Aerobic and resistance exercise training reverses age‐dependent decline in NAD+salvage capacity in human skeletal muscle
Open accessAbstract
Aging decreases skeletal muscle mass and strength, but aerobic and resistance exercise training maintains skeletal muscle function. NAD+ is a coenzyme for ATP production and a required substrate for enzymes regulating cellular homeostasis. In skeletal muscle, NAD+ is mainly generated by the NAD+ salvage pathway in which nicotinamide phosphoribosyltransferase (NAMPT) is rate-limiting. NAMPT decreases with age in human skeletal muscle, and aerobic exercise training increases NAMPT levels in young men. However, whether distinct modes of exercise training increase NAMPT levels in both young and old people is unknown. We assessed the effects of 12 weeks of aerobic and resistance exercise training on skeletal muscle abundance of NAMPT, nicotinamide riboside kinase 2 (NRK2), and nicotinamide mononucleotide adenylyltransferase (NMNAT) 1 and 3 in young (≤35 years) and older (≥55 years) individuals. NAMPT in skeletal muscle correlated negatively with age (r2 = 0.297, P < 0.001, n = 57), and VO2peak was the best predictor of NAMPT levels. Moreover, aerobic exercise training increased NAMPT abundance 12% and 28% in young and older individuals, respectively, whereas resistance exercise training increased NAMPT abundance 25% and 30% in young and in older individuals, respectively. None of the other proteins changed with exercise training. In a separate cohort of young and old people, levels of NAMPT, NRK1, and NMNAT1/2 in abdominal subcutaneous adipose tissue were not affected by either age or 6 weeks of high-intensity interval training. Collectively, exercise training reverses the age-dependent decline in skeletal muscle NAMPT abundance, and our findings highlight the value of exercise training in ameliorating age-associated deterioration of skeletal muscle function.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Aerobic exercise training can increase muscle NAMPT activity and NAD+.
“aerobic exercise training can increase muscle NAMPT activity and NAD+ [170, 172, 173].”
From Targeting Intramyocellular Lipids to Improve Aging Muscle Function (2025) · cites this paper as [173]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Age related changes in NAD+ metabolism oxidative stress and Sirt1 activity in wistar rats
Braidy, N., Guillemin, G. J., Mansour, H., Chan-Ling, T., Poljak, A., & Grant, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019194 · Cited by 594 · see citing works
RetractedLópez-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013) · Cell · doi:10.1016/j.cell.2013.05.039 · Cited by 14,982 · see citing works
Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase
Imai, S.-I., Armstrong, C. M., Kaeberlein, M., & Guarente, L. (2000) · Nature · doi:10.1038/35001622 · Cited by 3,510 · see citing works
PGC-1α, SIRT1 and AMPK, an energy sensing network that controls energy expenditure
Cantó, C., & Auwerx, J. (2009) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328328d0a4 · Cited by 1,624 · see citing works
The intersection between aging and cardiovascular disease
North, B. J., & Sinclair, D. A. (2012) · Circulation Research · doi:10.1161/circresaha.111.246876 · Cited by 1,585 · see citing works
NAD+ and sirtuins in aging and disease
Imai, S.-I., & Guarente, L. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.04.002 · Cited by 1,481 · see citing works
Decline in skeletal muscle mitochondrial function with aging in humans
Short, K. R., Bigelow, M. L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., & Nair, K. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501559102 · Cited by 1,333 · see citing works
A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis
Ahn, B.-H., Kim, H.-S., Song, S., Lee, I. H., Liu, J., Vassilopoulos, A., Deng, C.-X., & Finkel, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803790105 · Cited by 1,291 · see citing works
Zhang, H., Ryu, D., Wu, Y., Gariani, K., Wang, X., Luan, P., D’Amico, D., Ropelle, E. R., Lutolf, M. P., Aebersold, R., et al. (2016) · Science · doi:10.1126/science.aaf2693 · Cited by 1,255 · cited 2× · see citing works
“2012), and improves skeletal muscle and muscle stem cell function in mice with aging or muscular dystrophy (Ryu et al. 2016; Zhang et al. 2016).”
