Common polymorphisms in nitric oxide synthase (NOS) genes influence quality of aging and longevity in humans

Biogerontology

Volumn 14, Issue 2, 2013, Pages 177-186

  Montesanto, Alberto ^a   Crocco, Paolina ^a   Tallaro, Federica ^a   Pisani, Francesca ^a   Mazzei, Bruno ^b   Mari, Vincenzo ^b   Corsonello, Andrea ^b   Lattanzio, Fabrizia ^b   Passarino, Giuseppe ^a   Rose, Giuseppina ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b INRCA   (Italy)

Author keywords

Aging; Longevity; Nitric oxide; NOS; Polymorphisms

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ADULT; AGED; AGING; ARTICLE; COGNITION; CONTROLLED STUDY; DAILY LIFE ACTIVITY; DEPRESSION; EPISODIC MEMORY; EXON; FEMALE; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GERIATRIC DEPRESSION SCALE; HUMAN; LONGEVITY; MAJOR CLINICAL STUDY; MALE; MINI MENTAL STATE EXAMINATION; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; QUALITY OF LIFE; SINGLE NUCLEOTIDE POLYMORPHISM;

ACTIVITIES OF DAILY LIVING; ADULT; AGED; AGED, 80 AND OVER; AGING; CASE-CONTROL STUDIES; COGNITION; DEPRESSION; FEMALE; GERIATRIC ASSESSMENT; HUMANS; LONGEVITY; MALE; MIDDLE AGED; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84878615236     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-013-9421-z     Document Type: Article

References (67)

1. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265
2. Beckman JS, Koppenol WH (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271:C1424-C1437
3. Bros M, Boissel JP, Gödtel-Armbrust U, Förstermann U (2006) Transcription of human neuronal nitric oxide synthase mRNAs derived from different first exons is partly controlled by exon 1-specific promoter sequences. Genomics 87:463-473
4. Brown GC (2010) Nitric oxide and neuronal death. Nitric Oxide 23:153-165
5. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 8:766-775
6. Calcerrada P, Peluffo G, Radi R (2011) Nitric oxide-derived oxidants with a focus on peroxynitrite: molecular targets, cellular responses and therapeutic implications. Curr Pharm Des 17:3905-3932
7. Calle ML, Urrea V, Malats N, Van Steen K (2010) mbmdr: an R package for exploring gene-gene interactions associated with binary or quantitative traits. Bioinformatics 26:2198-2199
8. Cau SB, Carneiro FS, Tostes RC (2012) Differential modulation of nitric oxide synthases in aging: therapeutic opportunities. Front Physiol 3:218
9. Colas D, Gharib A, Bezin L, Morales A, Guidon G, Cespuglio R, Sarda N (2006) Regional age-related changes in neuronal nitric oxide synthase (nNOS), messenger RNA levels and activity in SAMP8 brain. BMC Neurosci 7:81
10. De Rango F, Montesanto A, Berardelli M, Mazzei B, Mari V, Lattanzio F, Corsonello A, Passarino G (2011) To grow old in southern Italy: a comprehensive description of the old and oldest old in Calabria. Gerontology 57:327-334
11. Dere E, De Souza Silva MA, Topic B, Fiorillo C, Li JS, Sadile AG, Frisch C, Huston JP (2002) Aged endothelial nitric oxide synthase knockout mice exhibit higher mortality concomitant with impaired open-field habituation and alterations in forebrain neurotransmitter levels. Genes Brain Behav 1:204-213
12. Domek-Łopacińska KU, Strosznajder JB (2010) Cyclic GMP and nitric oxide synthase in aging and Alzheimer's disease. Mol Neurobiol 41:129-137
13. Drew B, Leeuwenburgh C (2002) Aging and the role of reactive nitrogen species. Ann NY Acad Sci 959:66-81
14. Elfering SL, Sarkela TM, Giulivi C (2000) Biochemistry of mitochondrial nitric-oxide synthase. J Biol Chem 277:38079-38086
15. Feil R, Kleppisch T (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 184:529-560
16. Finocchietto PV, Franco MC, Holod S, Gonzalez AS, Converso DP, Arciuch VG, Serra MP, Poderoso JJ, Carreras MC (2009) Mitochondrial nitric oxide synthase: a masterpiece of metabolic adaptation, cell growth, transformation, and death. Exp Biol Med (Maywood) 234:1020-1028
17. Folstein MF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198
18. Förstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. Eur Heart J 33:829-837
19. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA (2001) Cardiovascular health study collaborative research group. Frailty in older adults: evidence for a phenotype. J Gerontol A 56:M146-M156
20. Gałecki P, Maes M, Florkowski A, Lewiński A, Gałecka E, Bienkiewicz M, Szemraj J (2011) Association between inducible and neuronal nitric oxide synthase polymorphisms and recurrent depressive disorder. J Affect Disord 129:175-182
21. Garthwaite J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27:2783-2802
22. Grigoletto F, Zappalà G, Anderson DW, Lebowitz BD (1999) Norms for the mini-mental state examination in a healthy population. Neurology 53:315-320
23. Hall DT, Ma JF, Marco SD, Gallouzi IE (2011) Inducible nitric oxide synthase (iNOS) in muscle wasting syndrome, sarcopenia, and cachexia. Aging (Albany NY) 3:702-715
24. Han S, Rudd JA, Hu ZY, Zhang L, Yew DT, Fang M (2010) Analysis of neuronal nitric oxide synthase expression and increasing astrogliosis in the brain of senescence-accelerated-prone 8 mice. Int J Neurosci 120:602-608
25. Hancock DB, Martin ER, Vance JM, Scott WK (2008) Nitric oxide synthase genes and their interactions with environmental factors in Parkinson's disease. Neurogenetics 9:249-262
26. Ibarrola-Villava M, Peña-Chilet M, Fernandez LP, Aviles JA, Mayor M, Martin-Gonzalez M, Gomez-Fernandez C, Casado B, Lazaro P, Lluch A, Benitez J, Lozoya R, Boldo E, Pizarro A, Martinez-Cadenas C, Ribas G (2011) Genetic polymorphisms in DNA repair and oxidative stress pathways associated with malignant melanoma susceptibility. Eur J Cancer 47:2618-2625
27. Jung J, Na C, Huh Y (2012) Alterations in nitric oxide synthase in the aged CNS. Oxid Med Cell Longev 2012:718976
28. Kader KN, Akella R, Ziats NP, Lakey LA, Harasaki H, Ranieri JP, Bellamkonda RV (2000) eNOS-overexpressing endothelial cells inhibit platelet aggregation and smooth muscle cell proliferation in vitro. Tissue Eng 6:241-251
29. Kanski J, Hong SJ, Schöneich C (2005) Proteomic analysis of protein nitration in aging skeletal muscle and identification of nitrotyrosine- containing sequences in vivo by nanoelectrospray ionization tandem mass spectrometry. J Biol Chem 280:24261-24266
30. Katz S, Downs TD, Cash HR, Grotz RC (1970) Progress in development of the index of ADL. Gerontologist 10:20-30
31. Kawamoto EM, Vasconcelos AR, Degaspari S, Böhmer AE, Scavone C et al (2012) Age-related changes in nitric oxide activity, cyclic GMP, and TBARS levels in platelets and erythrocytes reflect the oxidative status in central nervous system. Age (Dordr) 35(2):331-342
32. Kim CH, Zou Y, Kim DH, Kim ND, Yu BP, Chung HY (2006) Proteomic analysis of nitrated and 4-hydroxy-2- nonenal-modified serum proteins during aging. J Gerontol A 61:332-338
33. Kirchner L, Weitzdoerfer R, Hoeger H, Url A, Schmidt P, Engelmann M, Villar SR, Fountoulakis M, Lubec G, Lubec B (2004) Impaired cognitive performance in neuronal nitric oxide synthase knockout mice is associated with hippocampal protein derangements. Nitric Oxide 11:316-330
34. Law A, O'Donnell J, Gauthier S, Quirion R (2002) Neuronal and inducible nitric oxide synthase expressions and activities in the hippocampi and cortices of young adult, aged cognitively unimpaired, and impaired Long-Evans rats. Neuroscience 112:267-275
