A new mechanism for amyloid-β induction of iNOS: Vitamin D-VDR pathway disruption

Journal of Alzheimer's Disease

Volumn 36, Issue 3, 2013, Pages 459-474

  Dursun, Erdinç ^a   Gezen Ak, Duygu ^a   Yilmazer, Selma ^a  

^a ISTANBUL UNIVERSITY   (Turkey)

Author keywords

1,25 MARRS; Alzheimer's disease; amyloid beta; iNOS; VDR; vitamin D

Indexed keywords

AMYLOID BETA PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; STEROID BINDING PROTEIN; VITAMIN D; VITAMIN D RECEPTOR;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; VITAMIN SUPPLEMENTATION;

EID: 84881460365     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-130416     Document Type: Article

References (60)

1. Hardy J (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci 20, 154-159
2. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356
3. Nathan C, Calingasan N, Nezezon J, Ding A, Lucia MS, La Perle K, Fuortes M, Lin M, Ehrt S, Kwon NS, Chen J, Vodovotz Y, Kipiani K, Beal MF (2005) Protection from Alzheimer's-like disease in the mouse by genetic ablation of inducible nitric oxide synthase. J Exp Med 202, 1163-1169
4. WalshDM,Selkoe DJ (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44, 181-193
5. Moore AH, O'Banion MK (2002) Neuroinflammation and anti-inflammatory therapy for Alzheimer's disease. Adv Drug Deliv Rev 54, 1627-1656
6. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom, P EM, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti, G P-SC, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21, 383-421
7. Lee YB, Nagai A, Kim SU (2002) Cytokines, chemokines and cytokine receptors in human microglia. J Neurosci Res 69, 94-103
8. Luth HJ, Munch G, Arendt T (2002) Aberrant expression of NOS isoforms in Alzheimer's disease is structurally related to nitrotyrosine formation. Brain Res 953, 135-143
9. Fernandez-Vizarra P, Fernandez AP, Castro-Blanco S, Encinas JM, Serrano J, Bentura ML, Munoz P, Martinez-Murillo R, Rodrigo J (2004) Expression of nitric oxide system in clinically evaluated cases of Alzheimer's disease. Neurobiol Dis 15, 287-305
10. Heneka MT, Wiesinger H, Dumitrescu-Ozimek L, Riederer P, Feinstein DL, Klockgether T (2001) Neuronal and glial coexpression of argininosuccinate synthetase and inducible nitric oxide synthase in Alzheimer disease. J Neuropathol Exp Neurol 60, 906-916
11. Wong A, Luth HJ, Deuther-Conrad W, Dukic-Stefanovic S, Gasic-Milenkovic J, Arendt T, Munch G (2001) Advanced glycation endproducts co-localize with inducible nitric oxide synthase in Alzheimer's disease. Brain Res 920, 32-40
12. Lee SC, Zhao ML, Hirano A, Dickson DW (1999) Inducible nitric oxide synthase immunoreactivity in the Alzheimer disease hippocampus: Association with Hirano bodies, neurofibrillary tangles, and senile plaques. J Neuropathol Exp Neurol 58, 1163-1169
13. Brown GC (2007) Mechanisms of inflammatory neurodegeneration: INOS and NADPH oxidase. Biochem Soc Trans 35, 1119-1121
14. Bal-Price A, Brown GC (2001) Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J Neurosci 21, 6480-6491
15. Jekabsone A, Neher JJ, Borutaite V, Brown GC (2007) Nitric oxide from neuronal nitric oxide synthase sensitises neurons to hypoxia-induced death via competitive inhibition of cytochrome oxidase. J Neurochem 103, 346-356
16. (1982) IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN): Nomenclature of vitamin D. Recommendations 1981. Eur J Biochem 124, 223-227
17. Oudshoorn C, Mattace-Raso FUS, van der Velde N, Colin EM, van der Cammen TJM (2008) Higher serum vitamin D3 levels are associated with better cognitive test performance in patients with alzheimer's disease. Dement Geriatr Cogn Disord 25, 539-543
18. Annweiler C, Schott AM, Allali G, Bridenbaugh SA, Kressig RW, Allain P, Herrmann FR, Beauchet O (2010) Association of vitamin D deficiency with cognitive impairment in older women: Cross-sectional study. Neurology 74, 27-32
19. Cherniack EP, Florez H, Roos BA, Troen BR, Levis S (2008) Hypovitaminosis D in the elderly: From bone to brain. J Nutr Health Aging 12, 366-373
20. Evatt ML, DeLong MR, Khazai N, Rosen A, Triche S, Tangpricha V (2008) Prevalence of vitamin D insufficiency in patients with Parkinson disease and Alzheimer disease. Arch Neurol 65, 1348-1352