BackgroundCantó, 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. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.04.022 · Cited by 1,238 · see citing works
Regulation of pgc-1α, a nodal regulator of mitochondrial biogenesis
Fernandez-Marcos, P. J., & Auwerx, J. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.001917 · Cited by 1,237 · see citing works
Circadian Control of the NAD <sup>+</sup> Salvage Pathway by CLOCK-SIRT1
Nakahata, Y., Sahar, S., Astarita, G., Kaluzova, M., & Sassone-Corsi, P. (2009) · Science · doi:10.1126/science.1170803 · Cited by 1,198 · see citing works
Circadian Clock Feedback Cycle Through NAMPT-Mediated NAD <sup>+</sup> Biosynthesis
Ramsey, K. M., Yoshino, J., Brace, C. S., Abrassart, D., Kobayashi, Y., Marcheva, B., Hong, H.-K., Chong, J. L., Buhr, E. D., Lee, C., et al. (2009) · Science · doi:10.1126/science.1171641 · Cited by 1,126 · see citing works
Milanović, Z., Sporiš, G., & Weston, M. (2015) · Sports Medicine · doi:10.1007/s40279-015-0365-0 · Cited by 923 · see citing works
Nampt/PBEF/Visfatin Regulates Insulin Secretion in β Cells as a Systemic NAD Biosynthetic Enzyme
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. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.09.003 · Cited by 911 · see citing works
Bieganowski, P., & Brenner, C. (2004) · Cell · doi:10.1016/s0092-8674(04)00416-7 · Cited by 750 · see citing works
Borde, R., Hortobágyi, T., & Granacher, U. (2015) · Sports Medicine · doi:10.1007/s40279-015-0385-9 · Cited by 737 · see citing works
Plasma Visfatin Concentrations and Fat Depot–Specific mRNA Expression in Humans
Berndt, J., Klöting, N., Kralisch, S., Kovacs, P. L., Faßhauer, M., Schön, M. R., Stümvoll, M., & Blüher, M. (2005) · Diabetes · doi:10.2337/diabetes.54.10.2911 · Cited by 724 · see citing works
Nicotinamide riboside is uniquely and orally bioavailable in mice and humans
Trammell, S. A. J., Schmidt, M. S., Weidemann, B. J., Redpath, P., Jaksch, F., Dellinger, R. W., Li, Z., Abel, E. D., Migaud, M. E., & Brenner, C. (2016) · Nature Communications · doi:10.1038/ncomms12948 · Cited by 697 · see citing works
Oxidative capacity and ageing in human muscle
Conley, K. E., Jubrias, S. A., & Esselman, P. C. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00203.x · Cited by 651 · see citing works
Martens, C. R., Denman, B. A., Mazzo, M. R., Armstrong, M. L., Reisdorph, N., McQueen, M. B., Chonchol, M., & Seals, D. R. (2018) · Nature Communications · doi:10.1038/s41467-018-03421-7 · Cited by 588 · see citing works
SIRT3, a human SIR2 homologue, is an NAD- dependent deacetylase localized to mitochondria
Onyango, P. O., Celic, I., McCaffery, J. M., Boeke, J. D., & Feinberg, A. P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.222538099 · Cited by 573 · see citing works
Age-Associated Changes In Oxidative Stress and NAD+ Metabolism In Human Tissue
Massudi, H., Grant, R., Braidy, N., Guest, J., Farnsworth, B., & Guillemin, G. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042357 · Cited by 545 · cited 2× · see citing works
“In both humans and rodents, NAD+ concentrations and sirtuin activity reportedly decline with aging in a tissue-specific manner (Braidy et al. 2011; Massudi et al. 2012).”
BackgroundDiet and exercise signals regulate SIRT3 and activate AMPK and PGC-1α in skeletal muscle
Palacios, O. M., Carmona, J. J., Michan, S., Chen, K. Y., Manabe, Y., III, J. L. W., Goodyear, L. J., & Tong, Q. (2009) · Aging · doi:10.18632/aging.100075 · Cited by 487 · see citing works
Jing, E., Emanuelli, B., Hirschey, M. D., Boucher, J., Lee, K. Y., Lombard, D., Verdin, E. M., & Kahn, C. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111308108 · Cited by 469 · see citing works
Visceral fat and insulin resistance — causative or correlative?
