD, De La Motte CA, Hascall VC, Phillips AO: Renal proximal tubular epithelial cells transforming growth factor beta1 generation and monocyte binding. Am J Pathol 165: 763-773, 2004
23. Salier JP, Rouet P, Raguenez G, Daveau M: The inter-alpha inhibitor: From structure to regulation. Biochem J 315: 1-9, 1996
24. Janssen U, Thomas G, Giant T, Phillips AO: Regulation of inter-alpha-trypsin inhibitor (IalphaI) and tumour necrosis factor-stimulated gene 6 (TSG-6) expression in human renal proximal tubular epithelial cells. Kidney Int 60: 126-136, 2001
25. Zhuo L, Hascall VC, Kimata K: Inter-alpha-trypsin inhibitor, a covalent protein-glycosaminoglycan-protein complex. J Biol Chem 279: 38079-38082, 2004
26. Zhuo L, Yoneda M, Zhao M, Yingsung W, Yoshida N, Kitagawa Y, Kawamura K, Suzuki T, Kimata K: Defect in SHAP-hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice. J Biol Chem 276: 7693-7696, 2001
27. Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, Day AJ, Salustri A, Hascall VC, Glant TT, Mikecz K: Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130: 2253-2261, 2003
28. Kobayashi H, Gotoh J, Hirashima Y, Terao T: Inter alpha inhibitor bound to tumour cells is cleaved into the heavy chains and the light chain on the cell surface. J Biol Chem 271: 11362-11367, 1996
29. Chen L, Mao SJ, McLean LR, Powers RW, Larsen WJ: Proteins of the inter-alpha-trypsin inhibitor family stabilize the cumulus extracellular matrix through their direct binding with hyaluronic acid. J Biol Chem 269: 28282-28287, 1994
30. de La Motte CA, Hascall VC, Drazba J, Bandyopadhyay SK, Strong SA: 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 func tion. Am J Pathol 163: 121-133, 2003
31. Parkar AA, Day AJ: Overlapping sites on the link module of human TSG-6 mediate binding to hyaluronan and chondroitin-4-sulphate. FEBS Lett 410: 413-417, 1997
32. Parkar AA, Kahmann JD, Howat SL, Bayliss MT, Day AJ: TSG-6 interacts with hyaluronan and aggrecan in a pH-dependent manner via a common functional element: Implications for its regulation in inflamed cartilage. FEBS Lett 428: 171-176, 1998
33. Milner CM, Day AJ: TSG-6: A multifunctional protein associated with inflammation. J Cell Sci 116: 1863-1873, 2003
34. Cao TV, La M, Getting SJ, Day AJ, Perretti M: Inhibitory effects of TSG-6 Link module on leukocyte-endothelial cell interactions in vitro and in vivo. Microcirculation 11: 615-624, 2004
35. Lesley J, Gal I, Mahoney DJ, Cordell MR, Rugg MS, Hyman R, Day AJ, Mikecz K: TSG-6 modulates the interaction between hyaluronan and cell surface CD44. J Biol Chem 279: 25745-25754, 2004
36. Ryan MJ, Johnson G, Kirk J, Fuerstenberg SM, Zager RA, Torok-Storb B: HK-2: An immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int 45: 48-57, 1994
37. Yung S, Davies M: Mechanical injury of human peritoneal mesothelial cells is accompanied by an increase in hyaluronan synthesis. J Am Soc Nephrol 9: 531, 1998
38. Yung S, Davies M: Response of the human peritoneal mesothelial cell to injury: An in vitro model of peritoneal wound healing. Kidney Int 554: 2160-2169, 1998
39. Cheng S, Fockler C, Barnes WM, Higuchi R: Effective amplification of long targets from cloned inserts and human genomic DNA. Proc Natl Acad Sci U S A 91: 5695-5699, 1994
40. Lesley J, English NM, Gal I, Mikecz K, Day AJ, Hyman R: Hyaluronan binding properties of a CD44 chimera containing the link module of TSG-6. J Biol Chem 277: 26600-26608, 2002
41. Knudson W, Aguiar DJ, Hua Q, Knudson CB: CD-44 anhored hyaluronan-rich pericellular matrices: An ultrastructural and biochemical analysis. Exp Cell Res 228: 216-228, 1996
42. Laemmli UK: Cleavage of structural proteins during the assembly the head of bacteriophage T4. Nature 227: 680-685, 1970
43. de la Motte CA, Hascall VC, Calabro A, Yen-Lieberman B, Strong SA: 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: 30747-30755, 1999
44. Yung S, Thomas GJ, Davies M: Induction of hyaluronan metabolism after mechanical injury of human peritoneal mesothelial cells in vitro. Kidney Int 58: 1953-1962, 2000
45. Phillips AO, Steadman R, Topley N, Williams JD: Elevated D-glucose concentrations modulate TGF-beta1 synthesis by human cultured renal proximal tubular cells: The permissive role of platelet derived growth factor. Am J Pathol 147: 362-374, 1995
46. Lee TH, Wisniewski HG, Vilcek J: A novel secretory tumour 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: 545-557, 1992
