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Connective tissue growth factor modulates podocyte actin cytoskeleton and extracellular matrix synthesis and is induced in podocytes upon injury

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Abstract

Structural changes of podocytes and retraction of their foot processes are a critical factor in the pathogenesis of minimal change nephritis and glomerulosclerosis. Here we tested, if connective tissue growth factor (CTGF) is involved in podocyte injury during acute and chronic puromycin aminonucleoside nephrosis (PAN) as animal models of minimal change nephritis, and focal segmental glomerulosclerosis, respectively. Rats were treated once (acute PAN) or for 13 weeks (chronic PAN). In both experimental conditions, CTGF and its mRNA were found to be highly upregulated in podocytes. The upregulation correlated with onset and duration of proteinuria in acute PAN, and glomerulosclerosis and high expression of glomerular fibronectin, and collagens I, III, and IV in chronic PAN. In vitro, treatment of podocytes with recombinant CTGF increased amount and density of actin stress fibers, the expression of actin-associated molecules such as podocalyxin, synaptopodin, ezrin, and actinin-4, and activation of focal adhesion kinase (FAK) and extracellular signal-regulated kinase (ERK). Moreover, we observed increased podocyte expression of mRNA for transforming growth factor (TGF)-β2, TGF-β receptor II, fibronectin, and collagens I, III, and IV. Treatment of cultured podocytes with puromycin aminonucleoside resulted in loss of actin stress fibers and cell death, effects that were partially prevented when CTGF was added to the culture medium. Depletion of CTGF mRNA in cultured podocytes by RNA interference reduced both the number of actin stress fibers and the expression of actin-associated molecules. We propose that the expression of CTGF is acutely upregulated in podocytes as part of a cellular attempt to repair structural changes of the actin cytoskeleton. When the damaging effects on podocyte structure and function persist chronically, continuous CTGF expression in podocytes is a critical factor that promotes progressive accumulation of glomerular extracellular matrix and glomerulosclerosis.

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References

  • Babic AM, Chen CC, Lau LF (1999) Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin alphavbeta3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 19:2958–2966

    PubMed  CAS  Google Scholar 

  • Bohr DC, Koch M, Kritzenberger M, Fuchshofer R, Tamm ER (2011) Increased expression of olfactomedin-1 and myocilin in podocytes during puromycin aminonucleoside nephrosis. Nephrol Dial Transplant 26(1):83–92

    Google Scholar 

  • Böttinger EP, Bitzer M (2002) TGF-beta signaling in renal disease. J Am Soc Nephrol 13:2600–2610

    Article  PubMed  Google Scholar 

  • Cai YI, Sich M, Beziau A, Kleppel MM, Gubler MC (1996) Collagen distribution in focal and segmental glomerulosclerosis: an immunofluorescence and ultrastructural immunogold study. J Pathol 179:188–196

    Article  PubMed  CAS  Google Scholar 

  • Chaqour B, Goppelt-Struebe M (2006) Mechanical regulation of the Cyr61/CCN1 and CTGF/CCN2 proteins. Febs J 273:3639–3649

    Article  PubMed  CAS  Google Scholar 

  • Chen CC, Chen N, Lau LF (2001) The angiogenic factors Cyr61 and connective tissue growth factor induce adhesive signaling in primary human skin fibroblasts. J Biol Chem 276:10443–10452

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Abraham DJ, Shi-Wen X, Pearson JD, Black CM, Lyons KM, Leask A (2004) CCN2 (connective tissue growth factor) promotes fibroblast adhesion to fibronectin. Mol Biol Cell 15:5635–5646

    Article  PubMed  CAS  Google Scholar 

  • Cicha I, Yilmaz A, Klein M, Raithel D, Brigstock DR, Daniel WG, Goppelt-Struebe M, Garlichs CD (2005) Connective tissue growth factor is overexpressed in complicated atherosclerotic plaques and induces mononuclear cell chemotaxis in vitro. Arterioscler Thromb Vasc Biol 25:1008–1013