Frayn, K. N. (2000) · British Journal Of Nutrition · doi:10.1017/s0007114500000982 · Cited by 445 · see citing works
Jorge, M. L. M. P., de Oliveira, V. N., Resende, N. M., Paraíso, L. F., Calixto, A., Diniz, A. L. D., Resende, E. S., Ropelle, E. R., Carvalheira, J. B. C., Espíndola, F. S., et al. (2011) · Metabolism · doi:10.1016/j.metabol.2011.01.006 · Cited by 399 · see citing works
NRK1 controls nicotinamide mononucleotide and nicotinamide riboside metabolism in mammalian cells
Ratajczak, J., Joffraud, M., Trammell, S. A. J., Ras, R., Canela, N., Boutant, M., Kulkarni, S. S., Rodrigues, M., Redpath, P., Migaud, M. E., et al. (2016) · Nature Communications · doi:10.1038/ncomms13103 · Cited by 378 · cited 1× · see citing works
“1) (Bieganowski and Brenner 2004; Ratajczak et al. 2016).”
Determinants of Muscle and Bone Aging
Curtis, E., Litwic, A., Cooper, C., & Dennison, E. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.25001 · Cited by 375 · see citing works
Cheng, A., Yang, Y., Zhou, Y., Maharana, C., Lu, D., Peng, W., Liu, Y., Wan, R., Marosi, K., Misiak, M., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.10.013 · Cited by 371 · see citing works
Stain-Free technology as a normalization tool in Western blot analysis
Gürtler, A., Kunz, N., Gomolka, M., Hornhardt, S., Friedl, A. A., McDonald, K., Kohn, J. E., & Posch, A. (2012) · Analytical Biochemistry · doi:10.1016/j.ab.2012.10.010 · Cited by 369 · see citing works
Loss of NAD Homeostasis Leads to Progressive and Reversible Degeneration of Skeletal Muscle
Frederick, D. W., Loro, E., Liu, L., Davila, A., Chellappa, K., Silverman, I. M., Quinn, W. J., Gosai, S. J., Tichy, E. D., Davis, J. G., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.07.005 · Cited by 367 · cited 4× · see citing works
“, contractility and oxidative respiration) of skeletal muscle (Frederick et al. 2016; Agerholm et al. 2018), our findings highlight the importance of exercise training as an effective intervention to prevent aging-associated declines in skeletal muscle function.”
BackgroundInfluentialCrystal Structure of a SIR2 Homolog–NAD Complex
Min, J., Landry, J. W., Sternglanz, R., & Xu, R.-M. (2001) · Cell · doi:10.1016/s0092-8674(01)00317-8 · Cited by 326 · see citing works
Role of exercise on sarcopenia in the elderly.
