Loss of NAD Homeostasis Leads to Progressive and Reversible Degeneration of Skeletal Muscle

Cell Metabolism

Volumn 24, Issue 2, 2016, Pages 269-282

  Frederick, David W ^a   Loro, Emanuele ^a   Liu, Ling ^b   Davila, Antonio ^a   Chellappa, Karthikeyani ^a   Silverman, Ian M ^c   Quinn, William J ^a   Gosai, Sager J ^c   Tichy, Elisia D ^a   Davis, James G ^a   Mourkioti, Foteini ^a   Gregory, Brian D ^c   Dellinger, Ryan W ^d   Redpath, Philip ^e   Migaud, Marie E ^e   Nakamaru Ogiso, Eiko ^a   Rabinowitz, Joshua D ^b   Khurana, Tejvir S ^a   Baur, Joseph A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d ChromaDex Inc   (United States)

^e QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; NICOTINAMIDE RIBOSIDE; GLUCOSE; NICOTINAMIDE; NICOTINAMIDE-BETA-RIBOSIDE;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXERCISE; HOMEOSTASIS; MOUSE; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE NECROSIS; MUSCLE STRENGTH; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; TREADMILL EXERCISE; AGING; ANALOGS AND DERIVATIVES; ANIMAL; BIOAVAILABILITY; C57BL MOUSE; DEFICIENCY; ENERGY METABOLISM; ENZYMOLOGY; GENETIC TRANSCRIPTION; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; NECROSIS; ORAL DRUG ADMINISTRATION; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADMINISTRATION, ORAL; AGING; ANIMALS; BIOLOGICAL AVAILABILITY; ENERGY METABOLISM; GLUCOSE; HOMEOSTASIS; INFLAMMATION; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MUSCLE STRENGTH; MUSCLE, SKELETAL; NAD; NECROSIS; NIACINAMIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; ORGAN SIZE; PHYSICAL CONDITIONING, ANIMAL; TRANSCRIPTION, GENETIC;

EID: 84991088710     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.07.005     Document Type: Article

References (39)

