Overexpression of WldS or Nmnat2 in mauthner cells by single-cell electroporation delays axon degeneration in live zebrafish

Journal of Neuroscience Research

Volumn 88, Issue 15, 2010, Pages 3319-3327

  Feng, Yan ^a,b   Yan, Tingting ^a,b   Zheng, Jin ^a,c   Ge, Xinjian ^a,b   Mu, Yu ^b,d   Zhang, Yi ^a,b   Wu, Dongmei ^a,b   Du, Jiu lin ^b,d   Zhai, Qiwei ^a,b  

^a Institute for Nutritional Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ZHEJIANG SCI TECH UNIVERSITY   (China)

^d Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

Axon degeneration; Neurodegeneration; Nmnat2; Wallerian degeneration

Indexed keywords

NERVE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE 2; UNCLASSIFIED DRUG; WLD S PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ELECTROPORATION; EMBRYO; ENZYME SYNTHESIS; GENE OVEREXPRESSION; IN VIVO STUDY; MAUTHNER CELL; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ZEBRA FISH;

ANIMALS; AXONS; ELECTROPORATION; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NICOTINAMIDE-NUCLEOTIDE ADENYLYLTRANSFERASE; ZEBRAFISH;

EID: 78649399414     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22498     Document Type: Article

References (50)

1. S) with improved preservation of neuromuscular synapses. Eur J Neurosci 21:271-277.
2. Araki T, Sasaki Y, Milbrandt J. 2004. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305:1010-1013.
3. 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.
4. 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.
5. Becker CG, Becker T. 2008. Adult zebrafish as a model for successful central nervous system regeneration. Restor Neurol Neurosci 26:71-80.
6. S) nerves. BMC Neurosci 6:6.
7. S gene delays axonal but not somatic degeneration in a rat glaucoma model. Eur J Neurosci 28:1166-1179.
8. 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.
9. Best JD, Alderton WK. 2008. Zebrafish: an in vivo model for the study of neurological diseases. Neuropsychiatr Dis Treat 4:567-576.
10. Bestman JE, Ewald RC, Chiu SL, Cline HT. 2006. In vivo single-cell electroporation for transfer of DNA and macromolecules. Nat Protoc 1:1267-1272.
11. Bhatt DH, Otto SJ, Depoister B, Fetcho JR. 2004. Cyclic AMP-induced repair of zebrafish spinal circuits. Science 305:254-258.
12. Coleman M. 2005. Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 6:889-898.
13. Coleman MP, Perry VH. 2002. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci 25:532-537.
14. S) mouse. Proc Natl Acad Sci U S A 97:11377-11382.
15. Conforti L, Adalbert R, Coleman MP. 2007. Neuronal death: where does the end begin? Trends Neurosci 30:159-166.
16. Conforti L, Wilbrey A, Morreale G, Janeckova L, Beirowski B, Adalbert R, Mazzola F, Di Stefano M, Hartley R, Babetto E, Smith T, Gilley J, Billington RA, Genazzani AA, Ribchester RR, Magni G, Coleman M. 2009. Wld S protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice. J Cell Biol 184:491-500.
17. Emanuelli M, Carnevali F, Saccucci F, Pierella F, Amici A, Raffaelli N, Magni G. 2001. Molecular cloning, chromosomal localization, tissue mRNA levels, bacterial expression, and enzymatic properties of human NMN adenylyltransferase. J Biol Chem 276:406-412.
18. S, Nmnats and axon degeneration-progress in the past two decades. Prot Cell 1:237-245.
19. Ferri A, Sanes JR, Coleman MP, Cunningham JM, Kato AC. 2003. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr Biol 13:669-673.
20. Ge X, Jin Q, Zhang F, Yan T, Zhai Q. 2008. PCAF acetylates b-catenin and improves its stability. Mol Biol Cell 20:419-427.
21. Gilley J, Coleman MP. 2010. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 8:e1000300.
22. Glass JD. 2004. Wallerian degeneration as a window to peripheral neuropathy. J Neurol Sci 220:123-124.
23. Glass JD, Brushart TM, George EB, Griffin JW. 1993. Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon. J Neurocytol 22:311-321.
24. Haas K, Sin WC, Javaherian A, Li Z, Cline HT. 2001. Single-cell electroporation for gene transfer in vivo. Neuron 29:583-591.
25. Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O'Leary DD, Luo L. 2006. Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50:883-895.
26. Jia H, Yan T, Feng Y, Zeng C, Shi X, Zhai Q. 2007. Identification of a critical site in Wlds: sssential for Nmnat enzyme activity and axon-protective function. Neurosci Lett 413:46-51.
27. Kaneko S, Wang J, Kaneko M, Yiu G, Hurrell JM, Chitnis T, Khoury SJ, He Z. 2006. Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J Neurosci 26:9794-9804.
28. Kerschensteiner M, Schwab ME, Lichtman JW, Misgeld T. 2005. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat Med 11:572-577.
29. Lemmens R, Van Hoecke A, Hersmus N, Geelen V, D'Hollander I, Thijs V, Van Den Bosch L, Carmeliet P, Robberecht W. 2007. Overexpression of mutant superoxide dismutase 1 causes a motor axonopathy in the zebrafish. Hum Mol Genet 16:2359-2365.
30. Liu KS, Fetcho JR. 1999. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 23:325-335.
31. Lunn ER, Perry VH, Brown MC, Rosen H, Gordon S. 1989. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur J Neurosci 1:27-33.
32. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. 2006. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50:869-881.
33. Mack TG, Reiner M, Beirowski B, Mi W, Emanuelli M, Wagner D, Thomson D, Gillingwater T, Court F, Conforti L, Fernando FS, Tarlton A, Andressen C, Addicks K, Magni G, Ribchester RR, Perry VH, Coleman MP. 2001. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat Neurosci 4:1199-1206.
34. S, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 128:405-416.
35. Press C, Milbrandt J. 2008. Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J Neurosci 28:4861-4871.
36. Raff MC, Whitmore AV, Finn JT. 2002. Axonal self-destruction and neurodegeneration. Science 296:868-871.
37. Raffaelli N, Sorci L, Amici A, Emanuelli M, Mazzola F, Magni G. 2002. Identification of a novel human nicotinamide mononucleotide adenylyltransferase. Biochem Biophys Res Commun 297:835-840.
38. Ritter DA, Bhatt DH, Fetcho JR. 2001. In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J Neurosci 21:8956-8965.
39. Samsam M, Mi W, Wessig C, Zielasek J, Toyka KV, Coleman MP, Martini R. 2003. The Wlds mutation delays robust loss of motor and sensory axons in a genetic model for myelin-related axonopathy. J Neurosci 23:2833-2839.
40. Sasaki Y, Araki T, Milbrandt J. 2006. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J Neurosci 26:8484-8491.
41. 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.
42. Takahashi M, Narushima M, Oda Y. 2002. In vivo imaging of functional inhibitory networks on the mauthner cell of larval zebrafish. J Neurosci 22:3929-3938.
43. Vargas ME, Barres BA. 2007. Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci 30:153-179.
44. Waller AV. 1850. Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations on the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond B Biol Sci 140:423-429.
45. Wang J, Zhai Q, Chen Y, Lin E, Gu W, McBurney MW, He Z. 2005. A local mechanism mediates NAD-dependent protection of axon degeneration. J Cell Biol 170:349-355.
46. Yahata N, Yuasa S, Araki T. 2009. Nicotinamide mononucleotide adenylyltransferase expression in mitochondrial matrix delays Wallerian degeneration. J Neurosci 29:6276-6284.
47. Yalowitz JA, Xiao S, Biju MP, Antony AC, Cummings OW, Deeg MA, Jayaram HN. 2004. Characterization of human brain nicotinamide 50mononucleotide adenylyltransferase-2 and expression in human pancreas. Biochem J 377:317-326.
48. Yan T, Feng Y, Zhai Q. 2010a. Axon degeneration: mechanisms and implications of a distinct program from cell death. Neurochem Int 56:529-534.
49. Yan T, Feng Y, Zheng J, Ge X, Zhang Y, Wu D, Zhao J, Zhai Q. 2010b. Nmnat2 delays axon degeneration in superior cervical ganglia dependent on its NAD synthesis activity. Neurochem Int 56:101-106.
50. Zhang X, Kurnasov OV, Karthikeyan S, Grishin NV, Osterman AL, Zhang H. 2003. Structural characterization of a human cytosolic NMN/NaMN adenylyltransferase and implication in human NAD biosynthesis. J Biol Chem 278:13503-13511.