A novel, dual role of CCN3 in experimental glomerulonephritis: Pro-angiogenic and antimesangioproliferative effects

American Journal of Pathology

Volumn 180, Issue 5, 2012, Pages 1979-1990

  Van Roeyen, Claudia R C ^a   Boor, Peter ^a,b,c   Borkham Kamphorst, Erawan ^b   Rong, Song ^a   Kunter, Uta ^a   Martin, Ina V ^a   Kaitovic, Ana ^a   Fleckenstein, Stefan ^a   Perbal, Bernard ^d   Trautwein, Christian ^b   Weiskirchen, Ralf ^b   Ostendorf, Tammo ^a   Floege, Jrgen ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c Physics and Informatics   (Slovakia)

^d RandD l'Oréal USA ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 4; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET DERIVED GROWTH FACTOR C; PLATELET DERIVED GROWTH FACTOR D; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; VASCULOTROPIN;

ALLERGIC GLOMERULONEPHRITIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE OVEREXPRESSION; GLOMERULOSCLEROSIS; HUMAN; HUMAN CELL; IMMUNOHISTOLOGY; MALE; MESANGIUM CELL; NEPHRITIS; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

ACTINS; ACUTE DISEASE; ANGIOGENESIS INDUCING AGENTS; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE IV; DISEASE PROGRESSION; ELECTROCHEMOTHERAPY; ENDOTHELIAL CELLS; FIBRONECTINS; GENE THERAPY; GLOMERULAR MESANGIUM; GLOMERULONEPHRITIS, MEMBRANOPROLIFERATIVE; HUMANS; KIDNEY GLOMERULUS; MALE; MESANGIAL CELLS; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; RNA, MESSENGER;

EID: 84860235408     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.01.031     Document Type: Article

References (47)

