TGF-β/Smad signaling in renal fibrosis

Afrakhte, 1998, Induction of inhibitory Smad6 and Smad7 mRNA by TGF-beta family members, Biochem. Biophys. Res. Commun, 249, 505, 10.1006/bbrc.1998.9170

Ai, 2014, GQ5 hinders renal fibrosis in obstructive nephropathy by selectively inhibiting TGF-beta-induced Smad3 phosphorylation, J. Am. Soc. Nephrol, 10.1681/ASN.2014040363

Allison, 2013, Fibrosis: the source of myofibroblasts in kidney fibrosis, Nat. Rev. Nephrol, 9, 494, 10.1038/nrneph.2013.141

Attisano, 2002, Signal transduction by the TGF-beta superfamily, Science, 296, 1646, 10.1126/science.1071809

Border, 1998, Evidence that TGF-beta should be a therapeutic target in diabetic nephropathy, Kidney Int, 54, 1390, 10.1046/j.1523-1755.1998.00127.x

Bottinger, 2002, TGF-beta signaling in renal disease, J. Am. Soc. Nephrol, 13, 2600, 10.1097/01.ASN.0000033611.79556.AE

Chau, 2012, MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways, Sci. Transl. Med, 4, 121ra118, 10.1126/scitranslmed.3003205

Chen, 2011, The protective role of Smad7 in diabetic kidney disease: mechanism and therapeutic potential, Diabetes, 60, 590, 10.2337/db10-0403

Chen, 2014, MicroRNA-29b inhibits diabetic nephropathy in db/db mice, Mol. Ther, 22, 842, 10.1038/mt.2013.235

Chen, 1999, Stimulation of type I collagen transcription in human skin fibroblasts by TGF-beta: involvement of Smad 3, J. Invest. Dermatol, 112, 49, 10.1046/j.1523-1747.1999.00477.x

Cho, 2007, Pirfenidone slows renal function decline in patients with focal segmental glomerulosclerosis, Clin. J. Am. Soc. Nephrol, 2, 906, 10.2215/CJN.01050207

Choi, 2012, TGF-beta signaling via TAK1 pathway: role in kidney fibrosis, Semin. Nephrol, 32, 244, 10.1016/j.semnephrol.2012.04.003

Chung, 2013a, Smad7 suppresses renal fibrosis via altering expression of TGF-beta/Smad3-regulated microRNAs, Mol. Ther, 21, 388, 10.1038/mt.2012.251

Chung, 2010a, miR-192 mediates TGF-beta/Smad3-driven renal fibrosis, J. Am. Soc. Nephrol, 21, 1317, 10.1681/ASN.2010020134

Chung, 2009, Disruption of the Smad7 gene promotes renal fibrosis and inflammation in unilateral ureteral obstruction (UUO) in mice, Nephrol. Dial. Transplant, 24, 1443, 10.1093/ndt/gfn699

Chung, 2013b, MicroRNA and nephropathy: emerging concepts, Int. J. Nephrol. Renovasc. Dis, 6, 169, 10.2147/IJNRD.S37885

Chung, 2010b, Advanced glycation end-products induce tubular CTGF via TGF-beta-independent Smad3 signaling, J. Am. Soc. Nephrol, 21, 249, 10.1681/ASN.2009010018

Dennler, 1998, Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene, EMBO J, 17, 3091, 10.1093/emboj/17.11.3091

Derynck, 2003, Smad-dependent and Smad-independent pathways in TGF-beta family signalling, Nature, 425, 577, 10.1038/nature02006

Doi, 2011, Klotho inhibits transforming growth factor-beta1 (TGF-beta1) signaling and suppresses renal fibrosis and cancer metastasis in mice, J. Biol. Chem, 286, 8655, 10.1074/jbc.M110.174037

Du, 2010, High glucose down-regulates miR-29a to increase collagen IV production in HK-2 cells, FEBS Lett, 584, 811, 10.1016/j.febslet.2009.12.053

