Nicotinamide riboside, a form of Vitamin B3, protects against excitotoxicity-induced axonal degeneration

FASEB Journal

Volumn 31, Issue 12, 2017, Pages 5440-5452

  Vaur, Pauline ^a   Brugg, Bernard ^a   Mericskay, Mathias ^a,c   Li, Zhenlin ^b   Schmidt, Mark S ^d   Vivien, Denis ^e   Orset, Cyrille ^e   Jacotot, Etienne ^a   Brenner, Charles ^d   Duplus, Eric ^a  

^a Université Pierre et Marie Curie   (France)

^b Equipe de Recherche Labellisée ERL U1164   (France)

^c Universite Paris Sud   (France)

^d UNIVERSITY OF IOWA   (United States)

^e CAEN UNIVERSITY HOSPITAL   (France)

Author keywords

Cortical neurons; FK866; NAD+; NMDA; NR

Indexed keywords

MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE RIBOSIDE; N METHYLASPARTIC ACID; NEUROPROTECTIVE AGENT; NICOTINAMIDE; NICOTINAMIDE-BETA-RIBOSIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DAMAGE; CELL STRESS; CONTROLLED STUDY; EFFECTIVE CONCENTRATION; EMBRYO; EXCITOTOXICITY; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MALE; MOUSE; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; AXON; C57BL MOUSE; CELL CULTURE; CELL DEATH; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; AXONS; CELL DEATH; CELLS, CULTURED; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; NIACINAMIDE; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 85036511526     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201700221RR     Document Type: Article

References (56)

