Nicotinamide mononucleotide adenylyltransferase promotes hypoxic survival by activating the mitochondrial unfolded protein response

Cell Death and Disease

Volumn 7, Issue 2, 2016, Pages

  Mao, X R ^a   Kaufman, D M ^a,b   Crowder, C M ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; NMNAT1 PROTEIN, MOUSE; OXYGEN; PACLITAXEL;

ANIMAL; AXON; CAENORHABDITIS ELEGANS; CELL CULTURE; CELL HYPOXIA; CYTOLOGY; DRUG EFFECTS; GENE VECTOR; GENETICS; HIPPOCAMPUS; LONGEVITY; METABOLISM; MITOCHONDRION; MOUSE; PHENOTYPE; REPORTER GENE; TRANSGENIC ANIMAL; UNFOLDED PROTEIN RESPONSE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CAENORHABDITIS ELEGANS; CELL HYPOXIA; CELLS, CULTURED; GENES, REPORTER; GENETIC VECTORS; HIPPOCAMPUS; LONGEVITY; MICE; MITOCHONDRIA; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; OXYGEN; PACLITAXEL; PHENOTYPE; UNFOLDED PROTEIN RESPONSE;

EID: 84986250448     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.5     Document Type: Article

References (53)

1. Lunn ER, Perry VH, Brown MC, Rosen H, Gordon S. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur J Neurosci 1989; 1: 27-33.
2. Coleman MP, Conforti L, Buckmaster EA, Tarlton A, Ewing RM, Brown MC et al. An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse. Proc Natl Acad Sci USA 1998; 95: 9985-9990.
3. Conforti L, Tarlton A, Mack TG, Mi W, Buckmaster EA, Wagner D et al. A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc Natl Acad Sci USA 2000; 97: 11377-11382.
4. Mack TG, Reiner M, Beirowski B, Mi W, Emanuelli M, Wagner D et al. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat Neurosci 2001; 4: 1199-1206.
5. Araki T, Sasaki Y, Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 2004; 305: 1010-1013.
6. Avery MA, Sheehan AE, Kerr KS, Wang J, Freeman MR. Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J Cell Biol 2009; 184: 501-513.
7. Court FA, Coleman MP. Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci 2012; 35: 364-372.
8. Yahata N, Yuasa S, Araki T. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J Neurosci 2009; 29: 6276-6284.
9. Verghese PB, Sasaki Y, Yang D, Stewart F, Sabar F, Finn MB et al. Nicotinamide mononucleotide adenylyl transferase 1 protects against acute neurodegeneration in developing CNS by inhibiting excitotoxic-necrotic cell death. Proc Natl Acad Sci USA 2011; 108: 19054-19059.
10. Chen L, Chisholm AD. Axon regeneration mechanisms: insights from C. elegans. Trends Cell Biol 2011; 21: 577-584.
11. Butler JA, Mishur RJ, Bokov AF, Hakala KW, Weintraub ST, Rea SL. Profiling the anaerobic response of C. elegans using GC-MS. PLoS One 2012; 7: e46140.
12. Fawcett EM, Horsman JW, Miller DL. Creating defined gaseous environments to study the effects of hypoxia on C. elegans. J Vis Exp 2012; 65: e4088.
13. LaRue BL, Padilla PA. Environmental and genetic preconditioning for long-term anoxia responses requires AMPK in Caenorhabditis elegans. PLoS One 2011; 6: e16790.
14. Menuz V, Howell KS, Gentina S, Epstein S, Riezman I, Fornallaz-Mulhauser M et al. Protection of C. elegans from anoxia by HYL-2 ceramide synthase. Science 2009; 324: 381-384.
15. Powell-Coffman JA. Hypoxia signaling and resistance in C. elegans. Trends Endocrinol Metab 2010; 21: 435-440.
16. Scott B, Sun CL, Mao X, Yu C, Vohra BP, Milbrandt J et al. Role of oxygen consumption in hypoxia protection by translation factor depletion. J Exp Biol 2013; 216: 2283-2292.
17. Anderson LL, Mao X, Scott BA, Crowder CM. Survival from hypoxia in C. elegans by inactivation of aminoacyl-tRNA synthetases. Science 2009; 323: 630-633.
18. Mabon ME, Mao X, Jiao Y, Scott BA, Crowder CM. Systematic identification of gene activities promoting hypoxic death. Genetics 2009; 181: 483-496.
19. Mao XR, Crowder CM. Protein misfolding induces hypoxic preconditioning via a subset of the unfolded protein response machinery. Mol Cell Biol 2010; 30: 5033-5042.
20. Mabon ME, Scott BA, Crowder CM. Divergent mechanisms controlling hypoxic sensitivity and lifespan by the DAF-2/Insulin/IGF-receptor pathway. PLoS One 2009; 4: e7937.
21. Scott BA, Avidan MS, Crowder CM. Regulation of hypoxic death in C. elegans by the insulin/ IGF receptor homolog DAF-2. Science 2002; 296: 2388-2391.
22. Badiola N, Penas C, Minano-Molina A, Barneda-Zahonero B, Fado R, Sanchez-Opazo G et al. Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12. Cell Death Dis 2011; 2: e149.
23. Kim I, Xu W, Reed JC. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008; 7: 1013-1030.
