Accelerated epigenetic aging in brain is associated with pre-mortem HIV-associated neurocognitive disorders

Journal of NeuroVirology

Volumn 22, Issue 3, 2016, Pages 366-375

  Levine, Andrew J ^a   Quach, Austin ^a   Moore, David J ^b   Achim, Cristian L ^b   Soontornniyomkij, Virawudh ^b   Masliah, Eliezer ^b   Singer, Elyse J ^a   Gelman, Benjamin ^c   Nemanim, Natasha ^a   Horvath, Steve ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Epigenetic; Epigenetic clock; HANA; HAND; HIV; HIV associated neurocognitive disorder

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; AMYLOID BETA PROTEIN; COMPLEMENTARY DNA; GENOMIC DNA; GLIAL FIBRILLARY ACIDIC PROTEIN; HLA DR ANTIGEN; VIRUS DNA; VIRUS RNA;

ADULT; AGE; ARTICLE; AUTOPSY; BRAIN; CLINICAL EVALUATION; CONTROLLED STUDY; DEMOGRAPHY; DISEASE ASSOCIATION; DISEASE SEVERITY; DNA METHYLATION; EPIGENETIC CLOCK; EPIGENETICS; FEMALE; HISTOPATHOLOGY; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN TISSUE; MALE; MOLECULAR CLOCK; NEUROPATHOLOGY; OCCIPITAL CORTEX; PREMATURE AGING; PRIORITY JOURNAL; RETROSPECTIVE STUDY; VIROLOGY; VIRUS LOAD; ACCELERATION; AGING; COGNITIVE DEFECT; COMPLICATION; GENETIC EPIGENESIS; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; MIDDLE AGED; OCCIPITAL LOBE; PATHOLOGY;

ACCELERATION; ADULT; AGING; AUTOPSY; COGNITIVE DYSFUNCTION; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HIV INFECTIONS; HUMANS; MALE; MIDDLE AGED; OCCIPITAL LOBE; RETROSPECTIVE STUDIES;

EID: 84976594531     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-015-0406-3     Document Type: Article

References (80)