1. Benarroch, E. E. (2015) Acquired axonal degeneration and regeneration: recent insights and clinical correlations. Neurology 84, 2076–2085
2. Burke, R. E., and O’Malley, K. (2013) Axon degeneration in Parkinson’s disease. Exp. Neurol. 246, 72–83
3. Kanaan, N. M., Pigino, G. F., Brady, S. T., Lazarov, O., Binder, L. I., and Morfini, G. A. (2013) Axonal degeneration in Alzheimer’s disease: when signaling abnormalities meet the axonal transport system. Exp. Neurol. 246, 44–53
4. Selkoe, D. J. (2002) Alzheimer’s disease is a synaptic failure. Science 298, 789–791
5. Araki, T., Sasaki, Y., and Milbrandt, J. (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305, 1010–1013
6. Magnifico, S., Saias, L., Deleglise, B., Duplus, E., Kilinc, D., Miquel, M. C., Viovy, J. L., Brugg, B., and Peyrin, J. M. (2013) NAD+ acts on mitochondrial SirT3 to prevent axonal caspase activation and axonal degeneration. FASEB J. 27, 4712–4722
7. Sasaki, Y., Araki, T., and Milbrandt, J. (2006) Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J. Neurosci. 26, 8484–8491
8. Wang, J., Zhai, Q., Chen, Y., Lin, E., Gu, W., McBurney, M. W., and He, Z. (2005) A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 170, 349–355
9. Lyon, M. F., Ogunkolade, B. W., Brown, M. C., Atherton, D. J., and Perry, V. H. (1993) A gene affecting Wallerian nerve degeneration maps distally on mouse chromosome 4. Proc. Natl. Acad. Sci. USA 90, 9717–9720
10. Coleman, M. P., and Freeman, M. R. (2010) Wallerian degeneration, wld(s), and nmnat. Annu. Rev. Neurosci. 33, 245–267
11. Yahata, N., Yuasa, S., and Araki, T. (2009) Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J. Neurosci. 29, 6276–6284
12. Trammell, S. A., Weidemann, B. J., Chadda, A., Yorek, M. S., Holmes, A., Coppey, L. J., Obrosov, A., Kardon, R. H., Yorek, M. A., and Brenner, C. (2016) Nicotinamide riboside opposes type 2 diabetes and neuropathy in mice. Sci. Rep. 6, 26933
13. Osterloh, J. M., Yang, J., Rooney, T. M., Fox, A. N., Adalbert, R., Powell, E. H., Sheehan, A. E., Avery, M. A., Hackett, R., Logan, M. A., MacDonald, J. M., Ziegenfuss, J. S., Milde, S., Hou, Y. J., Nathan, C., Ding, A., Brown, R. H., Jr., Conforti, L., Coleman, M., Tessier-Lavigne, M., Züchner, S., and Freeman, M. R. (2012) dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337, 481–484
14. Gerdts, J., Summers, D. W., Milbrandt, J., and DiAntonio, A. (2016) Axon self-destruction: new links among SARM1, MAPKs, and NAD+ metabolism. Neuron 89, 449–460
15. Gilley, J., and Coleman, M. P. (2010) Endogenous Nmnat2 is an essentialsurvivalfactorformaintenanceofhealthyaxons.PLoSBiol.8, e1000300
16. Sasaki, Y., Nakagawa, T., Mao, X., DiAntonio, A., and Milbrandt, J. (2016) NMNAT1 inhibits axon degeneration via blockade of SARM1-mediated NAD(+) depletion. eLife 5, e19749
17. Kim, S. H. Lu, H. F., and Alano, C. C. (2011) Neuronal Sirt3 protects against excitotoxic injury in mouse cortical neuron culture. PLoS ONE 6, e14731
18. Liu, D., Pitta, M., and Mattson, M. P. (2008) Preventing NAD(+) depletion protects neurons against excitotoxicity: bioenergetic effects of mild mitochondrial uncoupling and caloric restriction. Ann. N. Y. Acad. Sci. 1147, 275–282
19. Liu, D., Gharavi, R., Pitta, M., Gleichmann, M., and Mattson, M. P. (2009) Nicotinamide prevents NAD+ depletion and protects neurons against excitotoxicity and cerebral ischemia: NAD+ consumption by SIRT1 may endanger energetically compromised neurons. Neuromolecular Med. 11, 28–42
20. Zhang, W., Xie, Y., Wang, T., Bi, J., Li, H., Zhang, L. Q., Ye, S. Q., and Ding, S. (2010) Neuronal protective role of PBEF in a mouse model of cerebral ischemia. J. Cereb. Blood Flow Metab. 30, 1962–1971
