Treatment with the matricellular protein CCN3 blocks and/or reverses fibrosis development in obesity with diabetic nephropathy

American Journal of Pathology

Volumn 184, Issue 11, 2014, Pages 2908-2921

  Riser, Bruce L ^a,b   Najmabadi, Feridoon ^a   Garchow, Kendra ^a   Barnes, Jeffrey L ^c   Peterson, Darryl R ^a   Sukowski, Ernest J ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b BLR Bio LLC   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LAMININ; MESSENGER RNA; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; PLACEBO;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG SAFETY; GENE EXPRESSION; HISTOLOGY; KIDNEY CORTEX; KIDNEY FIBROSIS; KIDNEY HYPERTROPHY; MALE; MESANGIUM CELL; MOUSE; NONHUMAN; OBESITY; PODOCYTE; TREATMENT DURATION; UPREGULATION; ANIMAL; COMPLICATION; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FIBROSIS; KIDNEY; PATHOLOGY; TREATMENT OUTCOME;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; FIBROSIS; KIDNEY; MALE; MICE; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; OBESITY; TREATMENT OUTCOME;

EID: 84908192671     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.07.009     Document Type: Article

References (39)

1. E. Ritz, I. Rychlik, F. Locatelli, and S. Halimi End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions Am J Kidney Dis 34 1999 795 808
2. H.H. Parving, and P. Hovind Microalbuminuria in type 1 and type 2 diabetes mellitus: evidence with angiotensin converting enzyme inhibitors and angiotensin II receptor blockers for treating early and preventing clinical nephropathy Curr Hypertens Rep 4 2002 387 393
3. National Kidney and Urologic Diseases Information Clearinghouse (NKUDIC) ESRD costs, Kidney Disease Statistics for the United States 2012 National Institutes of Health Bethesda, MD 11
4. B.L. Riser, P. Cortes, and J. Yee Modelling the effects of vascular stress in mesangial cells Curr Opin Nephrol Hypertens 9 2000 43 47
5. B.L. Riser, S. Ladson-Wofford, A. Sharba, P. Cortes, K. Drake, C.J. Guerin, J. Yee, M.E. Choi, P.R. Segarini, and R.G. Narins TGF-beta receptor expression and binding in rat mesangial cells: modulation by glucose and cyclic mechanical strain Kidney Int 56 1999 428 439
6. B.L. Riser, M. Denichilo, P. Cortes, C. Baker, J.M. Grondin, J. Yee, and R.G. Narins Regulation of connective tissue growth factor activity in cultured rat mesangial cells and its expression in experimental diabetic glomerulosclerosis J Am Soc Nephrol 11 2000 25 38
7. B.L. Riser, and P. Cortes Connective tissue growth factor and its regulation: a new element in diabetic glomerulosclerosis Ren Fail 23 2001 459 470
8. S.G. Adler, S.W. Kang, S. Feld, D.R. Cha, L. Barba, L. Striker, G. Striker, B.L. Riser, J. LaPage, and C.C. Nast Glomerular mRNAs in human type 1 diabetes: biochemical evidence for microalbuminuria as a manifestation of diabetic nephropathy Kidney Int 60 2001 2330 2336
9. F.W. Tam, B.L. Riser, K. Meeran, J. Rambow, C.D. Pusey, and A.H. Frankel Urinary monocyte chemoattractant protein-1 (MCP-1) and connective tissue growth factor (CCN2) as prognostic markers for progression of diabetic nephropathy Cytokine 47 2009 37 42
