Roles of vitamin D in amyotrophic lateral sclerosis: Possible genetic and cellular signaling mechanisms

Molecular Brain

Volumn 6, Issue 1, 2013, Pages

  Lng, Khanh Vinh Quc ^a,b   Nguyn, Lan Thi Hoàng ^a  

^a Vietnamese American Medical Research Foundation   (United States)

^b FACP   (United States)

Author keywords

ALS; Amyotrophic lateral sclerosis; Calcitriol; Vitamin D

Indexed keywords

BETA CATENIN; CALCIUM BINDING PROTEIN; COLECALCIFEROL; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN D1; GELATINASE B; GLUTAMIC ACID; HEME OXYGENASE 1; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; N(G) NITROARGININE METHYL ESTER; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE SYNTHASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROSTAGLANDIN; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TACALCITOL; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VITAMIN D; WNT PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ASTROCYTE; CEREBROSPINAL FLUID; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; DNA DAMAGE; DNA REPAIR; DOPAMINERGIC NERVE CELL; FUNCTIONAL STATUS; GENETIC ANALYSIS; HUMAN; INTRACELLULAR SIGNALING; LIFESPAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PATHOPHYSIOLOGY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VITAMIN D DEFICIENCY; VITAMIN SUPPLEMENTATION; WNT SIGNALING PATHWAY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; GENOME; HUMANS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; VITAMIN D;

MUS MUSCULUS;

EID: 84875901499     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-6-16     Document Type: Review

References (154)

1. Hypovitaminosis D and decreased bone mineral density in amyotrophic lateral sclerosis. Sato Y, Honda Y, Asoh T, Kikuyama M, Oizumi K, Eur Neurol 1997 37 225 229 10.1159/000117447 9208262
2. Calcium and vitamin D metabolism in Guamanian Chamorros with amyotrophic lateral sclerosis and parkinsonism-dementia. Yanagihara R, Garruto RM, Gajdusek DC, Tomita A, Uchikawa T, Ann Neurol 1984 15 42 48 10.1002/ana.410150108 6546847
3. Can vitamin D delay the progression of ALS? Karam C, Scelsa SN, Med Hypotheses 2011 76 643 645 10.1016/j.mehy.2011.01.021 21310542
4. Further support for vitamin D supplement in delaying the progression of ALS. Shen L, Med Hypotheses 2011 77 698 21855226
5. Association of molecular variants, haplotypes, and linkage disequilibrium within the human vitamin D-binding protein (DBP) gene with postmenopausal bone mineral density. Ezura Y, Nakajima T, Kajita M, Ishida R, Inoue S, J Bone Miner Res 2003 18 1642 1649 10.1359/jbmr.2003.18.9.1642 12968673
6. Biological and clinical aspects of the vitamin D binding protein (Gc-globulin) and its polymorphism. Speeckaert M, Huang G, Delanghe JR, Taes YE, Clin Chim Acta 2006 372 33 42 10.1016/j.cca.2006.03.011 16697362
7. The multifunctional properties and characteristics of vitamin D-binding protein. White P, Cooke N, Trends Endocrinol Metab 2000 11 320 327 10.1016/S1043-2760(00)00317-9 10996527
8. Proteomic analysis of plasma from Portuguese patients with familial amyotrophic lateral sclerosis. Palma AS, De Carvalho M, Grammel N, Pinto S, Barata N, Amyotroph Lateral Scler 2008 9 339 349 10.1080/17482960801934239 18608108
9. Lead exposure as a risk factor for amyotrophic lateral sclerosis. Kamel F, Umbach DM, Hu H, Munsat TL, Shefner JM, Neurodegener Dis 2005 2 195 201 10.1159/000089625 16909025
10. Associations of lead biomarkers and delta-aminolevulinic acid dehydratase and vitamin D receptor genotypes with hematopoietic outcomes in Korean lead workers. Lee SS, Lee BK, Lee GS, Stewart WF, Simon D, Scand J Work Environ Health 2001 27 402 411 10.5271/sjweh.633 11800328
11. Associations of blood lead, dimercaptosuccinic acid-chelatable lead, and tibia lead with polymorphisms in the vitamin D receptor and δ- aminolevulinic acid dehydratase genes. Schwartz BS, Lee BK, Lee GS, Stewart WF, Simon D, Environ Health Perspect 2000 108 949 954 11121361
12. Vitamin D§ssub§2§esub§ potentiates axon regeneration. Chabas JF, Alluin O, Rao G, Garcia S, Lavaut MN, J Neurotrauma 2008 25 1247 1256 10.1089/neu.2008.0593 18986226
13. Dietary vitamin D§ssub§3§esub§ supplementation at 10× the adequate intake improves functional capacity in the G93A transgenic mouse model of ALS, a pilot study. Gianforcaro A, Hamadeh MJ, CNS Neurosci Ther 2012 18 547 557 10.1111/j.1755-5949.2012.00316.x 22591278
14. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Kawamata T, Akiyama H, Yamada T, McGeer PL, Am J Pathol 1992 140 691 707 1347673
