Specific down-regulation of connective tissue growth factor attenuates progression of nephropathy in mouse models of type 1 and type 2 diabetes

FASEB Journal

Volumn 21, Issue 12, 2007, Pages 3355-3368

  Guha, Mausumee ^a   Xu, Zhong Gao ^b   Tung, David ^c   Lanting, Linda ^b   Natarajan, Rama ^b  

^a Kalypsys Inc   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^c PFIZER INC   (United States)

Author keywords

Antisense oligonucleotide; CTGF; Diabetic nephropathy; Glomerular mesangial cells

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; COLLAGEN TYPE 1; COLLAGEN TYPE 4; CONNECTIVE TISSUE GROWTH FACTOR; CREATININE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; FIBRONECTIN; GENE PRODUCT; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN PAI 1; STREPTOZOCIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ANTIBODY; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; HYBRID PROTEIN; IMMEDIATE EARLY PROTEIN; SCLEROPROTEIN; SIGNAL PEPTIDE;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHIMERA; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DIABETIC NEPHROPATHY; DOWN REGULATION; ENZYME PHOSPHORYLATION; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CELL; KIDNEY CORTEX; MESANGIUM; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEINURIA; RAT; STREPTOZOCIN DIABETES; TREATMENT RESPONSE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DISEASE COURSE; DISEASE MODEL; EXPERIMENTAL DIABETES MELLITUS; GENETICS; HUMAN; KIDNEY; METABOLISM; MOUSE MUTANT; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALIA; MURINAE; MUS;

ANIMALS; BIOLOGICAL MARKERS; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOWN-REGULATION; EXTRACELLULAR MATRIX PROTEINS; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY; MICE; MICE, INBRED C57BL; MICE, OBESE; OLIGONUCLEOTIDES, ANTISENSE; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS;

EID: 35248841125     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-6713com     Document Type: Article

References (41)

