Tubular overexpression of transforming growth factor-β1 induces autophagy and fibrosis but not mesenchymal transition of renal epithelial cells

American Journal of Pathology

Volumn 177, Issue 2, 2010, Pages 632-643

  Koesters, Robert ^a,b   Kaissling, Brigitte ^c   LeHir, Michel ^c   Picard, Nicolas ^c   Theilig, Franziska ^d   Gebhardt, Rolf ^e   Glick, Adam B ^f   Hähnel, Brunhilde ^a   Hosser, Hiltraud ^a   Gröne, Hermann Josef ^g   Kriz, Wilhelm ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Urgences Néphrologiques et Transplantation Rénale Hôpital Tenon 4   (France)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d HUMBOLDT UNIVERSITY   (Germany)

^e UNIVERSITY OF LEIPZIG   (Germany)

^f PENNSYLVANIA STATE UNIVERSITY   (United States)

^g GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FIBROSIS; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KIDNEY EPITHELIUM; KIDNEY TUBULE CELL; MOUSE; MYOFIBROBLAST; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

EID: 77957252460     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091012     Document Type: Article

References (45)

1. Miettinen P, Ebner R, Lopez A, Derynck R: TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994, 127:2021-2036
2. Fan J, Ng Y, Hill P, Nikolic-Paterson D, Mu W, Atkins R, Lan H: Transforming growth factor-beta regulates tubular epithelial myofibroblast transdifferentiation in vitro. Kidney Int 1999, 56:1455-1467 (Pubitemid 29451252)
3. Zavadil J, Bitzer M, Liang D, Yang Y, Massimi A, Kneitz S, Piek E, Bottinger E: Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 2001, 98:6686-6691 (Pubitemid 32538277)
4. Gotzmann J, Mikula M, Eger A, Schulte-Hermann R, Foisner R, Beug H, Mikulits W: Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. Mutat Res 2004, 566:9-20 (Pubitemid 38045586)
5. Zeisberg E, Kalluri R: The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med 2004, 82:175-181
6. Zeisberg E, Tarnavski O, Zeisberg M, Dorfman A, McMullen J, Gustafsson E, Chandraker A, Yuan X, Pu W, Roberts A, Neilson E, Sayegh M, Izumo S, Kalluri R: Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007, 13:952-961 (Pubitemid 47222040)
7. Kalluri R, Neilson E: Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003, 112:1776-1784 (Pubitemid 38063698)
8. Traykova-Brauch M, Schönig K, Greiner O, Miloud T, Jauch A, Bode M, Felsher D, Glick A, Kwiatowski D, Bujard H, Horst J, von Kebel Doeberitz M, Niggli F, Kriz W, Gröne H, Koesters R: An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat Med 2008, 14:979-984
9. Samuel S, Hurta R, Kondaiah P, Khalil N, Turley E, Wright J, Greenberg A: Autocrine induction of tumor protease production and invasion by a metallothionein-regulated TGF-beta 1 (Ser223,225). EMBO J 1992, 11:1599-1605
10. Liu X, Alexander V, Vijayachandra K, Bhogte E, Diamond I, Glick A: Conditional epidermal expression of TGFbeta 1 blocks neonatal lethality but causes a reversible hyperplasia and alopecia. Proc Natl Acad Sci USA 2001, 98:9139-9144 (Pubitemid 32743882)
11. Ueberham E, Löw R, Ueberham U, Schonig K, Bujard H, Gebhardt R: Conditional tetracycline-regulated expression of TGF-β1 in liver of transgenic mice leads to reversible intermediary fibrosis. Hepatology 2003, 37:1067-1078 (Pubitemid 36538683)
12. Schonig K, Schwenk F, Rajewsky K, Bujard H: Stringent doxycycline dependent control of CRE recombinase in vivo. Nucleic Acids Res 2002, 30:e134
13. Soriano P: Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999, 21:70-71
14. Kaissling B, Kriz W: Variability of intercellular spaces between macula densa cells: A transmission electron microscopic study in rabbits and rats. Kidney Int 1982, 22(Suppl 12):9-17
15. Richardson K, Jarett L, Finke E: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 1960, 35:313-325
16. Dawson T, Gandhi R, Le Hir M, Kaissling B: Ecto-5′-nucleotidase: localization in rat kidney by light microscopic histochemical methods. J Histochem Cytochem 1989, 37:39-47 (Pubitemid 19016540)
17. de Jong J, Leenen P, Voerman J, van der Sluijs-Gelling A, Ploemacher R: A monoclonal antibody (ER-HR3) against murine macrophages. II. Biochemical and functional aspects of the ER-HR3 antigen. Cell Tissue Res 1994, 275:577-585
18. Theilig F, Bostanjoglo M, Pavenstadt H, Grupp C, Holland G, Slosarek I, Gressner A, Russwurm M, Koesling D, Bachmann S: Cellular distribution and function of soluble guanylyl cyclase in rat kidney and liver. J Am Soc Nephrol 2001, 12:2209-2220 (Pubitemid 33021098)
19. Picard N, Baum O, Vogetseder A, Kaissling B, Le Hir M: Origin of renal myofibroblasts in the model of unilateral ureter obstruction in the rat. Histochem Cell Biol 2008, 130:141-155