Montero-Fernández, N., & Rexach, J. A. S. (2013) · PubMed · Cited by 306 · see citing works
Skeletal muscle NAMPT is induced by exercise in humans
Costford, S. R., Bajpeyi, S., Pasarica, M., Albarado, D. C., Thomas, S. C., Xie, H., Church, T. S., Jubrias, S. A., Conley, K. E., & Smith, S. R. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00318.2009 · Cited by 297 · see citing works
Scheduled exercise phase shifts the circadian clock in skeletal muscle
WOLFF, G., & ESSER, K. A. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318255cf4c · Cited by 291 · see citing works
Lifelong physical exercise delays age-associated skeletal muscle decline
Zampieri, S., Pietrangelo, L., Loefler, S., Fruhmann, H., Vogelauer, M., Burggraf, S., Pond, A., Grim-Stieger, M., Cvecka, J., Sedliak, M., et al. (2015) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glu006 · Cited by 282 · see citing works
Dollerup, O. L., Christensen, B., Svart, M., Schmidt, M. S., Sulek, K., Ringgaard, S., Stødkilde-Jørgensen, H., Møller, N., Brenner, C., Treebak, J. T., et al. (2018) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy132 · Cited by 282 · see citing works
Self-citationThe sirtuins, oxidative stress and aging: an emerging link
Merksamer, P. I., Liu, Y., He, W., Hirschey, M. D., Chen, D., & Verdin, E. (2013) · Aging · doi:10.18632/aging.100544 · Cited by 275 · see citing works
Ryu, D., Zhang, H., Ropelle, E. R., Sorrentino, V., Mázala, D. A. G., Mouchiroud, L., Marshall, P. L., Campbell, M. D., Ali, A. S., Knowels, G. M., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf5504 · Cited by 256 · see citing works
Time- and exercise-dependent gene regulation in human skeletal muscle
Zambon, A. C., McDearmon, E. L., Salomonis, N., Vranizan, K. M., Johansen, K. L., Adey, D., Takahashi, J. S., Schambelan, M., & Conklin, B. R. (2003) · Genome Biology · doi:10.1186/gb-2003-4-10-r61 · Cited by 254 · see citing works
Xu, X. J., Gauthier, M., Hess, D. T., Apovian, C. M., Cacicedo, J. M., Gokce, N., Farb, M. G., Valentine, R. J., & Ruderman, N. B. (2012) · Journal of Lipid Research · doi:10.1194/jlr.p022905 · Cited by 229 · see citing works
The brain, sirtuins, and ageing
Satoh, A., Imai, S., & Guarente, L. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.42 · Cited by 198 · see citing works
Bischof, G. N., & Park, D. C. (2015) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000212 · Cited by 182 · see citing works
Dellinger, R. W., Santos, S. R., Morris, M., Evans, M., Alminana, D., Guarente, L., & Marcotulli, E. (2017) · npj Aging and Mechanisms of Disease · doi:10.1038/s41514-017-0016-9 · Cited by 181 · see citing works
Physical Exercise as Therapy for Frailty
Aguirre, L. E., & Villareal, D. T. (2015) · Nestlé Nutrition Institute Workshop series · doi:10.1159/000382065 · Cited by 174 · see citing works
Vassilopoulos, A., Pennington, J. D., Andresson, T., Rees, D. M., Bosley, A. D., Fearnley, I. M., Ham, A., Flynn, C. R., Hill, S., Rose, K. L., et al. (2014) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5420 · Cited by 173 · see citing works
Maximal oxygen uptake and muscle fiber types in trained and untrained humans.
Bergh, U., Thorstensson, A., Sjödin, B., Hultén, B., Piehl, K., & Karlsson, J. (1978) · PubMed · Cited by 152 · see citing works
Larsen, S., Danielsen, J., Søndergård, S. D., Søgaard, D., Vigelsø, A., Dybboe, R., Skaaby, S., Dela, F., & Helge, J. W. (2014) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.12252 · Cited by 124 · see citing works
Self-citationVisfatin is released from 3T3-L1 adipocytes via a non-classical pathway
Tanaka, M., 野崎, 真., Fukuhara, A., Segawa, K., Aoki, N., Matsuda, M., Komuro, R., & Shimomura, I. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.05.096 · Cited by 123 · see citing works
Brandauer, J., Vienberg, S. G., Agerholm, M., Ringholm, S., Risis, S., Larsen, P. S., Kristensen, J. M., Frøsig, C., Leick, L., Fentz, J., et al. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.259515 · Cited by 105 · see citing works
Self-citationChang, Y., Chang, T., Lee, W., & Chuang, L. (2009) · Metabolism · doi:10.1016/j.metabol.2009.07.011 · Cited by 98 · see citing works
High-intensity interval training improves insulin sensitivity in older individuals.