15. Immunohistological alterations in muscle of patients with amyotrophic lateral sclerosis: mononuclear cell phenotypes and expression of MHC products. Troost D, Das PK, van den Oord JJ, Louwerse ES, Clin Neuropathol 1992 11 115 120 1611723
16. Expression of HLA-DR in peripheral nerve of amyotrophic lateral sclerosis. Oliveira AS, Isozaki E, Younger D, Gabbai AA, Hays AP, Arq Neuropsiquiatr 1994 52 493 500 10.1590/S0004-282X1994000400007 7611942
17. - 1 Alpha,25-dihydroxyvitamin D§ssub§3§esub§ inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. Penna G, Adorini L, J Immunol 2000 164 2405 2411 10679076
18. Inhibition of costimulatory pathways for T-cell activation by 1,25-dihydroxyvitamin D§ssub§3§esub§ Penna G, Adorini L, Transplant Proc 2001 33 2083 2084 10.1016/S0041-1345(01)01957-1 11377460
19. 1α,25-Dihydroxyvitamin D§ssub§3§esub§ and its analogs as modulators of human dendritic cells: A comparison dose-titration study. Ferreira GB, Overbergh L, Verstuyf A, Mathieu C, J Steroid Biochem Mol Biol 2012 [Epub ahead of print] 10.1016/j.jsbmb.2012.10.009
20. Immunomodulation by a novel, dissociated Vitamin D analogue. Zügel U, Steinmeyer A, May E, Lehmann M, Asadullah K, Exp Dermatol 2009 18 619 27 10.1111/j.1600-0625.2009.00845.x 19239489
21. 1-alpha-calcidol modulates major human monocyte antigens and toll-like receptors TRL2 and TRL4 in vitro. Scherberich J, Kellermeyer M, Ried C, Hartinger A, Eur J Med Res 2005 10 179 82 15946915
22. Human dendritic cell antigen presentation and chemotaxis are inhibited by intrinsic 25-hydroxy vitamin D activation. Bartels LE, Hvas CL, Agnholt J, Dahlerup JF, Agger R, Int Immunopharmacol 2010 10 922 8 10.1016/j.intimp.2010. 05.003 20483384
23. Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. Gowing G, Philips T, Van Wijmeersch B, Audet JN, Dewil M, J Neurosci 2008 28 10234 44 10.1523/JNEUROSCI.3494-08.2008 18842883
24. Exacerbation of Motor Neuron Disease by Chronic Stimulation of Innate Immunity in a Mouse Model of Amyotrophic Lateral Sclerosis. Nguyen MD, D'Aigle T, Gowing G, Julien J-P, Rivest S, J Neurosci 2004 24 1340 9 10.1523/JNEUROSCI.4786-03.2004 14960605
25. Screening of innate immune receptors in neurodegenerative diseases: a similar pattern. Letiembre M, Liu Y, Walter S, Hao W, Pfander T, Neurobiol Aging 2009 30 759 68 10.1016/j.neurobiolaging.2007.08.018 17905482
26. Expression of amyotrophic lateral sclerosis-linked SOD1 mutant increases the neurotoxic potential of microglia via TLR2. Liu Y, Hao W, Dawson A, Liu S, Fassbender K, J Biol Chem 2009 284 3691 9 19091752
27. Gene expression profiling in peripheral blood mononuclear cells from patients with sporadic amyotrophic lateral sclerosis (sALS). Zhang R, Hadlock KG, Do H, Yu S, Honrada R, J Neuroimmunol 2011 230 114 23 10.1016/j.jneuroim. 2010.08.012 20884065
28. Toll-like receptor signaling in amyotrophic lateral sclerosis spinal cord tissue. Casula M, Iyer AM, Spliet WG, Anink JJ, Steentjes K, Neuroscience 2011 179 233 43 21303685
29. Expression of a Cu Zn superoxide dismutase typical for familial amyotrophic lateral sclerosis increases the vulnerability of neuroblastoma cells to infectious injury. Goos M, Zech WD, Jaiswal MK, Balakrishnan S, Ebert S, BMC Infect Dis 2007 7 131 10.1186/1471-2334-7-131 17997855
30. Vitamin D§ssub§3§esub§ down-regulates monocyte TLR expression and triggers hyporesponsiveness to pathogen-associated molecular patterns. Sadeghi K, Wessner B, Laggner U, Ploder M, Tamandl D, Eur J Immunol 2006 36 361 70 10.1002/eji.200425995 16402404
31. Vitamin D§ssub§3§esub§ downregulates intracellular toll-like receptor 9 expression and toll-like receptor 9-induced IL-6 production in human monocytes. Dickie L, Church L, Coulthard L, Mathews R, Emery P, McDermott M, Rheumatol. 2010 48 1466 71
32. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Science 2006 311 1770 3 10.1126/science.1123933 16497887
33. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Krishnakumar R, Kraus WL, Mol Cell 2010 39 8 24 10.1016/j.molcel.2010.06.017 20603072
34. Widespread increased expression of the DNA repair enzyme PARP in brain in ALS. Kim SH, Engelhardt JI, Henkel JS, Siklós L, Soós J, Neurology 2004 62 319 22 10.1212/01.WNL.0000103291.04985.DC 14745081
35. PARP expression is increased in astrocytes but decreased in motor neurons in the spinal cord of sporadic ALS patients. Kim SH, Henkel JS, Beers DR, Sengun IS, Simpson EP, J Neuropathol Exp Neurol 2003 62 88 103 12528821