Ebisawa, 2001, Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation, J. Biol. Chem, 276, 12477, 10.1074/jbc.C100008200

Eddy, 2006, Chronic kidney disease progression, J. Am. Soc. Nephrol, 17, 2964, 10.1681/ASN.2006070704

Evans, 2003, TGF-beta1-mediated fibroblast-myofibroblast terminal differentiation-the role of Smad proteins, Exp. Cell Res, 282, 90, 10.1016/S0014-4827(02)00015-0

Fan, 1999, Transforming growth factor-beta regulates tubular epithelial-myofibroblast transdifferentiation in vitro, Kidney Int, 56, 1455, 10.1046/j.1523-1755.1999.00656.x

Fujimoto, 2003, Mice lacking Smad3 are protected against streptozotocin-induced diabetic glomerulopathy, Biochem. Biophys. Res. Commun, 305, 1002, 10.1016/S0006-291X(03)00885-4

Fukasawa, 2004, Down-regulation of Smad7 expression by ubiquitin-dependent degradation contributes to renal fibrosis in obstructive nephropathy in mice, Proc. Natl. Acad. Sci. U.S.A, 101, 8687, 10.1073/pnas.0400035101

Godwin, 2010, Identification of a microRNA signature of renal ischemia reperfusion injury, Proc. Natl. Acad. Sci. U.S.A, 107, 14339, 10.1073/pnas.0912701107

Hong, 2007, Differentiation of human circulating fibrocytes as mediated by transforming growth factor-beta and peroxisome proliferator-activated receptor gamma, J. Biol. Chem, 282, 22910, 10.1074/jbc.M703597200

Hou, 2005, Ultrasound-microbubble-mediated gene transfer of inducible Smad7 blocks transforming growth factor-beta signaling and fibrosis in rat remnant kidney, Am. J. Pathol, 166, 761, 10.1016/S0002-9440(10)62297-3

Howe, 2012, The miR-200 and miR-221/222 microRNA families: opposing effects on epithelial identity, J. Mammary Gland Biol. Neoplasia, 17, 65, 10.1007/s10911-012-9244-6

Hruska, 2000, Osteogenic protein-1 prevents renal fibrogenesis associated with ureteral obstruction, Am. J. Physiol. Renal Physiol, 279, F130, 10.1152/ajprenal.2000.279.1.F130

Huang, 2008a, Mice overexpressing latent TGF-beta1 are protected against renal fibrosis in obstructive kidney disease, Am. J. Physiol. Renal Physiol, 295, F118, 10.1152/ajprenal.00021.2008

Huang, 2008b, Latent TGF-beta1 protects against crescentic glomerulonephritis, J. Am. Soc. Nephrol, 19, 233, 10.1681/ASN.2007040484

Ka, 2007, Smad7 gene therapy ameliorates an autoimmune crescentic glomerulonephritis in mice, J. Am. Soc. Nephrol, 18, 1777, 10.1681/ASN.2006080901

Ka, 2012, Kidney-targeting Smad7 gene transfer inhibits renal TGF-beta/MAD homologue (SMAD) and nuclear factor kappaB (NF-kappaB) signalling pathways, and improves diabetic nephropathy in mice, Diabetologia, 55, 509, 10.1007/s00125-011-2364-5

Kantharidis, 2011, Diabetes complications: the microRNA perspective, Diabetes, 60, 1832, 10.2337/db11-0082

Kato, 2011, A microRNA circuit mediates transforming growth factor-beta1 autoregulation in renal glomerular mesangial cells, Kidney Int, 80, 358, 10.1038/ki.2011.43

Kato, 2007, MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors, Proc. Natl. Acad. Sci. U.S.A, 104, 3432, 10.1073/pnas.0611192104

Kavsak, 2000, Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation, Mol. Cell, 6, 1365, 10.1016/S1097-2765(00)00134-9