    Article  PubMed  CAS  Google Scholar 

  • di Mola FF, Di Sebastiano P, Gardini A, Innocenti P, Zimmermann A, Buchler MW, Friess H (2004) Differential expression of connective tissue growth factor in inflammatory bowel disease. Digestion 69:245–253

    Article  PubMed  CAS  Google Scholar 

  • Duncan MR, Frazier KS, Abramson S, Williams S, Klapper H, Huang X, Grotendorst GR (1999) Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: down-regulation by cAMP. Faseb J 13:1774–1786

    PubMed  CAS  Google Scholar 

  • Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P (2007) Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17:428–437

    Article  PubMed  CAS  Google Scholar 

  • Floege J, Alpers CE, Sage EH, Pritzl P, Gordon K, Johnson RJ, Couser WG (1992) Markers of complement-dependent and complement-independent glomerular visceral epithelial cell injury in vivo. Expression of antiadhesive proteins and cytoskeletal changes. Lab Invest 67:486–497

    PubMed  CAS  Google Scholar 

  • Fuchshofer R, Tamm ER (2009) Modulation of extracellular matrix turnover in the trabecular meshwork. Exp Eye Res 88:683–688

    Article  PubMed  CAS  Google Scholar 

  • Fuchshofer R, Birke M, Welge-Lüssen U, Kook D, Lütjen-Drecoll E (2005) Transforming growth factor-beta 2 modulated extracellular matrix component expression in cultured human optic nerve head astrocytes. Invest Ophthalmol Vis Sci 46:568–578

    Article  PubMed  Google Scholar 

  • Fuchshofer R, Yu AH, Welge-Lüssen U, Tamm ER (2007) Bone morphogenetic protein-7 is an antagonist of transforming growth factor-beta2 in human trabecular meshwork cells. Invest Ophthalmol Vis Sci 48:715–726

    Article  PubMed  Google Scholar 

  • Grotendorst GR (1997) Connective tissue growth factor: a mediator of TGF-β action on fibroblasts. Cytokine Growth Factor Rev 8:171–179

    Article  PubMed  CAS  Google Scholar 

  • Guha M, Xu ZG, Tung D, Lanting L, Natarajan R (2007) Specific down-regulation of connective tissue growth factor attenuates progression of nephropathy in mouse models of type 1 and type 2 diabetes. Faseb J 21:3355–3368

    Article  PubMed  CAS  Google Scholar 

  • Heusinger-Ribeiro J, Eberlein M, Wahab NA, Goppelt-Struebe M (2001) Expression of connective tissue growth factor in human renal fibroblasts: regulatory roles of RhoA and cAMP. J Am Soc Nephrol 12:1853–1861

    PubMed  CAS  Google Scholar 

  • Hishikawa K, Oemar BS, Nakaki T (2001) Static pressure regulates connective tissue growth factor expression in human mesangial cells. J Biol Chem 276:16797–16803

    Article  PubMed  CAS  Google Scholar 

  • Igarashi A, Nashiro K, Kikuchi K, Sato S, Ihn H, Grotendorst GR, Takehara K (1995) Significant correlation between connective tissue growth factor gene expression and skin sclerosis in tissue sections from patients with systemic sclerosis. J Invest Dermatol 105:280–284

    Article  PubMed  CAS  Google Scholar 

  • Ihn H (2002) Pathogenesis of fibrosis: role of TGF-β and CTGF. Curr Opin Rheumatol 14:681–685

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Aten J, Bende RJ, Oemar BS, Rabelink TJ, Weening JJ, Goldschmeding R (1998) Expression of connective tissue growth factor in human renal fibrosis. Kidney Int 53:853–861

    Article  PubMed  CAS  Google Scholar 

  • Jones CL, Buch S, Post M, McCulloch L, Liu E, Eddy AA (1992) Renal extracellular matrix accumulation in acute puromycin aminonucleoside nephrosis in rats. Am J Pathol 141:1381–1396

