Reducing expression of NAD+ synthesizing enzyme NMNAT1 does not affect the rate of Wallerian degeneration

FEBS Journal

Volumn 278, Issue 15, 2011, Pages 2666-2679

  Conforti, Laura ^a,b,c   Janeckova, Lucie ^a   Wagner, Diana ^b   Mazzola, Francesca ^d   Cialabrini, Lucia ^d   Di Stefano, Michele ^d,g   Orsomando, Giuseppe ^d   Magni, Giulio ^d   Bendotti, Caterina ^e   Smyth, Neil ^f   Coleman, Michael ^a,b  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^e MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^f UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^g UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

axon; Cre loxP knockout; NAD(P)+; NMNAT; Wallerian degeneration

Indexed keywords

MESSENGER RNA; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; FEMALE; GENE DISRUPTION; GENE EXPRESSION; GENE INACTIVATION; GENE LOCUS; GENE TARGETING; HETEROZYGOTE; KNOCKOUT MOUSE; MALE; MOUSE; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVE LESION; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SCIATIC NERVE; SURVIVAL RATE;

ANIMALS; AXONS; GENE TARGETING; MICE; MICE, KNOCKOUT; NAD; NERVE TISSUE PROTEINS; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; WALLERIAN DEGENERATION;

MUS; WALLERIA;

EID: 79960605733     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08193.x     Document Type: Article

References (45)