36. Reactive astrocytes express PARP in the central nervous system of SOD§ssup§G93A§esup§ transgenic mice. Chung YH, Joo KM, Lee YJ, Shin DH, Cha CI, Brain Res 2004 1003 199 204 10.1016/j.brainres.2004.01.010 15019581
37. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Eliasson MJ, Sampei K, Mandir AS, Hurn PD, Traystman RJ, Nat Med 1997 3 1089 95 10.1038/nm1097-1089 9334719
38. Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Mandir AS, Przedborski S, Jackson-Lewis V, Wang ZQ, Simbulan-Rosenthal CM, Proc Natl Acad Sci U S A 1999 96 5774 9 10.1073/pnas.96.10.5774 10318960
39. Poly(ADP-ribose)polymerase-1 modulates microglial responses to amyloid β Kauppinen TM, Suh SW, Higashi Y, Berman AE, Escartin C, J Neuroinflammation 2011 8 152 10.1186/1742-2094-8-152 22051244
40. Hydrogen peroxide-induced motoneuron apoptosis is prevented by poly ADP ribosyl synthetase inhibitors. Hivert B, Cerruti C, Camu W, Neuroreport 1998 9 1835 8 10.1097/00001756-199806010-00031 9665611
41. Effects of an inhibitor of poly(ADP-ribose) polymerase, desmethylselegiline, trientine, and lipoic acid in transgenic ALS mice. Andreassen OA, Dedeoglu A, Friedlich A, Ferrante KL, Hughes D, Exp Neurol 2001 168 419 24 10.1006/exnr.2001.7633 11259130
42. Treatment with dexamethasone and vitamin D§ssub§3§ esub§ attenuates neuroinflammatory age-related changes in rat hippocampus. Moore M, Piazza A, Nolan Y, Lynch MA, Synapse 2007 61 851 61 10.1002/syn.20433 17621647
43. Modulation of poly(ADP-ribose) polymerase during neurophilic and monocytic differentiation of promyelocytic (NB4) and myelocytic (HL-60) leakaemia cells. Bhatia M, Kirkland JB, Mecking-Gill KA, Biochem J 1995 308 131 7 7755555
44. Inhibition of poly(adenosine diphosphate-ribose) polymerase by the active form of vitamin D. Mabley JG, Wallace R, Pacher P, Murphy K, Szab C, Int J Mol Med 2007 9 6 947 952
45. Protective role of heme oxygenase-1 in renal ischemia. Takahashi T, Morita K, Akagi R, Sassa S, Antioxid Redox Signal 2004 6 867 77 15345147
46. Over-expression of heme oxygenase-1 promotes oxidative mitochondrial damage in rat astroglia. Song W, Su H, Song S, Paudel HK, Schipper HM, J Cell Physiol 2006 206 655 63 10.1002/jcp.20509 16222706
47. HO-1 induction in motor cortex and intestinal dysfunction in TDP-43 A315T transgenic mice. Guo Y, Wang Q, Zhang K, An T, Shi P, Brain Res 2012 1460 88 95 22578468
48. Decreased GLT-1 and increased SOD1 and HO-1 expression in astrocytes contribute to lumbar spinal cord vulnerability of SOD1-G93A transgenic mice. Guo Y, Duan W, Li Z, Huang J, Yin Y, FEBS Lett 2010 584 1615 22 10.1016/j.febslet.2010.03.025 20303959
49. Impaired response of hypoxic sensor protein HIF-1α and its downstream proteins in the spinal motor neurons of ALS model mice. Sato K, Morimoto N, Kurata T, Mimoto T, Miyazaki K, Brain Res 2012 1473 55 62 22871270
50. Pretreatment of vitamin D§ssub§3§esub§ ameliorates lung and muscle injury induced by reperfusion of bilateral femoral vessels in a rat model. Shih PK, Chen YC, Huang YC, Chang YT, Chen JX, Cheng CM, J Surg Res 2011 171 323 8 10.1016/j.jss.2010.03.008 20462603
51. Effects of 1α,25-didroxyvitamin D§ssub§3§esub§ on the expression of HO-1 and GFAP in glial cells of the photothrombotically lesioned cerebral cortex. Oermann E, Bidmon H-J, Witte O-W, Zilles K, J Chem Neuroanat 2004 28 225 38 10.1016/j.jchemneu.2004.07.003 15531134
52. Distribution of calcium binding protein mRNAs in rat cerebellar cortex. Kadowaki K, McGowan E, Mock G, Chandler S, Emson PC, Neurosci Lett 1993 153 80 4 10.1016/0304-3940(93)90082-V 8510828
53. Reduced calreticulin levels link endoplasmic reticulum stress and Fas-triggered cell death in motoneurons vulnerable to ALS. Bernard-Marissal N, Moumen A, Sunyach C, Pellegrino C, Dudley K, J Neurosci 2012 32 4901 12 10.1523/JNEUROSCI.5431-11.2012 22492046
54. Parvalbumin is a marker of ALS-resistant motor neurons. Elliott JL, Snider WD, Neuroreport 1995 6 449 52 10.1097/00001756-199502000-00011 7766841
55. The role of calcium-binding proteins in selective motoneuron vulnerability in amyotrophic lateral sclerosis. Alexianu ME, Ho BK, Mohamed AH, La Bella V, Smith RG, Appel SH, Ann Neurol 1994 36 846 58 10.1002/ana.410360608 7998770
56. Parvalbumin and calbindin D-28 k immunoreactivity in transgenic mice with a G93A mutant SOD1 gene. Sasaki S, Warita H, Komori T, Murakami T, Abe K, Iwata M, Brain Res 2006 1083 196 203 10.1016/j.brainres.2006.01.129 16546142
57. Decreased expression of calretinin in the cerebral cortex and hippocampus of SOD1§ssup§G93A§esup§ transgenic mice. Chung YH, Joo KM, Nam RH, Cho MH, Kim DJ, Brain Res 2005 1035 105 9 10.1016/j.brainres.2004.12.022 15713283