1. S. Klahr, G. Schreiner, I. Ichikawa The progression of renal disease N Engl J Med 318 1988 1657 1666
2. L.J. Striker, E.P. Peten, S.J. Elliot, T. Doi, G.E. Striker Mesangial cell turnover: effect of heparin and peptide growth factors Lab Invest 64 1991 446 456
3. J. Floege, R.J. Johnson Multiple roles for platelet-derived growth factor in renal disease Miner Electrolyte Metab 21 1995 271 282
4. R.J. Johnson, J. Floege, W.G. Couser, C.E. Alpers Role of platelet-derived growth factor in glomerular disease J Am Soc Nephrol 4 1993 119 128
5. J. Floege, F. Eitner, C.E. Alpers A new look at platelet-derived growth factor in renal disease J Am Soc Nephrol 19 2008 12 23
6. J. Floege, T. Ostendorf, U. Janssen, M. Burg, H.H. Radeke, C. Vargeese, S.C. Gill, L.S. Green, N. Janjic Novel approach to specific growth factor inhibition in vivo: antagonism of platelet-derived growth factor in glomerulonephritis by aptamers Am J Pathol 154 1999 169 179
7. T. Ostendorf, U. Kunter, H.J. Grone, F. Bahlmann, H. Kawachi, F. Shimizu, K.M. Koch, N. Janjic, J. Floege Specific antagonism of PDGF prevents renal scarring in experimental glomerulonephritis J Am Soc Nephrol 12 2001 909 918
8. T. Ostendorf, C.R. van Roeyen, J.D. Peterson, U. Kunter, F. Eitner, A.J. Hamad, G. Chan, X.C. Jia, J. Macaluso, G. Gazit-Bornstein, B.A. Keyt, H.S. Lichenstein, W.J. LaRochelle, J. Floege A fully human monoclonal antibody (CR002) identifies PDGF-D as a novel mediator of mesangioproliferative glomerulonephritis J Am Soc Nephrol 14 2003 2237 2247
9. T. Ostendorf, S. Rong, P. Boor, S. Wiedemann, U. Kunter, U. Haubold, C.R. van Roeyen, F. Eitner, H. Kawachi, G. Starling, E. Alvarez, G. Smithson, J. Floege Antagonism of PDGF-D by human antibody CR002 prevents renal scarring in experimental glomerulonephritis J Am Soc Nephrol 17 2006 1054 1062
10. P. Boor, A. Konieczny, L. Villa, U. Kunter, C.R. van Roeyen, W.J. LaRochelle, G. Smithson, S. Arrol, T. Ostendorf, J. Floege PDGF-D inhibition by CR002 ameliorates tubulointerstitial fibrosis following experimental glomerulonephritis Nephrol Dial Transplant 22 2007 1323 1331
11. C.R. van Roeyen, F. Eitner, T. Scholl, P. Boor, U. Kunter, N. Planque, H.J. Grone, A.M. Bleau, B. Perbal, T. Ostendorf, J. Floege CCN3 is a novel endogenous PDGF-regulated inhibitor of glomerular cell proliferation Kidney Int 73 2008 86 94
12. B. Perbal NOV (nephroblastoma overexpressed) and the CCN family of genes: structural and functional issues Mol Pathol 54 2001 57 79
13. S. Kocialkowski, H. Yeger, J. Kingdom, B. Perbal, P.N. Schofield Expression of the human NOV gene in first trimester fetal tissues Anat Embryol (Berl) 203 2001 417 427
14. M.J. Molnar, R. Gilbert, Y. Lu, A.B. Liu, A. Guo, N. Larochelle, K. Orlopp, H. Lochmuller, B.J. Petrof, J. Nalbantoglu, G. Karpati Factors influencing the efficacy, longevity, and safety of electroporation-assisted plasmid-based gene transfer into mouse muscles Mol Ther 10 2004 447 455
15. T. Muramatsu, S. Arakawa, K. Fukazawa, Y. Fujiwara, T. Yoshida, R. Sasaki, S. Masuda, H.M. Park In vivo gene electroporation in skeletal muscle with special reference to the duration of gene expression Int J Mol Med 7 2001 37 42
16. F. Eitner, T. Ostendorf, C. Van Roeyen, M. Kitahara, X. Li, K. Aase, H.J. Grone, U. Eriksson, J. Floege Expression of a novel PDGF isoform PDGF-C, in normal and diseased rat kidney J Am Soc Nephrol 13 2002 910 917
17. S. Kyurkchiev, H. Yeger, A.M. Bleau, B. Perbal Potential cellular conformations of the CCN3(NOV) protein Cell Commun Signal 2 2004 9
18. S.C. Satchell, C.H. Tasman, A. Singh, L. Ni, J. Geelen, C.J. von Ruhland, M.J. O'Hare, M.A. Saleem, L.P. van den Heuvel, P.W. Mathieson Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF Kidney Int 69 2006 1633 1640
19. P. Boor, C.R. van Roeyen, U. Kunter, L. Villa, E. Bucher, B. Hohenstein, C.P. Hugo, U. Eriksson, S.C. Satchell, P.W. Mathieson, F. Eitner, J. Floege, T. Ostendorf PDGF-C mediates glomerular capillary repair Am J Pathol 177 2010 58 69
20. T. Ostendorf, U. Kunter, F. Eitner, A. Loos, H. Regele, D. Kerjaschki, D.D. Henninger, N. Janjic, J. Floege VEGF(165) mediates glomerular endothelial repair J Clin Invest 104 1999 913 923
21. C.R. van Roeyen, T. Ostendorf, B. Denecke, D. Bokemeyer, I. Behrmann, F. Strutz, H.S. Lichenstein, W.J. LaRochelle, C.E. Pena, A. Chaudhuri, J. Floege Biological responses to PDGF-BB versus PDGF-DD in human mesangial cells Kidney Int 69 2006 1393 1402
22. N. Lazar, C. Manara, S. Navarro, A.M. Bleau, A. Llombart-Bosch, K. Scotlandi, N. Planque, B. Perbal Domain-specific CCN3 antibodies as unique tools for structural and functional studies J Cell Commun Signal 1 2007 91 102
23. B.L. Riser, F. Najmabadi, B. Perbal, D.R. Peterson, J.A. Rambow, M.L. Riser, E. Sukowski, H. Yeger, 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
24. B.L. Riser, F. Najmabadi, B. Perbal, J.A. Rambow, M.L. Riser, E. Sukowski, H. Yeger, S.C. Riser, D.R. Peterson CCN3/CCN2 regulation and the fibrosis of diabetic renal disease J Cell Commun Signal 4 2010 39 50
