The Wlds transgene reduces axon loss in a Charcot-Marie-Tooth disease 1A rat model and nicotinamide delays post-traumatic axonal degeneration

Neurobiology of Disease

Volumn 42, Issue 1, 2011, Pages 1-8

  Meyer zu Horste, Gerd ^b   Miesbach, Timo A ^a   Muller, Johanna I ^b   Fledrich, Robert ^a   Stassart, Ruth M ^a   Kieseier, Bernd C ^b   Coleman, Michael P ^c   Sereda, Michael W ^a,d  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c BABRAHAM INSTITUTE   (United Kingdom)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Axonal degeneration; Charcot Marie Tooth disease 1A; CMT1A; Hereditary neuropathy; Nicotinamide; Traumatic nerve injury; Wallerian degeneration slow

Indexed keywords

NICOTINAMIDE; PERIPHERAL MYELIN PROTEIN 22;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONTROLLED STUDY; DEMYELINATION; DRUG BLOOD LEVEL; FEMALE; HEREDITARY MOTOR SENSORY NEUROPATHY; IN VIVO STUDY; NERVE FIBER DEGENERATION; NEUROPROTECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; TRANSGENE; TRANSGENIC RAT; WLDS GENE;

ANIMALS; AXONS; CHARCOT-MARIE-TOOTH DISEASE; DISEASE MODELS, ANIMAL; FEMALE; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; NIACINAMIDE; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; SCIATIC NEUROPATHY; WALLERIAN DEGENERATION;

EID: 79751528889     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.12.006     Document Type: Article

References (54)