58. Over-expression of parvalbumin in transgenic mice rescues motoneurons from injury-induced cell death. Dekkers J, Bayley P, Dick JR, Schwaller B, Berchtold MW, Greensmith L, Neuroscience 2004 123 459 66 10.1016/j.neuroscience. 2003.07.013 14698753
59. Parvalbumin overexpression alters immune-mediated increases in intracellular calcium, and delays disease onset in a transgenic model of familial amyotrophic lateral sclerosis. Beers DR, Ho BK, Siklós L, Alexianu ME, Mosier DR, J Neurochem 2001 79 499 509 11701753
60. Expression of calbindin-D28K in motoneuron hybrid cells after retroviral infection with calbindin-D28K cDNA prevents amyotrophic lateral sclerosis IgG-mediated cytotoxicity. Ho BK, Alexianu ME, Colom LV, Mohamed AH, Serrano F, Appel SH, Proc Natl Acad Sci U S A 1996 93 6796 801 10.1073/pnas.93.13.6796 8692898
61. Overexpression of melatonin membrane receptors increases calcium-binding proteins and protects VSC4.1 motoneurons from glutamate toxicity through multiple mechanisms. Das A, Wallace G 4th, Reiter RJ, Varma AK, Ray SK, Banik NL, J Pineal Res 2012 [Epub ahead of print] 10.1111/j.1600-079X.2012.01022.x
62. Calbindin-D§ssub§28K§esub§, a 1 α,25- dihydroxyvitamin D§ssub§3§esub§-induced calcium-binding protein, binds five or six Ca§ssup§2+§esup§ ions with high affinity. Leathers VL, Linse S, Forsén S, Norman AW, J Biol Chem 1990 265 9838 41 2351677
63. Effects of calcitriol on calbindins gene expression and lipid peroxidation in human placenta. Halhali A, Figueras AG, Díaz L, Avila E, Barrera D, J Steroid Biochem Mol Biol 2010 121 448 51 10.1016/j.jsbmb.2010.03. 008 20214988
64. Parvalbumin increases in the caudate putamen of rats with vitamin D hypervitaminosis. de Viragh PA, Haglid KG, Celio MR, Proc Natl Acad Sci U S A 1989 86 3887 90 10.1073/pnas.86.10.3887 2542952
65. 1α, 25 dihydroxyvitamin D§ssub§3§esub§- dependent up-regulation of calcium-binding proteins in motoneuron cells. Alexianu ME, Robbins E, Carswell S, Appel SH, J Neurosci Res 1998 51 58 66 10.1002/(SICI)1097-4547(19980101)51:1<58::AID-JNR6>3.0.CO;2-K 9452309
66. Protein disulfide isomerase in ALS mouse glia links protein misfolding with NADPH oxidase-catalyzed superoxide production. Jaronen M, Vehviläinen P, Malm T, Keksa-Goldsteine V, Pollari E, Hum Mol Genet 2013 22 646 55 10.1093/hmg/dds472 23118353
67. SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. Harraz MM, Marden JJ, Zhou W, Zhang Y, Williams A, J Clin Invest 2008 118 659 70 18219391
68. Redox modifier genes in amyotrophic lateral sclerosis in mice. Marden JJ, Harraz MM, Williams AJ, Nelson K, Luo M, J Clin Invest 2007 117 2913 9 10.1172/JCI31265 17853944
69. Chimerization of astroglial population in the lumbar spinal cord after mesenchymal stem cell transplantation prolongs survival in a rat model of amyotrophic lateral sclerosis. Boucherie C, Schäfer S, Lavand'homme P, Maloteaux JM, Hermans E, J Neurosci Res 2009 87 2034 46 10.1002/jnr.22038 19267424
70. Effect of active vitamin D§ssub§3§esub§ on the levels of NADPH-dependent cytosolic 3,5,3§ssup§′§esup§- triiodo-L-thyronine-binding protein. Hashizume K, Suzuki S, Ichikawa K, Takeda T, Kobayashi M, Biochem Biophys Res Commun 1991 177 388 94 10.1016/0006-291X(91) 91995-O 2043122
71. Effect of vitamin D deficiency and 1,25-dihydroxyvitamin D§ssub§3§esub§ on rat heart metabolism. Stio M, Lunghi B, Iantomasi T, Vincenzini MT, Treves C, J Mol Cell Cardiol 1994 26 1421 8 10.1006/jmcc.1994.1161 7897666
72. Cellular utilization of cytosolic NADPH in kidney and liver cells from rats fed a normal or a vitamin D-deficient diet. Bachelet M, Bader C, Merlot AM, Laborde K, Snarska J, Ulmann A, Cell Biochem Funct 1983 1 25 9 10.1002/cbf.290010105 6678614
73. The Beneficial Role of Vitamin D in Alzheimer's Disease. Luong K, Nguyen L, Am J Alzheimers Dis Other Demen 2011 Nov 26 7 511 20 10.1177/1533317511429321
74. Role of vitamin d in Parkinson's disease. Luong K, Nguyen L, ISRN Neurol. 2012 2012 134289 22619734
75. Metabolic progression markers of neurodegeneration in the transgenic G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Niessen HG, Debska-Vielhaber G, Sander K, Angenstein F, Ludolph AC, Eur J Neurosci 2007 25 1669 77 10.1111/j.1460-9568.2007.05415.x 17432958
76. Magnetic resonance spectroscopy of regional brain metabolite markers in FALS mice and the effects of dietary creatine supplementation. Choi J-K, Küstermann E, Dedeoglu A, Jenkins BG, Eur J Neurosci 2009 30 2143 50 10.1111/j.1460-9568.2009.07015.x 19930399