21. Chung, R. S., McCormack, G. H., King, A. E., West, A. K., and Vickers, J. C. (2005) Glutamate induces rapid loss of axonal neurofilament proteins from cortical neurons in vitro. Exp Neurol 193, 481–488
22. Hosie, K. A., King, A. E., Blizzard, C. A., Vickers, J. C., and Dickson, T. C. (2012) Chronic excitotoxin-induced axon degeneration in a compartmented neuronal culture model. ASN Neuro 4
23. Bi, J., Li, H., Ye, S. Q., and Ding, S. (2012) Pre-B-cell colony-enhancing factor exerts a neuronal protection through its enzymatic activity and the reduction of mitochondrial dysfunction in in vitro ischemic models. J. Neurochem. 120, 334–346
24. Bogan, K. L., and Brenner, C. (2008) Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu. Rev. Nutr. 28, 115–130
25. Nikiforov, A., Dölle, C., Niere, M., and Ziegler, M. (2011) Pathways and subcellular compartmentation of NAD biosynthesis in human cells: from entry of extracellular precursors to mitochondrial NAD generation. J. Biol. Chem. 286, 21767–21778
26. Grozio, A., Sociali, G., Sturla, L., Caffa, I., Soncini, D., Salis, A., Raffaelli,N.,DeFlora,A.,Nencioni,A.,andBruzzone,S.(2013)CD73 protein as a source of extracellular precursors for sustained NAD+ biosynthesis in FK866-treated tumor cells. J. Biol. Chem. 288, 25938–25949
27. Di Stefano, M., Nascimento-Ferreira, I., Orsomando, G., Mori, V., Gilley, J., Brown, R., Janeckova, L., Vargas, M. E., Worrell, L. A., Loreto, A., Tickle, J., Patrick, J., Webster, J. R. M., Marangoni, M., Carpi, F. M., Pucciarelli, S., Rossi, F., Meng, W., Sagasti, A., Ribchester, R. R., Magni, G., Coleman, M. P., and Conforti, L. (2015) A rise in NAD precursor nicotinamide mononucleotide (NMN) after injury promotes axon degeneration. Cell Death Differ. 22, 731–742
28. Ratajczak, J., Joffraud, M., Trammell, S. A., Ras, R., Canela, N., Boutant, M., Kulkarni, S. S., Rodrigues, M., Redpath, P., Migaud, M. E., Auwerx, J., Yanes, O., Brenner, C., and Cantó, C. (2016) NRK1 controls nicotinamide mononucleotide and nicotinamide riboside metabolism in mammalian cells. Nat. Commun. 7, 13103
29. Zimmermann, H. (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch. Pharmacol. 362, 299–309
30. Fletcher, R. S., Ratajczak, J., Doig, C. L., Oakey, L. A., Callingham, R., Da Silva Xavier, G., Garten, A., Elhassan, Y. S., Redpath, P., Migaud, M. E., Philp, A., Brenner, C., Cantó, C., and Lavery, G. G. (2017) Nicotinamide riboside kinases display redundancy in mediating nicotinamide mononucleotide and nicotinamide riboside metabolism in skeletal muscle cells. Mol. Metab. 6, 819–832
31. Bieganowski, P., and Brenner, C. (2004) 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, 495–502
32. Trammell, S. A., Yu, L., Redpath, P., Migaud, M. E., and Brenner, C. (2016) Nicotinamide riboside is a major NAD+ precursor vitamin in cow milk. J. Nutr. 146, 957–963
33. Trammell, S. A., Schmidt, M. S., Weidemann, B. J., Redpath, P., Jaksch, F., Dellinger, R. W., Li, Z., Abel, E. D., Migaud, M. E., and Brenner, C. (2016) Nicotinamide riboside is uniquely and orally bioavailable in mice and humans. Nat. Commun. 7, 12948
34. Gong, B., Pan, Y., Vempati, P., Zhao, W., Knable, L., Ho, L., Wang, J., Sastre, M., Ono, K., Sauve, A. A., and Pasinetti, G. M. (2013) Nicotinamide riboside restores cognition through an upregulation of proliferator-activated receptor-g coactivator 1a regulated b-secretase 1 degradation and mitochondrial gene expression in Alzheimer’s mouse models. Neurobiol. Aging 34, 1581–1588
35. + precursor nicotinamide riboside protects from noise-induced hearing loss. Cell Metab. 20, 1059–1068
36. Hamity, M. V., White, S. R., Walder, R. Y., Schmidt, M. S., Brenner, C., and Hammond, D. L. (2017) Nicotinamide riboside, a form of vitamin B3 and NAD+ precursor, relieves the nociceptive and aversive dimensions of paclitaxel-induced peripheral neuropathy in female rats. Pain 158, 962–972