1. Kreisberg, J. I., and Ayo, S. H. (1993) The glomerular mesangium in diabetes mellitus. Kidney Int. 43, 109-113
2. Ziyadeh. F. N., and Han, D. C. (1997) Involvement of transforming growth factor-beta and its receptors in the pathogenesis of diabetic nephrology. Kidney Int. 60, S7-11
3. Reeves, W. B., and Andreoli, T. E. (2000) Transforming growth factor beta contributes to progressive diabetic nephropathy. Proc. Natl. Acad. Sci. U. S. A. 97, 7667-7669
4. Ziyadeh, F. N., Sharma, K., Ericksen, M., and Wolf, G. (1994) Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-β. J. Clin. Invest. 93, 536-542
5. Han, D. C., Isono, M., Hoffman, B. B., and Ziyadeh, F. N. (1999) High glucose stimulates proliferation and collagen type I synthesis in renal cortical fibroblasts: mediation by autocrine activation of TGF-beta. J. Am. Soc. Nephrol. 10, 1891-1899
6. Hoffman, B. B., Sharma, K., Zhu, Y., and Ziyadeh, F. N. (1998) Transcriptional activation of transforming growth factor-β1 in mesangial cell culture by high glucose concentration. Kidney Int. 54, 1107-1116
7. Sakharova, O. V., Taal, M. W., and Brenner, B. M. (2001) Pathogenesis of diabetic nephropathy: focus on transforming growth factor-beta and connective tissue growth factor. Curr. Opin. Nephrol. Hypertens. 10, 727-738
8. Bradham, D. M., Igarashi, A., Potter, R. L., and Grotendorst, G. R. (1991) Connective tissue growth factor: a cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10. J. Cell Biol. 114, 1285-1294
9. Bork, P. (1993) The modular architecture of a new family of growth regulators related to connective tissue growth factor. FEBS Lett. 327, 125-130
10. Brigstock, D. R. (1999) The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr. Rev. 20, 189-206
11. Lau, L. F., and Lam, S. C. (1999) The CCN family of angiogenic regulators: the integrin connection. Exp. Cell Res. 248, 44-57
12. Igarashi, A., Okochi, H., Bradham, D. M., and Grotendorst G. R. (1993) Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol. Biol. Cell 4, 637-645
13. Grotendorst, G. R., Okochi, H., and Hayashi, N. (1996) A novel transforming growth factor β response element controls the expression of the connective tissue growth factor gene. Cell Growth Differ. 7, 469-480
14. Murphy, M., Godson, C., Cannon, S., Kato, S., Mackenzie, H. S., Martin, F., and Brady, H. R. (1999) Suppression subtractive hybridization identifies high glucose levels as a stimulus for expression of connective tissue growth factor and other genes in human mesangial cells. J. Biol. Chem. 274, 5830-5834
15. Riser, B. L., Denichilo, M., Cortes, P., Baker, C., Grondin, J. M., Yee, J., and Narins, R. G. (2000) Regulation of connective tissue growth factor activity in cultured rat mesangial cells and its expression in experimental diabetic glomerulosclerosis. J. Am. Soc. Nephrol. 11, 25-38
16. Wahab, N. A., Yevdokimova, N., Weston, B. S., Roberts, T., Li, X. J., Brinkman, H., and Mason, R. M. (2001) Role of connective tissue growth factor in the pathogenesis of diabetic nephropathy. Biochem. J. 359, 77-87
17. Uchio, K, Graham. M., Dean. N. M., Rosenbaum. J., and Desmouliere, A. (2004) Down regulation of connective tissue growth factor and type 1 collagen mRNA expression by connective tissue growth factor antisense oligonucleotide during experimental fibrosis. Wound Repair Regen. 12, 60-66
18. Wang, S., Denichilo, M., Brubaker, C., and Hirschberg, R. (2001) Connective tissue growth factor in tubulointerstitial injury of diabetic nephropathy. Kidney Int. 60, 96-105
19. Yokoi, H., Mukoyoma, M., Nagae, T., Mori, K., Suganami, T., Sawai, K., Yoshioka, T., Koshikawa, M., Nishida, T., Takigawa, M., et al. (2004) Reduction in connective tissue growth factor by anstisense treatment ameliorates renal tubulointerstitial fibrosis. J. Am. Soc. Nephrol. 15, 1430-1440
20. Ziyadeh, F. N., Hoffman, B. B., Han, D. C., Iglesias-De La Cruz, M. C., Hong, S. W., Isono, M., Chen, S., McGowan, T. A., and Sharma, K. (2000) Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc. Natl. Acad. Sci. U. S. A. 97, 8015-8020
21. Iglesias-de la Cruz, M. C., Ziyadeh, F. N., Isono, M., Kouahou, M., Han, D. C., Kalluri, R., Mundel, P., and Chen, S. (2002) Effects of high glucose and TGF-β1 on the expression of collagen IV and vascular endothelial growth factor in mouse podocytes. Kidney Int. 62, 901-913
22. De Vriese, A. S., Tilton, R. G., Elger, M., Stephan, C. C., Kriz, W., and Lameire, N. H. (2001) Antibodies against vascular endothelial growth factor improve early renal dysfunction in experimental diabetes. J. Am. Soc. Nephrol. 12, 993-1000
