Conditional knockout of proximal tubule mitofusin 2 accelerates recovery and improves survival after renal ischemia

Journal of the American Society of Nephrology

Volumn 26, Issue 5, 2015, Pages 1092-1102

  Gall, Jonathan M ^a   Wang, Zhiyong ^a   Bonegio, Ramon G ^a   Havasi, Andrea ^a   Liesa, Marc ^a   Vemula, Pradheep ^a   Borkan, Steven C ^a  

^a BOSTON MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOFUSIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RAS PROTEIN; GUANOSINE TRIPHOSPHATASE; MFN2 PROTEIN, MOUSE;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; GENOTYPE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CORTEX; KIDNEY HOMOGENATE; KIDNEY ISCHEMIA; KIDNEY PROXIMAL TUBULE; MALE; METABOLIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SURVIVAL; ACUTE KIDNEY INJURY; ANIMAL; COMPLICATION; CONVALESCENCE; DISEASE MODEL; ISCHEMIA; KNOCKOUT MOUSE; METABOLISM; MORTALITY; PHYSIOLOGY; REGENERATION;

ACUTE KIDNEY INJURY; ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; GTP PHOSPHOHYDROLASES; ISCHEMIA; KIDNEY TUBULES, PROXIMAL; MALE; MAP KINASE SIGNALING SYSTEM; MICE, KNOCKOUT; RECOVERY OF FUNCTION; REGENERATION;

EID: 84929377156     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014010126     Document Type: Article

References (53)