37. Deleglise, B., Lassus, B., Soubeyre, V., Alleaume-Butaux, A., Hjorth, J. J., Vignes, M., Schneider, B., Brugg, B., Viovy, J. L., and Peyrin, J. M. (2013) Synapto-protective drugs evaluation in reconstructed neuronal network. PLoS One 8, e71103
38. Trammell, S. A., and Brenner, C. (2013) Targeted, LCMS-based metabolomics for quantitative measurement of NAD(+) metabolites. Comput. Struct. Biotechnol. J. 4, e201301012
39. Paxinos G., and Franklin K. (2012) Paxinos and Franklin’s the Mouse Brain in Stereotaxic Coordinates. 4th ed. Academic Press, Cambridge, MA, USA
40. Jullienne, A., Montagne, A., Orset, C., Lesept, F., Jane, D. E., Monaghan, D. T., Maubert, E., Vivien, D., and Ali, C. (2011) Selective inhibition of GluN2D-containing N-methyl-D-aspartate receptors prevents tissue plasminogen activator-promoted neurotoxicity both in vitro and in vivo. Mol. Neurodegener. 6, 68
41. Cohen, M. S., Ghosh, A. K., Kim, H. J., Jeon, N. L., and Jaffrey, S. R. (2012) Chemical genetic-mediated spatial regulation of protein expression in neurons reveals an axonal function for wld(s). Chem. Biol. 19, 179–187
42. Antenor-Dorsey, J. A. V., and O’Malley, K. L. (2012) WldS but not Nmnat1 protects dopaminergic neurites from MPP+ neurotoxicity. Mol. Neurodegener. 7, 5
43. Griffith, D. A., and Jarvis, S. M. (1996) Nucleoside and nucleobase transport systems of mammalian cells. Biochim. Biophys. Acta 1286, 153–181
44. 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., Gademann, K., Rinsch, C., Schoonjans, K., Sauve, A. A., and Auwerx, J. (2012) The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab. 15, 838–847
45. Belenky, P., Racette, F. G., Bogan, K. L., McClure, J. M., Smith, J. S., and Brenner, C. (2007) Nicotinamide riboside promotes Sir2 silencing and extends lifespan via Nrk and Urh1/Pnp1/Meu1 pathways to NAD+. Cell 129, 473–484
46. Hasmann, M., and Schemainda, I. (2003) FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res. 63, 7436–7442
47. Martire, S., Mosca, L., and d’Erme, M. (2015) PARP-1 involvement in neurodegeneration: a focus on Alzheimer’s and Parkinson’s diseases. Mech. Ageing Dev. 146–148, 53–64
48. Ghosh, D., LeVault, K. R., Barnett, A. J., and Brewer, G. J. (2012) A reversible early oxidized redox state that precedes macromolecular ROS damage in aging nontransgenic and 3xTg-AD mouse neurons. J. Neurosci. 32, 5821–5832
49. Verghese, P. B., Sasaki, Y., Yang, D., Stewart, F., Sabar, F., Finn, M. B., Wroge,C.M.,Mennerick,S.,Neil,J.J.,Milbrandt,J.,andHoltzman,D.M. (2011) Nicotinamide mononucleotide adenylyl transferase 1 protects against acute neurodegeneration in developing CNS by inhibiting excitotoxic-necroticcelldeath.Proc.Natl.Acad.Sci.USA108,19054–19059
50. Wang, X., Li, H., and Ding, S. (2014) The effects of NAD+ on apoptotic neuronal death and mitochondrial biogenesis and function after glutamate excitotoxicity. Int. J. Mol. Sci. 15, 20449–20468
51. Choi, D. W. (1987) Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7, 369–379
52. Milde, S., Gilley, J., and Coleman, M. P. (2013) Subcellular localization determines the stability and axon protective capacity of axon survival factor Nmnat2. PLoS Biol. 11, e1001539
53. Zhou, B., Yu, P., Lin, M. Y., Sun, T., Chen, Y., and Sheng, Z. H. (2016) Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits. J. Cell Biol. 214, 103–119
54. Gerdts, J., Summers, D. W., Sasaki, Y., DiAntonio, A., and Milbrandt, J. (2013) Sarm1-mediated axon degeneration requires both SAM and TIR interactions. J. Neurosci. 33, 13569–13580
55. + destruction. Science 348, 453–457
56. Young, J. D. (2016) The SLC28 (CNT) and SLC29 (ENT) nucleoside transporter families: a 30-year collaborative odyssey. Biochem. Soc. Trans. 44, 869–876