10. B.L. Riser, P. Cortes, M. DeNichilo, P.V. Deshmukh, P.S. Chahal, A.K. Mohammed, J. Yee, and D. Kahkonen Urinary CCN2 (CTGF) as a possible predictor of diabetic nephropathy: preliminary report Kidney Int 64 2003 451 458
11. M. Guha, Z.G. Xu, D. Tung, L. Lanting, and R. Natarajan Specific down-regulation of connective tissue growth factor attenuates progression of nephropathy in mouse models of type 1 and type 2 diabetes FASEB J 21 2007 3355 3368
12. H. Yokoi, M. Mukoyama, T. Nagae, K. Mori, T. Suganami, K. Sawai, T. Yoshioka, M. Koshikawa, T. Nishida, M. Takigawa, A. Sugawara, and K. Nakao Reduction in connective tissue growth factor by antisense treatment ameliorates renal tubulointerstitial fibrosis J Am Soc Nephrol 15 2004 1430 1440
13. D.R. Brigstock, R. Goldschmeding, K.I. Katsube, S.C. Lam, L.F. Lau, K. Lyons, C. Naus, B. Perbal, B. Riser, M. Takigawa, and H. Yeger Proposal for a unified CCN nomenclature Mol Pathol 56 2003 127 128
14. D.R. Brigstock The CCN family: a new stimulus package J Endocrinol 178 2003 169 175
15. B. Perbal CCN proteins: multifunctional signalling regulators Lancet 363 2004 62 64
16. B. Perbal NOV (nephroblastoma overexpressed) and the CCN family of genes: structural and functional issues Mol Pathol 54 2001 57 79
17. A.W. Rachfal, and D.R. Brigstock Structural and functional properties of CCN proteins Vitam Horm 70 2005 69 103
18. B.L. Riser, F. Najmabadi, B. Perbal, D.R. Peterson, J.A. Rambow, M.L. Riser, E. Sukowski, H. Yeger, and S.C. Riser CCN3 (NOV) is a negative regulator of CCN2 (CTGF) and a novel endogenous inhibitor of the fibrotic pathway in an in vitro model of renal disease Am J Pathol 174 2009 1725 1734
19. B.L. Riser, F. Najmabadi, B. Perbal, J.A. Rambow, M.L. Riser, E. Sukowski, H. Yeger, S.C. Riser, and D.R. Peterson CCN3/CCN2 regulation and the fibrosis of diabetic renal disease J Cell Commun Signal 4 2010 39 50
20. K. Sataranatarajan, M.M. Mariappan, M.J. Lee, D. Feliers, G.G. Choudhury, J.L. Barnes, and B.S. Kasinath Regulation of elongation phase of mRNA translation in diabetic nephropathy: amelioration by rapamycin Am J Pathol 171 2007 1733 1742
21. K. Sataranatarajan, D. Feliers, M.M. Mariappan, H.J. Lee, M.J. Lee, R.T. Day, H. Yelamanchili, G. Ghosh-Choudhury, J.L. Barnes, H. Van Remmen, A.G. Richardson, and B.S. Kasinath Molecular events in matrix protein metabolism in the aging kidney Aging Cell 11 2012 1065 1073
22. T.S. Ha, J.L. Barnes, J.L. Stewart, C.W. Ko, J.H. Miner, D.R. Abrahamson, J.R. Sanes, and B.S. Kasinath Regulation of renal laminin in mice with type II diabetes J Am Soc Nephrol 10 1999 1931 1939
23. J.W. Pippin, M.A. Sparks, S.T. Glenn, S. Buitrago, T.M. Coffman, J.S. Duffield, K.W. Gross, and S.J. Shankland Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease Am J Pathol 183 2013 542 557
24. K.L. Hudkins, W. Pichaiwong, T. Wietecha, J. Kowalewska, M.C. Banas, M.W. Spencer, A. Muhlfeld, M. Koelling, J.W. Pippin, S.J. Shankland, B. Askari, M.E. Rabaglia, M.P. Keller, A.D. Attie, and C.E. Alpers BTBR Ob/Ob mutant mice model progressive diabetic nephropathy J Am Soc Nephrol 21 2010 1533 1542
