Paracrine wnt1 drives interstitial fibrosis without inflammation by tubulointerstitial cross-talk

Journal of the American Society of Nephrology

Volumn 27, Issue 3, 2016, Pages 781-790

  Maarouf, Omar H ^a,b   Aravamudhan, Anusha ^a   Rangarajan, Deepika ^a   Kusaba, Tetsuro ^a   Zhang, Victor ^a   Welborn, Jeremy ^a   Gauvin, Daniel ^a   Hou, Xiuyun ^a   Kramann, Rafael ^a,c   Humphreys, Benjamin D ^a,b,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CD45 ANTIGEN; CREATININE; KIDNEY INJURY MOLECULE 1; LYMPHOID ENHANCER FACTOR 1; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; TAMOXIFEN; WNT1 PROTEIN; ACTIN; ALPHA-SMOOTH MUSCLE ACTIN, MOUSE; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; FIBRONECTIN; LIGAND; TRANSFORMING GROWTH FACTOR BETA;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL INFILTRATION; CELL PROLIFERATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; HISTOLOGY; IN VITRO STUDY; INTERSTITIAL NEPHRITIS; KIDNEY CORTEX; KIDNEY FIBROSIS; KIDNEY PROXIMAL TUBULE; LEUKOCYTE; MOLECULAR INTERACTION; MOUSE; MYOFIBROBLAST; NONHUMAN; PARACRINE SIGNALING; PATHOGENESIS; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL CORTICAL TISSUE; WNT SIGNALING PATHWAY; ANIMAL; COMPLICATION; DISEASE MODEL; FIBROSIS; GENE EXPRESSION; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS);

ACTINS; ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FIBRONECTINS; FIBROSIS; GENE EXPRESSION; INFLAMMATION; KIDNEY TUBULES, PROXIMAL; LIGANDS; MICE; MYOFIBROBLASTS; PARACRINE COMMUNICATION; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; TAMOXIFEN; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY; WNT1 PROTEIN;

EID: 84959860026     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014121188     Document Type: Article

References (49)