25. T. Minamizato, K. Sakamoto, T. Liu, H. Kokubo, K. Katsube, B. Perbal, S. Nakamura, A. Yamaguchi CCN3/NOV inhibits BMP-2-induced osteoblast differentiation by interacting with BMP and Notch signaling pathways Biochem Biophys Res Commun 354 2007 567 573
26. S. Rydziel, L. Stadmeyer, S. Zanotti, D. Durant, A. Smerdel-Ramoya, E. Canalis Nephroblastoma overexpressed (Nov) inhibits osteoblastogenesis and causes osteopenia J Biol Chem 282 2007 19762 19772
27. C.G. Lin, S.J. Leu, N. Chen, C.M. Tebeau, S.X. Lin, C.Y. Yeung, L.F. Lau CCN3 (NOV) is a novel angiogenic regulator of the CCN protein family J Biol Chem 278 2003 24200 24208
28. A.B. Fogo, V. Kon The glomerulus-a view from the inside-the endothelial cell Int J Biochem Cell Biol 42 2010 1388 1397
29. Y. Masuda, A. Shimizu, T. Mori, T. Ishiwata, H. Kitamura, R. Ohashi, M. Ishizaki, G. Asano, Y. Sugisaki, N. Yamanaka Vascular endothelial growth factor enhances glomerular capillary repair and accelerates resolution of experimentally induced glomerulonephritis Am J Pathol 159 2001 599 608
30. T. Shimoyama, S. Hiraoka, M. Takemoto, M. Koshizaka, H. Tokuyama, T. Tokuyama, A. Watanabe, M. Fujimoto, H. Kawamura, S. Sato, Y. Tsurutani, Y. Saito, B. Perbal, H. Koseki, K. Yokote CCN3 inhibits neointimal hyperplasia through modulation of smooth muscle cell growth and migration Arterioscler Thromb Vasc Biol 30 2010 675 680
31. Z. Lin, V. Natesan, H. Shi, A. Hamik, D. Kawanami, C. Hao, G.H. Mahabaleshwar, W. Wang, Z.G. Jin, G.B. Atkins, S.M. Firth, L. Rittie, B. Perbal, M.K. Jain A novel role of CCN3 in regulating endothelial inflammation J Cell Commun Signal 4 2010 141 153
32. S.J. Leu, S.C. Lam, L.F. Lau Pro-angiogenic activities of CYR61 (CCN1) mediated through integrins alphavbeta3 and alpha6beta1 in human umbilical vein endothelial cells J Biol Chem 277 2002 46248 46255
33. K. Grote, G. Salguero, M. Ballmaier, M. Dangers, H. Drexler, B. Schieffer The angiogenic factor CCN1 promotes adhesion and migration of circulating CD34+ progenitor cells: potential role in angiogenesis and endothelial regeneration Blood 110 2007 877 885
34. F.E. Mo, A.G. Muntean, C.C. Chen, D.B. Stolz, S.C. Watkins, L.F. Lau CYR61 (CCN1) is essential for placental development and vascular integrity Mol Cell Biol 22 2002 8709 8720
35. K. Sawai, K. Mori, M. Mukoyama, A. Sugawara, T. Suganami, M. Koshikawa, K. Yahata, H. Makino, T. Nagae, Y. Fujinaga, H. Yokoi, T. Yoshioka, A. Yoshimoto, I. Tanaka, K. Nakao Angiogenic protein Cyr61 is expressed by podocytes in anti-Thy-1 glomerulonephritis J Am Soc Nephrol 14 2003 1154 1163
36. N. Gupta, H. Wang, T.L. McLeod, C.C.G. Naus, S. Kyurkchiev, S. Advani, J. Yu, B. Perbal, R.R. Weichselbaum Inhibition of glioma cell growth and tumorigenic potential by CCN3 (NOV) Mol Pathol 54 2001 293 299
37. A.M. Bleau, N. Planque, N. Lazar, D. Zambelli, A. Ori, T. Quan, G. Fisher, K. Scotlandi, B. Perbal Antiproliferative activity of CCN3: involvement of the C-terminal module and post-translational regulation J Cell Biochem 101 2007 1475 1491
38. B. Perbal CCN proteins: multifunctional signalling regulators Lancet 363 2004 62 64
39. A. Gellhaus, X. Dong, S. Propson, K. Maass, L. Klein-Hitpass, M. Kibschull, O. Traub, K. Willecke, B. Perbal, S.J. Lye, E. Winterhager Connexin43 interacts with NOV: a possible mechanism for negative regulation of cell growth in choriocarcinoma cells J Biol Chem 279 2004 36931 36942
40. T. Takahashi, H. Abe, H. Arai, T. Matsubara, K. Nagai, M. Matsuura, N. Iehara, M. Yokode, S. Nishikawa, T. Kita, T. Doi Activation of STAT3/Smad1 is a key signaling pathway for progression to glomerulosclerosis in experimental glomerulonephritis J Biol Chem 280 2005 7100 7106
41. H. Nakamura, Y. Isaka, M. Tsujie, Y. Akagi, T. Sudo, N. Ohno, E. Imai, M. Hori Electroporation-mediated PDGF receptor-IgG chimera gene transfer ameliorates experimental glomerulonephritis Kidney Int 59 2001 2134 2145
42. K. Miyamoto, Y. Kitamoto, H. Tokunaga, M. Takeya, T. Ezaki, T. Imamura, K. Tomita Protective effect of vascular endothelial growth factor/vascular permeability factor 165 and 121 on glomerular endothelial cell injury in the rat Lab Invest 84 2004 1126 1136
43. H. Uchimura, T. Marumo, O. Takase, H. Kawachi, F. Shimizu, M. Hayashi, T. Saruta, K. Hishikawa, T. Fujita Intrarenal injection of bone marrow-derived angiogenic cells reduces endothelial injury and mesangial cell activation in experimental glomerulonephritis J Am Soc Nephrol 16 2005 997 1004
44. G. Le Dreau, L. Kular, A.B. Nicot, C. Calmel, S. Melik-Parsadaniantz, P. Kitabgi, M. Laurent, C. Martinerie NOV/CCN3 upregulates CCL2 and CXCL1 expression in astrocytes through beta1 and beta5 integrins Glia 58 2010 1510 1521
45. B. Perbal Nuclear localisation of NOVH protein: a potential role for NOV in the regulation of gene expression Mol Pathol 52 1999 84 91
46. H. Kawaki, S. Kubota, A. Suzuki, N. Lazar, T. Yamada, T. Matsumura, T. Ohgawara, T. Maeda, B. Perbal, K.M. Lyons, M. Takigawa Cooperative regulation of chondrocyte differentiation by CCN2 and CCN3 shown by a comprehensive analysis of the CCN family proteins in cartilage J Bone Miner Res 23 2008 1751 1764
47. E. Borkham-Kamphorst, C.R. van Roeyen, E. Van de Leur, J. Floege, 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