23. Bloom, I. E., van Dijk, A. J., Wieten, L., Duran, K., Ito, Y., Kleij, L., Denichilo, M., Rabelink, T. J., Weening, J. J., Aten, J., and Goldschmeding, R. (2001) In vitro evidence for differential involvement of CTGF, TGFβ, and PDGF-BB in mesangial response to injury. Nephrol. Dial. Transplant. 16, 1139-1148
24. Twigg, S. M., Chen, M. M., Joly, A. H., Chakrapani, S. D., Tsubaki, J., Kim, H. S., Oh, Y., and Rosenfeld, R. G. (2001) Advanced glycosylation end products up-regulate connective tissue growth factor (insulin-like growth factor-binding protein-related protein 2) in human fibroblasts: a potential mechanism for expansion of extracellular matrix in diabetes mellitus. Endocrinology 142, 1760-1769
25. Gilbert, R. E., Akdeniz, A., Weitz, S., Usinger, W. R., Molineaux, C., Jones, S. E., Langham, R. G., and Jerums, G. (2003) Urinary connective tissue growth factor excretion in patients with type 1 diabetes and nephropathy. Diabetes Care 26, 2632-2636
26. Riser, B. L., Cortes, P., DeNichilo, M., Deshmukh, P. V., Chahal, P. S., Mohammed, A. K., Yee, J., and Kahkonen, D. (2003) Urinary CCN2 (CTGF) as a possible predictor of diabetic nephropathy: preliminary report. Kidney Int. 64, 451-458
27. Adler, S. G., Kang, S. W., Feld, S., Cha, D. R., Barba, L., Striker, L., Striker, G., Riser, B.L.LaPage, J., and Nast, C. C. (2001) Glomerular mRNAs in human type 1 diabetes: biochemical evidence for microalbuminuria as a manifestation of diabetic nephropathy. Kidney Int. 60, 2330-2336
28. Okada, H., Kikuta, T., Kobayashi, T., Inoue, T., Kanno, Y., Takigawa, T., Sugaya, T., Kopp, J. B., and Suzuki, H. (2005) Connective tissue growth factor expressed in tubular epithelium plays a pivotal role in renal fibrogenesis. J. Am. Soc. Nephrol. 16, 133-143
29. Breyer, M. D., Bottinger, E., Brosius, F. C., 3rd, Coffman, T. M., Harris, R. C., Heilig, C. W., and Sharma, K. (2005) Mouse models of diabetic nephropathy. J. Am. Soc. Nephrol. 16, 27-45
30. Monia, B. P., Lesnik, E. A., Gonzalez, C., Lima, W. F., McGee, D., Guinosso, C. J., Kawasaki, A. M., Cook, P. D., and Freier, S. M. (1993) Evaluation of 2′-modified oligonucleotides containing 2′-deoxy gaps as antisense inhibitors of gene expression. J. Biol. Chem. 268, 14514-14522
31. Peng, B., Andrews, J., Nestorov, I., Brennan, B., Nicklin, P., Rowland, M. (2001) Tissue distribution and physiologically based pharmacokinetics of antisense oligonucleotide ISIS 1082 in rats. Antisense Nucleic Acid Drug Dev. 11, 15-27
32. Reddy, M. A., Adler, S. G., Kim, Y. S., Lanting, L., Rossi, J. J., Kang, S. W., Nadler, J. L., Shahed, A., and Natarajan, R. (2002) Interaction of MAPK and 12-lipoxygenase pathways in growth and matrix protein expression in mesangial cells. Am. J. Physiol. 283, F985-F994
33. Kim Y. S., Xu Z-G., Reddy M. A., Lanting L., Sharma K., Adler S. G., and Natarajan, R. (2005) Novel interactions between transforming growth factor-β1 actions and the 12/15-lipoxygenase pathway in mesangial cells. J. Am. Soc. Nephrol. 16, 352-362
34. Leask, A., and Abraham D. J. (2004) TGF-beta signaling and the fibrotic response. FASEB J. 18, 816-827
35. Abdel-Wahab, N., Weston, B. S., Roberts, T., and Mason, R. M. (2002) Connective tissue growth factor and regulation of the mesangial cell cycle: role in cellular hypertrophy. J. Am. Soc. Nephrol. 13, 2437-2445
36. Van Nieuwenhoven, F. A., Jensen, L. J., Flyvbjerg, A., and Goldschmeding R. (2005) Imbalance of growth factor signaling in diabetic kidney disease: is connective tissue growth factor (CTGF, CCN2) the perfect intervention point. Nephrol. Dial. Transplant. 20, 6-10
37. McLennan, S. V., Wang, X. Y., Moreno, V., Yue, D. K., and Twigg, S. M. (2004) Connective tissue growth factor mediates high glucose effects on matrix degradation through tissue inhibitor of matrix metalloproteinase type 1: implications for diabetic nephropathy. Endocrinology 145, 5646-5655
38. Crean, J. K., Finlay, D., Murphy, M., Moss, C., Godson, C., Martin, F., and Brady, H. R. (2002) The role of p42/44 MAPK and protein kinase B in connective tissue growth factor induced extracellular matrix protein production, cell migration, and actin cytoskeletal rearrangement in human mesangial cells. J. Biol. Chem. 277, 44187-44194
39. Kang S-W., Adler, S. G., LaPage, J., and Natarajan, R. (2001) p38MAPK and MAPK kinase 3/6 mRNA and activities are increased in early diabetic glomeruli. Kidney Int. 60, 543-552
40. Abreu, J. G., Ketpura, N. I., Reversade, B., and De Robertis, E. M. (2002) Connective-tissue growth factor (CTGF) modulates cell signaling by BMP and TGF-beta. Nat. Cell Biol. 4, 599-604
41. Mori, T., Kawara, S., Shinozaki, M., Hayashi, N., Kakinuma, T., Igarashi, A., Takigawa, M., Nakanishi, T., and Takehara K. (1999) Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: A mouse fibrosis model. J. Cell. Physiol. 181, 153-159