1. Asher, G., Sassone-Corsi, P., Time for food: the intimate interplay between nutrition, metabolism, and the circadian clock. Cell 161 (2015), 84–92.
2. Bieganowski, P., Brenner, C., Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss-Handler independent route to NAD+ in fungi and humans. Cell 117 (2004), 495–502.
3. Bothe, G.W., Haspel, J.A., Smith, C.L., Wiener, H.H., Burden, S.J., Selective expression of Cre recombinase in skeletal muscle fibers. Genesis 26 (2000), 165–166.
4. Braidy, N., Guillemin, G.J., Mansour, H., Chan-Ling, T., Poljak, A., Grant, R., Age related changes in NAD+ metabolism oxidative stress and Sirt1 activity in wistar rats. PLoS ONE, 6, 2011, e19194.
5. + precursor nicotinamide riboside protects from noise-induced hearing loss. Cell Metab. 20 (2014), 1059–1068.
6. Cantó, C., Houtkooper, R.H., Pirinen, E., Youn, D.Y., Oosterveer, M.H., Cen, Y., Fernandez-Marcos, P.J., Yamamoto, H., Andreux, P.A., Cettour-Rose, P., et al. The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab. 15 (2012), 838–847.
7. Cantó, C., Menzies, K.J., Auwerx, J., NAD(+) Metabolism and the Control of Energy Homeostasis: A Balancing Act between Mitochondria and the Nucleus. Cell Metab. 22 (2015), 31–53.
8. Cárdenas, C., Miller, R.A., Smith, I., Bui, T., Molgó, J., Müller, M., Vais, H., Cheung, K.-H., Yang, J., Parker, I., et al. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142 (2010), 270–283.
9. Cerutti, R., Pirinen, E., Lamperti, C., Marchet, S., Sauve, A.A., Li, W., Leoni, V., Schon, E.A., Dantzer, F., Auwerx, J., et al. NAD(+)-dependent activation of sirt1 corrects the phenotype in a mouse model of mitochondrial disease. Cell Metab. 19 (2014), 1042–1049.
10. Chalkiadaki, A., Igarashi, M., Nasamu, A.S., Knezevic, J., Guarente, L., Muscle-specific SIRT1 gain-of-function increases slow-twitch fibers and ameliorates pathophysiology in a mouse model of duchenne muscular dystrophy. PLoS Genet., 10, 2014, e1004490.
11. Diaz, F., Thomas, C.K., Garcia, S., Hernandez, D., Moraes, C.T., Mice lacking COX10 in skeletal muscle recapitulate the phenotype of progressive mitochondrial myopathies associated with cytochrome c oxidase deficiency. Hum. Mol. Genet. 14 (2005), 2737–2748.
12. Frederick, D.W., Davis, J.G., Dávila, A. Jr., Agarwal, B., Michan, S., Puchowicz, M.A., Nakamaru-Ogiso, E., Baur, J.A., Increasing NAD synthesis in muscle via nicotinamide phosphoribosyltransferase is not sufficient to promote oxidative metabolism. J. Biol. Chem. 290 (2015), 1546–1558.
13. Gomes, A.P., Price, N.L., Ling, A.J.Y., Moslehi, J.J., Montgomery, M.K., Rajman, L., White, J.P., Teodoro, J.S., Wrann, C.D., Hubbard, B.P., et al. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155 (2013), 1624–1638.
14. Gong, B., Pan, Y., Vempati, P., Zhao, W., Knable, L., Ho, L., Wang, J., Sastre, M., Ono, K., Sauve, A.A., Pasinetti, G.M., Nicotinamide riboside restores cognition through an upregulation of proliferator-activated receptor-γ coactivator 1α regulated β-secretase 1 degradation and mitochondrial gene expression in Alzheimer's mouse models. Neurobiol. Aging 34 (2013), 1581–1588.
15. Goody, M.F., Kelly, M.W., Reynolds, C.J., Khalil, A., Crawford, B.D., Henry, C.A., NAD+ biosynthesis ameliorates a zebrafish model of muscular dystrophy. PLoS Biol., 10, 2012, e1001409.
16. Graham, B.H., Waymire, K.G., Cottrell, B., Trounce, I.A., MacGregor, G.R., Wallace, D.C., A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet. 16 (1997), 226–234.
17. Grozio, A., Sociali, G., Sturla, L., Caffa, I., Soncini, D., Salis, A., Raffaelli, N., De Flora, A., Nencioni, A., Bruzzone, S., CD73 protein as a source of extracellular precursors for sustained NAD+ biosynthesis in FK866-treated tumor cells. J. Biol. Chem. 288 (2013), 25938–25949.
18. Ha, H.C., Snyder, S.H., Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. USA 96 (1999), 13978–13982.
19. Haslett, J.N., Kang, P.B., Han, M., Kho, A.T., Sanoudou, D., Volinski, J.M., Beggs, A.H., Kohane, I.S., Kunkel, L.M., The influence of muscle type and dystrophin deficiency on murine expression profiles. Mamm. Genome 16 (2005), 739–748.
20. Hikosaka, K., Ikutani, M., Shito, M., Kazuma, K., Gulshan, M., Nagai, Y., Takatsu, K., Konno, K., Tobe, K., Kanno, H., Nakagawa, T., Deficiency of nicotinamide mononucleotide adenylyltransferase 3 (nmnat3) causes hemolytic anemia by altering the glycolytic flow in mature erythrocytes. J. Biol. Chem. 289 (2014), 14796–14811.
