PGC1α drives NAD biosynthesis linking oxidative metabolism to renal protection

Nature

Volumn 531, Issue 7595, 2016, Pages 528-532

  Tran, Mei T ^a   Zsengeller, Zsuzsanna K ^a   Berg, Anders H ^a   Khankin, Eliyahu V ^a   Bhasin, Manoj K ^a   Kim, Wondong ^b   Clish, Clary B ^c   Stillman, Isaac E ^a   Karumanchi, S Ananth ^a,d   Rhee, Eugene P ^b,c   Parikh, Samir M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; AMINO ACID; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROSTAGLANDIN; PROSTAGLANDIN E2; CYTOKINE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE, MOUSE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

BIOTECHNOLOGY; ENZYME ACTIVITY; FAT; METABOLISM; MITOCHONDRION; OXIDATION; PLATINUM GROUP ELEMENT;

AEROBIC METABOLISM; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; KIDNEY FUNCTION; KIDNEY INJURY; LIPID STORAGE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RENAL PROTECTION; SIGNAL TRANSDUCTION; STRESS; TRANSGENIC MOUSE; UPREGULATION; ACUTE KIDNEY INJURY; ADIPOSE TISSUE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; HUMAN; ISCHEMIA; KIDNEY; MALE; METABOLISM; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

MUS; MUS MUSCULUS;

3-HYDROXYBUTYRIC ACID; ACUTE KIDNEY INJURY; ADIPOSE TISSUE; AMINO ACIDS; ANIMALS; CYTOKINES; DINOPROSTONE; HUMANS; ISCHEMIA; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NAD; NIACINAMIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; OXIDATION-REDUCTION; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84961724213     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature17184     Document Type: Article

References (45)