1. Brooks C, Cho SG, Wang CY, Yang T, Dong Z: Fragmented mitochondria are sensitized to Bax insertion and activation during apoptosis. Am J Physiol Cell Physiol 300: C447-C455, 2011
2. Vanhooren V, Liu XE, Desmyter L, Fan YD, Vanwalleghem L, Van Molle W, Dewaele S, Praet M, Contreras R, Libert C, Chen C: Over-expression of heat shock protein 70 in mice is associated with growth retardation, tumor formation, and early death. Rejuvenation Res 11: 1013-1020, 2008
3. Brooks C, Wei Q, Feng L, Dong G, Tao Y, Mei L, Xie Z-J, Dong Z: Bak regulates mitochondrial morphology and pathology during apoptosis by interacting with mitofusins. Proc Natl Acad Sci U S A 104: 11649-11654, 2007
4. Gall JM, Wang Z, Liesa M, Molina A, Havasi A, Schwartz JH, Shirihai O, Borkan SC, Bonegio RG: Role of mitofusin 2 in the renal stress response. PLoS ONE 7: e31074, 2012
5. Brooks C, Wei Q, Cho SG, Dong Z: Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. J Clin Invest 119: 1275-1285, 2009
6. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K: Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282: 11521-11529, 2007
7. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, Otera H, Nakanishi Y, Nonaka I, Goto Y, Taguchi N, Morinaga H, Maeda M, Takayanagi R, Yokota S, Mihara K: Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11: 958-966, 2009
8. Twig G, Elorza A, Molina AJA, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS: Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:433-446, 2008
9. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC: Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-289, 2010
10. Sebastián D, Hernández-Alvarez MI, Segalés J, Sorianello E, Muñoz JP, Sala D, Waget A, Liesa M, Paz JC, Gopalacharyulu P, Orešič M, Pich S, Burcelin R, Palacín M, Zorzano A: Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. Proc Natl Acad Sci U S A 109: 5523-5528, 2012
11. Chen KH, Guo X, Ma D, Guo Y, Li Q, Yang D, Li P, Qiu X, Wen S, Xiao RP, Tang J: Dysregulation of HSG triggers vascular proliferative disorders. Nat Cell Biol 6: 872-883, 2004
12. Chen KH, Dasgupta A, Ding J, Indig FE, Ghosh P, Longo DL: Role of mitofusin 2 (Mfn2) in controlling cellular proliferation. FASEB J 28: 382-394, 2014
13. Wan-Xin T, Tian-Lei C, Ben W, Wei-Hua W, Ping F: Effect of mitofusin 2 overexpression on the proliferation and apoptosis of high-glucose-induced rat glomerular mesangial cells. J Nephrol 25: 1023-1030, 2012
14. Chen J, Chen JK, Harris RC: Deletion of the epidermal growth factor receptor in renal proximal tubule epithelial cells delays recovery from acute kidney injury. Kidney Int 82: 45-52, 2012
15. Kwon DS, Kwon CH, Kim JH, Woo JS, Jung JS, Kim YK: Signal transduction of MEK/ERK and PI3K/Akt activation by hypoxia/reoxygenation in renal epithelial cells. Eur J Cell Biol 85: 1189-1199, 2006
16. Jang HS, Han SJ, Kim JI, Lee S, Lipschutz JH, Park KM: Activation of ERK accelerates repair of renal tubular epithelial cells, whereas it inhibits progression of fibrosis following ischemia/reperfusion injury. Biochim Biophys Acta 1832: 1998-2008, 2013
17. Wang Z, Havasi A, Gall JM, Mao H, Schwartz JH, Borkan SC: Beta-catenin promotes survival of renal epithelial cells by inhibiting Bax. J Am Soc Nephrol 20: 1919-1928, 2009
18. Li H, Zhou X, Davis DR, Xu D, Sigmund CD: An androgen-inducible proximal tubule-specific Cre recombinase transgenic model. Am J Physiol Renal Physiol 294: F1481-F1486, 2008
19. Ueki S, Takagi J, Saito Y: Dual functions of transglutaminase in novel cell adhesion. J Cell Sci 109: 2727-2735, 1996
20. Wang Z, Havasi A, Gall J, Bonegio R, Li Z, Mao H, Schwartz JH, Borkan SC: GSK3beta promotes apoptosis after renal ischemic injury. J Am Soc Nephrol 21: 284-294, 2010
21. Wang Z, Gall JM, Bonegio RG, Havasi A, Hunt CR, Sherman MY, Schwartz JH, Borkan SC: Induction of heat shock protein 70 inhibits ischemic renal injury. Kidney Int 79: 861-870, 2011
22. Shin DM, Jeon JH, Kim CW, Cho SY, Kwon JC, Lee HJ, Choi KH, Park SC, Kim IG: Cell type-specific activation of intracellular transglutaminase 2 by oxidative stress or ultraviolet irradiation: implications of transglutaminase 2 in age-related cataractogenesis. J Biol Chem 279: 15032-15039, 2004
23. Padanilam BJ: Cell death induced by acute renal injury: A perspective on the contributions of apoptosis and necrosis. Am J Physiol Renal Physiol 284: F608-F627, 2003
24. Venkatachalam MA, Bernard DB, Donohoe JF, Levinsky NG: Ischemic damage and repair in the rat proximal tubule: Differences among the S1, S2, and S3 segments. Kidney Int 14: 31-49, 1978
25. Rosen S, Heyman SN: Difficulties in understanding human "acute tubular necrosis": Limited data and flawed animal models. Kidney Int 60: 1220-1224, 2001
26. Papanicolaou KN, Khairallah RJ, Ngoh GA, Chikando A, Luptak I, O'Shea KM, Riley DD, Lugus JJ, Colucci WS, Lederer WJ, Stanley WC, Walsh K: Mitofusin-2 maintains mitochondrial structure and contributes to stress-induced permeability transition in cardiac myocytes. Mol Cell Biol 31: 1309-1328, 2011
