Cholecalciferol (Vitamin D3) Improves Myelination and Recovery after Nerve Injury

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Chabas, Jean Francois ^a,b   Stephan, Delphine ^a   Marqueste, Tanguy ^c   Garcia, Stephane ^d,e   Lavaut, Marie Noelle ^d,e   Nguyen, Catherine ^f   Legre, Regis ^b   Khrestchatisky, Michel ^a   Decherchi, Patrick ^c   Feron, Francois ^a  

^a Mediterranée University   (France)

^b HÔPITAL DE LA CONCEPTION   (France)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e AIX MARSEILLE UNIVERSITY   (France)

^f Aix Marseille university   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLECALCIFEROL; ERGOCALCIFEROL; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING; CONTROLLED STUDY; CONVALESCENCE; DRUG EFFICACY; DRUG MEGADOSE; GENE EXPRESSION; GENE IDENTIFICATION; IN VITRO STUDY; LOCOMOTION; MALE; MOTOR PERFORMANCE; MUSCLE ATROPHY; MYELINATION; NERVE CELL CULTURE; NERVE FIBER REGENERATION; NEURITE; NONHUMAN; PERIPHERAL NERVE INJURY; PERONEUS NERVE; RAT; SCHWANN CELL; SPINAL GANGLION; VITAMIN SUPPLEMENTATION;

ANIMALS; AXONS; CHOLECALCIFEROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; MALE; MOTOR ACTIVITY; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYELIN SHEATH; NERVE REGENERATION; NEUROGENESIS; ORGAN SIZE; PERIPHERAL NERVE INJURIES; PERONEAL NERVE; RATS; SIGNAL TRANSDUCTION; TIME FACTORS;

ANIMALIA; RATTUS;

EID: 84878571443     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065034     Document Type: Article

References (68)