21. Llewellyn DJ, Langa KM, Lang IA (2009) Serum 25-hydroxyvitamin D concentration and cognitive impairment. J Geriatr Psychiatry Neurol 22, 188-195
22. Llewellyn DJ, Lang IA, LangaKM, Muniz-Terrera G, Phillips CL, Cherubini A, Ferrucci L, Melzer D (2010) Vitamin D and risk of cognitive decline in elderly persons. Arch Intern Med 170, 1135-1141
23. McCann J, Ames BN (2008) Is there convincing biological or behavioral evidence linking vitamin D deficiency to brain dysfunction? FASEB J 22, 982-1001
24. Wilkins CH, Sheline YI, Roe CM, Birge SJ, Morris JC (2006) Vitamin D deficiency is associated with low mood and worse cognitive performance in older adults. Am J Geriat Psychiat 14, 1032-1040
25. Chabas JF, Alluin O, Rao G, Garcia S, Lavaut MN, Risso JJ, Legre R, Magalon G, Khrestchatisky M, Marqueste T, Decherchi P, Feron F (2008) Vitamin D2 potentiates axon regeneration. J Neurotrauma 25, 1247-1256
26. Dursun E, Gezen-Ak D, Yilmazer S (2011) A novel perspective for Alzheimer's disease: Vitamin D receptor suppression by amyloid- and preventing the amyloid-β induced alterations by vitamin D in cortical neurons. J Alzheimers Dis 23, 207-219
27. Yu J, Gattoni-Celli M, Zhu H, Bhat NR, Sambamurti K, Gattoni-Celli S, Kindy MS (2011) Vitamin D3-enriched diet correlates with a decrease of amyloid plaques in the brain of A-PP transgenic mice. J Alzheimers Dis 25, 295-307
28. Gezen-Ak D, Dursun E, Yilmazer S (2011) The effects of vitamin D receptor silencing on the expression of LVSCCA1C and LVSCC-A1D and the release of NGF in cortical neurons. PLOS ONE 6, e17553
29. Masoumi A, Goldenson B, Ghirmai S, Avagyan H, Zaghi J, Abel K, Zheng X, Espinosa-Jeffrey A, Mahanian M, Liu PT, Hewison M, Mizwickie M, Cashman J, Fiala M (2009) 1alpha,25-dihydroxyvitamin D3 interacts with curcuminoids to stimulate amyloid-beta clearance by macrophages of Alzheimer's disease patients. J Alzheimers Dis 17, 703-717
30. Mizwicki MT, Menegaz D, Zhang J, Barrientos-Durán A, Tse S, Cashman JR, Griffin PR, Fiala M (2011) Genomic and nongenomic signaling induced by 1β,25(OH)2-vitamin D3 promotes the recovery of amyloid-β phagocytosis by Alzheimer's disease macrophages. J Alzheimers Dis 29, 51-62
31. Fiala M, Mizwicki MT (2011) Neuroprotective and immune effects of active forms of vitamin D3 and docosahexaenoic acid in Alzheimer disease patients. Funct Foods Health Dis 12, 545-554
32. Gezen-Ak D, Dursun E,Yilmazer S (2012) Vitamin D inquiry in hippocampal neurons: Consequences of vitamin D-VDR pathway disruption on calcium channel and the vitamin D requirement. Neurol Sci, doi: 10.1007/s10072-10012-11268-10076
33. Gezen-Ak D, Dursun E, Ertan T, Hanagasi H, Gurvit H, Emre M, Eker E, Ozturk M, Engin F, Yilmazer S (2007) Association between vitamin D receptor gene polymorphism and Alzheimer's disease. Tohoku J Exp Med 212, 275-282
34. Kuningas M, Mooijaart SP, Jolles J, Slagboom PE, Westendorp RGJ, Van Heemst D(2009) VDR gene variants associate with cognitive function and depressive symptoms in old age. Neurobiol Aging 30, 466-473
35. Beydoun MA, Ding EL, Beydoun HA, Tanaka T, Ferrucci L, Zonderman AB (2012) Vitamin D receptor and megalin gene polymorphisms and their associations with longitudinal cognitive change in US adults. Am J Clin Nutr 95, 163-178
36. Lehmann DJ, Refsum H, Warden DR, Medway C, Wilcock GK, Smith DA (2011) The vitamin D receptor gene is associated with Alzheimer's disease. Neurosci Let 504, 79-82
37. Beecham GW, Martin ER, Li YJ, Slifer MA, Gilbert JR, Haines JL, Pericak-Vance MA (2009) Genome-wide association study implicates a chromosome 12 risk locus for late-onset Alzheimer disease. Am J Hum Genet 84, 35-43
38. ButlerMW, Burt A, Edwards TL, Zuchner S, Scott WK,Martin ER, Vance JM,Wang L (2011) Vitamin D receptor gene as a candidate gene for Parkinson disease. Ann Hum Genet 75, 201-210
39. Gezen-Ak D, Dursun E, Bilgiç B, Hanaǧasi H, Ertan T,Gürvit H, Emre M, Eker E, Ulutin T, Uysal Ö, Yilmazer S (2012) Vitamin D receptor gene haplotype is associated with lateonset Alzheimer's disease. Tohoku J Exp Med 228, 189-196