Søgaard, D., Lund, M. T., Scheuer, C. M., Dehlbæk, M. S., Dideriksen, S. G., Abildskov, C. V., Christensen, K. K., Dohlmann, T. L., Larsen, S., Vigelsø, A. H., et al. (2018) · Acta Physiologica · doi:10.1111/apha.13009 · Cited by 98 · see citing works
Self-citationRelationship between regional fat distribution and insulin resistance
Bonora, E. (2000) · International Journal of Obesity · doi:10.1038/sj.ijo.0801274 · Cited by 97 · see citing works
Sirtuins and the circadian clock: Bridging chromatin and metabolism
Masri, S., & Sassone‐Corsi, P. (2014) · Science Signaling · doi:10.1126/scisignal.2005685 · Cited by 88 · see citing works
Effects of aging, exercise, and disease on force transfer in skeletal muscle
Hughes, D. C., Wallace, M. A., & Baar, K. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00095.2015 · Cited by 86 · see citing works
Johnson, M. L., Irving, B. A., Lanza, I. R., Vendelbo, M. H., Konopka, A. R., Robinson, M. M., Henderson, G. C., Klaus, K. A., Morse, D. M., Heppelmann, C. J. H., et al. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu221 · Cited by 84 · see citing works
Retnakaran, R. R., Youn, B., Liu, Y., Hanley, A. J., Lee, N. S., Park, J. W., Song, E. S., Vu, V. P., Kim, W. I., Tungtrongchitr, R., et al. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03264.x · Cited by 83 · see citing works
Calcium mobilizing second messengers derived from NAD
Guse, A. H. (2015) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2014.12.015 · Cited by 82 · see citing works
Nielsen, K. N., Peics, J., Ma, T., Karavaeva, I. E., Dall, M., Chubanava, S., Basse, A. L., Dmytriyeva, O., Treebak, J. T., & Gerhart‐Hines, Z. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.02.014 · Cited by 81 · see citing works
Self-citationVisfatin mRNA expression in human subcutaneous adipose tissue is regulated by exercise
Frydelund‐Larsen, L., Akerstrom, T. C. A., Nielsen, S. J., Keller, P., Keller, C., & Pedersen, B. K. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00113.2006 · Cited by 80 · see citing works
Yasumoto, Y., Nakao, R., & Oishi, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116476 · Cited by 77 · see citing works
NMNAT: It’s an NAD+ synthase… It’s a chaperone… It’s a neuroprotector
Brazill, J. M., Li, C. V., Zhu, Y., & Zhai, R. G. (2017) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2017.03.014 · Cited by 73 · see citing works
Boone, J., Barstow, T. J., Celie, B., Prieur, F., & Bourgois, J. (2016) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2015-0261 · Cited by 70 · see citing works
Metabolic and molecular insights into an essential role of nicotinamide phosphoribosyltransferase
Zhang, L. Q., van Haandel, L., Xiong, M., Huang, P., Heruth, D. P., Bi, C., Gaedigk, R., Jiang, X., Li, D.-Y., Wyckoff, G. J., et al. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.132 · Cited by 69 · see citing works
Adyshev, D., Elangovan, V., Moldobaeva, N., Mapes, B. L., Sun, X.-G., & Garcia, J. G. N. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2013-0292oc · Cited by 61 · see citing works
Sun, X., Elangovan, V. R., Mapes, B. L., et al. (2014) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2014-0117oc · Cited by 56 · see citing works
Bürkle, A. (2006) · Free Radical Research · doi:10.1080/10715760600915288 · Cited by 55 · see citing works
Seo, D.-I., So, W.-Y., Ha, S., Yoo, E.-J., Kim, D., Singh, H., Fahs, C. A., Rossow, L. M., Bemben, D. A., Bemben, M. G., et al. (2011) · Europe PMC (PubMed Central) · Cited by 50 · see citing works
Hsieh, C.-J., Wang, P.-W., & Chen, T.-Y. (2014) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-6-49 · Cited by 48 · see citing works