    PubMed  CAS  Google Scholar 

  • Junglas B, Yu AH, Welge-Lussen U, Tamm ER, Fuchshofer R (2009) Connective tissue growth factor induces extracellular matrix deposition in human trabecular meshwork cells. Exp Eye Res 88:1065–1075

    Article  PubMed  CAS  Google Scholar 

  • Kennedy L, Liu S, Shi-Wen X, Chen Y, Eastwood M, Sabetkar M, Carter DE, Lyons KM, Black CM, Abraham DJ, Leask A (2007) CCN2 is necessary for the function of mouse embryonic fibroblasts. Exp Cell Res 313:952–964

    Article  PubMed  CAS  Google Scholar 

  • Kerjaschki D (2001) Caught flat-footed: podocyte damage and the molecular bases of focal glomerulosclerosis. J Clin Invest 108:1583–1587

    PubMed  CAS  Google Scholar 

  • Kessler D, Dethlefsen S, Haase I, Plomann M, Hirche F, Krieg T, Eckes B (2001) Fibroblasts in mechanically stressed collagen lattices assume a “synthetic” phenotype. J Biol Chem 276:36575–36585

    Article  PubMed  CAS  Google Scholar 

  • Kivela R, Kyrolainen H, Selanne H, Komi PV, Kainulainen H, Vihko V (2007) A single bout of exercise with high mechanical loading induces the expression of Cyr61/CCN1 and CTGF/CCN2 in human skeletal muscle. J Appl Physiol 103:1395–1401

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Kang YS, Dai C, Kiss LP, Wen X, Liu Y (2008) Epithelial-to-mesenchymal transition is a potential pathway leading to podocyte dysfunction and proteinuria. Am J Pathol 172:299–308

    Article  PubMed  CAS  Google Scholar 

  • Ma LJ, Jha S, Ling H, Pozzi A, Ledbetter S, Fogo AB (2004) Divergent effects of low versus high dose anti-TGF-beta antibody in puromycin aminonucleoside nephropathy in rats. Kidney Int 65:106–115

    Article  PubMed  CAS  Google Scholar 

  • McLennan SV, Wang XY, Moreno V, Yue DK, Twigg SM (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

    Article  PubMed  CAS  Google Scholar 

  • Muehlich S, Cicha I, Garlichs CD, Krueger B, Posern G, Goppelt-Struebe M (2007) Actin-dependent regulation of connective tissue growth factor. Am J Physiol Cell Physiol 292:C1732–C1738

    Article  PubMed  CAS  Google Scholar 

  • Mundel P, Kriz W (1995) Structure and function of podocytes: an update. Anat Embryol 192:385–397

    Article  PubMed  CAS  Google Scholar 

  • Mundel P, Heid HW, Mundel TM, Kruger M, Reiser J, Kriz W (1997) Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J Cell Biol 139:193–204

    Article  PubMed  CAS  Google Scholar 

  • Nakamura T, Ebihara I, Fukui M, Osada S, Nagaoka I, Horikoshi S, Tomino Y, Koide H (1993) Messenger RNA expression for growth factors in glomeruli from focal glomerular sclerosis. Clin Immunol Immunopathol 66:33–42

    Article  PubMed  CAS  Google Scholar 

  • Nishida T, Kawaki H, Baxter RM, Deyoung RA, Takigawa M, Lyons KM (2007) CCN2 (connective tissue growth factor) is essential for extracellular matrix production and integrin signaling in chondrocytes. J Cell Commun Signal 1:45–58

    Article  PubMed  Google Scholar 

  • Oemar BS, Werner A, Garnier JM, Do DD, Godoy N, Nauck M, Marz W, Rupp J, Pech M, Luscher TF (1997) Human connective tissue growth factor is expressed in advanced atherosclerotic lesions. Circulation 95:831–839