1. Magni G, Amici A, Emanuelli M, Orsomando G, Raffaelli N, &, Ruggieri S, (2004) Structure and function of nicotinamide mononucleotide adenylyltransferase. Curr Med Chem 11, 873-885. (Pubitemid 38425921)
2. Berger F, Lau C, Dahlmann M, &, Ziegler M, (2005) Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem 280, 36334-36341. (Pubitemid 41633907)
3. Emanuelli M, Amici A, Carnevali F, Pierella F, Raffaelli N, &, Magni G, (2003) Identification and characterization of a second NMN adenylyltransferase gene in Saccharomyces cerevisiae. Protein Expr Purif 27, 357-364. (Pubitemid 36339308)
4. Yalowitz JA, Xiao S, Biju MP, Antony AC, Cummings OW, Deeg MA, &, Jayaram HN, (2004) Characterization of human brain nicotinamide 5′-mononucleotide adenylyltransferase-2 and expression in human pancreas. Biochem J 377, 317-326. (Pubitemid 38142187)
5. Koch-Nolte F, Haag F, Guse AH, Lund F, &, Ziegler M, (2009) Emerging roles of NAD+ and its metabolites in cell signaling. Sci Signal 2, mr1.
6. Lau C, Doelle C, Gossmann TI, Agledal L, Niere M, &, Ziegler M, (2010) Isoform-specific targeting and interaction domains (ISTIDs) in human nicotinamide mononucleotide adenylyltransferases (NMNATs). J Biol Chem 285, 18868-18876.
7. Beirowski B, Babetto E, Gilley J, Mazzola F, Conforti L, Janeckova L, Magni G, Ribchester RR, &, Coleman MP, (2009) Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo. J Neurosci 29, 653-668.
8. Guarente L, &, Picard F, (2005) Calorie restriction-the SIR2 connection. Cell 120, 473-482. (Pubitemid 40269762)
9. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong HK, Chong JL, Buhr ED, Lee C, et al. (2009) Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324, 651-654.
10. van der Veer E, Ho C, O'Neil C, Barbosa N, Scott R, Cregan SP, &, Pickering JG, (2007) Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J Biol Chem 282, 10841-10845. (Pubitemid 47100731)
11. Zhang T, Berrocal JG, Frizzell KM, Gamble MJ, DuMond ME, Krishnakumar R, Yang T, Sauve AA, &, Kraus WL, (2009) Enzymes in the NAD+ salvage pathway regulate SIRT1 activity at target gene promoters. J Biol Chem 284, 20408-20417.
12. Chiarugi A, (2002) Inhibitors of poly(ADP-ribose) polymerase-1 suppress transcriptional activation in lymphocytes and ameliorate autoimmune encephalomyelitis in rats. Br J Pharmacol 137, 761-770. (Pubitemid 35404175)
13. Berger F, Lau C, &, Ziegler M, (2007) Regulation of poly(ADP-ribose) polymerase 1 activity by the phosphorylation state of the nuclear NAD biosynthetic enzyme NMN adenylyl transferase 1. Proc Natl Acad Sci USA 104, 3765-3770. (Pubitemid 47181528)
14. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, &, Swanson RA, (2010) NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30, 2967-2978.
15. Liu D, Gharavi R, Pitta M, Gleichmann M, &, Mattson MP, (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.
16. Kitaoka Y, Hayashi Y, Kumai T, Takeda H, Munemasa Y, Fujino H, Ueno S, Sadun AA, &, Lam TT, (2009) Axonal and cell body protection by nicotinamide adenine dinucleotide in tumor necrosis factor-induced optic neuropathy. J Neuropathol Exp Neurol 68, 915-927.
17. Babetto E, Beirowski B, Janeckova L, Brown R, Gilley J, Thomson D, Ribchester RR, &, Coleman MP, (2010) Targeting NMNAT1 to axons and synapses transforms its neuroprotective potency in vivo. J Neurosci 30, 13291-13304.
18. Sasaki Y, &, Milbrandt J, (2010) Axonal degeneration is blocked by nicotinamide mononucleotide adenylyltransferase (Nmnat) protein transduction into transected axons. J Biol Chem 285, 41211-41215.
19. Coleman MP, &, Freeman MR, (2010) Wallerian degeneration, Wld(S), and Nmnat. Annu Rev Neurosci 33, 245-267.
20. Avery MA, Sheehan AE, Kerr KS, Wang J, &, Freeman MR, (2009) Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J Cell Biol 184, 501-513.
21. Conforti L, Wilbrey A, Morreale G, Janeckova L, Beirowski B, Adalbert R, Mazzola F, Di Stefano M, Hartley R, Babetto E, et al. (2009) Wld S protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice. J Cell Biol 184, 491-500.
22. Conforti L, Fang G, Beirowski B, Wang MS, Sorci L, Asress S, Adalbert R, Silva A, Bridge K, Huang XP, et al. (2007) NAD(+) and axon degeneration revisited: Nmnat1 cannot substitute for Wld(S) to delay Wallerian degeneration. Cell Death Differ 14, 116-127. (Pubitemid 44911899)
23. Araki T, Sasaki Y, &, Milbrandt J, (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305, 1010-1013. (Pubitemid 39071777)
24. Laser H, Conforti L, Morreale G, Mack TG, Heyer M, Haley JE, Wishart TM, Beirowski B, Walker SA, Haase G, et al. (2006) The slow Wallerian degeneration protein, WldS, binds directly to VCP/p97 and partially redistributes it within the nucleus. Mol Biol Cell 17, 1075-1084. (Pubitemid 43376531)
25. Morreale G, Conforti L, Coadwell J, Wilbrey AL, &, Coleman MP, (2009) Evolutionary divergence of valosin-containing protein/cell division cycle protein 48 binding interactions among endoplasmic reticulum-associated degradation proteins. FEBS J 276, 1208-1220.
26. Gilley J, &, Coleman MP, (2010) Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 8, e1000300.
27. Hafner M, Wenk J, Nenci A, Pasparakis M, Scharffetter-Kochanek K, Smyth N, Peters T, Kess D, Holtkotter O, Shephard P, et al. (2004) Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 38, 176-181. (Pubitemid 38590848)
28. Conforti L, Tarlton A, Mack TG, Mi W, Buckmaster EA, Wagner D, Perry VH, &, Coleman MP, (2000) A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc Natl Acad Sci USA 97, 11377-11382.
29. Fernando FS, Conforti L, Tosi S, Smith AD, &, Coleman MP, (2002) Human homologue of a gene mutated in the slow Wallerian degeneration (C57BL/Wld(s)) mouse. Gene 284, 23-29. (Pubitemid 34219397)
30. Di Stefano M, Galassi L, &, Magni G, (2010) Unique expression pattern of human nicotinamide mononucleotide adenylyltransferase isozymes in red blood cells. Blood Cells Mol Dis 45, 33-39.
31. Sorci L, Cimadamore F, Scotti S, Petrelli R, Cappellacci L, Franchetti P, Orsomando G, &, Magni G, (2007) Initial-rate kinetics of human NMN-adenylyltransferases: substrate and metal ion specificity, inhibition by products and multisubstrate analogues, and isozyme contributions to NAD+ biosynthesis. Biochemistry 46, 4912-4922. (Pubitemid 46651212)
32. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, &, Sanes JR, (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51.
33. Beirowski B, Berek L, Adalbert R, Wagner D, Grumme DS, Addicks K, Ribchester RR, &, Coleman MP, (2004) Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice. J Neurosci Methods 134, 23-35. (Pubitemid 38224184)
34. Beirowski B, Adalbert R, Wagner D, Grumme DS, Addicks K, Ribchester RR, &, Coleman MP, (2005) The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci 6, 6.
35. Eckel-Mahan K, &, Sassone-Corsi P, (2009) Metabolism control by the circadian clock and vice versa. Nat Struct Mol Biol 16, 462-467.
36. Nakahata Y, Sahar S, Astarita G, Kaluzova M, &, Sassone-Corsi P, (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324, 654-657.
37. Chiarugi A, &, Moskowitz MA, (2002) Cell biology. PARP-1-a perpetrator of apoptotic cell death? Science 297, 200-201. (Pubitemid 34761269)
38. Zhai RG, Cao Y, Hiesinger PR, Zhou Y, Mehta SQ, Schulze KL, Verstreken P, &, Bellen HJ, (2006) Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity. PLoS Biol 4, e416.
39. Zhai RG, Zhang F, Hiesinger PR, Cao Y, Haueter CM, &, Bellen HJ, (2008) NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature 452, 887-891. (Pubitemid 351550857)
40. Sasaki Y, Vohra BP, Baloh RH, &, Milbrandt J, (2009) Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J Neurosci 29, 6526-6534.
41. Balducci E, Emanuelli M, Raffaelli N, Ruggieri S, Amici A, Magni G, Orsomando G, Polzonetti V, &, Natalini P, (1995) Assay methods for nicotinamide mononucleotide adenylyltransferase of wide applicability. Anal Biochem 228, 64-68.
42. Billington RA, Travelli C, Ercolano E, Galli U, Roman CB, Grolla AA, Canonico PL, Condorelli F, &, Genazzani AA, (2008) Characterization of NAD uptake in mammalian cells. J Biol Chem 283, 6367-6374.
43. Pfaffl MW, Horgan GW, &, Dempfle L, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30, e36.
44. Buckmaster EA, Perry VH, &, Brown MC, (1995) The rate of Wallerian degeneration in cultured neurons from wild type and C57BL/WldS mice depends on time in culture and may be extended in the presence of elevated K+ levels. Eur J Neurosci 7, 1596-1602.
45. Sasaki Y, Vohra BP, Lund FE, &, Milbrandt J, (2009) Nicotinamide mononucleotide adenylyl transferase-mediated axonal protection requires enzymatic activity but not increased levels of neuronal nicotinamide adenine dinucleotide. J Neurosci 29, 5525-5535.