Promoter methylation and age-related downregulation of Klotho in rhesus monkey

Age

Volumn 34, Issue 6, 2012, Pages 1405-1419

  King, Gwendalyn D ^a,c   Rosene, Douglas L ^a,b   Abraham, Carmela R ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Age downregulation; Methylation; Oxidation; Pyrosequencing; White matter

Indexed keywords

CYTOSINE; KLOTHO PROTEIN; MESSENGER RNA; 5 METHYLCYTOSINE; BETA GLUCURONIDASE; TRANSCRIPTION FACTOR;

AGE DISTRIBUTION; AGING; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PROMOTER REGION; RHESUS MONKEY; WHITE MATTER; ANIMAL; BRAIN; CELL LINE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

5-METHYLCYTOSINE; AGING; ANIMALS; BRAIN; CELL LINE; CYTOSINE; DNA METHYLATION; DOWN-REGULATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GLUCURONIDASE; MACACA MULATTA; MALE; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84873050679     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-011-9315-4     Document Type: Article

References (62)

1. Arking DE, Krebsova A, Macek M Sr, Macek M Jr, Arking A, Mian IS, Fried L, Hamosh A, Dey S, McIntosh I, Dietz HC (2002) Association of human aging with a functional variant of klotho. Proc Natl Acad Sci U S A 99(2):856-861. doi: 10.1073/pnas.022484299
2. Arking DE, Becker DM, Yanek LR, Fallin D, Judge DP, Moy TF, Becker LC, Dietz HC (2003) KLOTHO allele status and the risk of early-onset occult coronary artery disease. Am J Hum Genet 72(5):1154-61
3. Arking DE, Atzmon G, Arking A, Barzilai N, Dietz HC (2005) Association between a functional variant of the KLOTHO gene and high-density lipoprotein cholesterol, blood pressure, stroke, and longevity. Circ Res 96(4):412-8
4. Brooks PJ, Marietta C, Goldman D (1996) DNA mismatch repair and DNA methylation in adult brain neurons. J Neurosci 16(3):939-945
5. Brownstein CA, Adler F, Nelson-Williams C, Iijima J, Li P, Imura A, Nabeshima Y, Reyes-Mugica M, Carpenter TO, Lifton RP (2008) A translocation causing increased alpha-klotho level results in hypophosphatemic rickets and hyperparathyroidism. Proc Natl Acad Sci U S A 105(9):3455-3460
6. Camilli TC, Xu M, O'Connell MP, Chien B, Frank BP, Subaran S, Indig FE, Morin PJ, Hewitt SM, Weeraratna AT (2010) Loss of Klotho during melanoma progression leads to increased filamin cleavage, increased Wnt5A expression, and enhanced melanoma cell motility. Pigment Cell Melanoma Res 24(1):175-186. doi: 10.1111/j.1755-148X.2010.00792.x
7. Chang YM, Rosene DL, Killiany RJ, Mangiamele LA, Luebke JI (2005) Increased action potential firing rates of layer 2/3 pyramidal cells in the prefrontal cortex are significantly related to cognitive performance in aged monkeys. Cereb Cortex 15(4):409-418
8. Chen CD, Podvin S, Gillespie E, Leeman SE, Abraham CR (2007) Insulin stimulates the cleavage and release of the extracellular domain of Klotho by ADAM10 and ADAM17. Proc Natl Acad Sci U S A 104(50):19796-197801
9. Chen B, Wang X, Zhao W, Wu J (2010) Klotho inhibits growth and promotes apoptosis in human lung cancer cell line A549. J Exp Clin Cancer Res 29:99
10. Choi BH, Kim CG, Lim Y, Lee YH, Shin SY (2010) Transcriptional activation of the human Klotho gene by epidermal growth factor in HEK293 cells; role of Egr-1. Gene 450(1-2):121-127
11. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, Nelson HH, Karagas MR, Padbury JF, Bueno R, Sugarbaker DJ, Yeh RF, Wiencke JK, Kelsey KT (2009) Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet 5(8):e1000602. doi: 10.1371/journal.pgen.1000602
12. Chu MW, Siegmund KD, Eckstam CL, Kim JY, Yang AS, Kanel GC, Tavare S, Shibata D (2007) Lack of increases in methylation at three CpG-rich genomic loci in non-mitotic adult tissues during aging. BMC Med Genet 8:50
13. Desjardins S, Mayo W, Vallee M, Hancock D, Le Moal M, Simon H, Abrous DN (1997) Effect of aging on the basal expression of c-Fos, c-Jun, and Egr-1 proteins in the hippocampus. Neurobiol Aging 18(1):37-44
14. Duce JA, Podvin S, Hollander W, Kipling D, Rosene DL, Abraham CR (2008) Gene profile analysis implicates Klotho as an important contributor to aging changes in brain white matter of the rhesus monkey. Glia 56(1):106-117. doi: 10.1002/glia.20593
15. Golbus J, Palella TD, Richardson BC (1990) Quantitative changes in T cell DNA methylation occur during differentiation and ageing. Eur J Immunol 20(8):1869-1872. doi: 10.1002/eji.1830200836
16. Hernandez DG, Nalls MA, Gibbs JR, Arepalli S, van der Brug M, Chong S, Moore M, Longo DL, Cookson MR, Traynor BJ, Singleton AB (2011) Distinct DNA methylation changes highly correlated with chronological age in the human brain. Hum Mol Genet
17. Herndon JG, Moss MB, Rosene DL, Killiany RJ (1997) Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 87(1):25-34
18. Hinman JD, Abraham CR (2007) What's behind the decline? The role of white matter in brain aging. Neurochem Res 32(12):2023-2031. doi: 10.1007/s11064-007-9341-x
19. Hinman JD, Peters A, Cabral H, Rosene DL, Hollander W, Rasband MN, Abraham CR (2006) Age-related molecular reorganization at the node of Ranvier. J Comp Neurol 495(4):351-362. doi: 10.1002/cne.20886
20. Hinman JD, Chen CD, Oh SY, Hollander W, Abraham CR (2008) Age-dependent accumulation of ubiquitinated 2′,3′-cyclic nucleotide 3′-phosphodiesterase in myelin lipid rafts. Glia 56(1):118-133. doi: 10.1002/glia.20595
21. Ichikawa S, Imel EA, Kreiter ML, Yu X, Mackenzie DS, Sorenson AH, Goetz R, Mohammadi M, White KE, Econs MJ (2007) A homozygous missense mutation in human KLOTHO causes severe tumoral calcinosis. J Clin Invest 117(9):2684-2691. doi: 10.1172/JCI31330
22. Invidia L, Salvioli S, Altilia S, Pierini M, Panourgia MP, Monti D, De Rango F, Passarino G, Franceschi C (2010) The frequency of Klotho KL-VS polymorphism in a large Italian population, from young subjects to centenarians, suggests the presence of specific time windows for its effect. Biogerontology 11(1):67-73. doi: 10.1007/s10522-009-9229-z
23. Kuro-o M (2009) Klotho and aging. Biochim Biophys Acta 1790(10):1049-1058
24. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390(6655):45-51. doi: 10.1038/36285
25. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P, McGuinness OP, Chikuda H, Yamaguchi M, Kawaguchi H, Shimomura I, Takayama Y, Herz J, Kahn CR, Rosenblatt KP, Kuro-o M (2005) Suppression of aging in mice by the hormone Klotho. Science 309(5742):1829-1833
26. Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, Baum MG, Schiavi S, Hu MC, Moe OW, Kuro-o M (2006) Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 281(10):6120-6123
27. Lee J, Jeong DJ, Kim J, Lee S, Park JH, Chang B, Jung SI, Yi L, Han Y, Yang Y, Kim KI, Lim JS, Yang I, Jeon S, Bae DH, Kim CJ, Lee MS (2010) The anti-aging gene KLOTHO is a novel target for epigenetic silencing in human cervical carcinoma. Mol Cancer 9(9):109