1. Chabas JF, Alluin O, Rao G, Garcia S, Lavaut MN, et al. (2008) Vitamin D2 potentiates axon regeneration. J Neurotrauma 25: 1247-1256.
2. Fernandes de Abreu DA, Eyles D, Feron F, (2009) Vitamin D, a neuro-immunomodulator: implications for neurodegenerative and autoimmune diseases. Psychoneuroendocrinology 34Suppl 1: S265-277.
3. Eyles DW, Smith S, Kinobe R, Hewison M, McGrath JJ, (2005) Distribution of the vitamin D receptor and 1 alpha-hydroxylase in human brain. J Chem Neuroanat 29: 21-30.
4. Langub MC, Herman JP, Malluche HH, Koszewski NJ, (2001) Evidence of functional vitamin D receptors in rat hippocampus. Neuroscience 104: 49-56.
5. Stumpf WE, O'Brien LP, (1987) 1,25 (OH)2 vitamin D3 sites of action in the brain. An autoradiographic study. Histochemistry 87: 393-406.
6. Stumpf WE, Sar M, Clark SA, DeLuca HF, (1982) Brain target sites for 1,25-dihydroxyvitamin D3. Science 215: 1403-1405.
7. Veenstra TD, Prufer K, Koenigsberger C, Brimijoin SW, Grande JP, et al. (1998) 1,25-Dihydroxyvitamin D3 receptors in the central nervous system of the rat embryo. Brain Res 804: 193-205.
8. Walbert T, Jirikowski GF, Prufer K, (2001) Distribution of 1,25-dihydroxyvitamin D3 receptor immunoreactivity in the limbic system of the rat. Horm Metab Res 33: 525-531.
9. Wang TT, Tavera-Mendoza LE, Laperriere D, Libby E, MacLeod NB, et al. (2005) Large-scale in silico and microarray-based identification of direct 1,25-dihydroxyvitamin D3 target genes. Mol Endocrinol 19: 2685-2695.
10. Saporito MS, Brown ER, Hartpence KC, Wilcox HM, Vaught JL, et al. (1994) Chronic 1,25-dihydroxyvitamin D3-mediated induction of nerve growth factor mRNA and protein in L929 fibroblasts and in adult rat brain. Brain Res 633: 189-196.
11. Neveu I, Naveilhan P, Jehan F, Baudet C, Wion D, et al. (1994) 1,25-dihydroxyvitamin D3 regulates the synthesis of nerve growth factor in primary cultures of glial cells. Brain Res Mol Brain Res 24: 70-76.
12. Brown J, Bianco JI, McGrath JJ, Eyles DW, (2003) 1,25-dihydroxyvitamin D3 induces nerve growth factor, promotes neurite outgrowth and inhibits mitosis in embryonic rat hippocampal neurons. Neurosci Lett 343: 139-143.
13. Neveu I, Naveilhan P, Baudet C, Brachet P, Metsis M, (1994) 1,25-dihydroxyvitamin D3 regulates NT-3, NT-4 but not BDNF mRNA in astrocytes. Neuroreport 6: 124-126.
14. Naveilhan P, Neveu I, Wion D, Brachet P, (1996) 1,25-Dihydroxyvitamin D3, an inducer of glial cell line-derived neurotrophic factor. Neuroreport 7: 2171-2175.
15. Eyles D, Brown J, Mackay-Sim A, McGrath J, Feron F, (2003) Vitamin D3 and brain development. Neuroscience 118: 641-653.
16. Feron F, Burne TH, Brown J, Smith E, McGrath JJ, et al. (2005) Developmental Vitamin D3 deficiency alters the adult rat brain. Brain Res Bull 65: 141-148.
17. Baas D, Prufer K, Ittel ME, Kuchler-Bopp S, Labourdette G, et al. (2000) Rat oligodendrocytes express the vitamin D(3) receptor and respond to 1,25-dihydroxyvitamin D(3). Glia 31: 59-68.
18. Cornet A, Baudet C, Neveu I, Baron-Van Evercooren A, Brachet P, et al. (1998) 1,25-Dihydroxyvitamin D3 regulates the expression of VDR and NGF gene in Schwann cells in vitro. J Neurosci Res 53: 742-746.
19. Barger-Lux MJ, Heaney RP, Dowell S, Chen TC, Holick MF, (1998) Vitamin D and its major metabolites: serum levels after graded oral dosing in healthy men. Osteoporos Int 8: 222-230.
20. Kimball S, Vieth R, (2008) Self-prescribed high-dose vitamin D3: effects on biochemical parameters in two men. Ann Clin Biochem 45: 106-110.
21. Burton JM, Kimball S, Vieth R, Bar-Or A, Dosch HM, et al. (2010) A phase I/II dose-escalation trial of vitamin D3 and calcium in multiple sclerosis. Neurology 74: 1852-1859.
22. Ilahi M, Armas LA, Heaney RP, (2008) Pharmacokinetics of a single, large dose of cholecalciferol. Am J Clin Nutr 87: 688-691.
23. Bain JR, Mackinnon SE, Hunter DA, (1989) Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 83: 129-138.
24. Esau SA, Bellemare F, Grassino A, Permutt S, Roussos C, et al. (1983) Changes in relaxation rate with diaphragmatic fatigue in humans. J Appl Physiol 54: 1353-1360.
