Impaired wound healing in hypoxic renal tubular cells: Roles of hypoxia-inducible factor-1 and glycogen synthase kinase 3β/β-catenin signaling

Journal of Pharmacology and Experimental Therapeutics

Volumn 340, Issue 1, 2012, Pages 176-184

  Peng, Jianping ^a,c   Ramesh, Ganesan ^a   Sun, Lin ^b   Dong, Zheng ^a,d,e  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; HYPOXIA INDUCIBLE FACTOR 1; OXYGEN; SHORT HAIRPIN RNA;

ARTICLE; CELL HYPOXIA; CELL MIGRATION; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; KIDNEY TUBULE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WILD TYPE; WOUND HEALING IMPAIRMENT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BETA CATENIN; BLOTTING, WESTERN; CELL HYPOXIA; CELL MOVEMENT; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOGEN SYNTHASE KINASE 3; HYPOXIA-INDUCIBLE FACTOR 1; KIDNEY TUBULES, PROXIMAL; LENTIVIRUS; MICE; RATS; RNA; SIGNAL TRANSDUCTION; TRANSFECTION; WOUND HEALING;

EID: 84055223413     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.187427     Document Type: Article

References (41)

1. Benizri E, Ginouvès A, and Berra E (2008) The magic of the hypoxia-signaling cascade. Cell Mol Life Sci 65:1133-1149.
2. Bernhardt WM, Câmpean V, Kany S, Jürgensen JS, Weidemann A, Warnecke C, Arend M, Klaus S, Günzler V, Amann K, et al. (2006) Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol 17:1970-1978. (Pubitemid 44036181)
3. Brembeck FH, Rosário M, and Birchmeier W (2006) Balancing cell adhesion and Wnt signaling, the key role of β-catenin. Curr Opin Genet Dev 16:51-59. (Pubitemid 43089612)
4. Carroll TJ, Park JS, Hayashi S, Majumdar A, and McMahon AP (2005) 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. (Pubitemid 41051746)
5. Chen Y, Whetstone HC, Lin AC, Nadesan P, Wei Q, Poon R, and Alman BA (2007) β-Catenin signaling plays a disparate role in different phases of fracture repair: implications for therapy to improve bone healing. PLoS Med 4:e249.
6. Cheon S, Poon R, Yu C, Khoury M, Shenker R, Fish J, and Alman BA (2005) Prolonged β-catenin stabilization and tcf-dependent transcriptional activation in hyperplastic cutaneous wounds. Lab Invest 85:416-425. (Pubitemid 40333158)
7. Cheon SS, Cheah AY, Turley S, Nadesan P, Poon R, Clevers H, and Alman BA (2002) β-Catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A 99:6973-6978. (Pubitemid 34526242)
8. Dai C, Stolz DB, Kiss LP, Monga SP, Holzman LB, and Liu Y (2009) Wnt/β-catenin signaling promotes podocyte dysfunction and albuminuria. J Am Soc Nephrol 20:1997-2008.
9. Dihlmann S, Kloor M, Fallsehr C, and von Knebel Doeberitz M (2005) Regulation of AKT1 expression by β-catenin/Tcf/Lef signaling in colorectal cancer cells. Carcinogenesis 26:1503-1512. (Pubitemid 41236043)
10. Fraisl P, Aragonés J, and Carmeliet P (2009) Inhibition of oxygen sensors as a therapeutic strategy for ischaemic and inflammatory disease. Nat Rev Drug Discov 8:139-152.
11. Gunaratnam L and Bonventre JV (2009) HIF in kidney disease and development. J Am Soc Nephrol 20:1877-1887.
12. Haase VH (2006) Hypoxia-inducible factors in the kidney. Am J Physiol Renal Physiol 291:F271-F281.
13. He W, Dai C, Li Y, Zeng G, Monga SP, and Liu Y (2009) Wnt/β-catenin signaling promotes renal interstitial fibrosis. J Am Soc Nephrol 20:765-776.
14. He W, Kang YS, Dai C, and Liu Y (2011) Blockade of Wnt/β-catenin signaling by paricalcitol ameliorates proteinuria and kidney injury. J Am Soc Nephrol 22:90-103.
15. Higgins DF, Kimura K, Bernhardt WM, Shrimanker N, Akai Y, Hohenstein B, Saito Y, Johnson RS, Kretzler M, Cohen CD, et al. (2007) Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 117:3810-3820. (Pubitemid 350224091)
16. Hill P, Shukla D, Tran MG, Aragones J, Cook HT, Carmeliet P, and Maxwell PH (2008) Inhibition of hypoxia inducible factor hydroxylases protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 19:39-46.
17. Iglesias DM, Hueber PA, Chu L, Campbell R, Patenaude AM, Dziarmaga AJ, Quinlan J, Mohamed O, Dufort D, and Goodyer PR (2007) Canonical WNT signaling during kidney development. Am J Physiol Renal Physiol 293:F494-F500. (Pubitemid 47358119)
18. Kaelin WG Jr and Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393-402.
19. Lan R, Geng H, Hwang Y, Mishra P, Skloss WL, Sprague EA, Saikumar P, and Venkatachalam M (2010) A novel wounding device suitable for quantitative biochemical analysis of wound healing and regeneration of cultured epithelium. Wound Repair Regen 18:159-167.