25. K.A. Grunwald, K. Schueler, P.J. Uelmen, B.A. Lipton, M. Kaiser, K. Buhman, and A.D. Attie Identification of a novel Arg - >Cys mutation in the LDL receptor that contributes to spontaneous hypercholesterolemia in pigs J Lipid Res 40 1999 475 485
26. J.B. Flowers, A.T. Oler, S.T. Nadler, Y. Choi, K.L. Schueler, B.S. Yandell, C.M. Kendziorski, and A.D. Attie Abdominal obesity in BTBR male mice is associated with peripheral but not hepatic insulin resistance Am J Physiol Endocrinol Metab 292 2007 E936 E945
27. M.J. Soler, M. Riera, and D. Batlle New experimental models of diabetic nephropathy in mice models of type 2 diabetes: efforts to replicate human nephropathy Exp Diabetes Res 2012 2012 616313
28. H. Ha, E.Y. Oh, and H.B. Lee The role of plasminogen activator inhibitor 1 in renal and cardiovascular diseases Nat Rev Nephrol 5 2009 203 211
29. S. Krag, C.C. Danielsen, P. Carmeliet, J. Nyengaard, and L. Wogensen Plasminogen activator inhibitor-1 gene deficiency attenuates TGF-beta1-induced kidney disease Kidney Int 68 2005 2651 2666
30. A.K. Ghosh, and D.E. Vaughan PAI-1 in tissue fibrosis J Cell Physiol 227 2012 493 507
31. N.A. Wahab, B.S. Weston, and R.M. Mason Modulation of the TGFbeta/Smad signaling pathway in mesangial cells by CTGF/CCN2 Exp Cell Res 307 2005 305 314
32. S.B. Nicholas, E. Aguiniga, Y. Ren, J. Kim, J. Wong, N. Govindarajan, M. Noda, W. Wang, Y. Kawano, A. Collins, and W.A. Hsueh Plasminogen activator inhibitor-1 deficiency retards diabetic nephropathy Kidney Int 67 2005 1297 1307
33. K. Sharma, P. McCue, and S.R. Dunn Diabetic kidney disease in the db/db mouse Am J Physiol Renal Physiol 284 2002 F1138 F1144
34. S. Setty, A.A. Michael, A.J. Fish, S.M. Mauer, R.J. Butkowski, I. Virtanen, and Y. Kim Differential expression of laminin isoforms in diabetic nephropathy and other renal diseases Mod Pathol 25 2012 859 868
35. C.R. van Roeyen, F. Eitner, T. Scholl, P. Boor, U. Kunter, N. Planque, H.J. Grone, A.M. Bleau, B. Perbal, T. Ostendorf, and J. Floege CCN3 is a novel endogenous PDGF-regulated inhibitor of glomerular cell proliferation Kidney Int 73 2008 86 94
36. Y. Ito, R. Goldschmeding, R. Bende, N. Claessen, M. Chand, L. Kleij, T. Rabelink, J. Weening, and J. Aten Kinetics of connective tissue growth factor expression during experimental proliferative glomerulonephritis J Am Soc Nephrol 12 2001 472 484
37. B.L. Riser, N. Bhagavathula, P. Perone, K. Garchow, Y. Xu, G.J. Fisher, F. Najmabadi, D. Attili, and J. Varani Gadolinium-induced fibrosis is counter-regulated by CCN3 in human dermal fibroblasts: a model for potential treatment of nephrogenic systemic fibrosis J Cell Commun Signal 6 2012 97 105
38. C.R. van Roeyen, P. Boor, E. Borkham-Kamphorst, S. Rong, U. Kunter, I.V. Martin, A. Kaitovic, S. Fleckenstein, B. Perbal, C. Trautwein, R. Weiskirchen, T. Ostendorf, and J. Floege A novel, dual role of CCN3 in experimental glomerulonephritis: pro-angiogenic and antimesangioproliferative effects Am J Pathol 180 2012 1979 1990
39. E. Borkham-Kamphorst, C.R. van Roeyen, E. Van de Leur, J. Floege, and R. Weiskirchen CCN3/NOV small interfering RNA enhances fibrogenic gene expression in primary hepatic stellate cells and cirrhotic fat storing cell line CFSC J Cell Commun Signal 6 2012 11 25