25. Decherchi P, Dousset E, Jammes Y, (2007) Respiratory and cardiovascular responses evoked by tibialis anterior muscle afferent fibers in rats. Exp Brain Res 183: 299-312.
26. Darques JL, Jammes Y, (1997) Fatigue-induced changes in group IV muscle afferent activity: differences between high- and low-frequency electrically induced fatigues. Brain Res 750: 147-154.
27. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
28. Decherchi P, Darques JL, Jammes Y, (1998) Modifications of afferent activities from Tibialis anterior muscle in rat by tendon vibrations, increase of interstitial potassium or lactate concentration and electrically-induced fatigue. J Peripher Nerv Syst 3: 267-276.
29. Decherchi P, Vuillon-Cacciutolo G, Darques JL, Jammes Y, (2001) Changes in afferent activities from tibialis anterior muscle after nerve repair by self-anastomosis. Muscle Nerve 24: 59-68.
30. Armas LA, Hollis BW, Heaney RP, (2004) Vitamin D2 is much less effective than vitamin D3 in humans. J Clin Endocrinol Metab 89: 5387-5391.
31. Heaney RP, Recker RR, Grote J, Horst RL, Armas LA, (2011) Vitamin D(3) is more potent than vitamin D(2) in humans. J Clin Endocrinol Metab 96: E447-452.
32. Horst RL, Napoli JL, Littledike ET, (1982) Discrimination in the metabolism of orally dosed ergocalciferol and cholecalciferol by the pig, rat and chick. Biochem J 204: 185-189.
33. Norman P, Moss I, Sian M, Gosling M, Powell J, (2002) Maternal and postnatal vitamin D ingestion influences rat aortic structure, function and elastin content. Cardiovasc Res 55: 369-374.
34. Roder JD, Stair EL (1999) An overview of cholecalciferol toxicosis. Vet Hum Toxicol 41: 344, 343.
35. Brouwer DA, van Beek J, Ferwerda H, Brugman AM, van der Klis FR, et al. (1998) Rat adipose tissue rapidly accumulates and slowly releases an orally-administered high vitamin D dose. Br J Nutr 79: 527-532.
36. Vieth R, (1999) Vitamin D supplementation, 25-hydroxyvitamin D concentrations, and safety. Am J Clin Nutr 69: 842-856.
37. Birge SJ, Haddad JG, (1975) 25-hydroxycholecalciferol stimulation of muscle metabolism. J Clin Invest 56: 1100-1107.
38. Wassner SJ, Li JB, Sperduto A, Norman ME, (1983) Vitamin D Deficiency, hypocalcemia, and increased skeletal muscle degradation in rats. J Clin Invest 72: 102-112.
39. Burne TH, McGrath JJ, Eyles DW, Mackay-Sim A, (2005) Behavioural characterization of vitamin D receptor knockout mice. Behav Brain Res 157: 299-308.
40. Sorensen OH, Lund B, Saltin B, Andersen RB, Hjorth L, et al. (1979) Myopathy in bone loss of ageing: improvement by treatment with 1 alpha-hydroxycholecalciferol and calcium. Clin Sci (Lond) 56: 157-161.
41. Sato Y, Iwamoto J, Kanoko T, Satoh K, (2005) Low-dose vitamin D prevents muscular atrophy and reduces falls and hip fractures in women after stroke: a randomized controlled trial. Cerebrovasc Dis 20: 187-192.
42. Moreira-Pfrimer LD, Pedrosa MA, Teixeira L, Lazaretti-Castro M, (2009) Treatment of vitamin D deficiency increases lower limb muscle strength in institutionalized older people independently of regular physical activity: a randomized double-blind controlled trial. Ann Nutr Metab 54: 291-300.
43. Cannell JJ, Hollis BW, Sorenson MB, Taft TN, Anderson JJ, (2009) Athletic performance and vitamin D. Med Sci Sports Exerc. 41: 1102-1110.
44. Garcion E, Sindji L, Leblondel G, Brachet P, Darcy F, (1999) 1,25-dihydroxyvitamin D3 regulates the synthesis of gamma-glutamyl transpeptidase and glutathione levels in rat primary astrocytes. J Neurochem 73: 859-866.
45. Garcion E, Sindji L, Montero-Menei C, Andre C, Brachet P, et al. (1998) Expression of inducible nitric oxide synthase during rat brain inflammation: regulation by 1,25-dihydroxyvitamin D3. Glia 22: 282-294.
46. Ibi M, Sawada H, Nakanishi M, Kume T, Katsuki H, et al. (2001) Protective effects of 1 alpha,25-(OH)(2)D(3) against the neurotoxicity of glutamate and reactive oxygen species in mesencephalic culture. Neuropharmacology 40: 761-771.
47. Shinpo K, Kikuchi S, Sasaki H, Moriwaka F, Tashiro K, (2000) Effect of 1,25-dihydroxyvitamin D(3) on cultured mesencephalic dopaminergic neurons to the combined toxicity caused by L-buthionine sulfoximine and 1-methyl-4-phenylpyridine. J Neurosci Res 62: 374-382.