21. Khan, N.A., Auranen, M., Paetau, I., Pirinen, E., Euro, L., Forsström, S., Pasila, L., Velagapudi, V., Carroll, C.J., Auwerx, J., Suomalainen, A., Effective treatment of mitochondrial myopathy by nicotinamide riboside, a vitamin B3. EMBO Mol. Med. 6 (2014), 721–731.
22. Klover, P., Chen, W., Zhu, B.-M., Hennighausen, L., Skeletal muscle growth and fiber composition in mice are regulated through the transcription factors STAT5a/b: linking growth hormone to the androgen receptor. FASEB J. 23 (2009), 3140–3148.
23. Krishnamurthy, J., Torrice, C., Ramsey, M.R., Kovalev, G.I., Al-Regaiey, K., Su, L., Sharpless, N.E., Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 114 (2004), 1299–1307.
24. Kulikova, V., Shabalin, K., Nerinovski, K., Dölle, C., Niere, M., Yakimov, A., Redpath, P., Khodorkovskiy, M., Migaud, M.E., Ziegler, M., Nikiforov, A., Generation, release, and uptake of the NAD precursor nicotinic acid riboside by human cells. J. Biol. Chem. 290 (2015), 27124–27137.
25. Lu, A., Poddar, M., Tang, Y., Proto, J.D., Sohn, J., Mu, X., Oyster, N., Wang, B., Huard, J., Rapid depletion of muscle progenitor cells in dystrophic mdx/utrophin-/- mice. Hum. Mol. Genet. 23 (2014), 4786–4800.
26. Mouchiroud, L., Houtkooper, R.H., Moullan, N., Katsyuba, E., Ryu, D., Cantó, C., Mottis, A., Jo, Y.-S., Viswanathan, M., Schoonjans, K., et al. The NAD(+)/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 154 (2013), 430–441.
27. Pastoret, C., Sebille, A., Age-related differences in regeneration of dystrophic (mdx) and normal muscle in the mouse. Muscle Nerve 18 (1995), 1147–1154.
28. Revollo, J.R., Grimm, A.A., Imai, S., The regulation of nicotinamide adenine dinucleotide biosynthesis by Nampt/PBEF/visfatin in mammals. Curr. Opin. Gastroenterol. 23 (2007), 164–170.
29. Revollo, J.R., Körner, A., Mills, K.F., Satoh, A., Wang, T., Garten, A., Dasgupta, B., Sasaki, Y., Wolberger, C., Townsend, R.R., et al. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab. 6 (2007), 363–375.
30. Rongvaux, A., Galli, M., Denanglaire, S., Van Gool, F., Drèze, P.L., Szpirer, C., Bureau, F., Andris, F., Leo, O., Nicotinamide phosphoribosyl transferase/pre-B cell colony-enhancing factor/visfatin is required for lymphocyte development and cellular resistance to genotoxic stress. J. Immunol. 181 (2008), 4685–4695.
31. Rybalka, E., Timpani, C.A., Cooke, M.B., Williams, A.D., Hayes, A., Defects in mitochondrial ATP synthesis in dystrophin-deficient mdx skeletal muscles may be caused by complex I insufficiency. PLoS ONE, 9, 2014, e115763.
32. Sacco, A., Mourkioti, F., Tran, R., Choi, J., Llewellyn, M., Kraft, P., Shkreli, M., Delp, S., Pomerantz, J.H., Artandi, S.E., Blau, H.M., Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143 (2010), 1059–1071.
33. Sousa-Victor, P., Gutarra, S., García-Prat, L., Rodriguez-Ubreva, J., Ortet, L., Ruiz-Bonilla, V., Jardí, M., Ballestar, E., González, S., Serrano, A.L., et al. Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506 (2014), 316–321.
34. Stein, L.R., Imai, S., Specific ablation of Nampt in adult neural stem cells recapitulates their functional defects during aging. EMBO J. 33 (2014), 1321–1340.
35. Tan, B., Young, D.A., Lu, Z.-H., Wang, T., Meier, T.I., Shepard, R.L., Roth, K., Zhai, Y., Huss, K., Kuo, M.-S., et al. Pharmacological inhibition of nicotinamide phosphoribosyltransferase (NAMPT), an enzyme essential for NAD+ biosynthesis, in human cancer cells: metabolic basis and potential clinical implications. J. Biol. Chem. 288 (2013), 3500–3511.
36. Weinstein, R.S., Hutson, M.S., Decreased trabecular width and increased trabecular spacing contribute to bone loss with aging. Bone 8 (1987), 137–142.
37. Xu, W., Barrientos, T., Mao, L., Rockman, H.A., Sauve, A.A., Andrews, N.C., Lethal cardiomyopathy in mice lacking transferrin receptor in the heart. Cell Rep. 13 (2015), 533–545.
38. Yoshino, J., Mills, K.F., Yoon, M.J., Imai, S., Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 14 (2011), 528–536.
39. Zhao, X., Yamazaki, D., Park, K.H., Komazaki, S., Tjondrokoesoemo, A., Nishi, M., Lin, P., Hirata, Y., Brotto, M., Takeshima, H., Ma, J., Ca2+ overload and sarcoplasmic reticulum instability in tric-a null skeletal muscle. J. Biol. Chem. 285 (2010), 37370–37376.