1. Thadhani, R., Pascual, M. & Bonventre, J. V. Acute renal failure. N. Engl. J. Med. 334, 1448-1460 (1996).
2. Lewington, A. J., Cerda, J. & Mehta, R. L. Raising awareness of acute kidney injury: a global perspective of a silent killer. Kidney Int. 84, 457-467 (2013).
3. Puigserver, P. et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839 (1998).
4. Ruas, J. L. et al. A PGC-1? isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151, 1319-1331 (2012).
5. Hanson, J. et al. Nicotinic acid-And monomethyl fumarate-induced flushing involves GPR109A expressed by keratinocytes and COX-2-dependent prostanoid formation in mice. J. Clin. Invest. 120, 2910-2919 (2010).
6. Pagliarini, D. J. et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123 (2008).
7. Tran, M. et al. PGC-1? promotes recovery after acute kidney injury during systemic inflammation in mice. J. Clin. Invest. 121, 4003-4014 (2011).
8. Arany, Z. et al. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1?. Nature 451, 1008-1012 (2008).
9. Agudelo, L. Z. et al. Skeletal muscle PGC-1?1 modulates kynurenine metabolism and mediates resilience to stress-induced depression. Cell 159, 33-45 (2014).
10. Arany, Z. et al. Transverse aortic constriction leads to accelerated heart failure in micelacking PPAR-? coactivator 1?. Proc. Natl Acad. Sci. USA 103, 10086-10091 (2006).
11. St-Pierre, J. et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127, 397-408 (2006).
12. Weidemann, M. J. & Krebs, H. A. The fuel of respiration of rat kidney cortex. Biochem. J. 112, 149-166 (1969).
13. Collins, P. B. & Chaykin, S. The management of nicotinamide and nicotinic acid in the mouse. J. Biol. Chem. 247, 778-783 (1972).
14. Traykova-Brauch, M. et al. An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nature Med. 14, 979-984 (2008).
15. Revollo, J. R., Grimm, A. A. & Imai, S. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J. Biol. Chem. 279, 50754-50763 (2004).
16. Bai, P. et al. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 13, 461-468 (2011).
17. Gomes, A. P. et al. Declining NAD+ induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155, 1624-1638 (2013).
18. Garcia Soriano, F. et al. Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nature Med. 7, 108-113 (2001).
19. Jesinkey, S. R. et al. Formoterol restores mitochondrial and renal function after ischemia-reperfusion injury. J. Am. Soc. Nephrol. 25, 1157-1162 (2014).
20. Boström, P. et al. A PGC1-?-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463-468 (2012).
21. Breyer, M. D., Jacobson, H. R. & Breyer, R. M. Functional and molecular aspects of renal prostaglandin receptors. J. Am. Soc. Nephrol. 7, 8-17 (1996).
22. Papanicolaou, N., Callard, P., Bariety, J. & Milliez, P. The effect of indomethacin and prostaglandin (PGE2) on renal failure due to glycerol in saline-loaded rats. Clin. Sci. Mol. Med. 49, 507-510 (1975).
23. Mauk, R. H., Patak, R. V., Fadem, S. Z., Lifschitz, M. D. & Stein, J. H. Effect of prostaglandin E administration in a nephrotoxic and a vasoconstrictor model of acute renal failure. Kidney Int. 12, 122-130 (1977).
24. Sketch, M. H., Jr. et al. Prevention of contrast media-induced renal dysfunction with prostaglandin E1: a randomized, double-blind, placebo-controlled study. Am. J. Ther. 8, 155-162 (2001).
25. Feldkamp, T. et al. Preservation of complex I function during hypoxiareoxygenation-induced mitochondrial injury in proximal tubules. Am. J. Physiol. Renal Physiol. 286, F749-F759 (2004).
26. Morigi, M. et al. Sirtuin 3-dependent mitochondrial dynamic improvements protect against acute kidney injury. J. Clin. Invest. 125, 715-726 (2015).
27. Ebrahimkhani, M. R. et al. Aag-initiated base excision repair promotes ischemia reperfusion injury in liver, brain, and kidney. Proc. Natl Acad. Sci. USA 111, E4878-E4886 (2014).
28. Rajakumar, S. V. et al. Deficiency or inhibition of CD73 protects in mild kidney ischemia-reperfusion injury. Transplantation 90, 1260-1264 (2010).
29. Wang, G. et al. P7C3 neuroprotective chemicals function by activating therate-limiting enzyme in NAD salvage. Cell 158, 1324-1334 (2014).
30. Kraus, D. et al. Nicotinamide N-methyltransferase knockdown protects against diet-induced obesity. Nature 508, 258-262 (2014).
31. Tran, M. et al. PGC-1? promotes recovery after acute kidney injury during systemic inflammation in mice. J. Clin. Invest. 121, 4003-4014 (2011).
32. Traykova-Brauch, M. et al. An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nature Med. 14, 979-984 (2008).
33. Rask-Andersen, M., Almen, M. S. & Schioth, H. B. Trends in the exploitation of novel drug targets. Nature Rev. Drug Discov. 10, 579-590 (2011).
34. Singh, V. et al. Mycobacterium tuberculosis-driven targeted recalibration of macrophage lipid homeostasis promotes the foamy phenotype. Cell Host Microbe 12, 669-681 (2012).
35. Feingold, K. R., Moser, A., Shigenaga, J. K. & Grunfeld, C. Inflammation stimulates niacin receptor (GPR109A/HCA2) expression in adipose tissue and macrophages. J. Lipid Res. 55, 2501-2508 (2014).
36. Zsengellér, Z. K. et al. Cisplatin nephrotoxicity involves mitochondrial injury with impaired tubular mitochondrial enzyme activity. J. Histochem. Cytochem. 60, 521-529 (2012).
37. Rhee, E. P. et al. A genome-wide association study of the human metabolome in a community-based cohort. Cell Metab. 18, 130-143 (2013).
38. Kang, C. & Ji, L. L. Muscle immobilization and remobilization downregulates PGC-1? signaling and the mitochondrial biogenesis pathway. J. Appl. Physiol. (1985) 115, 1618-1625 (2013).
39. Ruas, J. L. et al. A PGC-1? isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151, 1319-1331 (2012).
40. Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M. & Sassone-Corsi, P. Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324, 654-657 (2009).
41. Agudelo, L. Z. et al. Skeletal muscle PGC-1?1 modulates kynurenine metabolism and mediates resilience to stress-induced depression. Cell 159, 33-45 (2014).
42. Liu, L. et al. Nutrient sensing by the mitochondrial transcription machinery dictates oxidative phosphorylation. J. Clin. Invest. 124, 768-784 (2014).
43. Hasmann, M. & Schemainda, I. FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res. 63, 7436-7442 (2003).
44. Qi, Z. et al. Serial determination of glomerular filtration rate in conscious mice using FITC-inulin clearance. Am. J. Physiol. Renal Physiol. 286, F590-F596 (2004).
45. Antonica, F. et al. Generation of functional thyroid from embryonic stem cells. Nature 491, 66-71 (2012).