Kim, 2005, The endogenous ratio of Smad2 and Smad3 influences the cytostatic function of Smad3, Mol. Biol. Cell, 16, 4672, 10.1091/mbc.E05-01-0054

Kopp, 1996, Transgenic mice with increased plasma levels of TGF-beta 1 develop progressive renal disease, Lab. Invest, 74, 991

Korpal, 2008, The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2, J. Biol. Chem, 283, 14910, 10.1074/jbc.C800074200

Kriegel, 2012, MiR-382 targeting of kallikrein 5 contributes to renal inner medullary interstitial fibrosis, Physiol. Genomics, 44, 259, 10.1152/physiolgenomics.00173.2011

Krupa, 2010, Loss of MicroRNA-192 promotes fibrogenesis in diabetic nephropathy, J. Am. Soc. Nephrol, 21, 438, 10.1681/ASN.2009050530

Lan, 2012, TGF-beta/Smad signaling in kidney disease, Semin. Nephrol, 32, 236, 10.1016/j.semnephrol.2012.04.002

Lan, 2003, Inhibition of renal fibrosis by gene transfer of inducible Smad7 using ultrasound-microbubble system in rat UUO model, J. Am. Soc. Nephrol, 14, 1535, 10.1097/01.ASN.0000067632.04658.B8

LeBleu, 2013, Origin and function of myofibroblasts in kidney fibrosis, Nat. Med, 19, 1047, 10.1038/nm.3218

Li, 2003, Role of TGF-beta signaling in extracellular matrix production under high glucose conditions, Kidney Int, 63, 2010, 10.1046/j.1523-1755.2003.00016.x

Li, 2004, Advanced glycation end products activate Smad signaling via TGF-beta-dependent and independent mechanisms: implications for diabetic renal and vascular disease, FASEB J, 18, 176, 10.1096/fj.02-1117fje

Li, 2010, Blockade of endothelial-mesenchymal transition by a Smad3 inhibitor delays the early development of streptozotocin-induced diabetic nephropathy, Diabetes, 59, 2612, 10.2337/db09-1631

Li, 2009, Inhibition of integrin-linked kinase attenuates renal interstitial fibrosis, J. Am. Soc. Nephrol, 20, 1907, 10.1681/ASN.2008090930

Liu, 2008, Arkadia regulates TGF-beta signaling during renal tubular epithelial to mesenchymal cell transition, Kidney Int, 73, 588, 10.1038/sj.ki.5002713

Liu, 2013, Disruption of Smad7 promotes ANG II-mediated renal inflammation and fibrosis via Sp1-TGF-beta/Smad3-NF.kappaB-dependent mechanisms in mice, PLoS ONE, 8, e53573, 10.1371/journal.pone.0053573

Liu, 2014, Smad7 inhibits AngII-mediated hypertensive nephropathy in a mouse model of hypertension, Clin. Sci, 127, 195, 10.1042/CS20130706

Liu, 2010, New insights into epithelial-mesenchymal transition in kidney fibrosis, J. Am. Soc. Nephrol, 21, 212, 10.1681/ASN.2008121226

Liu, 2010, Renal medullary microRNAs in Dahl salt-sensitive rats: miR-29b regulates several collagens and related genes, Hypertension, 55, 974, 10.1161/HYPERTENSIONAHA.109.144428

Liu, 2012, Smad3 mediates ANG II-induced hypertensive kidney disease in mice, Am. J. Physiol. Renal Physiol, 302, F986, 10.1152/ajprenal.00595.2011

Loeffler, 2014, Transforming growth factor-beta and the progression of renal disease, Nephrol. Dial. Transplant, 29(Suppl. 1), i37, 10.1093/ndt/gft267

Lopez-Hernandez, 2012, Role of TGF-beta in chronic kidney disease: an integration of tubular, glomerular and vascular effects, Cell Tissue Res, 347, 141, 10.1007/s00441-011-1275-6