1. Venkatachalam MA, Griffin KA, Lan R, Geng H, Saikumar P, Bidani AK: Acute kidney injury: A springboard for progression in chronic kidney disease. Am J Physiol Renal Physiol 298: F1078-F1094, 2010
2. Geng H, Lan R, Wang G, Siddiqi AR, Naski MC, Brooks AI, Barnes JL, Saikumar P, Weinberg JM, Venkatachalam MA: Inhibition of autoregulated TGFbeta signaling simultaneously enhances proliferation and differentiation of kidney epithelium and promotes repair following renal ischemia. Am J Pathol 174: 1291-1308, 2009
3. Forbes JM, Hewitson TD, Becker GJ, Jones CL: Ischemic acute renal failure: Long-termhistology of cell and matrix changes in the rat. Kidney Int 57: 2375-2385, 2000
4. Huen SC, Cantley LG: Macrophage-mediated injury and repair after ischemic kidney injury. Pediatr Nephrol 30: 199-209, 2015
5. Lan R, Geng H, Polichnowski AJ, Singha PK, Saikumar P, McEwen DG, Griffin KA, Koesters R,Weinberg JM, Bidani AK, Kriz W, Venkatachalam MA: PTEN loss defines a TGF-b-induced tubule phenotype of failed differentiation and JNK signaling during renal fibrosis. Am J Physiol Renal Physiol 302: F1210-F1223, 2012
6. Maarouf OH, Ikeda Y, Humphreys BD: Wnt signaling in kidney tubulointerstitium during disease. Histol Histopathol 30: 163-171, 2015
7. Moon RT, Kohn AD, De Ferrari GV, Kaykas A: WNT and beta-catenin signalling: Diseases and therapies. Nat Rev Genet 5: 691-701, 2004
8. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP: Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 9: 283-292, 2005
9. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, Clevers H: Wnt signaling through inhibition of b-catenin degradation in an intact Axin1 complex. Cell 149: 1245-1256, 2012
10. Clevers H, Nusse R: Wnt/b-catenin signaling and disease. Cell 149: 1192-1205, 2012
11. Ren S, Johnson BG, Kida Y, Ip C, Davidson KC, Lin SL, Kobayashi A, Lang RA, Hadjantonakis AK, Moon RT, Duffield JS: LRP-6 is a coreceptor for multiple fibrogenic signaling pathways in pericytes and myofibroblasts that are inhibited by DKK-1. Proc Natl Acad Sci U S A 110: 1440-1445, 2013
12. Dirocco DP, Kobayashi A, Taketo MM, McMahon AP, Humphreys BD: Wnt4/b-catenin signaling in medullary kidney myofibroblasts. J Am Soc Nephrol 24: 1399-1412, 2013
13. He W, Dai C, Li Y, Zeng G, Monga SP, Liu Y: Wnt/beta-catenin signaling promotes renal interstitial fibrosis. J Am Soc Nephrol 20: 765-776, 2009
14. Zhang P, Cai Y, Soofi A, Dressler GR: Activation of Wnt11 by transforming growth factor-b drives mesenchymal gene expression through non-canonical Wnt protein signaling in renal epithelial cells. J Biol Chem 287: 21290-21302, 2012
15. Akhmetshina A, Palumbo K, Dees C, Bergmann C, Venalis P, Zerr P, Horn A, Kireva T, Beyer C, Zwerina J, Schneider H, Sadowski A, Riener MO, MacDougald OA, Distler O, Schett G, Distler JH: Activation of canonical Wnt signalling is required for TGF-b-mediated fibrosis. Nat Commun 3: 735, 2012
16. Beyer C, SchrammA,Akhmetshina A, Dees C, Kireva T, GelseK, Sonnylal S, deCrombrugghe B, TaketoMM,Distler O, SchettG, Distler JH: b-catenin is a centralmediator of pro-fibrotic Wnt signaling in systemic sclerosis. Ann Rheum Dis 71: 761-767, 2012
17. Distler A, Ziemer C, Beyer C, Lin NY, Chen CW, Palumbo-Zerr K, Dees C, Weidemann A, Distler O, Schett G, Distler JH: Inactivation of evenness interrupted (EVI) reduces experimental fibrosis by combined inhibition of canonical and non-canonical Wnt signalling. Ann Rheum Dis 73: 624-627, 2014
18. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, Charlat O, Wiellette E, Zhang Y, Wiessner S, Hild M, Shi X, Wilson CJ, Mickanin C, Myer V, Fazal A, Tomlinson R, Serluca F, Shao W, Cheng H, ShultzM, Rau C, SchirleM, Schlegl J,Ghidelli S, Fawell S, Lu C, Curtis D, Kirschner MW, Lengauer C, Finan PM, Tallarico JA, Bouwmeester T, Porter JA, Bauer A, Cong F: Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461: 614-620, 2009
19. Zhou S, Zawel L, Lengauer C, Kinzler KW, Vogelstein B: Characterization of human FAST-1, a TGF beta and activin signal transducer. Mol Cell 2: 121-127, 1998
20. ZhouB, LiuY,KahnM,AnnDK,HanA,WangH,NguyenC, FlodbyP,Zhong Q, Krishnaveni MS, Liebler JM, Minoo P, Crandall ED, Borok Z: Interactions between b-catenin and transforming growth factor-b signaling pathways mediate epithelial-mesenchymal transition and are dependent on the transcriptional co-activator cAMP-response element-binDing protein (CREB)-binDing protein (CBP). J Biol Chem 287: 7026-7038, 2012
21. Zhang M, Wang M, Tan X, Li TF, Zhang YE, Chen D: Smad3 prevents beta-catenin degradation and facilitates beta-catenin nuclear translocation in chondrocytes. J Biol Chem285: 8703-8710, 2010
22. Tian X, Zhang J, Tan TK, Lyons JG, Zhao H, Niu B, Lee SR, Tsatralis T, Zhao Y, Wang Y, Cao Q, Wang C, Wang Y, Lee VW, Kahn M, Zheng G, Harris DC: Association of b-catenin with P-Smad3 but not LEF-1 dissociates in vitro profibrotic from anti-inflammatory effects of TGF-b1. J Cell Sci 126: 67-76, 2013