1. Adalbert R., et al. A rat model of slow Wallerian degeneration (WldS) with improved preservation of neuromuscular synapses. Eur. J. Neurosci. 2005, 21:271-277.
2. Araki T., et al. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 2004, 305:1010-1013.
3. Avery M.A., et al. Wld S requires Nmnat1 enzymatic activity and N16-VCP interactions to suppress Wallerian degeneration. J. Cell Biol. 2009, 184:501-513.
4. Babetto E., et al. Targeting NMNAT1 to axons and synapses transforms its neuroprotective potency in vivo. J. Neurosci. 2010, 30:13291-13304.
5. Beirowski B., et al. Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice. J. Neurosci. Methods 2004, 134:23-35.
6. Beirowski B., et al. The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci. 2005, 6:6.
7. Beirowski B., et al. Non-nuclear Wld(S) determines its neuroprotective efficacy for axons and synapses in vivo. J. Neurosci. 2009, 29:653-668.
8. Cai A.L., et al. Zinc neurotoxicity is dependent on intracellular NAD levels and the sirtuin pathway. Eur. J. Neurosci. 2006, 24:2169-2176.
9. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
10. Coleman M.P., Perry V.H. Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 2002, 25:532-537.
11. Coleman M.P., et al. An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse. Proc. Natl Acad. Sci. USA 1998, 95:9985-9990.
12. Conforti L., et al. NAD(+) and axon degeneration revisited: Nmnat1 cannot substitute for Wld(S) to delay Wallerian degeneration. Cell Death Differ. 2007, 14:116-127.
13. Conforti L., et al. Wld S protein requires Nmnat activity and a short N-terminal sequence to protect axons in mice. J. Cell Biol. 2009, 184:491-500.
14. Dragovic J., et al. Nicotinamide pharmacokinetics in patients. Radiother. Oncol. 1995, 36:225-228.
15. Emanuelli M., et al. Molecular cloning, chromosomal localization, tissue mRNA levels, bacterial expression, and enzymatic properties of human NMN adenylyltransferase. J. Biol. Chem. 2001, 276:406-412.
16. Feng Y., et al. Nicotinamide reduces hypoxic ischemic brain injury in the newborn rat. Brain Res. Bull. 2006, 69:117-122.
17. Ferri A., et al. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr. Biol. 2003, 13:669-673.
18. Garavaglia S., et al. Structure of human NMN adenylyltransferase. A key nuclear enzyme for NAD homeostasis. J. Biol. Chem. 2002, 277:8524-8530.
19. Gilley J., Coleman M.P. Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol. 2010, 8:e1000300.
20. Kaneko S., et al. Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J. Neurosci. 2006, 26:9794-9804.
21. Karlsson U., Schultz R.L. Fixation of the central nervous system from electron microscopy by aldehyde perfusion. I. Preservation with aldehyde perfusates versus direct perfusion with osmium tetroxide with special reference to membranes and the extracellular space. J. Ultrastruct. Res. 1965, 12:160-186.
22. Kimura N., et al. Comparison of metabolic fates of nicotinamide, NAD+ and NADH administered orally and intraperitoneally; characterization of oral NADH. J. Nutr. Sci. Vitaminol. (Tokyo) 2006, 52:142-148.
23. Luft J.H. Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol. 1961, 9:409-414.
24. Lunn E.R., et al. Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur. J. Neurosci. 1989, 1:27-33.
25. Lupski J.R., Chance P.F. Hereditary motor and sensory neuropathies involving altered dosage or mutation of PMP22: the CMT1A duplication and HNPP deletion. Peripheral Neuropathy 2005, 1659-1680. Elsevier Saunders, Philadelphia. P.J. Dyck, P.K. Thomas (Eds.).
26. Mack T.G., et al. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 2001, 4:1199-1206.
27. Magni G., et al. Enzymology of NAD+ synthesis. Adv. Enzymol. Relat. Areas Mol. Biol. 1999, 73:135-182. xi.
28. Maynard K.I., et al. Delayed multidose treatment with nicotinamide extends the degree and duration of neuroprotection by reducing infarction and improving behavioral scores up to two weeks following transient focal cerebral ischemia in Wistar rats. Ann. NY Acad. Sci. 2001, 939:416-424.
29. Meyer zu Horste G., Nave K.A. Animal models of inherited neuropathies. Curr. Opin. Neurol. 2006, 19:464-473.
30. Meyer zu Horste G., et al. Antiprogesterone therapy uncouples axonal loss from demyelination in a transgenic rat model of CMT1A neuropathy. Ann. Neurol. 2007, 61:61-72.
31. Meyer O.A., et al. A method for the routine assessment of fore- and hindlimb grip strength of rats and mice. Neurobehav. Toxicol. 1979, 1:233-236.
32. Nave K.A., et al. Mechanisms of disease: inherited demyelinating neuropathies - from basic to clinical research. Nat. Clin. Pract. Neurol. 2007, 3:453-464.
33. Pareyson D., Marchesi C. Natural history and treatment of peripheral inherited neuropathies. Adv. Exp. Med. Biol. 2009, 652:207-224.
34. Passage E., et al. Ascorbic acid treatment corrects the phenotype of a mouse model of Charcot-Marie-Tooth disease. Nat. Med. 2004, 10:396-401.
35. Press C., Milbrandt J. Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J. Neurosci. 2008, 28:4861-4871.
36. Ribchester R.R., et al. Persistence of neuromuscular junctions after axotomy in mice with slow Wallerian degeneration (C57BL/WldS). Eur. J. Neurosci. 1995, 7:1641-1650.
37. Sadanaga-Akiyoshi F., et al. Nicotinamide attenuates focal ischemic brain injury in rats: with special reference to changes in nicotinamide and NAD+ levels in ischemic core and penumbra. Neurochem. Res. 2003, 28:1227-1234.
38. Sahenk Z., et al. Effects of PMP22 duplication and deletions on the axonal cytoskeleton. Ann. Neurol. 1999, 45:16-24.
39. Sahenk Z., et al. NT-3 promotes nerve regeneration and sensory improvement in CMT1A mouse models and in patients. Neurology 2005, 65:681-689.
40. Sakakibara Y., et al. Delayed treatment with nicotinamide (vitamin B3) reduces the infarct volume following focal cerebral ischemia in spontaneously hypertensive rats, diabetic and non-diabetic Fischer 344 rats. Brain Res. 2002, 931:68-73.
41. Samsam M., et al. The Wlds mutation delays robust loss of motor and sensory axons in a genetic model for myelin-related axonopathy. J. Neurosci. 2003, 23:2833-2839.
42. Sasaki Y., et al. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J. Neurosci. 2006, 26:8484-8491.
43. Sasaki Y., et al. Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J. Neurosci. 2009, 29:6526-6534.
44. Sasaki Y., et al. 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.
45. Sereda M.W., Nave K.A. Animal models of Charcot-Marie-Tooth disease type 1A (CMT1A). Neuromolecular Med. 2006, 8:205-215.
46. Sereda M.W., et al. A transgenic rat model of Charcot-Marie-Tooth disease. Neuron 1996, 16:1049-1060.
47. Sereda M.W., et al. Therapeutic administration of progesterone antagonist in a model of Charcot-Marie-Tooth disease (CMT-1A). Nat. Med. 2003, 9:1533-1537.
48. Shy M.E., et al. Hereditary motor and sensory neuropathies: an overview of clinical, genetic, electrophysiologic, and pathologic features. Peripheral Neuropathy 2005, 1623-1658. Elsevier Saunders, Philadelphia. P.J. Dyck, P.K. Thomas (Eds.).
49. Timmerman V., et al. Molecular genetics, biology, and therapy for inherited peripheral neuropathies. Neuromolecular Med. 2006, 8:1-2.
50. Tsao J.W., et al. Loss of the compound action potential: an electrophysiological, biochemical and morphological study of early events in axonal degeneration in the C57BL/Ola mouse. Eur. J. Neurosci. 1994, 6:516-524.
51. Wang M.S., et al. The WldS protein protects against axonal degeneration: a model of gene therapy for peripheral neuropathy. Ann. Neurol. 2001, 50:773-779.
52. Wang M.S., et al. WldS mice are resistant to paclitaxel (taxol) neuropathy. Ann. Neurol. 2002, 52:442-447.
53. Wang J., et al. A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 2005, 170:349-355.
54. Zhai R.G., et al. NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature 2008, 452:887-891.