Deficiency in apoptosis-inducing factor recapitulates chronic kidney disease via aberrant mitochondrial homeostasis

Diabetes

Volumn 65, Issue 4, 2016, Pages 1085-1098

  Coughlan, Melinda T ^a,b   Higgins, Gavin C ^a   Nguyen, Tuong Vi ^a   Penfold, Sally A ^a   Thallas Bonke, Vicki ^a   Tan, Sih Min ^a,b   Ramm, Georg ^b   Van Bergen, Nicole J ^c   Henstridge, Darren C ^a   Sourris, Karly C ^a,b   Harcourt, Brooke E ^d   Trounce, Ian A ^c   Robb, Portia M ^a   Laskowski, Adrienne ^d   McGee, Sean L ^e   Genders, Amanda J ^e   Walder, Ken ^e   Drew, Brian G ^a   Gregorevic, Paul ^a   Qian, Hongwei ^a   Thomas, Merlin C ^a   Jerums, George ^f   Macisaac, Richard J ^g   Skene, Alison ^f   Power, David A ^f,g   Ekinci, Elif I ^f,g,h   Wijeyeratne, Xiaonan W ⁱ   Gallo, Linda A ^j   Herman Edelstein, Michal ^k   Ryan, Michael T ^b   Cooper, Mark E ^a,b   Thorburn, David R ^d   Forbes, Josephine M ^a,j   more..

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c ROYAL VICTORIAN EYE AND EAR HOSPITAL   (Australia)

^d ROYAL CHILDREN'S HOSPITAL   (Australia)

^e DEAKIN UNIVERSITY   (Australia)

^f AUSTIN HEALTH   (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

^h MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

ⁱ LA TROBE UNIVERSITY   (Australia)

^j UNIVERSITY OF QUEENSLAND   (Australia)

^k TEL AVIV UNIVERSITY   (Israel)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALBUMIN; APOPTOSIS INDUCING FACTOR; COLLAGEN TYPE 4; CYSTATIN C; GLUCOSE; MITOFUSIN 1; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE; PDCD8 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENERGY; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; CREATININE CLEARANCE; DIABETIC NEPHROPATHY; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE SILENCING; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN TISSUE; KIDNEY CORTEX; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONTENT; RISK FACTOR; TURNOVER TIME; UPREGULATION; URINARY EXCRETION; ANIMAL; C57BL MOUSE; CBA MOUSE; CELL CULTURE; CELL RESPIRATION; CHRONIC KIDNEY FAILURE; COMPLICATION; EXPERIMENTAL DIABETES MELLITUS; GENETIC PREDISPOSITION; GENETICS; HOMEOSTASIS; METABOLISM; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS INDUCING FACTOR; CELL RESPIRATION; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; GENETIC PREDISPOSITION TO DISEASE; HOMEOSTASIS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; RENAL INSUFFICIENCY, CHRONIC; RISK FACTORS;

EID: 84962169583     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db15-0864     Document Type: Article

References (50)