35. Le Gouill E, Jimenez M, Binnert C, Pierre-Yves J, Thalmann S, Nicod P, Scherrer U, Vollenweider P (2007) eNOS knock-out mice have defective mitochondrial beta-oxidation. Diabetes 56:2690-2696
36. Liaudet L, Soriano FG, Szabó C (2000) Biology of nitric oxide signaling. Crit Care Med 28:N37-N52
37. Lòpez LC, Escames G, Tapias V, Utrilla P, Leo′n J, Acuna-Castroviejo D (2006) Identification of an inducible nitric oxide synthase in diaphragm mitochondria from septic mice: its relation with mitochondrial dysfunction and prevention by melatonin. Int J Biochem Cell Biol 38:267-278
38. Maes M, Yirmyia R, Noraberg J, Brene S, Hibbeln J, Perini G, Kubera M, Bob P, Lerer B, Maj M (2009) The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab Brain Dis 24:27-53
39. McCann SM, Licinio J, Wong ML, Yu WH, Karanth S, Rettori V (1998) The nitric oxide hypothesis of aging. Exp Gerontol 33:813-826
40. Moilanen E, Moilanen T, Knowles R, Charles I, Kadoya Y, Al-Saffar N, Revell PA, Moncada S (1997) Nitric oxide synthase is expressed in human macrophages during foreign body inflammation. Am J Pathol 150:881-887
41. Moncada S, Higgs EA (2006) The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 147:S193-S201
42. Montesanto A, Lagani V, Martino C, Dato S, De Rango F, Berardelli M, Corsonello A, Mazzei B, Mari V, Lattanzio F, Conforti D, Passarino G (2010) A novel population-specific approach to define frailty. Age (Dordr) 32(3):385-395
43. Napoli C, Ignarro LJ (2009) Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res 32:1103-1108
44. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Carruba MO (2003) Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299:896-899
45. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310:314-317
46. Oess S, Icking A, Fulton D, Govers R, Müller-Esterl W (2006) Subcellular targeting and trafficking of nitric oxide synthases. Biochem J 396:401-409
47. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424
48. Passarino G, Montesanto A, Dato S, Giordano S, Domma F, Mari V, Feraco E, De Benedictis G (2006) Sex and age specificity of susceptibility genes modulating survival at old age. Hum Hered 62:213-220
49. Paul V, Ekambaram P (2011) Involvement of nitric oxide in learning & memory processes. Indian J Med Res 133:471-478
50. Reif A, Grünblatt E, Herterich S, Wichart I, Rainer MK, Jungwirth S, Danielczyk W, Deckert J, Tragl KH, Riederer P, Fischer P (2011a) Association of a functional NOS1 promoter repeat with Alzheimer's disease in the VITA cohort. J Alzheimers Dis 23:327-333
51. Reif A, Schecklmann M, Eirich E, Jacob CP, Jarczok TA, Kittel-Schneider S, Lesch KP, Fallgatter AJ, Ehlis AC (2011b) A functional promoter polymorphism of neuronal nitric oxide synthase moderates prefrontal functioning in schizophrenia. J Neuropsychopharmacol 14:887-897
52. Sheikh JI, Yesavage JA (1986) Geriatric Depression Scale (GDS): recent evidence and development of a shorter version. Clinical gerontology: a guide to assessment and intervention. Haworth, New York, pp 165-173
53. So HC, Sham PC (2011) Robust association tests under different genetic models, allowing for binary or quantitative traits and covariates. Behav Genet 41:768-775
54. Strosznajder JB, JeÅko H, Zambrzycka A, Eckert A, Chalimoniuk M (2004) Age-related alteration of activity and gene expression of endothelial nitric oxide synthase in different parts of the brain in rats. Neurosci Lett 370:175-179
55. Taddei S, Virdis A, Ghiadoni L (2001) Age-related reduction of NO availability and oxidative stress in humans. Hypertension 38:274-279
56. Toprakci M, Ozmen D, Mutaf I, Turgan N, Parildar Z, Habif S, Guner I, Bayindir O (2000) Age-associated changes in nitric oxide metabolites nitrite and nitrate. Int J Clin Lab Res 30:83-85
57. Torregrossa AC, Aranke M, Bryan NS (2011) Nitric oxide and geriatrics: implications in diagnostics and treatment of the elderly. J Geriatr Cardiol 8:230-242
58. Tsutsui M, Shimokawa H, Otsuji Y, Ueta Y, Sasaguri Y, Yanagihara N (2009) Nitric oxide synthases and cardiovascular diseases: insights from genetically modified mice. Circ J 73:986-993
59. van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, Palacios-Callender M, Erusalimsky JD, Quaschning T, Malinski T, Gygi D, Ullrich V, Lüscher TF (2000) Enhanced peroxynitrite formation is associated with vascular aging. JExp Med 192:1731-1744
60. Villanueva C, Giulivi C (2010) Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease. Free Radic Biol Med 49:307-316
61. Weitzdoerfer R, Hoeger H, Engidawork E, Engelmann M, Singewald N, Lubec G, Lubec B (2004) Neuronal nitric oxide synthase knock-out mice show impaired cognitive performance. Nitric Oxide 10:130-140
62. Wigginton JE, Cutler DJ, Abecasis GR (2005) A note on exact tests of Hardy-Weinberg equilibrium. Am J Hum Genet 76:887-893
63. Wink DA, Hines HB, Cheng RY, Switzer CH, Flores-Santana W, Vitek MP, Ridnour LA, Colton CA (2011) Nitric oxide and redox mechanisms in the immune response. J Leukoc Biol 89:873-891
64. Yang B, Larson DF, Watson RR (2004) Modulation of iNOS activity in age-related cardiac dysfunction. Life Sci 75:655-667
65. Yoon HJ, Cho SW, Ahn BW, Yang SY (2010) Alterations in the activity and expression of endothelial NO synthase in aged human endothelial cells. Mech Ageing Dev 131:119-123
66. Zhou QG, Hu Y, Hua Y, Hu M, Luo CX, Han X, Zhu XJ, Wang B, Xu JS, Zhu DY (2007) Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J Neurochem 103:1843-1854
67. Zoubovsky SP, Pogorelov VM, Taniguchi Y, Kim SH, Yoon P, Nwulia E, Sawa A, Pletnikov MV, Kamiya A (2011) Working memory deficits in neuronal nitric oxide synthase knockout mice: potential impairments in prefrontal cortex mediated cognitive function. Biochem Biophys Res Commun 408:707-712