77. Plasma glutamate and glycine levels in patients with amyotrophic lateral sclerosis. Andreadou E, Kapaki E, Kokotis P, Paraskevas GP, Katsaros N, In Vivo 2008 22 137 41 18396796
78. Altered metabolism of excitatory amino acids, N-acetyl-aspartate and N-acetyl-aspartyl-glutamate in amyotrophic lateral sclerosis. Plaitakis A, Constantakakis E, Brain Res Bull 1993 30 381 6 10.1016/0361-9230(93)90269-H 8457887
79. Decreased platelet glutamate uptake in patients with amyotrophic lateral sclerosis. Ferrarese C, Sala G, Riva R, Begni B, Zoia C, Neurology 2001 56 270 2 10.1212/WNL.56.2.270 11160972
80. Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. Rothstein JD, Martin LJ, Kuncl RW, N Engl J Med 1992 326 1464 8 10.1056/NEJM199205283262204 1349424
81. Increased glutamine synthetase but normal EAAT2 expression in platelets of ALS patients. Bos IW, Hoogland G, Meine Jansen CF, Willigen G, Spierenburg HA, Neurochem Int 2006 48 306 11 10.1016/j.neuint.2005.09.009 16426705
82. The protective effect of riluzole on manganese caused disruption of glutamate-glutamine cycle in rats. Deng Y, Xu Z, Xu B, Tian Y, Xin X, Brain Res 2009 1289 106 17 19615351
83. Progesterone with vitamin D affords better neuroprotection against excitotoxicity in cultured cortical neurons than progesterone alone. Atif F, Sayeed I, Ishrat T, Stein DG, Mol Med 2009 15 328 36 19603099
84. Protective effects of 1 alpha,25-(OH) §ssub§2§esub§D§ssub§3§esub§ against the neurotoxicity of glutamate and reactive oxygen species in mesencephalic culture. Ibi M, Sawada H, Nakanishi M, Kume T, Katsuki H, Neuropharmacology 2001 40 761 71 10.1016/S0028-3908(01)00009-0 11369030
85. Neuroprotection by co-treatment and post-treating with calcitriol following the ischemic and excitotoxic insult in vivo and in vitro. Kajta M, Makarewicz D, Ziemińska E, Jantas D, Domin H, Neurochem Int 2009 55 265 74 10.1016/j.neuint.2009.03.010 19576513
86. Chronic vitamin D§ssub§3§esub§ treatment protects against neurotoxicity by glutamate in association with upregulation of vitamin D receptor mRNA expression in cultured rat cortical neurons. Taniura H, Ito M, Sanada N, Kuramoto N, Ohno Y, J Neurosci Res 2006 83 1179 89 10.1002/jnr.20824 16521124
87. Matrix metalloproteinases in the neocortex and spinal cord of amyotrophic lateral sclerosis patients. Lim GP, Backstrom JR, Cullen MJ, Miller CA, Atkinson RD, Tökés ZA, J Neurochem 1996 67 251 9 8666998
88. Matrix metalloproteinase-9 is elevated in serum of patients with amyotrophic lateral sclerosis. Beuche W, Yushchenko M, Mäder M, Maliszewska M, Felgenhauer K, Weber F, Neuroreport 2000 11 3419 22 10.1097/00001756- 200011090-00003 11095490
89. Matrix metalloproteinases and their tissue inhibitors in serum and cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Niebroj-Dobosz I, Janik P, Sokołowska B, Kwiecinski H, Eur J Neurol 2010 17 226 31 10.1111/j.1468-1331.2009.02775.x 19796283
90. Linking neuron and skin: matrix metalloproteinases in amyotrophic lateral sclerosis (ALS). Fang L, Huber-Abel F, Teuchert M, Hendrich C, Dorst J, J Neurol Sci 2009 285 62 6 10.1016/j.jns.2009.05.025 19523650
91. MMP-2 and MMP-9 are elevated in spinal cord and skin in a mouse model of ALS. Fang L, Teuchert M, Huber-Abel F, Schattauer D, Hendrich C, J Neurol Sci 2010 294 51 6 10.1016/j.jns.2010.04.005 20441996
92. The pro and the active form of matrix metalloproteinase-9 is increased in serum of patients with amyotrophic lateral sclerosis. Demestre M, Parkin-Smith G, Petzold A, Pullen AH, J Neuroimmunol 2005 159 146 54 10.1016/j.jneuroim.2004. 09.015 15652414
93. Matrix metalloproteinase-9 regulates TNF-alpha and FasL expression in neuronal, glial cells and its absence extends life in a transgenic mouse model of amyotrophic lateral sclerosis. Kiaei M, Kipiani K, Calingasan NY, Wille E, Chen J, Exp Neurol 2007 205 74 81 10.1016/j.expneurol.2007.01.036 17362932
94. The matrix metalloproteinases inhibitor Ro 28-2653 [correction of Ro 26-2853] extends survival in transgenic ALS mice. Lorenzl S, Narr S, Angele B, Krell HW, Gregorio J, Exp Neurol 2006 200 166 71 10.1016/j.expneurol.2006.01.026 16516196
95. Deletion of vitamin D receptor leads to premature emphysema/COPD by increased matrix metalloproteinase and lymphoid aggregates formation. Sundar I, Hwang J, Wu S, Sun J, Rahman I, Biochem Biophys Res Commun 2011 406 127 33 10.1016/j.bbrc.2011.02.011 21300024
96. Circulating MMP9, vitamin D and variation in the TIMP-1 response with VDR genotype: mechanisms for inflammatory damage in chronic disorders? Timms P, Mannan N, Hitman G, Q J Med 2002 95 787 96 10.1093/qjmed/95.12.787