Luo, 2010, Bone morphogenetic protein-7 inhibits proximal tubular epithelial cell Smad3 signaling via increased SnoN expression, Am. J. Pathol, 176, 1139, 10.2353/ajpath.2010.090459

Lyons, 1990, Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin, J. Cell Biol, 110, 1361, 10.1083/jcb.110.4.1361

Massague, 2000, Transcriptional control by the TGF-beta/Smad signaling system, EMBO J, 19, 1745, 10.1093/emboj/19.8.1745

Meng, 2013, Role of the TGF-beta/BMP-7/Smad pathways in renal diseases, Clin. Sci, 124, 243, 10.1042/CS20120252

Meng, 2010, Smad2 protects against TGF-beta/Smad3-mediated renal fibrosis, J. Am. Soc. Nephrol, 21, 1477, 10.1681/ASN.2009121244

Meng, 2012a, Diverse roles of TGF-beta receptor II in renal fibrosis and inflammation in vivo and in vitro, J. Pathol, 227, 175, 10.1002/path.3976

Meng, 2012b, Disruption of Smad4 impairs TGF-beta/Smad3 and Smad7 transcriptional regulation during renal inflammation and fibrosis in vivo and in vitro, Kidney Int, 81, 266, 10.1038/ki.2011.327

Meng, 2014, Inflammatory processes in renal fibrosis, Nat. Rev. Nephrol, 10, 493, 10.1038/nrneph.2014.114

Midgley, 2013, Transforming growth factor-beta1 (TGF-beta1)-stimulated fibroblast to myofibroblast differentiation is mediated by hyaluronan (HA)-facilitated epidermal growth factor receptor (EGFR) and CD44 co-localization in lipid rafts, J. Biol. Chem, 288, 14824, 10.1074/jbc.M113.451336

Moon, 2006, IN-1130, a novel transforming growth factor-beta type I receptor kinase (ALK5) inhibitor, suppresses renal fibrosis in obstructive nephropathy, Kidney Int, 70, 1234, 10.1038/sj.ki.5001775

Munger, 1999, The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis, Cell, 96, 319, 10.1016/S0092-8674(00)80545-0

Murakami, 1997, Urinary transforming growth factor-beta in patients with glomerular diseases, Pediatr. Nephrol, 11, 334, 10.1007/s004670050289

Ng, 2009, Pentoxifylline inhibits transforming growth factor-beta signaling and renal fibrosis in experimental crescentic glomerulonephritis in rats, Am. J. Nephrol, 29, 43, 10.1159/000150600

Nikolic-Paterson, 2014, Macrophages promote renal fibrosis through direct and indirect mechanisms, Kidney Int. Suppl, 4, 34, 10.1038/kisup.2014.7

Oba, 2010, miR-200b precursor can ameliorate renal tubulointerstitial fibrosis, PLoS ONE, 5, e13614, 10.1371/journal.pone.0013614

Petersen, 2008, Oral administration of GW788388, an inhibitor of TGF-beta type I and II receptor kinases, decreases renal fibrosis, Kidney Int, 73, 705, 10.1038/sj.ki.5002717

Phanish, 2006, The differential role of Smad2 and Smad3 in the regulation of pro-fibrotic TGFbeta1 responses in human proximal-tubule epithelial cells, Biochem. J, 393, 601, 10.1042/BJ20051106

Piek, 2001, Functional characterization of transforming growth factor beta signaling in Smad2- and Smad3-deficient fibroblasts, J. Biol. Chem, 276, 19945, 10.1074/jbc.M102382200

Putta, 2012, Inhibiting microRNA-192 ameliorates renal fibrosis in diabetic nephropathy, J. Am. Soc. Nephrol, 23, 458, 10.1681/ASN.2011050485

Qin, 2011, TGF-beta/Smad3 signaling promotes renal fibrosis by inhibiting miR-29, J. Am. Soc. Nephrol, 22, 1462, 10.1681/ASN.2010121308

