Do changes in transglutaminase activity alter latent transforming growth factor beta activation in experimental diabetic nephropathy?

Nephrology Dialysis Transplantation

Volumn 25, Issue 12, 2010, Pages 3897-3910

  Huang, Linghong ^a   Haylor, John L ^a   Fisher, Marie ^a   Hau, Zoe ^a   El Nahas, A Meguid ^a   Griffin, Martin ^b   Johnson, Timothy S ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b ASTON UNIVERSITY   (United Kingdom)

Author keywords

diabetic nephropathy; extracellular matrix; fibrosis; transforming growth factor ; transglutaminase

Indexed keywords

BINDING PROTEIN; ENZYME INHIBITOR; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; KIDNEY PROXIMAL TUBULE; MINK; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; COCULTURE TECHNIQUES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FIBROSIS; GTP-BINDING PROTEINS; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MINK; OPOSSUMS; PROTEIN ISOFORMS; RATS; RATS, WISTAR; STREPTOZOCIN; SWISS 3T3 CELLS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TRANSGLUTAMINASES;

EID: 78649497500     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gfq291     Document Type: Article

References (58)

1. Taipale J, Saharinen J, Keski-Oja J. Extracellular matrix-associated transforming growth factor-beta: role in cancer cell growth and invasion. Adv Cancer Res 1998; 75: 87-134
2. Laiho M, Keski-Oja J. Transforming growth factors-beta as regulators of cellular growth and phenotype. Crit Rev Oncog 1992; 3: 1-26
3. Xie L, Law BK, Aakre ME et al. Transforming growth factor beta-regulated gene expression in a mouse mammary gland epithelial cell line. Breast Cancer Res 2003; 5: R187-R198
4. Chin SL, Johnson SA, Quinn J et al. A role for alphaV integrin sub-unit in TGF-beta-stimulated osteoclastogenesis. Biochem Biophys Res Commun 2003; 307: 1051-1058
5. Lijnen P, Petrov V. Transforming growth factor-beta 1-induced collagen production in cultures of cardiac fibroblasts is the result of the appearance of myofibroblasts. Meth Find Exp Clin Pharmacol 2002; 24: 333-344 (Pubitemid 34857097)
6. Roberts IS, Burrows C, Shanks JH et al. Interstitial myofibroblasts: predictors of progression in membranous nephropathy. J Clin Pathol 1997; 50: 123-127
7. Kim SJ, Denhez F, Kim KY et al. Activation of the second promoter of the transforming growth factor-beta 1 gene by transforming growth factor-beta 1 and phorbol ester occurs through the same target sequences. J Biol Chem 1989; 264: 19373-19378
8. Miyazono K, Olofsson A, Colosetti P et al. A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1. EMBO J 1991; 10: 1091-1101
9. Munger JS, Harpel JG, Gleizes PE et al. Latent transforming growth factor-beta: structural features and mechanisms of activation. Kidney Int 1997; 51: 1376-1382
10. Fisher M, Jones RA, Huang L et al. Modulation of tissue transgluta-minase in tubular epithelial cells alters extracellular matrix levels: a potential mechanism of tissue scarring. Matrix Biol 2009; 28: 20-31
11. Johnson TS, Griffin M, Thomas GL et al. The role of transglutami-nase in the rat subtotal nephrectomy model of renal fibrosis. J Clin Invest 1997; 99: 2950-2960
12. Johnson TS, Skill NJ, El Nahas AM et al. Transglutaminase transcription and antigen translocation in experimental renal scarring. J Am Soc Nephrol 1999; 10: 2146-2157
13. Skill NJ, Griffin M, El Nahas AM et al. Increases in renal epsilon-(gamma-glutamyl)-lysine crosslinks result from compartment-specific changes in tissue transglutaminase in early experimental diabetic nephropathy: pathologic implications. Lab Invest 2001; 81: 705-716
14. Nunes I, Gleizes PE, Metz CN et al. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta. J Cell Biol 1997; 136: 1151-1163
15. Kojima S, Nara K, Rifkin DB. Requirement for transglutaminase in the activation of latent transforming growth factor-beta in bovine endothelial cells. J Cell Biol 1993; 121: 439-448 (Pubitemid 23110886)