    PubMed  CAS  Google Scholar 

  • Ott C, Iwanciw D, Graness A, Giehl K, Goppelt-Struebe M (2003) Modulation of the expression of connective tissue growth factor by alterations of the cytoskeleton. J Biol Chem 278:44305–44311

    Article  PubMed  CAS  Google Scholar 

  • Paradis V, Dargere D, Vidaud M, De Gouville AC, Huet S, Martinez V, Gauthier JM, Ba N, Sobesky R, Ratziu V, Bedossa P (1999) Expression of connective tissue growth factor in experimental rat and human liver fibrosis. Hepatology 30:968–976

    Article  PubMed  CAS  Google Scholar 

  • Pavenstädt H, Kriz W, Kretzler M (2003) Cell biology of the glomerular podocyte. Physiol Rev 83:253–307

    PubMed  Google Scholar 

  • Phanish MK, Winn SK, Dockrell ME (2009) Connective tissue growth factor-(CTGF, CCN2)—a marker, mediator and therapeutic target for renal fibrosis. Nephron Exp Nephrol 114:e83–e92

    Article  PubMed  Google Scholar 

  • Pippin JW, Brinkkoetter PT, Cormack-Aboud FC, Durvasula RV, Hauser PV, Kowalewska J, Krofft RD, Logar CM, Marshall CB, Ohse T, Shankland SJ (2009) Inducible rodent models of acquired podocyte diseases. Am J Physiol Renal Physiol 296:F213–F229

    Article  PubMed  CAS  Google Scholar 

  • Ponticos M, Holmes AM, Shi-Wen X, Leoni P, Khan K, Rajkumar VS, Hoyles RK, Bou-Gharios G, Black CM, Denton CP, Abraham DJ, Leask A, Lindahl GE (2009) Pivotal role of connective tissue growth factor in lung fibrosis: MAPK-dependent transcriptional activation of type I collagen. Arthritis Rheum 60:2142–2155

    Article  PubMed  CAS  Google Scholar 

  • Ransom RF, Lam NG, Hallett MA, Atkinson SJ, Smoyer WE (2005) Glucocorticoids protect and enhance recovery of cultured murine podocytes via actin filament stabilization. Kidney Int 68:2473–2483

    Article  PubMed  CAS  Google Scholar 

  • Ren S, Babelova A, Moreth K, Xin C, Eberhardt W, Doller A, Pavenstadt H, Schaefer L, Pfeilschifter J, Huwiler A (2009) Transforming growth factor-beta2 upregulates sphingosine kinase-1 activity, which in turn attenuates the fibrotic response to TGF-beta2 by impeding CTGF expression. Kidney Int 76:857–867

    Article  PubMed  CAS  Google Scholar 

  • Riser BL, Denichilo M, Cortes P, Baker C, Grondin JM, Yee J, Narins RG (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

    PubMed  CAS  Google Scholar 

  • Roestenberg P, van Nieuwenhoven FA, Joles JA, Trischberger C, Martens PP, Oliver N, Aten J, Hoppener JW, Goldschmeding R (2006) Temporal expression profile and distribution pattern indicate a role of connective tissue growth factor (CTGF/CCN-2) in diabetic nephropathy in mice. Am J Physiol Renal Physiol 290:F1344–F1354

    Article  PubMed  CAS  Google Scholar 

  • Saleem MA, O’Hare MJ, Reiser J, Coward RJ, Inward CD, Farren T, Xing CY, Ni L, Mathieson PW, Mundel P (2002) A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 13:630–638

    PubMed  CAS  Google Scholar 

  • Sanwal V, Pandya M, Bhaskaran M, Franki N, Reddy K, Ding G, Kapasi A, Valderrama E, Singhal PC (2001) Puromycin aminonucleoside induces glomerular epithelial cell apoptosis. Exp Mol Pathol 70:54–64