1. Soltoff SP. ATP and the regulation of renal cell function. Annu Rev Physiol 1986; 48:9-31
2. Forbes JM, Ke BX, Nguyen T.V., et al. Deficiency in mitochondrial complex I activity due to Ndufs6 gene trap insertion induces renal disease. Antioxid Redox Signal 2013; 19:331-343
3. Kang HM, Ahn SH, Choi P, et al Defective fatty acid oxidation in renal tubular epithelial cells has a key role in kidney fibrosis development. Nat Med 2015; 21:37-46
4. Coughlan MT, Thorburn DR, Penfold S.A., et al. RAGE-induced cytosolic ROS promote mitochondrial superoxide generation in diabetes. J Am Soc Nephrol 2009; 20:742-752
5. Forbes JM, Coughlan MT, Cooper ME Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 2008; 57:1446-1454
6. Sharma K, Karl B, Mathew A.V., et al. Metabolomics reveals signature of mitochondrial dysfunction in diabetic kidney disease. J Am Soc Nephrol 2013; 24: 1901-1912
7. Sivitz WI, Yorek MA Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal 2010; 12:537-577
8. Daehn I, Casalena G, Zhang T., et al. Endothelial mitochondrial oxidative stress determines podocyte depletion in segmental glomerulosclerosis. J Clin Invest 2014; 124:1608-1621
9. Che R, Yuan Y, Huang S., Zhang A. Mitochondrial dysfunction in the pathophysiology of renal diseases. Am J Physiol Renal Physiol 2014; 306: F367-F378
10. Hall AM, Unwin RJ The not so "mighty chondrion": emergence of renal diseases due to mitochondrial dysfunction. Nephron Physiol 2007; 105:1-10
11. Susin SA, Lorenzo HK, Zamzami N, et al Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397:441-446
12. Miramar MD, Costantini P, Ravagnan L., et al. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J Biol Chem 2001; 276:16391-16398
13. Klein JA, Longo-Guess CM, Rossmann M.P., et al. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002; 419:367-374
14. Bénit P., Goncalves S, Dassa E.P., Brière JJ, Rustin P. The variability of the harlequin mouse phenotype resembles that of human mitochondrial-complex I-deficiency syndromes. PLoS One 2008; 3:e3208
15. Vahsen N, Candé C, Brière JJ, et al. AIF deficiency compromises oxidative phosphorylation. EMBO J 2004; 23:4679-4689
16. Tan AL, Sourris KC, Harcourt B.E., et al. Disparate effects on renal and oxidative parameters following RAGE deletion, AGE accumulation inhibition, or dietary AGE control in experimental diabetic nephropathy. Am J Physiol Renal Physiol 2010; 298:F763-F770
17. Saito T, Sumithran E, Glasgow E.F., Atkins RC. The enhancement of aminonucleoside nephrosis by the co-administration of protamine. Kidney Int 1987; 32:691-699
18. Thallas-Bonke V., Thorpe SR, Coughlan M.T., et al. Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-alpha-dependent pathway. Diabetes 2008; 57:460-469
19. Coughlan MT, Yap FY, Tong D.C., et al. Advanced glycation end products are direct modulators of β-cell function. Diabetes 2011; 60:2523-2532
20. Drew B, Leeuwenburgh C. Method for measuring ATP production in isolated mitochondria: ATP production in brain and liver mitochondria of Fischer-344 rats with age and caloric restriction. Am J Physiol Regul Integr Comp Physiol 2003; 285:R1259-R1267
21. Henstridge DC, Bruce CR, Drew B.G., et al. Activating HSP72 in rodent skeletal muscle increases mitochondrial number and oxidative capacity and decreases insulin resistance. Diabetes 2014; 63:1881-1894
22. Lee S, Sheck L, Crowston J.G., et al. Impaired complex-I-linked respiration and ATP synthesis in primary open-angle glaucoma patient lymphoblasts. Invest Ophthalmol Vis Sci 2012; 53:2431-2437
23. McKenzie M, Lazarou M, Thorburn D.R., Ryan MT. Analysis of mitochondrial subunit assembly into respiratory chain complexes using Blue Native poly-acrylamide gel electrophoresis. Anal Biochem 2007; 364:128-137
24. Wang Y, Kim NS, Haince J.F., et al. Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 2011; 4:ra20
25. Nicholls PK, Stanton PG, Rainczuk K.E., Qian H., Gregorevic P, Harrison CA. Lentiviral transduction of rat Sertoli cells as a means to modify gene expression. Spermatogenesis 2012; 2:279-284
26. Martin SD, Morrison S, Konstantopoulos N., McGee SL. Mitochondrial dysfunction has divergent, cell type-dependent effects on insulin action. Mol Metab 2014; 3:408-418
27. McGee SL, Sadli N, Morrison S., Swinton C, Suphioglu C. DHA protects against zinc mediated alterations in neuronal cellular bioenergetics. Cell Physiol Biochem 2011; 28:157-162
28. Herman-Edelstein M., Scherzer P, Tobar A., Levi M, Gafter U. Altered renal lipid metabolism and renal lipid accumulation in human diabetic nephropathy. J Lipid Res 2014; 55:561-572
29. Han WK, Bailly V, Abichandani R., Thadhani R, Bonventre JV. Kidney injury molecule-1 (KIM-1): a novel biomarker for human renal proximal tubule injury. Kidney Int 2002; 62:237-244
30. Zhang Z, Humphreys BD, Bonventre JV Shedding of the urinary biomarker kidney injury molecule-1 (KIM-1) is regulated by MAP kinases and juxtamem-brane region. J Am Soc Nephrol 2007; 18:2704-2714
31. Song S, Meyer M, Türk TR, et al. Serum cystatin C in mouse models: a reliable and precise marker for renal function and superior to serum creatinine. Nephrol Dial Transplant 2009; 24:1157-1161
32. Viau A, El Karoui K, Laouari D, et al Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 2010; 120:4065-4076
33. Jha JC, Gray SP, Barit D, et al Genetic targeting or pharmacologic inhibition of NADPH oxidase nox4 provides renoprotection in long-term diabetic nephropathy. J Am Soc Nephrol 2014; 25:1237-1254
34. Schägger H. Respiratory chain supercomplexes. IUBMB Life 2001; 52:119-128
35. Anand R, Wai T, Baker M.J., et al. The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission. J Cell Biol 2014; 204: 919-929
36. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 2010; 11:872-884
37. Wang W, Wang Y, Long J., et al. Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab 2012; 15:186-200
38. Galloway CA, Yoon Y. Mitochondrial morphology in metabolic diseases. Antioxid Redox Signal 2013; 19:415-430
39. Otera H, Wang C, Cleland M.M., et al. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 2010; 191:1141-1158
40. Westermann B. Bioenergetic role of mitochondrial fusion and fission. Biochim Biophys Acta 2012; 1817:1833-1838
41. Legros F, Lombès A, Frachon P., Rojo M. Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol Biol Cell 2002; 13:4343-4354
42. Zanna C, Ghelli A, Porcelli A.M., et al. OPA1 mutations associated with dominant optic atrophy impair oxidative phosphorylation and mitochondrial fusion. Brain 2008; 131:352-367
43. Cheung EC, Joza N, Steenaart N.A., et al. Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis. EMBO J 2006; 25:4061-4073
44. Brooks C, Wei Q, Cho S.G., Dong Z. Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. J Clin Invest 2009; 119:1275-1285
45. Galloway CA, Lee H, Nejjar S., et al. Transgenic control of mitochondrial fission induces mitochondrial uncoupling and relieves diabetic oxidative stress. Diabetes 2012; 61:2093-2104
46. Zhan M, Usman IM, Sun L, Kanwar YS Disruption of renal tubular mitochondrial quality control by Myo-inositol oxygenase in diabetic kidney disease. J Am Soc Nephrol 2015; 26:1304-1321
47. Hangen E, Blomgren K, Bénit P, Kroemer G., Modjtahedi N. Life with or without AIF. Trends Biochem Sci 2010; 35:278-287
48. Ghezzi D, Sevrioukova I, Invernizzi F., et al. Severe X-linked mitochondrial encephalomyopathy associated with a mutation in apoptosis-inducing factor. Am J Hum Genet 2010; 86:639-649
49. Otera H, Ohsakaya S, Nagaura Z., Ishihara N, Mihara K. Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J 2005; 24:1375-1386
50. Sevrioukova IF. Apoptosis-inducing factor: structure, function, and redox regulation. Antioxid Redox Signal 2011; 14:2545-2579