97. Vitamin D regulation of metalloproteinase activity in matrix vesicles. Dean DD, Schwartz Z, Schmitz J, Muniz OE, Lu Y, Connect Tissue Res 1996 35 331 6 10.3109/03008209609029208 9084672
98. 1,25-dihydroxyvitamin D§ssub§3§esub§ dissociates production of interstitial collagenase and 92-kDa gelatinase in human mononuclear phagocytes. Lacraz S, Dayer J, Nicod L, Welgus H, J Biol Chem 1994 269 6485 90 7509804
99. Pathological roles of MAPK signaling pathways in human diseases. Kim EK, Choi EJ, Biochim Biophys Acta 1802 2010 396 405
100. Activated p38MAPK is a novel component of the intracellular inclusions found in human amyotrophic lateral sclerosis and mutant SOD1 transgenic mice. Bendotti C, Atzori C, Piva R, Tortarolo M, Strong MJ, J Neuropathol Exp Neurol 2004 63 113 9 14989597
101. Activation of the stress-activated MAP kinase, p38, but not JNK in cortical motor neurons during early presymptomatic stages of amyotrophic lateral sclerosis in transgenic mice. Holasek SS, Wengenack TM, Kandimalla KK, Montano C, Gregor DM, Brain Res 2005 1045 185 98 10.1016/j.brainres.2005.03.037 15910777
102. Persistent activation of p38 mitogen-activated protein kinase in a mouse model of familial amyotrophic lateral sclerosis correlates with disease progression. Tortarolo M, Veglianese P, Calvaresi N, Botturi A, Rossi C, Mol Cell Neurosci 2003 23 180 92 10.1016/S1044-7431(03)00022-8 12812752
103. Activation of the p38MAPK cascade is associated with upregulation of TNF alpha receptors in the spinal motor neurons of mouse models of familial ALS. Veglianese P, Lo Coco D, Bao Cutrona M, Magnoni R, Pennacchini D, Mol Cell Neurosci 2006 31 218 31 10.1016/j.mcn.2005.09.009 16219474
104. Inhibition of p38 mitogen activated protein kinase activation and mutant SOD1§ssup§G93A§esup§-induced motor neuron death. Dewil M, dela Cruz VF, Van Den Bosch L, Robberecht W, Neurobiol Dis 2007 26 332 41 10.1016/j.nbd.2006.12.023 17346981
105. p38 MAPK regulates calcium signal-mediated lipid accumulation through changing VDR expression in primary preadipocytes of mice. Sun C, Qi R, Wang L, Yan J, Wang Y, Mol Biol Rep 2012 39 3179 84 10.1007/s11033-011-1084-8 21701827
106. Vitamin D inhibits the activation of stress-activated protein kinases by physiological and environmental stresses in keratinocytes. Ravid A, Rubinstein E, Gamady A, Rotem C, Liberman UA, Koren R, J Endocrinol 2002 173 525 32 10.1677/joe.0.1730525 12065242
107. Vitamin D inhibits monocyte/macrophage proinflammatory cytokine production by targeting MAPK phosphatase-1. Zhang Y, Leung DY, Richers BN, Liu Y, Remigio LK, J Immunol 2012 188 2127 35 10.4049/jimmunol.1102412 22301548
108. Neuroprotective effects of (24R)-1,24-dihydroxycholecalciferol in human neuroblastoma SH-SY5Y cell line. Tetich M, Kutner A, Leskiewicz M, Budziszewska B, Lasoń W, J Steroid Biochem Mol Biol 2004 89-90 365 70 22154810
109. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Parr BA, Shea MJ, Vassileva G, McMahon AP, Development 1993 119 247 61 8275860
110. Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by beta-amyloid fibrils. Lorca RA, Chacón M, Barría MI, Inestrosa NC, Huidobro-Toro JP, Mol Psychiatry 2003 8 195 208 10.1038/sj.mp.4001208 12610652
111. The role of Wnt signaling in neuronal dysfunction in Alzheimer's Disease. Inestrosa NC, Toledo EM, Mol Neurodegener 2008 3 9 10.1186/1750-1326-3-9 18652670
112. Emerging roles of Wnts in the adult nervous system. Inestrosa NC, Arenas E, Nat Rev Neurosci 2010 11 77 86 10.1038/nrn2755 20010950
113. Wnt signaling pathway is involved in the pathogenesis of amyotrophic lateral sclerosis in adult transgenic mice. Chen Y, Guan Y, Zhang Z, Liu H, Wang S, Neurol Res 2012 34 390 9 22643084
114. Activation of the Wnt/β-catenin signaling pathway is associated with glial proliferation in the adult spinal cord of ALS transgenic mice. Chen Y, Guan Y, Liu H, Wu X, Yu L, Biochem Biophys Res Commun 2012 420 397 403 10.1016/j.bbrc.2012.03.006 22426476
115. Vitamin D§ssub§3§esub§ promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of beta-catenin signaling. Pálmer HG, González-Sancho JM, Espada J, Berciano MT, Puig I, J Cell Biol 2001 154 369 87 10.1083/jcb.200102028 11470825
116. Vitamin D and the regulation of Wnt/beta-catenin signaling and innate immunity in colorectal cancer. Byers S, Shah S, Nutr Rev 2007 65 118 20 10.1301/nr.2007.aug.S118-S120 17867386
117. Prostaglandin E2 is increased in amyotrophic lateral sclerosis patients. Iłzecka J, Acta Neurol Scand 2003 108 125 9 10.1034/j.1600-0404.2003. 00102.x 12859290