    Article  PubMed  CAS  Google Scholar 

  • Sato S, Nagaoka T, Hasegawa M, Tamatani T, Nakanishi T, Takigawa M, Takehara K (2000) Serum levels of connective tissue growth factor are elevated in patients with systemic sclerosis: association with extent of skin sclerosis and severity of pulmonary fibrosis. J Rheumatol 27:149–154

    PubMed  CAS  Google Scholar 

  • Schild C, Trueb B (2002) Mechanical stress is required for high-level expression of connective tissue growth factor. Exp Cell Res 274:83–91

    Article  PubMed  CAS  Google Scholar 

  • Schild C, Trueb B (2004) Three members of the connective tissue growth factor family CCN are differentially regulated by mechanical stress. Biochim Biophys Acta 1691:33–40

    Article  PubMed  CAS  Google Scholar 

  • Shankland SJ (2006) The podocyte’s response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 69:2131–2147

    Article  PubMed  CAS  Google Scholar 

  • Shi-wen X, Stanton LA, Kennedy L, Pala D, Chen Y, Howat SL, Renzoni EA, Carter DE, Bou-Gharios G, Stratton RJ, Pearson JD, Beier F, Lyons KM, Black CM, Abraham DJ, Leask A (2006) CCN2 is necessary for adhesive responses to transforming growth factor-beta1 in embryonic fibroblasts. J Biol Chem 281:10715–10726

    Article  PubMed  Google Scholar 

  • Smoyer WE, Ransom RF (2002) Hsp27 regulates podocyte cytoskeletal changes in an in vitro model of podocyte process retraction. Faseb J 16:315–326

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Takemura H, Noiri E, Nosaka K, Toda A, Taniguchi S, Uchida K, Fujita T, Kimura S, Nakao A (2001) Puromycin aminonucleoside induces apoptosis and increases HNE in cultured glomerular epithelial cells. Free Radic Biol Med 31:615–623

    Article  PubMed  CAS  Google Scholar 

  • Turk T, Leeuwis JW, Gray J, Torti SV, Lyons KM, Nguyen TQ, Goldschmeding R (2009) BMP signaling and podocyte markers are decreased in human diabetic nephropathy in association with CTGF overexpression. J Histochem Cytochem 57:623–631

    Article  PubMed  CAS  Google Scholar 

  • Twigg SM, Chen MM, Joly AH, Chakrapani SD, Tsubaki J, Kim HS, Oh Y, Rosenfeld RG (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

    Article  PubMed  CAS  Google Scholar 

  • Twigg SM, Cao Z, MC SV, Burns WC, Brammar G, Forbes JM, Cooper ME (2002) Renal connective tissue growth factor induction in experimental diabetes is prevented by aminoguanidine. Endocrinology 143:4907–4915

    Article  PubMed  CAS  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

    Google Scholar 

  • Wada T, Pippin JW, Marshall CB, Griffin SV, Shankland SJ (2005) Dexamethasone prevents podocyte apoptosis induced by puromycin aminonucleoside: role of p53 and Bcl-2-related family proteins. J Am Soc Nephrol 16:2615–2625

    Article  PubMed  CAS  Google Scholar 

  • Wahab NA, Brinkman H, Mason RM (2001a) Uptake and intracellular transport of the connective tissue growth factor: a potential mode of action. Biochem J 359:89–97

    Article  PubMed  CAS  Google Scholar 

  • Wahab NA, Yevdokimova N, Weston BS, Roberts T, Li XJ, Brinkman H, Mason RM (2001b) Role of connective tissue growth factor in the pathogenesis of diabetic nephropathy. Biochem J 359:77–87

    Article  PubMed  CAS  Google Scholar 

  • Wang X, McLennan SV, Allen TJ, Tsoutsman T, Semsarian C, Twigg SM (2009) Adverse effects of high glucose and free fatty acid on cardiomyocytes are mediated by connective tissue growth factor. Am J Physiol Cell Physiol 297:C1490–C1500