Samarakoon, 2012, TGF-beta1 –> SMAD/p53/USF2 –> PAI-1 transcriptional axis in ureteral obstruction-induced renal fibrosis, Cell Tissue Res, 347, 117, 10.1007/s00441-011-1181-y

Sanderson, 1995, Hepatic expression of mature transforming growth factor beta 1 in transgenic mice results in multiple tissue lesions, Proc. Natl. Acad. Sci. U.S.A, 92, 2572, 10.1073/pnas.92.7.2572

Sato, 2003, Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction, J. Clin. Invest, 112, 1486, 10.1172/JCI200319270

Sharma, 2011, Pirfenidone for diabetic nephropathy, J. Am. Soc. Nephrol, 22, 1144, 10.1681/ASN.2010101049

Shen, 2013, Inhibition of TGF-beta1-receptor posttranslational core fucosylation attenuates rat renal interstitial fibrosis, Kidney Int, 84, 64, 10.1038/ki.2013.82

Shi, 2003, Mechanisms of TGF-beta signaling from cell membrane to the nucleus, Cell, 113, 685, 10.1016/S0092-8674(03)00432-X

Sugimoto, 2007, Renal fibrosis and glomerulosclerosis in a new mouse model of diabetic nephropathy and its regression by bone morphogenic protein-7 and advanced glycation end product inhibitors, Diabetes, 56, 1825, 10.2337/db06-1226

Tampe, 2014, Potential approaches to reverse or repair renal fibrosis, Nat. Rev. Nephrol, 10, 226, 10.1038/nrneph.2014.14

Trachtman, 2011, A phase 1, single-dose study of fresolimumab, an anti-TGF-beta antibody, in treatment-resistant primary focal segmental glomerulosclerosis, Kidney Int, 79, 1236, 10.1038/ki.2011.33

Tsakas, 2006, Accurate measurement and clinical significance of urinary transforming growth factor-beta1, Am. J. Nephrol, 26, 186, 10.1159/000093178

Tsuchida, 2003, Role of Smad4 on TGF-beta-induced extracellular matrix stimulation in mesangial cells, Kidney Int, 63, 2000, 10.1046/j.1523-1755.2003.00009.x

van Rooij, 2008, Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis, Proc. Natl. Acad. Sci. U.S.A, 105, 13027, 10.1073/pnas.0805038105

Vindevoghel, 1998, SMAD3/4-dependent transcriptional activation of the human type VII collagen gene (COL7A1) promoter by transforming growth factor beta, Proc. Natl. Acad. Sci. U.S.A, 95, 14769, 10.1073/pnas.95.25.14769

Wada, 2007, Fibrocytes: a new insight into kidney fibrosis, Kidney Int, 72, 269, 10.1038/sj.ki.5002325

Wang, 2010, E-cadherin expression is regulated by miR-192/215 by a mechanism that is independent of the profibrotic effects of transforming growth factor-beta, Diabetes, 59, 1794, 10.2337/db09-1736

Wang, 2014, Transforming growth factor-beta1-mediated renal fibrosis is dependent on the regulation of transforming growth factor receptor 1 expression by let-7b, Kidney Int, 85, 352, 10.1038/ki.2013.372

Wang, 2011, miR-200a Prevents renal fibrogenesis through repression of TGF-beta2 expression, Diabetes, 60, 280, 10.2337/db10-0892

Wang, 2013, Effect of miR-21 on renal fibrosis by regulating MMP-9 and TIMP1 in kk-ay diabetic nephropathy mice, Cell Biochem. Biophys, 67, 537, 10.1007/s12013-013-9539-2

Wang, 2006a, Renal bone morphogenetic protein-7 protects against diabetic nephropathy, J. Am. Soc. Nephrol, 17, 2504, 10.1681/ASN.2006030278

Wang, 2006b, Essential role of Smad3 in angiotensin II-induced vascular fibrosis, Circ. Res, 98, 1032, 10.1161/01.RES.0000218782.52610.dc