16. Verderio E, Gaudry C, Gross S et al. Regulation of cell surface tissue transglutaminase: effects on matrix storage of latent transforming growth factor-beta binding protein-1. J Histochem Cytochem 1999; 47: 1417-1432
17. Rosenthal AK, Gohr CM, Henry LA et al. Participation of trans-glutaminase in the activation of latent transforming growth factor beta1 in aging articular cartilage. Arthritis Rheum 2000; 43: 1729-1733
18. Szondy Z, Sarang Z, Molnar P et al. Transglutaminase 2-/- mice reveal a phagocytosis-associated crosstalk between macrophages and apoptotic cells. Proc Natl Acad Sci USA 2003; 100: 7812-7817
19. Shweke N, Boulos N, Jouanneau C et al. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 2008; 173: 631-642
20. Huang L, Haylor JL, Hau Z et al. Transglutaminase inhibition ameliorates experimental diabetic nephropathy. Kidney Int 2009; 76: 383-394
21. Remuzzi G, Schieppati A, Ruggenenti P. Clinical practice. Nephro-pathy in patients with type 2 diabetes. N Engl J Med 2002; 346: 1145-1151
22. El Nahas AM, Abo-Zenah H, Skill NJ et al. Elevated epsilon-(gamma- glutamyl)lysine in human diabetic nephropathy results from increased expression and cellular release of tissue transglutaminase. Nephron Clin Pract 2004; 97: c108-c117
23. Griffin M, Mongeot A, Collighan R et al. Synthesis of potent water-soluble tissue transglutaminase inhibitors. Bioorg Med Chem Lett 2008; 18: 5559-5562
24. Abe M, Harpel JG, Metz CN et al. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator in-hibitor-1 promoter-luciferase construct. Anal Biochem 1994; 216: 276-284
25. Gentile V, Thomazy V, Piacentini M et al. Expression of tissue trans-glutaminase in Balb-C 3T3 fibroblasts: effects on cellular morphology and adhesion. J Cell Biol 1992; 119: 463-474
26. Verderio E, Nicholas B, Gross S et al. Regulated expression of tissue transglutaminase in Swiss 3T3 fibroblasts: effects on the processing of fibronectin, cell attachment, and cell death. Exp Cell Res 1998; 239: 119-138
27. Millan FA, Denhez F, Kondaiah P et al. Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 1991; 111: 131-143
28. Douthwaite JA, Johnson TS, Haylor JL et al. Effects of transforming growth factor-beta1 on renal extracellular matrix components and their regulating proteins. J Am Soc Nephrol 1999; 10: 2109-2119
29. Annes JP, Chen Y, Munger JS et al. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J Cell Biol 2004; 165: 723-734
30. Van Waarde MA, Van Assen AJ, Kampinga HH et al. Quantification of transforming growth factor-beta in biological material using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 1997; 247: 45-51
31. Parker E, Sun L, Johnson TS. Upregulation of Tissue Transglutami-nase in Transforming Growth Factor-b Induced Epithelial Mesenchy-mal Transdifferentiation in Rat Tubular Epithelial Cells. In Renal Association 2006; Harrogate, UK 387
32. Haneda M, Koya D, Isono M et al. Overview of glucose signaling in mesangial cells in diabetic nephropathy. J Am Soc Nephrol 2003; 14: 1374-1382
33. Mason RM, Wahab NA. Extracellular matrix metabolism in diabetic nephropathy. J Am Soc Nephrol 2003; 14: 1358-1373
34. Navarro JF, Mora C. Diabetes, inflammation, proinflammatory cyto-kines, and diabetic nephropathy. ScientificWorldJournal 2006; 6: 908-917
35. Ando T, Okuda S, Tamaki K et al. Localization of transforming growth factor-beta and latent transforming growth factor-beta binding protein in rat kidney. Kidney Int 1995; 47: 733-739
36. Lesort M, AttanaVanich K, Zhang J et al. Distinct nuclear localization and activity of tissue transglutaminase. J Biol Chem 1998; 273: 11991-11994 (Pubitemid 28240553)
37. Johnson TS, Fisher M, Wang B et al. Upregulation and Cellular Release of Transglutaminase in a Novel Model of Chronic Acidosis Using Porcine Proximal Tubular Epithelial Cells. In Renal Association. UK: York University, 2002