28. Li H, Mitchell JR, Hasty P (2008) DNA double-strand breaks: a potential causative factor for mammalian aging? Mech Ageing Dev 129(7-8):416-424
29. Liang R, Bates DJ, Wang E (2009) Epigenetic Control of MicroRNA Expression and Aging. Curr Genomics 10(3):184-193. doi: 10.2174/ 138920209788185225
30. Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, Malide D, Rovira II, Schimel D, Kuo CJ, Gutkind JS, Hwang PM, Finkel T (2007) Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317(5839):803-806
31. Liu L, van Groen T, Kadish I, Tollefsbol TO (2009) DNA methylation impacts on learning and memory in aging. Neurobiol Aging 30(4):549-560
32. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429(6994):883-891. doi: 10.1038/nature02661
33. Lubin FD, Roth TL, Sweatt JD (2008) Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28(42):10576-10586
34. Luebke J, Barbas H, Peters A (2010) Effects of normal aging on prefrontal area 46 in the rhesus monkey. Brain Res Rev 62(2):212-232
35. Maes OC, An J, Sarojini H, Wang E (2008) Murine microRNAs implicated in liver functions and aging process. Mech Ageing Dev 129(9):534-541
36. Matsumura Y, Aizawa H, Shiraki-Iida T, Nagai R, Kuro-o M, Nabeshima Y (1998) Identification of the human klotho gene and its two transcripts encoding membrane and secreted klotho protein. Biochem Biophys Res Commun 242(3):626-630
37. Nabeshima Y (2002) Ectopic calcification in Klotho mice. Clin Calcium 12(8):1114-1117
38. Nabeshima Y (2008) The discovery of alpha-Klotho and FGF23 unveiled new insight into calcium and phosphate homeostasis. Cell Mol Life Sci 65(20):3218-3230. doi: 10.1007/s00018-008-8177-0
39. Nagai T, Yamada K, Kim HC, Kim YS, Noda Y, Imura A, Nabeshima Y, Nabeshima T (2003) Cognition impairment in the genetic model of aging klotho gene mutant mice: a role of oxidative stress. FASEB J 17(1):50-52. doi: 10.1096/fj.02-0448fje
40. Pan J, Zhong J, Gan LH, Chen SJ, Jin HC, Wang X, Wang LJ (2011) Klotho, an anti-senescence related gene, is frequently inactivated through promoter hypermethylation in colorectal cancer. Tumour Biol. doi: 10.1007/s13277-011- 0174-5
41. Penner MR, Roth TL, Chawla MK, Hoang LT, Roth ED, Lubin FD, Sweatt JD, Worley PF, Barnes CA (2010) Age-related changes in Arc transcription and DNA methylation within the hippocampus. Neurobiol Aging
42. Peters A (2009) The effects of normal aging on myelinated nerve fibers in monkey central nervous system. Front Neuroanat 3:11. doi: 10.3389/neuro.05.011. 2009
43. Peters A, Sethares C, Moss MB (1998) The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey. Cereb Cortex 8(8):671-684
44. Peters A, Moss MB, Sethares C (2000) Effects of aging on myelinated nerve fibers in monkey primary visual cortex. J Comp Neurol 419(3):364-376. doi: 10.1002/(SICI)1096-9861(20000410)419:3<364::AID-CNE8>3.0.CO;2-R
45. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16(3):675-686
46. Shih PH, Yen GC (2007) Differential expressions of antioxidant status in aging rats: the role of transcriptional factor Nrf2 and MAPK signaling pathway. Biogerontology 8(2):71-80. doi: 10.1007/s10522-006-9033-y
