Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney

EMBO Journal

Volumn 25, Issue 23, 2006, Pages 5603-5613

  Boutet, Agnès ^a   De Frutos, Cristina A ^a   Maxwell, Patrick H ^b   Mayol, M José ^c   Romero, J ^c   Nieto, M Angela ^a  

^a INSTITUTO DE NEUROCIENCIAS   (Spain)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c Department of Anatomopathology and Urology   (Spain)

Author keywords

Cadherin 16; Epithelial mesenchymal transition; HNF 1 ; Renal fibrosis; Snail transcription factors

Indexed keywords

CADHERIN; CADHERIN 16; HEPATOCYTE NUCLEAR FACTOR 1BETA; TRANSCRIPTION FACTOR SNAIL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM; GENE; GENE ACTIVATION; GENE REPRESSION; GENE SILENCING; HOMEOSTASIS; HUMAN; HUMAN TISSUE; KIDNEY DEVELOPMENT; KIDNEY DISEASE; KIDNEY EPITHELIUM; KIDNEY FAILURE; KIDNEY FIBROSIS; MESENCHYME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SNAIL GENE; TRANSGENIC MOUSE; TUMOR GROWTH;

ANIMALS; CADHERINS; EMBRYO; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; FIBROSIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 1-BETA; HOMEOSTASIS; HUMANS; KIDNEY; KIDNEY DISEASES; MESODERM; MICE; MICE, TRANSGENIC; RNA, MESSENGER; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

GASTROPODA; MUS MUSCULUS;

EID: 33751582928     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601421     Document Type: Article

References (47)