23. Labbé E, Letamendia A, Attisano L: Association of Smads with lymphoid enhancer binDing factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways. Proc Natl Acad Sci U S A 97: 8358-8363, 2000
24. Jian H, Shen X, Liu I, Semenov M, He X, Wang XF: Smad3-dependent nuclear translocation of beta-catenin is required for TGF-beta1-induced proliferation of bone marrow-derived adult human mesenchymal stem cells. Genes Dev 20: 666-674, 2006
25. van Es JH, Jay P, Gregorieff A, vanGijnME, Jonkheer S, Hatzis P, Thiele A, van den Born M, Begthel H, Brabletz T, Taketo MM, Clevers H: Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7: 381-386, 2005
26. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL: A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423: 409-414, 2003
27. Lam AP, Flozak AS, Russell S, Wei J, Jain M, Mutlu GM, Budinger GR, Feghali-Bostwick CA, Varga J,Gottardi CJ:Nuclear b-catenin is increased in systemic sclerosis pulmonary fibrosis and promotes lung fibroblast migration and proliferation. Am J Respir CellMol Biol 45: 915-922, 2011
28. Kabashima K, Sakabe J, Yoshiki R, Tabata Y, Kohno K, Tokura Y: Involvement ofWnt signaling in dermal fibroblasts. Am J Pathol 176: 721-732, 2010
29. Kim SE, Choi KY: EGF receptor is involved in WNT3a-mediated proliferation and motility of NIH3T3 cells via ERK pathway activation. Cell Signal 19: 1554-1564, 2007
30. Kusaba T, Lalli M, Kramann R, Kobayashi A, Humphreys BD: Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci U S A 111: 1527-1532, 2014
31. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176: 85-97, 2010
32. Duffield JS: Cellular andmolecular mechanisms in kidney fibrosis. JClin Invest 124: 2299-2306, 2014
33. Saunders AE, Johnson P: Modulation of immune cell signalling by the leukocyte common tyrosine phosphatase, CD45. Cell Signal 22: 339-348, 2010
34. Ichimura T, Bonventre JV, Bailly V, Wei H, Hession CA, Cate RL, Sanicola M: Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is upregulated in renal cells after injury. J Biol Chem 273: 4135-4142, 1998
35. Wallin A, Zhang G, Jones TW, Jaken S, Stevens JL: Mechanism of the nephrogenic repair response. Studies on proliferation and vimentin expression after 35S-1,2-dichlorovinyl-L-cysteine nephrotoxicity in vivo and in cultured proximal tubule epithelial cells. Lab Invest 66: 474-484, 1992
36. Henderson NC, Arnold TD, Katamura Y, Giacomini MM, Rodriguez JD, McCarty JH, Pellicoro A, Raschperger E, Betsholtz C, Ruminski PG, GriggsDW, Prinsen MJ,Maher JJ, Iredale JP, Lacy-Hulbert A, Adams RH, Sheppard D: Targeting of av integrin identifies a core molecular pathway that regulates fibrosis in several organs. Nat Med 19: 1617-1624, 2013
37. Kramann R, Schneider RK, Dirocco DP, Machado F, Fleig S, Bondzie PA, Henderson JM, Ebert BL, Humphreys BD: Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 16: 51-66, 2015
38. Gabbiani G: The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200: 500-503, 2003
39. Sugimoto H, Mundel TM, Kieran MW, Kalluri R: Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 5: 1640-1646, 2006
40. Meran S, Steadman R: Fibroblasts and myofibroblasts in renal fibrosis. Int J Exp Pathol 92: 158-167, 2011
41. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV: Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 16: 535-543, 2010
42. Lee S,Huen S, NishioH, Nishio S, LeeHK, Choi BS, RuhrbergC, Cantley LG: Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 22: 317-326, 2011
43. Lin SL, Li B, Rao S, Yeo EJ, Hudson TE,Nowlin BT, PeiH, Chen L, Zheng JJ, Carroll TJ, Pollard JW, McMahon AP, Lang RA, Duffield JS: Macrophage Wnt7b is critical for kidney repair and regeneration. Proc Natl Acad Sci U S A 107: 4194-4199, 2010
44. Ko GJ, Boo CS, Jo SK, Cho WY, Kim HK: Macrophages contribute to the development of renal fibrosis following ischaemia/reperfusioninduced acute kidney injury. Nephrol Dial Transplant 23: 842-852, 2008
45. Traykova-Brauch M, Schönig K, Greiner O,Miloud T, Jauch A, BodeM, Felsher DW, Glick AB, Kwiatkowski DJ, Bujard H, Horst J, von Knebel Doeberitz M, Niggli FK, Kriz W, Gröne HJ, Koesters R: An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat Med 14: 979-984, 2008
46. Koesters R, Kaissling B, Lehir M, Picard N, Theilig F, Gebhardt R, Glick AB, Hähnel B, Hosser H, Gröne HJ, Kriz W: Tubular overexpression of transforming growth factor-beta1 induces autophagy and fibrosis but not mesenchymal transition of renal epithelial cells. Am J Pathol 177: 632-643, 2010
47. Labbé E, Lock L, Letamendia A, Gorska AE,Gryfe R, Gallinger S,Moses HL, Attisano L: Transcriptional cooperation between the transforming growth factor-beta and Wnt pathways in mammary and intestinal tumorigenesis. Cancer Res 67: 75-84, 2007
48. Shi M, Zhu J,Wang R, Chen X, Mi L,Walz T, Springer TA: Latent TGF-b structure and activation. Nature 474: 343-349, 2011
49. Venkatachalam MA, Weinberg JM, Kriz W, Bidani AK: Failed tubule recovery, AKI-CKD transition, and kidney disease progression [published online ahead of print March 25, 2015]. J Am Soc Nephrol doi: ASN. 2015010006