24. Sasaki Y, Vohra BP, Lund FE, Milbrandt J. Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J Neurosci 2009; 29: 5525-5535.
25. Calixto A, Jara JS, Court FA. Diapause formation and downregulation of insulin-like signaling via DAF-16/FOXO delays axonal degeneration and neuronal loss. PLoS Genet 2012; 8: e1003141.
26. Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol Cell 2010; 37: 529-540.
27. Haynes CM, Petrova K, Benedetti C, Yang Y, Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev Cell 2007; 13: 467-480.
28. Nargund AM, Fiorese CJ, Pellegrino MW, Deng P, Haynes CM. Mitochondrial and nuclear accumulation of the transcription factor ATFS-1 promotes OXPHOS recovery during the UPR (mt). Mol Cell 2015; 58: 123-133.
29. Nargund AM, Pellegrino MW, Fiorese CJ, Baker BM, Haynes CM. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 2012; 337: 587-590.
30. Yoneda T, Benedetti C, Urano F, Clark SG, Harding HP, Ron D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J Cell Sci 2004; 117: 4055-4066.
31. Hammarlund M, Jorgensen EM, Bastiani MJ. Axons break in animals lacking beta-spectrin. J Cell Biol 2007; 176: 269-275.
32. Bhattacharya MR, Gerdts J, Naylor SA, Royse EX, Ebstein SY, Sasaki Y et al. A model of toxic neuropathy in Drosophila reveals a role for MORN4 in promoting axonal degeneration. J Neurosci 2012; 32: 5054-5061.
33. Sahenk Z, Barohn R, New P, Mendell JR. Taxol neuropathy. Electrodiagnostic and sural nerve biopsy findings. Arch Neurol 1994; 51: 726-729.
34. Bennett GJ, Liu GK, Xiao WH, Jin HW, Siau C. Terminal arbor degeneration - a novel lesion produced by the antineoplastic agent paclitaxel. Eur J Neurosci 2011; 33: 1667-1676.
35. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002; 415: 92-96.
36. Ali YO, McCormack R, Darr A, Zhai RG. Nicotinamide mononucleotide adenylyltransferase is a stress response protein regulated by the heat shock factor/hypoxia-inducible factor 1 (alpha) pathway. J Biol Chem 2011; 286: 19089-19099.
37. Coleman MP, Freeman MR. Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 2010; 33: 245-267.
38. Vohra BP, Sasaki Y, Miller BR, Chang J, DiAntonio A, Milbrandt J. Amyloid precursor protein cleavage-dependent and -independent axonal degeneration programs share a common nicotinamide mononucleotide adenylyltransferase 1-sensitive pathway. J Neurosci 2010; 30: 13729-13738.
39. Wang JT, Medress ZA, Barres BA. Axon degeneration: molecular mechanisms of a selfdestruction pathway. J Cell Biol 2012; 196: 7-18.
40. Hill S, Van Remmen H. Mitochondrial stress signaling in longevity: a new role for mitochondrial function in aging. Redox Biol 2014; 2: 936-944.
41. Sasaki Y, Araki T, Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J Neurosci 2006; 26: 8484-8491.
42. Avery MA, Rooney TM, Pandya JD, Wishart TM, Gillingwater TH, Geddes JW et al. Wld(S) prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca(2+) buffering. Curr Biol 2012; 22: 596-600.
43. Fang Y, Soares L, Teng X, Geary M, Bonini NM. A novel Drosophila model of nerve injury reveals an essential role of nmnat in maintaining axonal integrity. Curr Biol 2012; 22: 590-595.
44. Kaufman DM, Crowder CM. Mitochondrial proteostatic collapse leads to hypoxic injury. Curr Biol 2015; 25: 2171-2176.
45. Mouchiroud L, Houtkooper RH, Moullan N, Katsyuba E, Ryu D, Canto C et al. The NAD (+)/sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 2013; 154: 430-441.
46. Verdin E. The many faces of sirtuins: coupling of NAD metabolism, sirtuins and lifespan. Nat Med 2014; 20: 25-27.
47. Nikiforov A, Dolle C, Niere M, Ziegler M. Pathways and subcellular compartmentation of NAD biosynthesis in human cells: from entry of extracellular precursors to mitochondrial NAD generation. J Biol Chem 2011; 286: 21767-21778.
48. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974; 77: 71-94.
49. Fay DS Classical genetic methods (December 30, 2013), WormBook, ed. The C. elegans Research Community, WormBook.
50. Mahoney MB, Parks AL, Ruddy DA, Tiong SY, Esengil H, Phan AC et al. Presenilin-based genetic screens in Drosophila melanogaster identify novel notch pathway modifiers. Genetics 2006; 172: 2309-2324.
51. Evans TC (ed). Transformation and microinjection (April 6, 2006), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.108.1, doi/10.1895/wormbook.1.165.1.
52. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 2008; 40: 1375-1383.
53. Apfeld J, Kenyon C. Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature 1999; 402: 804-809.