47. Nentwich HA, Mustafa Z, Rugg MS, Marsden BD, Cordell MR, Mahoney DJ, Jenkins SC, Dowling B, Fries E, Milner CM, Loughlin J, Day AJ: A novel allelic variant of the human TSG-6 gene encoding an amino acid difference in the CUB module. Chromosomal localization, frequency analysis, modeling, and expression. J Biol Chem 277: 15354-15362, 2002
48. Mahoney DJ, Blundell CD, Day AJ: Mapping the hyaluronan-binding site on the link module from human tumor necrosis factor-stimulated gene-6 by site-directed mutagenesis. J Biol Chem 276: 22764-22771, 2001
49. Getting SJ, Mahoney DJ, Cao T, Rugg MS, Fries E, Milner CM, Perretti M, Day AJ: The link module from human TSG-6 inhibits neutrophil migration in a hyaluronan- and inter-alpha-inhibitor-independent manner. J Biol Chem 277: 51068-51076, 2002
50. Ito T, Williams JD, Al-Assaf S, Phillips GO, Phillips AO: Hyaluronan and proximal tubular epithelial cell migration. Kidney Int 65: 823-833, 2004
51. Zhang XL, Selbi WD, De La Motte CA, Hascall VC, Phillips AO: BMP-7 inhibits monocyte stimulated TGF-beta1 generation in renal proximal tubular epithelial cells. J Am Soc Nephrol 1: 79-89, 2005
52. Enghild JJ, Thogersen IB, Pizzo SV, Salvesen G: Analysis of inter-alpha-trypsin inhibitor and a novel trypsin inhibitor, pre-alpha-trypsin inhibitor, from human plasma. Polypeptide chain stoichiometry and assembly by glycan. J Biol Chem 264: 15975-15981, 1989
53. Mukhopadhyay D, Hascall VC, Day AJ, Salustri A, Fulop C: 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: 173-181, 2001
54. Rugg MS, Willis AC, Mukhopadhyay D, Hascall VC, Fries E, Fulop C, Milner CM, Day AJ: Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains on to hyaluronan. J Biol Chem 280: 25674-25686, 2005
55. Ochsner SA, Day AJ, Rugg MS, Breyer RM, Gomer RH, Richards JS: Disrupted function of tumor necrosis factor-alpha-stimulated gene 6 blocks cumulus cell-oocyte complex expansion. Endocrinology 144: 4376-4384, 2003
56. Blundell CD, Mahoney DJ, Almond A, DeAngelis PL, Kahmann JD, Teriete P, Pickford AR, Campbell ID, Day AJ: The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding. J Biol Chem 278: 49261-49270, 2003
57. Tammi MI, Day AJ, Turley EA: Hyaluronan and homeostasis: A balancing act. J Biol Chem 277: 4581-4584, 2002
58. Zoltan-Jones A, Huang L, Ghatak S, Toole BP: Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J Biol Chem 278: 45801-45810, 2003
59. Weigel PH, Hascall VC, Tammi M: Hyaluronan synthases. J Biol Chem 272: 13997-14000, 1997
60. Spicer AP, Kaback LA, Smith TJ, Seldin MF: Molecular cloning and characterisation of the human and mouse UDP-glucose dehydrogenase genes. J Biol Chem 273: 25117-25124, 1998
61. Nishida Y, Knudson CB, Nietfeld JJ, Margulis A, Knudson W: Antisense inhibition of hyaluronan synthase-2 in human articular chondrocytes inhibits proteoglycan retention and matrix assembly. J Biol Chem 274: 21893-21899, 1999
62. Culty M, Shizari M, Thompson EW, Underhill CB: Binding and degradation of hyaluronan by human breast cancer cell lines expressing different forms of CD44: Correlation with invasive potential. J Cell Physiol 160: 275-286, 1994
63. Hua Q, Knudson CB, Knudson W: Internalisation of hyaluronan by chondrocytes occurs via receptor mediated endocytosis. J Cell Sci 106: 365-375, 1993
64. Collis L, Hall C, Lange L, Ziebell M, Prestwich R, Turley EA: Rapid hyaluronan uptake is associated with enhanced motility: Implications for an intracellular mode of action. FEBS Lett 440: 444-449, 1998
65. Savani RC, Cao G, Pooler PM, Zaman A, Zhou Z, DeLisser HM: Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J Biol Chem 276: 36770-36778, 2001
66. Nedvetzki S, Gonen E, Assayag N, Reich R, Williams RO, Thurmond RL, Huang JF, Neudecker BA, Wang FS, Turley EA, Naor D: RHAMM, a receptor for hyaluronan-mediated motility, compensates for CD44 in inflamed CD44-knockout mice: A different interpretation of redundancy. Proc Natl Acad Sci U S A 101: 18081-18086, 2004
67. Fieber C, Baumann P, Vallon R, Termeer C, Simon JC, Hofmann M, Angel P, Herrlich P, Sleeman JP: Hyaluronan-oligosaccharide-induced transcription of metalloproteases. J Cell Sci 117: 359-367, 2004
68. De La Motte CA, Hascall VC, Drazba J, Strong SA: Poly I:C induces mononuclear leukocyte-adhesive hyaluronan structures on colon smooth muscle cells: IαI and versican facilitate adhesion. In: Hyaluronan 2000, Edited by Kennedy JF, Phillips GO, Williams PA, Wrexham, Woodhead Publishing Ltd., 2000, pages 381-388