20. Longo KA, Kennell JA, Ochocinska MJ, Ross SE, Wright WS, and MacDougald OA (2002) Wnt signaling protects 3T3-L1 preadipocytes from apoptosis through induction of insulin-like growth factors. J Biol Chem 277:38239-38244. (Pubitemid 35154678)
21. Lyons JP, Miller RK, Zhou X, Weidinger G, Deroo T, Denayer T, Park JI, Ji H, Hong JY, Li A, et al. (2009) Requirement of Wnt/β-catenin signaling in pronephric kidney development. Mech Dev 126:142-159.
22. Ma D, Lim T, Xu J, Tang H, Wan Y, Zhao H, Hossain M, Maxwell PH, and Maze M (2009) Xenon preconditioning protects against renal ischemic-reperfusion injury via HIF-1α activation. J Am Soc Nephrol 20:713-720.
23. 2 regulates stem cells through Wnt/β-catenin signalling. Nat Cell Biol 12:1007-1013.
24. Nelson WJ and Nusse R (2004) Convergence of Wnt, β-catenin, and cadherin pathways. Science 303:1483-1487. (Pubitemid 38314410)
25. Patel S and Woodgett J (2008) Glycogen synthase kinase-3 and cancer: good cop, bad cop? Cancer Cell 14:351-353.
26. Price VR, Reed CA, Lieberthal W, and Schwartz JH (2002) ATP depletion of tubular cells causes dissociation of the zonula adherens and nuclear translocation of β-catenin and LEF-1. J Am Soc Nephrol 13:1152-1161. (Pubitemid 34441395)
27. Pulkkinen K, Murugan S, and Vainio S (2008) Wnt signaling in kidney development and disease. Organogenesis 4:55-59. (Pubitemid 351881300)
28. Rosenberger C, Mandriota S, Jürgensen JS, Wiesener MS, Hörstrup JH, Frei U, Ratcliffe PJ, Maxwell PH, Bachmann S, and Eckardt KU (2002) Expression of hypoxia-inducible factor-1α and -2α in hypoxic and ischemic rat kidneys. J AmSoc Nephrol 13:1721-1732. (Pubitemid 34700596)
29. Semenza GL (2007) Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007: cm8.
30. Stojadinovic O, Brem H, Vouthounis C, Lee B, Fallon J, Stallcup M, Merchant A, Galiano RD, and Tomic-CanicM(2005) Molecular pathogenesis of chronic wounds: the role of β-catenin and c-myc in the inhibition of epithelialization and wound healing. Am J Pathol 167:59-69. (Pubitemid 40884770)
31. Sutton TA, Wilkinson J, Mang HE, Knipe NL, Plotkin Z, Hosein M, Zak K, Wittenborn J, and Dagher PC (2008) p53 regulates renal expression of HIF-1α and pVHL under physiological conditions and after ischemia-reperfusion injury. Am J Physiol Renal Physiol 295:F1666-F1677.
32. Tandara AA and Mustoe TA (2004) Oxygen in wound healing-more than a nutrient. World J Surg 28:294-300. (Pubitemid 38375532)
33. Wang J, Biju MP, Wang MH, Haase VH, and Dong Z (2006) Cytoprotective effects of hypoxia against cisplatin-induced tubular cell apoptosis: involvement of mitochondrial inhibition and p53 suppression. J Am Soc Nephrol 17:1875-1885. (Pubitemid 44036172)
34. Wang W, Reeves WB, and Ramesh G (2009a) Netrin-1 increases proliferation and migration of renal proximal tubular epithelial cells via the UNC5B receptor. Am J Physiol Renal Physiol 296:F723-F729.
35. Wang Z, Havasi A, Gall J, Bonegio R, Li Z, Mao H, Schwartz JH, and Borkan SC (2010) GSK3β promotes apoptosis after renal ischemic injury. J Am Soc Nephrol 21:284-294.
36. Wang Z, Havasi A, Gall JM, Mao H, Schwartz JH, and Borkan SC (2009b) β-Catenin promotes survival of renal epithelial cells by inhibiting Bax. J Am Soc Nephrol 20:1919-1928.
37. Weidemann A, Bernhardt WM, Klanke B, Daniel C, Buchholz B, Câmpean V, Amann K, Warnecke C, Wiesener MS, Eckardt KU, et al. (2008) HIF activation protects from acute kidney injury. J Am Soc Nephrol 19:486-494. (Pubitemid 351355392)
38. Yang CC, Lin LC, Wu MS, Chien CT, and Lai MK (2009) Repetitive hypoxic preconditioning attenuates renal ischemia/reperfusion induced oxidative injury via upregulating HIF-1α-dependent bcl-2 signaling. Transplantation 88:1251-1260.
39. Zeng R, Yao Y, Han M, Zhao X, Liu XC, Wei J, Luo Y, Zhang J, Zhou J, Wang S, et al. (2008) Biliverdin reductase mediates hypoxia-induced EMT via PI3-kinase and Akt. J Am Soc Nephrol 19:380-387. (Pubitemid 351240659)
40. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, and Semenza GL (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283:10892-10903.
41. Zhuang S, Duan M, and Yan Y (2011) Src family kinases regulate renal epithelial dedifferentiation through activation of EGFR/PI3K signaling. J Cell Physiol http:// dx.doi.org/10.1002/jcp.22946.