118. Increased levels of the pro-inflammatory prostaglandin PGE2 in CSF from ALS patients. Almer G, Teismann P, Stevic Z, Halaschek-Wiener J, Deecke L, Neurology 2002 58 1277 9 10.1212/WNL.58.8.1277 11971099
119. Expression and localization of cyclooxygenase-1 and -2 in human sporadic amyotrophic lateral sclerosis. Maihöfner C, Probst-Cousin S, Bergmann M, Neuhuber W, Neundörfer B, Heuss D, Eur J Neurosci 2003 18 1527 34 10.1046/j.1460-9568.2003.02879.x 14511332
120. The prostaglandin E§ssub§2§esub§ EP§ssub§ 2§esub§ receptor accelerates disease progression and inflammation in a model of amyotrophic lateral sclerosis. Liang X, Wang Q, Shi J, Lokteva L, Breyer RM, Ann Neurol 2008 64 304 14 10.1002/ana.21437 18825663
121. Expression of microsomal prostaglandin E synthase-1 in the spinal cord in a transgenic mouse model of amyotrophic lateral sclerosis. Miyagishi H, Kosuge Y, Ishige K, Ito Y, J Pharmacol Sci 2012 118 225 36 10.1254/jphs.11221FP 22302024
122. Concurrent blockade of free radical and microsomal prostaglandin E synthase-1-mediated PGE2 production improves safety and efficacy in a mouse model of amyotrophic lateral sclerosis. Shin JH, Lee YA, Lee JK, Lee YB, Cho W, J Neurochem 2012 122 952 61 10.1111/j.1471-4159.2012.07771.x 22537108
123. Marked increase in cyclooxygenase-2 in ALS spinal cord: implications for therapy. Yasojima K, Tourtellotte WW, McGeer EG, McGeer PL, Neurology 2001 57 952 6 11571316
124. Increased expression of neuronal cyclooxygenase-2 in the hippocampus in amyotrophic lateral sclerosis both with and without dementia. Yokota O, Terada S, Ishizu H, Ishihara T, Nakashima H, Acta Neuropathol 2004 107 399 405 10.1007/s00401-004-0826-2 14991384
125. Induction of cyclooxygenase-2 in reactive glial cells by the CD40 pathway: relevance to amyotrophic lateral sclerosis. Okuno T, Nakatsuji Y, Kumanogoh A, Koguchi K, Moriya M, J Neurochem 2004 91 404 12 10.1111/j.1471-4159.2004.02727.x 15447673
126. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Drachman DB, Frank K, Dykes-Hoberg M, Teismann P, Almer G, Ann Neurol 2002 52 771 8 10.1002/ana.10374 12447931
127. Integrative role of cPLA with COX-2 and the effect of non-steriodal anti-inflammatory drugs in a transgenic mouse model of amyotrophic lateral sclerosis. Kiaei M, Kipiani K, Petri S, Choi DK, Chen J, J Neurochem 2005 93 403 11 10.1111/j.1471-4159.2005.03024.x 15816863
128. Association between bone mineral density and the use of nonsteroidal anti-inflammatory drugs and aspirin: impact of cyclooxygenase selectivity. Carbone LD, Tylavsky FA, Cauley JA, Harris TB, Lang TF, J Bone Miner Res 2003 18 1795 802 10.1359/jbmr.2003.18.10.1795 14584890
129. Regulation of prostaglandin metabolism by calcitriol attenuates growth stimulation in prostate cancer cells. Moreno J, Krishnan AV, Swami S, Nonn L, Peehl DM, Feldman D, Cancer Res 2005 65 7917 25 16140963
130. 1,25-Dihydroxyvitamin D§ssub§3§esub§ pretreatment limits prostaglandin biosynthesis by cytokine-stimulated adult human osteoblast-like cells. Keeting PE, Li CH, Whipkey DL, Thweatt R, Xu J, J Cell Biochem 1998 68 237 46 10.1002/(SICI)1097-4644(19980201)68:2<237::AID- JCB10>3.0.CO;2-C 9443079
131. Selective inhibition of cyclooxygenase-2 (COX-2) by 1 α,25-dihydroxy- 16-ene-23-yne-vitamin D§ssub§3§esub§, a less calcemic vitamin D analog. Aparna R, Subhashini J, Roy KR, Reddy GS, Robinson M, J Cell Biochem 2008 104 1832 42 10.1002/jcb.21749 18348265
132. 1,25-dihydroxyvitamin D§ssub§3§esub§ induces NAD§ssup§+§esup§-dependent 15-hydroxyprostaglandin dehydrogenase in human neonatal monocytes. Pichaud F, Roux S, Frendo JL, Delage-Mourroux R, Maclouf J, Blood 1997 89 2105 12 9058733
133. Prostaglandin E1 increases in vivo and in vitro calcitriol biosynthesis in rabbits. Velásquez-Forero F, García P, Triffitt JT, Llach F, Prostaglandins Leukot Essent Fatty Acids 2006 75 107 15 10.1016/j.plefa.2006.03. 011 16876395
134. Oxidative stress biomarkers in sporadic ALS. Mitsumoto H, Santella RM, Liu X, Bogdanov M, Zipprich J, Amyotroph Lateral Scler 2008 9 177 83 10.1080/17482960801933942 18574762
135. Increased reactive oxygen species in familial amyotrophic lateral sclerosis with mutations in SOD1. Said Ahmed M, Hung WY, Zu JS, Hockberger P, Siddique T, J Neurol Sci 2000 176 88 94 10.1016/S0022-510X(00)00317-8 10930589
136. The roles of free radicals in amyotrophic lateral sclerosis: reactive oxygen species and elevated oxidation of protein, DNA, and membrane phospholipids. Liu D, Wen J, Liu J, Li L, FASEB J 1999 13 2318 28 10593879