1. Alexakis C, Maxwell P, Bou-Gharios G (2005) Organ-specific collagen expression: implications for renal disease. Nephron Exp Nephrol 102: e71-e75
2. Aybar M, Nieto MA, Mayor R (2003) Snail precedes Slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development 130: 483-494
3. Bai Y, Pontoglio M, Hiesberger T, Sinclair AM, Igarashi P (2002) Regulation of kidney-specific Ksp-cadherin gene promoter by hepatocyte nuclear factor-1β. Am J Physiol Renal Physiol 283: F839-F851
4. Barrallo-Gimeno A, Nieto MA (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132: 3151-3161
5. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2: 84-89
6. Blanco MJ, Moreno-Bueno G, Sarrio D, Locascio A, Cano A, Palacios J, Nieto MA (2002) Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21: 3241-3246
7. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A (2003) The transcription factor Slug represses E-cadherin expression induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 116: 499-511
8. Burzynski SR (2005) Aging: gene silencing or gene activation? Med Hypotheses 64: 201-208
9. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83
10. Cheng CW, Wu PE, Yu JC, Huang CS, Yue CT, Wu CW, Shen CY (2001) Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 20: 3814-3823
11. Chilosi M, Poletti V, Zamo A, Lestani M, Montagna L, Piccoli P, Pedron S, Bertaso M, Scarpa A, Murer B, Cancellieri A, Maestro R, Semenzato G, Doglioni C (2003) Aberrant Wnt/β-catenin pathway activation in idiopathic pulmonary fibrosis. Am J Pathol 162: 1495-1502
12. del Barrio MG, Nieto MA (2002) Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development 129: 1583-1593
13. Dressler GR (2002) Development of the excretory system. In Mouse Development, J Rossant and PPL Tam (eds) pp 395-420. Canada: Academic Press
14. Edghill EL, Bingham C, Ellard S, Hattersley AT (2006) Mutations in hepatocyte nuclear factor-1-beta and their related phenotypes. J Med Genet 43: 84-90
15. Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D, Chambon P (1996) Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA 93: 10887-10890
16. Fraga MF, Herranz M, Espada J, Ballestar E, Paz MF, Ropero S, Erkek E, Bozdogan O, Peinado H, Niveleau A, Mao JH, Balmain A, Cano A, Esteller M (2004) A mouse skin multistage carcinogenesis model reflects the aberrant DNA methylation patterns of human tumors. Cancer Res 64: 5527-5534
17. Gresh L, Fischer E, Reimann A, Tanguy M, Garbay S, Shao X, Hiesberger T, Fiette L, Igarashi P, Yaniv M, Pontoglio M (2004) A transcriptional network in polycystic kidney disease. EMBO J 23: 1657-1668
18. Hiesberger T, Shao X, Gourley E, Reimann A, Pontoglio M, Igarashi P (2004) Mutation of hepatocyte nuclear factor-1β inhibits Pkhd1 gene expression and produces renal cysts in mice. J Clin Invest 113: 814-825
19. Hogan B, Beddington R, Constantini F, Lacy E (1994) Manipulating the Mouse Embryo. A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press
20. Huber MA, Kraut N, Beug H (2005) Molecular requirements for epithelial-mesenchymal transition during tumour progression. Curr Opin Cell Biol 17: 548-558
21. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350
22. Jinde K, Nikolic-Paterson DJ, Huang XR, Sakai H, Kurokawa K, Atkins RC, Lan HY (2001) Tubular phenotypic change in progressive tubulointerstitial fibrosis in human glomerulonephritis. Am J Kidney Dis 38: 761-769
23. Kalluri R, Neilson EG (2003) Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784
24. Li Y, Yang J, Dai C, Wu C, Liu Y (2003) Role for integrin-linked kinase in mediating tubular epithelial to mesenchymal transition and renal interstitial fibrogenesis. J Clin Invest 112: 503-516
25. Lin J, Patel SR, Cheng X, Cho EA, Levitan I, Ullenbruch M, Phan SH, Park JM, Dressler GR (2005) Kielin/chordin-like protein, a novel enhancer of BMP signaling, attenuates renal fibrotic disease. Nat Med 11: 387-393
26. Liu Y (2004) Epithelial to mesenchymal transition in renal fibrogenesis: pathological significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 15: 1-12
27. Liu Y (2006) Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 69: 213-217
28. McMorrow T, Gaffney MM, Slattery C, Campbell E, Ryan MP (2005) Cyclosporine A induced epithelial-mesenchymal transition in human renal proximal tubular epithelial cells. Nephrol Dial Transplant 20: 2215-2225
29. Melk A (2005) Transcriptional analysis of the molecular basis of human kidney aging cDNA microarray profiling. Kidney Int 68: 2667-2679
30. Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166
31. Postlethwaite AE, Shigemitsu H, Kanangat S (2004) Cellular origins of fibroblasts: possible implications for organ fibrosis in systemic sclerosis. Curr Opin Rheumatol 16: 733-738
32. Rastaldi MP, Ferrario F, Giardino L, Dell'Antonio G, Grillo C, Grillo P, Strutz F, Muller GA, Colasanti G, D'Amico G (2002) Epithelial-mesenchymal transition of tubular epithelial cells in human renal biopsies. Kidney Int 62: 137-146
33. Ryu JK, Song SU, Han JY, Chu YC, Lee M, Kim JS, Kim SJ, Suh JK 2005 Establishment of penile fibrosis model in a rat using mouse NIH 3T3 fibroblasts expressing transforming growth factor β1. Biol Reprod 72: 916-921
34. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A (2003) Targeted disruption of TGF-β1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 112: 1486-1494
35. Sefton M, Sanchez S, Nieto MA (1998) Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125: 3111-3121
36. Shao X, Johnson JE, Richardson JA, Hiesberger T, Igarashi P (2002) A minimal Ksp-cadherin promoter linked to a green fluorescent protein reporter gene exhibits tissue-specific expression in the developing kidney and genitourinary tract. J Am Soc Nephrol 13: 1824-1836
37. Slattery C, Campbell E, McMorrow T, Ryan MP (2005) Cyclosporine A-induced renal fibrosis: a role for epithelial-mesenchymal transition. Am J Pathol 167: 395-407
38. Strutz F, Okada H, Lo CW, Danoff T, Carone RL, Tomaszewski JE, Neilson EG (1995) Identification and characterization of a fibroblast marker: FSP1. J Cell Biol 130: 393-405
39. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142
40. Thomson RB, Igarashi P, Biemesderfer D, Kim R, Abu-Alfa A, Soleimani M, Aronson S (1995) Isolation and cDNA cloning of Ksp-cadherin, a novel kidney-specific member of the cadherin multigene family. J Biol Chem 270: 17594-17601
41. Valdés F, Alvarez AM, Locascio A, Vega S, Herrera B, Fernandez M, Benito M, Nieto MA, Fabregat I (2002) The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor b in fetal rat hepatocytes. Mol Cancer Res 1: 68-78
42. Vongwiwatana A, Tasanarong A, Rayner DC, Melk A, Halloran PF (2005) Epithelial to mesenchymal transition during late deterioration of human kidney transplants: the role of tubular cells in fibrogenesis. Am J Transplant 5: 1367-1374
43. Wertz K, Herrmann BG (1999) Kidney-specific cadherin (cdh16) is expressed in embryonic kidney, lung, and sex ducts. Mech Dev 84: 185-188
44. Whyte DA, Li C, Thomson RB, Nix SL, Zanjani R, Karp SL, Aronson PS, Igarashi P (1999) Ksp-cadherin gene promoter I characterization and renal epithelial cell-specific activity. Am J Physiol 277: F587-F598
45. Yañez-Mo M, Lara-Pezzi E, Selgas R, Ramirez-Huesca M, Dominguez-Jimenez C, Jimenez-Heffernan JA, Aguilera A, Sanchez-Tomero JA, Bajo MA, Alvarez V, Castro MA, del Peso G, Cirujeda A, Gamallo C, Sanchez-Madrid F, Lopez-Cabrera M (2003) Peritoneal dialysis and epithelial-to-mesenchymal transition of mesothelial cells. N Engl J Med 348: 403-413
46. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R (2003) BMP-7 counteracts TGF-β1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 9: 964-968
47. Zeisberg M, Kalluri R (2004) The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med 82: 175-181