20. Chai Q, Krag S, Chai S, Ledet T, Wogensen L: Localisation and phenotypical characterisation of collagen-producing cells in TGF-β1-induced renal interstitial fibrosis. Histochem Cell Biol 2003, 119:267-280 (Pubitemid 36570749)
21. Kriz W, Hosser H, Haehnel B, Gretz N, Provoost A: From segmental glomerulosclerosis to total nephron degeneration and interstitial fibrosis: a histopathological study in rat models and human glomerulopathies. Nephrol Dial Transplant 1998, 13:2781-2798 (Pubitemid 28479524)
22. Kriz W, Haehnel B, Hosser H, Ostendorf T, Kränzlin B, Gretz N, Shimizu F, Floege J: Pathways to recovery and loss of nephrons in anti-Thy-1 nephritis. J Am Soc Nephrol 2003, 14:1904-1926 (Pubitemid 36750488)
23. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Oshumi Y, Yoshimori T: LC3, GABARAP, and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004, 117:2805-2812 (Pubitemid 38997262)
24. Mizushima N: Methods for monitoring autophagy. IJBCB 2004, 36:2491-2502
25. Schelling J, Cleveland R: Involvement of Fas-dependent apoptosis in renal tubular epithelial cell deletion in chronic renal failure. Kidney Int 1999, 56:1313-1316 (Pubitemid 29451238)
26. Bursch W, Ellinger A, Gerner C, Fröhwein U, Schulte-Hermann R: Programmed cell death (PCD): apoptosis, autophagic PCD, or others? Ann NY Acad Sci 2000, 926:1-12
27. Cuervo A: Autophagy: many paths to the same end. Mol Biol Cell 2004, 263:55-72
28. Kundu M, Thompson C: Autophagy: basic principles and relevance to disease. Annu Rev Pathol 2008, 3:427-455 (Pubitemid 351488288)
29. Scarlatti F, Granata R, Meijer A, Codogno P: Does autophagy have a license to kill mammalian cells? Cell Death Differ 2009, 16:12-20
30. Periyasamy-Thandavan S, Jiang M, Wei Q, Smith R, Yin X, Dong Z: Autophagy is cytoprotective during cisplatin injury of renal proximal tubule cells. Kidney Int 2008, 74:631-640
31. Pallet N, Bouvier N, Legendre C, Gilleron J, Codogno P, Beaune P, Thervet E, Anglicheau D: Autophagy protects renal tubular cells against cyclosporine toxicity. Autophagy 2008, 4:783-791
32. Lieberthal W: Macroautophagy: a mechanism for mediating cell death or for promoting cell survival? Kidney Int 2009, 74:555-557
33. Hoyer-Hansen M, Jäättelä M: Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007, 14:1576-1582 (Pubitemid 47278843)
34. Fung C, Lock R, Gao S, Salas E, Debnath J: Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 2008, 19:797-806 (Pubitemid 351481798)
35. Kriz W, Le Hir M: Pathways to nephron loss starting from glomerular diseases - Insights from animal models. Kidney Int 2005, 67:404-419 (Pubitemid 40139832)
36. Faulkner J, Szcykalski L, Springer F, Barnes J: Origin of interstitial fibroblasts in an accelerated model of angiotensin II-induced renal fibrosis. Am J Pathol 2005, 167:1193-1205 (Pubitemid 41541407)
37. Duymelinck C, Dauwe S, De Greef K, Ysebaert D, Verpooten G, De Broe M: TIMP-1 gene expression and PAI-1 antigen after unilateral ureteral obstruction in the adult male rat. Kidney Int 2000, 58:1186-1201
38. Kuusniemi A-M, Merenimes J, Lahdenkari A-T, Holmberg C, Salmela K, Karikoski R, Rapola J, Jalanko H: Glomerular sclerosis in kidneys with congenital nephrotic syndrome (NPHS1). Kidney Int 2006, 70:1423-1431 (Pubitemid 44527311)
39. Fujigaki Y, Sun D, Fujimoto T, Yonemura K, Morioka T, Yaoita E, Hishida A: Cytokines and cell cycle regulation in the fibrous progression of crescent formation in antiglomerular basement membrane nephritis of WKY rats. Virchows Arch 2004, 439:35-45 (Pubitemid 32662516)
40. Pozdzik A, Salmon I, Debelle F, Decaestecker C, Van den Branden C, Verbeelen D, Deschodt-Lanckman M, Vanherwghem J, Nortier J: Aristolochic acid induces proximal tubule apoptosis and epithelial to mesenchymal transformation. Kidney Int 2008, 73:595-607 (Pubitemid 351264108)
41. Lin SL, Kisseleva T, Brenner D, Duffield J: Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 2009, 173:1617-1627
42. Humphreys B, Lin SL, Kobayashi A, Hudosn T, Nowlin B, Bonventre J, Valerius M, McMahon A, Duffield J: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 2010, 176:85-97
43. Schnaper H, Jandeska S, Runyan C, Hubchak S, Basu R, Curley J, Smith R, Hayashida T: TGF-beta signal transduction in chronic kidney disease. Front Biosci 2009, 14:2448-2465 19273211
44. Hagedorn L, Floris J, Suter U, Sommer L: Autonomic neurogenesis and apoptosis are alternative fates of progenitor cell communities induced by TGFbeta. Dev Biol 2000, 228:57-72 11087626
45. Wu D, Bitzer M, Ju W, Mundel P, Bottinger E: TGF-beta concentration specifies differential signaling profiles of growth arrest/differentiation and apoptosis in podocytes. J Am Soc Nephrol 2005, 16:3211-3221 (Pubitemid 46179327)