48. Wang Y, Chiang YH, Su TP, Hayashi T, Morales M, et al. (2000) Vitamin D(3) attenuates cortical infarction induced by middle cerebral arterial ligation in rats. Neuropharmacology 39: 873-880.
49. Wang JY, Wu JN, Cherng TL, Hoffer BJ, Chen HH, et al. (2001) Vitamin D(3) attenuates 6-hydroxydopamine-induced neurotoxicity in rats. Brain Res 904: 67-75.
50. Sanchez B, Relova JL, Gallego R, Ben-Batalla I, Perez-Fernandez R, (2009) 1,25-Dihydroxyvitamin D3 administration to 6-hydroxydopamine-lesioned rats increases glial cell line-derived neurotrophic factor and partially restores tyrosine hydroxylase expression in substantia nigra and striatum. J Neurosci Res 87: 723-732.
51. Marini F, Bartoccini E, Cascianelli G, Voccoli V, Baviglia MG, et al. (2009) Effect of 1alpha,25-dihydroxyvitamin D3 in embryonic hippocampal cells. Hippocampus 20: 696-705.
52. Caroni P, Schneider C, Kiefer MC, Zapf J, (1994) Role of muscle insulin-like growth factors in nerve sprouting: suppression of terminal sprouting in paralyzed muscle by IGF-binding protein 4. J Cell Biol 125: 893-902.
53. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F, (1995) Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14: 717-730.
54. Gao WQ, Shinsky N, Ingle G, Beck K, Elias KA, et al. (1999) IGF-I deficient mice show reduced peripheral nerve conduction velocities and decreased axonal diameters and respond to exogenous IGF-I treatment. J Neurobiol 39: 142-152.
55. Cheng CM, Mervis RF, Niu SL, Salem N Jr, Witters LA, et al. (2003) Insulin-like growth factor 1 is essential for normal dendritic growth. J Neurosci Res 73: 1-9.
56. Nishino J, Yamashita K, Hashiguchi H, Fujii H, Shimazaki T, et al. (2004) Meteorin: a secreted protein that regulates glial cell differentiation and promotes axonal extension. EMBO J 23: 1998-2008.
57. Nguyen T, Di Giovanni S, (2008) NFAT signaling in neural development and axon growth. Int J Dev Neurosci 26: 141-145.
58. Endo M, Ohashi K, Mizuno K, (2007) LIM kinase and slingshot are critical for neurite extension. J Biol Chem 282: 13692-13702.
59. Rosso S, Bollati F, Bisbal M, Peretti D, Sumi T, et al. (2004) LIMK1 regulates Golgi dynamics, traffic of Golgi-derived vesicles, and process extension in primary cultured neurons. Mol Biol Cell 15: 3433-3449.
60. Takemura M, Mishima T, Wang Y, Kasahara J, Fukunaga K, et al. (2009) Ca2+/calmodulin-dependent protein kinase IV-mediated LIM kinase activation is critical for calcium signal-induced neurite outgrowth. J Biol Chem 284: 28554-28562.
61. Zhou X, Babu JR, da Silva S, Shu Q, Graef IA, et al. (2007) Unc-51-like kinase 1/2-mediated endocytic processes regulate filopodia extension and branching of sensory axons. Proc Natl Acad Sci U S A 104: 5842-5847.
62. Tomoda T, Kim JH, Zhan C, Hatten ME, (2004) Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes Dev 18: 541-558.
63. Marchesi C, Milani M, Morbin M, Cesani M, Lauria G,et al. Four novel cases of periaxin-related neuropathy and review of the literature. Neurology 75: 1830-1838.
64. Birling MC, Tait S, Hardy RJ, Brophy PJ, (1999) A novel rat tetraspan protein in cells of the oligodendrocyte lineage. J Neurochem 73: 2600-2608.
65. Terada N, Baracskay K, Kinter M, Melrose S, Brophy PJ, et al. (2002) The tetraspanin protein, CD9, is expressed by progenitor cells committed to oligodendrogenesis and is linked to beta1 integrin, CD81, and Tspan-2. Glia 40: 350-359.
66. Chabas D, Baranzini SE, Mitchell D, Bernard CC, Rittling SR, et al. (2001) The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294: 1731-1735.
67. Selvaraju R, Bernasconi L, Losberger C, Graber P, Kadi L, et al. (2004) Osteopontin is upregulated during in vivo demyelination and remyelination and enhances myelin formation in vitro. Mol Cell Neurosci 25: 707-721.
68. Zhao C, Fancy SP, Ffrench-Constant C, Franklin RJ, (2008) Osteopontin is extensively expressed by macrophages following CNS demyelination but has a redundant role in remyelination. Neurobiol Dis 31: 209-217.