Windisch, S., Seiberl, W., Schwirtz, A., & Hahn, D. (2017) · Scientific Reports · doi:10.1038/srep44590 · Cited by 46 · see citing works
Agerholm, M., Dall, M., Jensen, B. A. H., Prats, C., Madsen, S., Basse, A. L., Graae, A.-S., Risis, S., Goldenbaum, J., Quistorff, B., et al. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00213.2017 · Cited by 43 · see citing works
Self-citationImpairments in Site-Specific AS160 Phosphorylation and Effects of Exercise Training
Consitt, L. A., Meter, J. V., Newton, C. A., Collier, D. N., Dar, M. S., Wojtaszewski, J. F. P., Treebak, J. T., Tanner, C. J., & Houmard, J. A. (2013) · Diabetes · doi:10.2337/db13-0229 · Cited by 41 · see citing works
Self-citationBunprajun, T., Henriksen, T. I., Scheele, C. C., Pedersen, B. K., & Green, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066628 · Cited by 37 · see citing works
Mancini, A., Vitucci, D., Labruna, G., Imperlini, E., Randers, M. B., Schmidt, J. F., Hagman, M., Andersen, T. R., Russo, R., Orrù, S., et al. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3562-8 · Cited by 27 · see citing works
The Effects of Fitness on the Aging Process
Vopat, B. G., Klinge, S. A., McClure, P. K., & Fadale, P. D. (2014) · Journal of the American Academy of Orthopaedic Surgeons · doi:10.5435/jaaos-22-09-576 · Cited by 26 · see citing works
Elangovan, V. R., Camp, S. M., Kelly, G. T., et al. (2016) · Pulmonary Circulation · doi:10.1086/688761 · Cited by 26 · see citing works
Alfieri, A., Martone, D., Randers, M. B., Labruna, G., Mancini, A., Nielsen, J., Bangsbo, J., Krustrup, P., & Buono, P. (2014) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2014.11.003 · Cited by 23 · see citing works
An Old Problem: Aging and Skeletal-Muscle-Strain Injury
Baker, B. A. (2017) · Journal of Sport Rehabilitation · doi:10.1123/jsr.2016-0075 · Cited by 22 · see citing works
Anwar, S., & Noohu, M. M. (2016) · PubMed · Cited by 16 · see citing works
Owczarek, A. J., Olszanecka‐Glinianowicz, M., Kocełak, P., Bożentowicz‐Wikarek, M., Brzozowska, A., Mossakowska, M., Puzianowska‐Kuźnicka, M., Grodzicki, T. K., Więcek, A., & Chudek, J. T. (2016) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365513.2016.1230884 · Cited by 14 · see citing works
Mehdizadeh, A., Hamzezadeh, S., & Tofighi, A. (2016) · Journal of Diabetes & Metabolism · doi:10.4172/2155-6156.1000703 · Cited by 13 · see citing works
Kocełak, P., Olszanecka‐Glinianowicz, M., Owczarek, A. J., Krupa, W., Obirek, P., Bożentowicz‐Wikarek, M., Brzozowska, A., Mossakowska, M., Zdrojewski, T. R., Skalska, A., et al. (2015) · Polskie Archiwum Medycyny Wewnętrznej · doi:10.20452/pamw.2878 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
NAD+ metabolism and its roles in cellular processes during ageing
Covarrubias, A. J., Perrone, R., Grozio, A., & Verdin, E. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00313-x · Cited by 1,617 · see citing works
Egan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278 · see citing works
Remie, C. M., Roumans, K. H., Moonen, M. P., Connell, N. J., Havekes, B., Mevenkamp, J., Lindeboom, L., de Wit, V. H., van de Weijer, T., Aarts, S. A., et al. (2020) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa072 · Cited by 160 · see citing works
Dollerup, O. L., Chubanava, S., Agerholm, M., Søndergård, S. D., Altıntaş, A., Møller, A. B., Høyer, K. F., Ringgaard, S., Stødkilde‐Jørgensen, H., Lavery, G. G., et al. (2020) · The Journal of Physiology · doi:10.1113/jp278752 · Cited by 145 · see citing works
Self-citationHealthy aging and muscle function are positively associated with NAD+ abundance in humans