Wei, 2013, Kindlin-2 mediates activation of TGF-beta/Smad signaling and renal fibrosis, J. Am. Soc. Nephrol, 24, 1387, 10.1681/ASN.2012101041

Wrana, 1994, Mechanism of activation of the TGF-beta receptor, Nature, 370, 341, 10.1038/370341a0

Wu, 2013, Transforming growth factor beta-1 stimulates profibrotic epithelial signaling to activate pericyte-myofibroblast transition in obstructive kidney fibrosis, Am. J. Pathol, 182, 118, 10.1016/j.ajpath.2012.09.009

Wynn, 2012, Mechanisms of fibrosis: therapeutic translation for fibrotic disease, Nat. Med, 18, 1028, 10.1038/nm.2807

Xavier, 2014, Curtailing endothelial TGF-beta signaling is sufficient to reduce endothelial-mesenchymal transition and fibrosis in CKD, J. Am. Soc. Nephrol, 10.1681/ASN.2013101137

Xiao, 2012, miR-29 inhibits bleomycin-induced pulmonary fibrosis in mice, Mol. Ther, 20, 1251, 10.1038/mt.2012.36

Xiong, 2012, The miR-200 family regulates TGF-beta1-induced renal tubular epithelial to mesenchymal transition through Smad pathway by targeting ZEB1 and ZEB2 expression, Am. J. Physiol. Renal Physiol, 302, F369, 10.1152/ajprenal.00268.2011

Xu, 2012, Delayed ischemic preconditioning contributes to renal protection by upregulation of miR-21, Kidney Int, 82, 1167, 10.1038/ki.2012.241

Yamamoto, 1996, Expression of transforming growth factor-beta isoforms in human glomerular diseases, Kidney Int, 49, 461, 10.1038/ki.1996.65

Yang, 2009, Angiotensin II induces connective tissue growth factor and collagen I expression via transforming growth factor-beta-dependent and -independent Smad pathways: the role of Smad3, Hypertension, 54, 877, 10.1161/HYPERTENSIONAHA.109.136531

Yang, 2010, Essential role for Smad3 in angiotensin II-induced tubular epithelial-mesenchymal transition, J. Pathol, 221, 390, 10.1002/path.2721

Yang, 2003a, Downregulation of Smad transcriptional corepressors SnoN and Ski in the fibrotic kidney: an amplification mechanism for TGF-beta1 signaling, J. Am. Soc. Nephrol, 14, 3167, 10.1097/01.ASN.0000099373.33259.B2

Yang, 2003b, Hierarchical model of gene regulation by transforming growth factor beta, Proc. Natl. Acad. Sci. U.S.A, 100, 10269, 10.1073/pnas.1834070100

Yuan, 2001, Transforming growth factor-beta repression of matrix metalloproteinase-1 in dermal fibroblasts involves Smad3, J. Biol. Chem, 276, 38502, 10.1074/jbc.M107081200

Zeisberg, 2008, Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition, J. Am. Soc. Nephrol, 19, 2282, 10.1681/ASN.2008050513

Zeisberg, 2003, BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury, Nat. Med, 9, 964, 10.1038/nm888

Zhong, 2013, miR-21 is a key therapeutic target for renal injury in a mouse model of type 2 diabetes, Diabetologia, 56, 663, 10.1007/s00125-012-2804-x

Zhong, 2011, Smad3-mediated upregulation of miR-21 promotes renal fibrosis, J. Am. Soc. Nephrol, 22, 1668, 10.1681/ASN.2010111168

Zhou, 2010, Mechanism of chronic aristolochic acid nephropathy: role of Smad3, Am. J. Physiol. Renal Physiol, 298, F1006, 10.1152/ajprenal.00675.2009

Zhu, 1999, Smad7 differentially regulates transforming growth factor beta-mediated signaling pathways, J. Biol. Chem, 274, 32258, 10.1074/jbc.274.45.32258