27. Devarajan P: Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 17: 1503-1520, 2006
28. Havasi A, Haegele JA, Gall JM, Blackmon S, Ichimura T, Bonegio RG, Panchenko MV: Histone acetyl transferase (HAT) HBO1 and JADE1 in epithelial cell regeneration. Am J Pathol 182: 152-162, 2013
29. Duffield JS, Park KM, Hsiao LL, Kelley VR, Scadden DT, Ichimura T, Bonventre JV: Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 115: 1743-1755, 2005
30. Racusen LC, Fivush BA, Li YL, Slatnik I, Solez K: Dissociation of tubular cell detachment and tubular cell death in clinical and experimental "acute tubular necrosis". Lab Invest 64: 546-556, 1991
31. Wen X, Murugan R, Peng Z, Kellum JA: Pathophysiology of acute kidney injury: a new perspective. Contrib Nephrol 165: 39-45, 2010
32. Lee PT, Lin HH, Jiang ST, Lu PJ, Chou KJ, Fang HC, Chiou YY, Tang MJ: Mouse kidney progenitor cells accelerate renal regeneration and prolong survival after ischemic injury. Stem Cells 28: 573-584, 2010
33. 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
34. Hertig A, Verine J, Mougenot B, Jouanneau C, Ouali N, Sebe P, Glotz D, Ancel PY, Rondeau E, Xu-Dubois YC: Risk factors for early epithelial to mesenchymal transition in renal grafts. Am J Transplant 6: 2937-2946, 2006
35. Chen CC, Liu ZM, Wang HH, He W, Wang Y, Wu WD: Effects of ulinastatin on renal ischemia-reperfusion injury in rats. Acta Pharmacol Sin 25: 1334-1340, 2004
36. Pombo CM, Bonventre JV, Avruch J, Woodgett JR, Kyriakis JM, Force T: The stress-activated protein kinases are major c-Jun amino-terminal kinases activated by ischemia and reperfusion. J Biol Chem 269: 26546-26551, 1994
37. Fiaschi-Taesch NM, Santos S, Reddy V, Van Why SK, Philbrick WF, Ortega A, Esbrit P, Orloff JJ, Garcia-Ocaña A: Prevention of acute ischemic renal failure by targeted delivery of growth factors to the proximal tubule in transgenic mice: The efficacy of parathyroid hormone-related protein and hepatocyte growth factor. J Am Soc Nephrol 15: 112-125, 2004
38. Watton SJ, Downward J: Akt/PKB localisation and 3' phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr Biol 9: 433-436, 1999
39. Takeda R, Nishimatsu H, Suzuki E, Satonaka H, Nagata D, Oba S, Sata M, Takahashi M, Yamamoto Y, Terauchi Y, Kadowaki T, Kangawa K, Kitamura T, Nagai R, Hirata Y: Ghrelin improves renal function in mice with ischemic acute renal failure. J Am Soc Nephrol 17: 113-121, 2006
40. Johnson GL, Lapadat R: Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298: 1911-1912, 2002
41. Arany I, Megyesi JK, Kaneto H, Tanaka S, Safirstein RL: Activation of ERK or inhibition of JNK ameliorates H(2)O(2) cytotoxicity in mouse renal proximal tubule cells. Kidney Int 65: 1231-1239, 2004
42. Arany I, Megyesi JK, Nelkin BD, Safirstein RL: STAT3 attenuates EGFR-mediated ERK activation and cell survival during oxidant stress in mouse proximal tubular cells. Kidney Int 70: 669-674, 2006
43. Ishizuka S, Yano T, Hagiwara K, Sone M, Nihei H, Ozasa H, Horikawa S: Extracellular signal-regulated kinase mediates renal regeneration in rats with myoglobinuric acute renal injury. Biochem Biophys Res Commun 254: 88-92, 1999
44. Alderliesten M, de Graauw M, Oldenampsen J, Qin Y, Pont C, van Buren L, van de Water B: Extracellular signal-regulated kinase activation during renal ischemia/reperfusion mediates focal adhesion dissolution and renal injury. Am J Pathol 171: 452-462, 2007
45. Kim YK, Kim HJ, Kwon CH, Kim JH, Woo JS, Jung JS, Kim JM: Role of ERK activation in cisplatin-induced apoptosis in OK renal epithelial cells. J Appl Toxicol 25: 374-382, 2005
46. Wang S, Wei Q, Dong G, Dong Z: ERK-mediated suppression of cilia in cisplatin-induced tubular cell apoptosis and acute kidney injury. Biochim Biophys Acta 1832: 1582-1590, 2013
47. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC: Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200, 2003
48. Ruchalski K, Mao H, Singh SK, Wang Y, Mosser DD, Li F, Schwartz JH, Borkan SC: HSP72 inhibits apoptosis-inducing factor release in ATP-depleted renal epithelial cells. Am J Physiol Cell Physiol 285: C1483-C1493, 2003
49. Li F, Mao HP, Ruchalski KL, Wang YH, Choy W, Schwartz JH, Borkan SC: Heat stress prevents mitochondrial injury in ATP-depleted renal epithelial cells. Am J Physiol Cell Physiol 283: C917-C926, 2002
50. Borkan SC, Wang YH, Lam KT, Brecher P, Schwartz JH: Hepatic alpha 2 mu-globulin: A potential metabolic role in the rat proximal tubule. Am J Physiol 271: F527-F538, 1996
51. Ruchalski K, Mao H, Li Z, Wang Z, Gillers S, Wang Y, Mosser DD, Gabai V, Schwartz JH, Borkan SC: Distinct hsp70 domains mediate apoptosis-inducing factor release and nuclear accumulation. J Biol Chem 281: 7873-7880, 2006
52. Doctor RB, Bacallao R, Mandel LJ: Method for recovering ATP content and mitochondrial function after chemical anoxia in renal cell cultures. Am J Physiol 266: C1803-C1811, 1994
53. Havasi A, Wang Z, Gall JM, Spaderna M, Suri V, Canlas E, Martin JL, Schwartz JH, Borkan SC: Hsp27 inhibits sublethal, Src-mediated renal epithelial cell injury. Am J Physiol Renal Physiol 297: F760-F768, 2009