Janssens, G. E., Grevendonk, L., Perez, R. Z., Schomakers, B. V., de Vogel-van den Bosch, J., Geurts, J. M. W., van Weeghel, M., Schrauwen, P., Houtkooper, R. H., & Hoeks, J. (2022) · Nature Aging · doi:10.1038/s43587-022-00174-3 · Cited by 103 · see citing works
Fan, L., Cacicedo, J. M., & Ido, Y. (2020) · Journal of Diabetes Investigation · doi:10.1111/jdi.13303 · Cited by 86 · see citing works
Lamb, D. A., Moore, J. H., Mesquita, P. H. C., Smith, M. A., Vann, C. G., Osburn, S. C., Fox, C. D., Lopez, H. L., Ziegenfuss, T. N., Huggins, K. W., et al. (2020) · Aging · doi:10.18632/aging.103218 · Cited by 62 · see citing works
Manickam, R., Tur, J., Badole, S. L., Chapalamadugu, K. C., Sinha, P., Wang, Z., Russ, D. W., Brotto, M., & Tipparaju, S. M. (2022) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12887 · Cited by 50 · see citing works
Jensen, J. B., Dollerup, O. L., Møller, A. B., Billeskov, T. B., Dalbram, E., Chubanava, S., Damgaard, M. V., Dellinger, R. W., Trošt, K., Moritz, T., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.158314 · Cited by 39 · see citing works
Self-citationConnell, N., Grevendonk, L., Fealy, C., Moonen-Kornips, E., Bruls, Y., Schrauwen-Hinderling, V., de Vogel, J., Hageman, R., Geurts, J., Zapata-Perez, R., et al. (2021) · The Journal of Nutrition · doi:10.1093/jn/nxab193 · Cited by 33 · see citing works
Targeting Intramyocellular Lipids to Improve Aging Muscle Function
Russ, D. W., Manickam, R., & Tipparaju, S. M. (2025) · Lipids in Health and Disease · doi:10.1186/s12944-025-02622-6 · Cited by 15 · see citing works
- Authors
- de Guia, R. M., Agerholm, M., Nielsen, T. S., Consitt, L. A., Søgaard, D., Helge, J. W., Larsen, S., Brandauer, J., Houmard, J. A., & Treebak, J. T.
- Affiliations
- Novo Nordisk Foundation Center for Basic Metabolic Research Faculty of Health and Medical Sciences University of Copenhagen Copenhagen Denmark
- University of Copenhagen (DK)
- Ohio University (US)
- Gettysburg College (US)
- East Carolina University (US)
- Corresponding author
- Treebak, Jonas T.
- ORCID
- Venue
- Physiological Reports
- Publisher
- Wiley
- Published
- 2019-06
- Volume
- 7
- Issue
- 12
- Pages
- e14139-e14139
- ISSN
- 2051-817X (ISSN-L)
- PMC
- PMC6577427
- OpenAlex
- W2950596378
- Cited by
- 99
- References
- 83
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 13 · 2023: 16 · 2022: 16 · 2021: 11 · 2020: 15 · 2019: 2
- FWCI
- 5.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Physiological Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
- The Scholarship East Carolina University's Institutional Repository (East Carolina University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (AG‐025205, DK‐56112)
- Det Frie Forskningsråd (DFF 4004‐00235, DFF 6110‐00132)
- Novo Nordisk Fonden (NNF14OC0009315)
- Topics
- Health Sciences › Medicine › Geriatrics and Gerontology › Sirtuins and Resveratrol in Medicine
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- NAD+ salvage pathway, visfatin, aerobic exercise training, resistance training, aging, skeletal muscle, nicotinamide mononucleotide adenylyltransferase, high-intensity interval training, peak oxygen uptake, subcutaneous adipose tissue, age-related muscle loss
- MeSH terms
- Adipose Tissue, Adolescent, Adult, Aged, Aged, 80 and over, Aging, Anthropometry, Blood Glucose, Exercise Therapy, Female, Humans, Insulin, Male, Middle Aged, NAD, Nicotinamide-Nucleotide Adenylyltransferase, Cytokines, Phosphotransferases (Alcohol Group Acceptor), Muscle, Skeletal, Intracellular Signaling Peptides and Proteins, Nicotinamide Phosphoribosyltransferase, Resistance Training, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review