40. Fleet JC (2004) Rapid, membrane-initiated actions of 1,25dihydroxyvitamin D: What are they and what do they mean? J Nutr 134, 3215-3218
41. Erickson RR, Dunning LM, Olson DA, Cohen SJ, Davis AT, Wood WG, Kratzke RA, Holtzman JL (2005) In cerebrospinal fluid ER chaperones ERp57 and calreticulin bind beta-Amyloid. Biochem Biophys Res Commun 332, 50-57
42. Tohda C, Urano T, Umezaki M, Nemere I, Kuboyama T (2012) Diosgenin is an exogenous activator of 1,25D3-MARRS/Pdia3/ERp57 and improves Alzheimer's disease pathologies in 5XFAD mice. Sci Rep 2, 535
43. Price P, Brewer GJ (1998) Serum-free media for neural cell cultures. In Protocols for Neural Cell Culture, Fedoroff S, Richardson A, ed. Humana Press, New Jersey, pp. 255-264
44. Brewer LD, Thibault V, Chen KC, Langub MC, Landfield PW, Porter NM (2001) Vitamin D hormone confers neuroprotection in parallel with downregulation of L-type calcium channel expression in hippocampal neurons. J Neurosci 21, 98-108
45. Nolan T, Hands BE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protocol 1, 1556-1582
46. Tuppo EE, Arias HR (2005) The role of inflammation in Alzheimer's disease. Int J Biochem Cell Biol 37, 289-305
47. Rogers J, Lue LF (2001) Microglial chemotaxis, activation, and phagocytosis of amyloid β-peptide as linked phenomena in Alzheimer's disease. Neurochem Int 39, 333-340
48. Dursun E, Gezen-Ak D, Ertan T, Bilgiç B, Gürvit H, Emre M, Eker E, Engin F, Uysal Ö, Yilmazer S (2009) Interleukin-1β-889 C/T polymorphism in Turkish patients with late-onset Alzheimer's disease. Dement Geriatr Cogn Disord 27, 82-87
49. Akama KT, Van Eldik LJ (2000) Beta-Amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1beta-And tumor necrosis factor-Alpha (TNFalpha)-dependent, and involves a TNFalpha receptorassociated factor-And NFkappaB-inducing kinase-dependent signaling mechanism. J Biol Chem 275, 7918-7924
50. Vodovotz Y, Lucia MS, Flanders KC, Chesler L, Xie QW, Smith TW, Weidner J, Mumford R, Webber R, Nathan C, Roberts AB, Lippa CF, Sporn MB (1996) Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease. J Exp Med 184, 1425-1433
51. Garcion E, Sindji L, Montero-Menei C, Andre C, Brachet P, Darcy F (1998) Expression of inducible nitric oxide synthase during rat brain inflammation: Regulation by 1,25-dihydroxyvitamin D3. Glia 22, 282-294
52. Garcion E, Nataf S, Berod A, Darcy F, Brachet P (1997) 1,25-Dihydroxyvitamin D3 inhibits the expression of inducible nitric oxide synthase in rat central nervous system during experimental allergic encephalomyelitis. Brain Res Mol Brain Res 45, 255-267
53. Chang JM, Kuo MC, Kuo HT, Hwang SJ, Tsai JC, Chen HC, Lai YH (2004) 1-Alpha,25-Dihydroxyvitamin D3 regulates inducible nitric oxide synthase messenger RNA expression and nitric oxide release in macrophage-like RAW264.7 cells. J Lab Clin Med 143, 14-22
54. Neveu I, Naveilhan P, Menaa C, Wion D, Brachet P, Garab́ edianM(1994) Synthesis of 1,25-dihydroxyvitamin D3 by rat brain macrophages in vitro. J Neurosci Res 38, 214-220
55. Moon M, Song H, Hong HJ, Nam DW, Cha MY, Oh MS, Yu. J, Hoon R, Mook-Jung I (2013) Vitamin D-binding protein interacts withAβand suppressesAβ- mediated pathology. Cell Death Differ 20, 630-638
56. Willems HM, van den Heuvel EG, Carmeliet G, Schaafsma A, Klein-Nulend J, Bakker AD (2012) VDR dependent and independent effects of 1,25-dihydroxyvitamin D3 on nitric oxide production by osteoblasts. Steroids 77, 126-131
57. Dursun E, Gezen-Ak D,Yilmazer S (2013) Beta amyloid suppresses the expression of the vitamin D receptor gene and induces the expression of the vitamin D catabolic enzyme gene in hippocampal neurons. Dement Geriatr Cogn Disord, doi: 10.1159-000350319
58. Thota C, Farmer T, Garfield RE, Menon R, Al-Hendy A (2013) Vitamin D elicits anti-inflammatory response, inhibits contractile-Associated proteins, and modulates toll-like receptors in human myometrial cells. Reprod Sci 20, 463-475
59. Fernandes de Abreu DA, Eyles D, F́eron F (2009) Vitamin D, a neuro-immunomodulator: Implications for neurodegenerative and autoimmune diseases. Psychoneuroendocrinology 34, 265-277
60. Liu PT, Krutzik SR, Modlin RL (2007) Therapeutic implications of the TLR and VDR partnership. Trends Mol Med 13, 117-124