38. Skill NJ, Johnson TS, Coutts IG et al. Inhibition of transglutaminase activity reduces extracellular matrix accumulation induced by high glucose levels in proximal tubular epithelial cells. J Biol Chem 2004; 279: 47754-47762
39. Johnson TS, El-Koraie AF, Skill NJ et al. Tissue transglutaminase and the progression of human renal scarring. J Am Soc Nephrol 2003; 14: 2052-2062
40. Schittny JC, Paulsson M, Vallan C et al. Protein cross-linking mediated by tissue transglutaminase correlates with the maturation of extracellular matrices during lung development. Am J Respir Cell Mol Biol 1997; 17: 334-343
41. Mirza A, Liu SL, Frizell E et al. A role for tissue transglutaminase in hepatic injury and fibrogenesis, and its regulation by NF-kappaB. Am J Physiol 1997; 272: G281-G288
42. Balklava Z, Verderio E, Collighan R et al. Analysis of tissue trans-glutaminase function in the migration of Swiss 3T3 fibroblasts: the active-state conformation of the enzyme does not affect cell motil-ity but is important for its secretion. J Biol Chem 2002; 277: 16567-16575
43. Munger JS, Huang X, Kawakatsu H et al. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999; 96: 319-328
44. Arend LJ, Smart AM, Briggs JP. Mouse beta(6) integrin sequence, pattern of expression, and role in kidney development. J Am Soc Nephrol 2000; 11: 2297-2305
45. Ma LJ, Yang H, Gaspert A et al. Transforming growth factor-beta-dependent and -independent pathways of induction of tubulointersti-tial fibrosis in beta6(-/-) mice. Am J Pathol 2003; 163: 1261-1273
46. Derynck R, Zhang Y, Feng XH. Smads: transcriptional activators of TGF-beta responses. Cell 1998; 95: 737-740
47. Schultz-Cherry S, Ribeiro S, Gentry L et al. Thrombospondin binds and activates the small and large forms of latent transforming growth factor-beta in a chemically defined system. J Biol Chem 1994; 269: 26775-26782
48. Ribeiro SM, Poczatek M, Schultz-Cherry S et al. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem 1999; 274: 13586-13593
49. Yung S, Lee CY, Zhang Q et al. Elevated glucose induction of thrombospondin-1 up-regulates fibronectin synthesis in proximal renal tubular epithelial cells through TGF-{beta}1 dependent and TGF-{beta}1 independent pathways. Nephrol Dial Transplant 2006; 21: 1504-1513
50. Thakar CV, Zahedi K, Revelo MPet al. Identification of thrombospon-din 1 (TSP-1) as a novel mediator of cell injury in kidney ischemia. J Clin Invest 2005; 115: 3451-3459
51. Holmes DI, Abdel-Wahab N, Mason RM. Identification of glucose-regulated genes in human mesangial cells by mRNA differential display. Biochem Biophys Res Commun 1997; 238: 179-184
52. Yevdokimova N, Wahab NA, Mason RM. Thrombospondin-1 is the key activator of TGF-beta1 in human mesangial cells exposed to high glucose. J Am Soc Nephrol 2001; 12: 703-712
53. Daniel C, Wiede J, Krutzsch HC et al. Thrombospondin-1 is a major activator of TGF-beta in fibrotic renal disease in the rat in vivo. Kidney Int 2004; 65: 459-468
54. Baricos WH, Cortez SL, Deboisblanc M et al. Transforming growth factor-beta is a potent inhibitor of extracellular matrix degradation by cultured human mesangial cells. J Am Soc Nephrol 1999; 10: 790-795
55. Yamamoto T, Nakamura T, Noble NA et al. Expression of transforming growth factor beta is elevated in human and experimental diabetic nephropathy. Proc Natl Acad Sci USA 1993; 90: 1814-1818
56. Lee EA, Seo JY, Jiang Z et al. Reactive oxygen species mediate high glucose-induced plasminogen activator inhibitor-1 up-regulation in mesangial cells and in diabetic kidney. Kidney Int 2005; 67: 1762-1771 57.
57. Singh R, Song RH, Alavi N et al. High glucose decreases matrix metalloproteinase-2 activity in rat mesangial cells via transforming growth factor-beta1. Exp Nephrol 2001; 9: 249-257
58. Wang SN, LaPage J, Hirschberg R. Role of glomerular ultrafiltration of growth factors in progressive interstitial fibrosis in diabetic ne-phropathy. Kidney Int 2000; 57: 1002-1014