47. Shiozaki M, Yoshimura K, Shibata M, Koike M, Matsuura N, Uchiyama Y, Gotow T (2008) Morphological and biochemical signs of age-related neurodegenerative changes in klotho mutant mice. Neuroscience 152(4):924-941
48. Siegmund KD, Connor CM, Campan M, Long TI, Weisenberger DJ, Biniszkiewicz D, Jaenisch R, Laird PW, Akbarian S (2007) DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2(9):e895. doi: 10.1371/journal.pone.0000895
49. Sloane JA, Hollander W, Moss MB, Rosene DL, Abraham CR (1999) Increased microglial activation and protein nitration in white matter of the aging monkey. Neurobiol Aging 20(4):395-405
50. Sloane JA, Hollander W, Rosene DL, Moss MB, Kemper T, Abraham CR (2000) Astrocytic hypertrophy and altered GFAP degradation with age in subcortical white matter of the rhesus monkey. Brain Res 862(1-2):1-10
51. Sloane JA, Hinman JD, Lubonia M, Hollander W, Abraham CR (2003) Age-dependent myelin degeneration and proteolysis of oligodendrocyte proteins is associated with the activation of calpain-1 in the rhesus monkey. J Neurochem 84(1):157-168
52. Takasugi M (2011) Progressive age-dependent DNA methylation changes start before adulthood in mouse tissues. Mech Ageing Dev
53. Tigges J, Gordon TP, McClure HM, Hall EC, Peters A (1988) Survival rate and life span of rhesus monkeys at Yerkes Regional Primate Research Center. Am J Primatol 15:263-73
54. Uchida A, Komiya Y, Tashiro T, Yorifuji H, Kishimoto T, Nabeshima Y, Hisanaga S (2001) Neurofilaments of Klotho, the mutant mouse prematurely displaying symptoms resembling human aging. J Neurosci Res 64(4):364-370
55. Utsugi T, Ohno T, Ohyama Y, Uchiyama T, Saito Y, Matsumura Y, Aizawa H, Itoh H, Kurabayashi M, Kawazu S, Tomono S, Oka Y, Suga T, Kuro-o M, Nabeshima Y, Nagai R (2000) Decreased insulin production and increased insulin sensitivity in the klotho mutant mouse, a novel animal model for human aging. Metabolism 49(9):1118-1123
56. Wilson VL, Smith RA, Ma S, Cutler RG (1987) Genomic 5-methyldeoxycytidine decreases with age. J Biol Chem 262(21):9948-51
57. Wisco JJ, Killiany RJ, Guttmann CR, Warfield SK, Moss MB, Rosene DL (2008) An MRI study of age-related white and gray matter volume changes in the rhesus monkey. Neurobiol Aging 29(10):1563-1575
58. Wolf I, Levanon-Cohen S, Bose S, Ligumsky H, Sredni B, Kanety H, Kuro-o M, Karlan B, Kaufman B, Koeffler HP, Rubinek T (2008) Klotho: a tumor suppressor and a modulator of the IGF-1 and FGF pathways in human breast cancer. Oncogene 27(56):7094-7105
59. Wolf I, Laitman Y, Rubinek T, Abramovitz L, Novikov I, Beeri R, Kuro OM, Koeffler HP, Catane R, Freedman LS, Levy-Lahad E, Karlan BY, Friedman E, Kaufman B (2010) Functional variant of KLOTHO: a breast cancer risk modifier among BRCA1 mutation carriers of Ashkenazi origin. Oncogene 29(1):26-33
60. Yamamoto M, Clark JD, Pastor JV, Gurnani P, Nandi A, Kurosu H, Miyoshi M, Ogawa Y, Castrillon DH, Rosenblatt KP, Kuro-o M (2005) Regulation of oxidative stress by the anti-aging hormone klotho. J Biol Chem 280(45):38029-38034
61. Yang Y, Gozen O, Vidensky S, Robinson MB, Rothstein JD (2010) Epigenetic regulation of neuron-dependent induction of astroglial synaptic protein GLT1. Glia 58(3):277-286. doi: 10.1002/glia.20922
62. Zschocke J, Allritz C, Engele J, Rein T (2007) DNA methylation dependent silencing of the human glutamate transporter EAAT2 gene in glial cells. Glia 55(7):663-674. doi: 10.1002/glia.20497