137. Decrease in Cu/Zn- and Mn-superoxide dismutase activities in brain and spinal cord of patients with amyotrophic lateral sclerosis. Uchino M, Ando Y, Tanaka Y, Nakamura T, Uyama E, J Neurol Sci 1994 127 61 7 10.1016/0022-510X(94) 90136-8 7699393
138. Low levels of ALS-linked Cu/Zn superoxide dismutase increase the production of reactive oxygen species and cause mitochondrial damage and death in motor neuron-like cells. Rizzardini M, Mangolini A, Lupi M, Ubezio P, Bendotti C, Cantoni L, J Neurol Sci 2005 232 95 103 10.1016/j.jns.2005.02.004 15850589
139. Overexpression of manganese superoxide dismutase attenuates neuronal death in human cells expressing mutant (G37R) Cu/Zn-superoxide dismutase. Flanagan SW, Anderson RD, Ross MA, Oberley LW, J Neurochem 2002 81 170 7 10.1046/j.1471-4159.2002.00812.x 12067230
140. Mutant SOD1-induced neuronal toxicity is mediated by increased mitochondrial superoxide levels. Zimmerman MC, Oberley LW, Flanagan SW, J Neurochem 2007 102 609 18 10.1111/j.1471-4159.2007.04502.x 17394531
141. Increase in oxidized NO products and reduction in oxidized glutathione in cerebrospinal fluid from patients with sporadic form of amyotrophic lateral sclerosis. Tohgi H, Abe T, Yamazaki K, Murata T, Ishizaki E, Isobe C, Neurosci Lett 1999 260 204 6 10.1016/S0304-3940(98)00986-0 10076903
142. Depletion of reduced glutathione enhances motor neuron degeneration in vitro and in vivo. Chi L, Ke Y, Luo C, Gozal D, Liu R, Neuroscience 2007 144 991 1003 10.1016/j.neuroscience.2006.09.064 17150307
143. - 1 alpha,25 Dihydroxyvitamin D§ssub§3§esub§ and mononuclear phagocytes: enhancement of mouse macrophage and human monocyte hydrogen peroxide production without alteration of tumor cytolysis. Gluck WL, Weinberg JB, J Leukoc Biol 1987 42 498 503 3119753
144. 1,25-Dihydroxyvitamin D§ssub§3§esub§ activates secretion of hydrogen peroxide by human monocytes. Cohen MS, Mesler DE, Snipes RG, Gray TK, J Immunol 1986 136 1049 53 3079794
145. Effect of 1,25-dihydroxyvitamin D§ssub§3§esub§, lipopolysaccharide, or lipoteichoic acid on the expression of NADPH oxidase components in cultured human monocytes. Levy R, Malech HL, J Immunol 1991 147 3066 71 1655903
146. Protective role of 1α, 25-dihydroxyvitamin D§ssub§3§ esub§ against oxidative stress in nonmalignant human prostate epithelial cells. Bao BY, Ting HJ, Hsu JW, Lee YF, Int J Cancer 2008 122 2699 2706 10.1002/ijc.23460 18348143
147. Vitamin D metabolites and analogs induce lipoxygenase mRNA expression and activity as well as reactive oxygen species (ROS) production in human bone cell line. Somjen D, Katzburg S, Grafi-Cohen M, Knoll E, Sharon O, Posner GH, J Steroid Biochem Mol Biol 2011 123 85 89 10.1016/j.jsbmb.2010.11.010 21111046
148. 1,25-dihydroxyvitamin D§ssub§3§esub§ regulates the synthesis of γ-glutamyl transpeptidase and glutathione levels in rat primary astrocytes. Garcion E, Sindji L, Leblondel G, Brachet P, Darcy F, J Neurochem 1999 73 859 66 10428085
149. Cu/Zn superoxide dismutase (SOD1) mutations associated with familial amyotrophic lateral sclerosis (ALS) affect cellular free radical release in the presence of oxidative stress. Cookson MR, Menzies FM, Manning P, Eggett CJ, Figlewicz DA, Amyotroph Lateral Scler Other Motor Neuron Disord 2002 3 75 85 12215229
150. Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. Almer G, Vukosavic S, Romero N, Przedborski S, J Neurochem 1999 72 2415 25 10349851
151. 1-α,25-Dihydroxyvitamin D§ssub§3§esub§ regulates inducible nitric oxide synthase messenger RNA expression and nitric oxide release in macrophage-like RAW264.7 cells. Chang JM, Kuo MC, Kuo HT, Hwang SJ, Tsai JC, J Lab Clin Med 2004 143 14 22 10.1016/j.lab.2003.08.002 14749681
152. 1,25-Dihydroxyvitamin D§ssub§3§esub§ inhibits the expression of inducible nitric oxide synthase in rat central nervous system during experimental allergic encephalomyelitis. Garcion E, Nataf S, Berod A, Darcy F, Brachet P, Brain Res Mol Brain Res 1997 45 255 67 10.1016/S0169- 328X(96)00260-4 9149100
153. 1,25-Dihydroxyvitamin D§ssub§3§esub§ inhibits lipopolysaccharide-induced immune activation in human endothelial cells. Equils O, Naiki Y, Shapiro AM, Michelsen K, Lu D, Clin Exp Immunol 2006 143 58 64 10.1111/j.1365-2249.2005.02961.x 16367934
154. Vitamin D insufficiency is associated with impaired vascular endothelial and smooth muscle function and hypertension in young rats. Tare M, Emmett SJ, Coleman HA, Skordilis C, Eyles DW, J Physiol 2011 589 4777 86 10.1113/jphysiol.2011.214726 21807617