    Article  PubMed  CAS  Google Scholar 

  • Weston BS, Wahab NA, Mason RM (2003) CTGF mediates TGF-beta-induced fibronectin matrix deposition by upregulating active alpha5beta1 integrin in human mesangial cells. J Am Soc Nephrol 14:601–610

    Article  PubMed  CAS  Google Scholar 

  • Wolf G, Ziyadeh FN (1999) Molecular mechanisms of diabetic renal hypertrophy. Kidney Int 56:393–405

    Article  PubMed  CAS  Google Scholar 

  • Wolf G, Chen S, Ziyadeh FN (2005) From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54:1626–1634

    Article  PubMed  CAS  Google Scholar 

  • Wong M, Siegrist M, Goodwin K (2003) Cyclic tensile strain and cyclic hydrostatic pressure differentially regulate expression of hypertrophic markers in primary chondrocytes. Bone 33:685–693

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto T, Sawada Y, Katayama I, Nishioka K (2005) Nodular scleroderma: increased expression of connective tissue growth factor. Dermatology 211:218–223

    Article  PubMed  CAS  Google Scholar 

  • Yamashiro T, Fukunaga T, Kobashi N, Kamioka H, Nakanishi T, Takigawa M, Takano-Yamamoto T (2001) Mechanical stimulation induces CTGF expression in rat osteocytes. J Dent Res 80:461–465

    Article  PubMed  CAS  Google Scholar 

  • Yang DH, Kim HS, Wilson EM, Rosenfeld RG, Oh Y (1998) Identification of glycosylated 38-kDa connective tissue growth factor (IGFBP-related protein 2) and proteolytic fragments in human biological fluids, and up-regulation of IGFBP-rP2 expression by TGF-beta in Hs578T human breast cancer cells. J Clin Endocrinol Metab 83:2593–2596

    Article  PubMed  CAS  Google Scholar 

  • Yaoita E, Kawasaki K, Yamamoto T, Kihara I (1990) Variable expression of desmin in rat glomerular epithelial cells. Am J Pathol 136:899–908

    PubMed  CAS  Google Scholar 

  • Yokoi H, Mukoyama M, Sugawara A, Mori K, Nagae T, Makino H, Suganami T, Yahata K, Fujinaga Y, Tanaka I, Nakao K (2002) Role of connective tissue growth factor in fibronectin expression and tubulointerstitial fibrosis. Am J Physiol Renal Physiol 282:F933–F942

    PubMed  CAS  Google Scholar 

  • Yokoi H, Mukoyama M, Mori K, Kasahara M, Suganami T, Sawai K, Yoshioka T, Saito Y, Ogawa Y, Kuwabara T, Sugawara A, Nakao K (2008) Overexpression of connective tissue growth factor in podocytes worsens diabetic nephropathy in mice. Kidney Int 73:446–455

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Yaoita E, Watanabe Y, Yoshida Y, Nameta M, Li H, Qu Z, Yamamoto T (2006) Upregulation of nestin, vimentin, and desmin in rat podocytes in response to injury. Virchows Arch 448:485–492

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Katharina Fizia, Angelika Pach, Elke Stauber, and Tina Steil for excellent technical assistance. This study was supported by a pilot project grant of the University of Regensburg.

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  1. Institute of Human Anatomy and Embryology, University of Regensburg, Universitätstr. 31, 93053, Regensburg, Germany

    Rudolf Fuchshofer, Sabrina Ullmann, Ludwig F. Zeilbeck, Matti Baumann, Benjamin Junglas & Ernst R. Tamm

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  1. Rudolf Fuchshofer
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Fuchshofer, R., Ullmann, S., Zeilbeck, L.F. et al. Connective tissue growth factor modulates podocyte actin cytoskeleton and extracellular matrix synthesis and is induced in podocytes upon injury. Histochem Cell Biol 136, 301–319 (2011). https://doi.org/10.1007/s00418-011-0844-9

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