1. Achim CL, Adame A, Dumaop W, Everall IP, Masliah E (2009) Increased accumulation of intraneuronal amyloid beta in HIV-infected patients. J Neuroimmune Pharm 4(2):190–199
2. Alisch RS, Barwick BG, Chopra P, Myrick LK, Satten GA, Conneely KN, Warren ST (2012) Age-associated DNA methylation in pediatric populations. Genome Res 22(4):623–632. doi:10.1101/gr.125187.111
3. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M … Wojna VE (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69(18):1789–1799
4. Bell JT, Tsai P-C, Yang T-P, Pidsley R, Nisbet J, Glass D … The Mu TC (2012) Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet 8(4):e1002629. doi:10.1371/journal.pgen.1002629
5. Bocklandt S, Lin W, Sehl ME, Sanchez FJ, Sinsheimer JS, Horvath S, Vilain E (2011) Epigenetic predictor of age. PLoS One 6(6):e14821. doi:10.1371/journal.pone.0014821
6. Boks MP, Derks EM, Weisenberger DJ, Strengman E, Janson E, Sommer IE … Ophoff RA (2009) The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PLoS One 4(8):e6767. doi:10.1371/journal.pone.0006767
7. Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H … Baccarelli A (2009) Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev. 130(4):234–239. doi:10.1016/j.mad.2008.12.003
8. Brew BJ, Pemberton L, Blennow K, Wallin A, Hagberg L (2005) CSF amyloid β42 and tau levels correlate with AIDS dementia complex. Neurology 65(9):1490–1492
9. Cassol E, Misra V, Dutta A, Morgello S, Gabuzda D (2014) Cerebrospinal fluid metabolomics reveals altered waste clearance and accelerated aging in HIV patients with neurocognitive impairment. AIDS. doi:10.1097/QAD.0000000000000303
10. Chang L, Holt JL, Yakupov R, Jiang CS, Ernst T (2013) Lower cognitive reserve in the aging human immunodeficiency virus-infected brain. Neurobiol Aging 34(4):1240–1253. doi:10.1016/j.neurobiolaging.2012.10.012
11. Cherner M, Ellis RJ, Lazzaretto D, Young C, Mindt MR, Atkinson JH … Heaton RK (2004) Effects of HIV-1 infection and aging on neurobehavioral functioning: preliminary findings. AIDS 18(Suppl 1):S27–S34
12. Christensen B, Houseman E, Marsit C, Zheng S, Wrensch M, Wiemels J … Kelsey K (2009) Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet 5(8):e1000602
13. Clinical confirmation of the American academy of neurology algorithm for HIV-1-associated cognitive/motor disorder. The dana consortium on therapy for hiv dementia and related cognitive disorders. (1996) Neurology 47(5):1247–1253
14. Day K, Waite L, Thalacker-Mercer A, West A, Bamman M, Brooks J … Absher D (2013) Differential DNA methylation with age displays both common and dynamic features across human tissues that are influenced by CpG landscape. Genome Biol 14(9):R102
15. Deeks SG (2011) HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med 62(1):141–155. doi:10.1146/annurev-med-042909-093756
16. Desplats P, Dumaop W, Smith D, Adame A, Everall I, Letendre S … Masliah E (2013) Molecular and pathologic insights from latent HIV-1 infection in the human brain. Neurology 80(15):1415–1423. doi:10.1212/WNL.0b013e31828c2e9e
17. Desquilbet L, Jacobson LP, Fried LP, Phair JP, Jamieson BD, Holloway M, Margolick JB (2011) A frailty-related phenotype before HAART initiation as an independent risk factor for AIDS or death after HAART among HIV-infected men. J Gerontol Ser A Biol Med Sci 66A(9):1030–1038. doi:10.1093/gerona/glr097
18. Dunning M, Barbosa-Morais N, Lynch A, Tavare S, Ritchie M (2008) Statistical issues in the analysis of Illumina data. BMC Bioinforma 9(1):85
19. Fausto A, Bongiovanni M, Cicconi P, Menicagli L, Ligabò EV, Melzi S … Monforte AdA (2006) Potential predictive factors of osteoporosis in HIV-positive subjects. Bone 38(6):893–897
20. Gannon P, Khan MZ, Kolson DL (2011) Current understanding of HIV-associated neurocognitive disorders pathogenesis. Curr Opin Neurol 24(3):275–283. doi:10.1097/WCO.0b013e32834695fb
21. Gelman BB, Lisinicchia JG, Chen T, Johnson KM, Jennings K, Freeman DH Jr, Soukup VM (2012) Prefrontal dopaminergic and enkephalinergic synaptic accommodation in HIV-associated neurocognitive disorders and encephalitis. J Neuroimmune Pharm 7(3):686–700. doi:10.1007/s11481-012-9345-4
22. Gelman BB, Lisinicchia JG, Morgello S, Masliah E, Commins D, Achim CL … Soukup VM (2013) Neurovirological correlation with HIV-associated neurocognitive disorders and encephalitis in a HAART-era cohort. J Acquir Immune Defic Syndr 62(5):487–495. doi:10.1097/QAI.0b013e31827f1bdb
23. Giesbrecht CJ, Thornton AE, Hall-Patch C, Maan EJ, Cote HC, Money DM … Pick N (2014) Select neurocognitive impairment in HIV-infected women: associations with HIV viral load, hepatitis C virus, and depression, but not leukocyte telomere length. PLoS One 9(3):e89556. doi:10.1371/journal.pone.0089556
24. Green DA, Masliah E, Vinters HV, Beizai P, Moore DJ, Achim CL (2005) Brain deposition of beta-amyloid is a common pathologic feature in HIV positive patients. AIDS 19(4):407–411
25. Greene M, Justice AC, Lampiris HW, Valcour V (2013) Management of human immunodeficiency virus infection in advanced age. JAMA 309(13):1397–1405. doi:10.1001/jama.2013.2963
26. Grinspoon S, Carr A (2005) Cardiovascular risk and body-fat abnormalities in HIV-infected adults. N Engl J Med 352(1):48–62. doi:10.1056/NEJMra041811
27. Hannum G, Guinney J, Zhao L, Zhang L, Hughe G, Sadda S … Zhang K (2013) Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell 49(2):359–367
28. Hernandez DG, Nalls MA, Gibbs JR, Arepalli S, van der Brug M, Chong S … Singleton AB (2011) Distinct DNA methylation changes highly correlated with chronological age in the human brain. Hum Mol Genet 20(6):1164–1172. doi:10.1093/hmg/ddq561
29. Holt JL, Kraft-Terry SD, Chang L (2012) Neuroimaging studies of the aging HIV-1-infected brain. J Neurovirol 18(4):291–302. doi:10.1007/s13365-012-0114-1
30. Horvath S (2013a) DNA methylation age of human tissues and cell types. Genome Biol 14(10):R115. doi:10.1186/gb-2013-14-10-r115
31. Horvath S (2013b) Webpage: http://labs.genetics.ucla.edu/horvath/dnamage
32. Horvath S, Levine AJ (2015) HIV-1 infection accelerates age according to the epigenetic clock. J Infect Dis. doi:10.1093/infdis/jiv277
33. Horvath S, Zhang Y, Langfelder P, Kahn R, Boks M, van Eijk K … Ophoff RA (2012) Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol 13:R97
34. Horvath S, Erhart W, Brosch M, Ammerpohl O, von Schonfels W, Ahrens M … Hampe J (2014) Obesity accelerates epigenetic aging of human liver. Proc Natl Acad Sci USA 111(43):15538–15543. doi:10.1073/pnas.1412759111
35. Horvath S, Garagnani P, Bacalini MG, Pirazzini C, Salvioli S, Gentilini D … Franceschi C (2015a) Accelerated epigenetic aging in Down syndrome. Aging Cell 14(3):491–495. doi:10.1111/acel.12325
36. Horvath S, Mah V, Lu AT, Woo JS, Choi OW, Jasinska AJ … Coles LS (2015b) The cerebellum ages slowly according to the epigenetic clock. Aging (Albany NY) 7(5):294–306
37. Jaffe A, Irizarry R (2014) Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol 15(2):R31
38. Johansson A, Enroth S, Gyllensten U (2013) Continuous aging of the human DNA methylome throughout the human lifespan. PLoS One 8(6):e67378. doi:10.1371/journal.pone.0067378
39. Jung M, Pfeifer GP (2015) Aging and DNA methylation. BMC Biol 13:7. doi:10.1186/s12915-015-0118-4
40. Kallianpur AR, Levine AJ (2014) Host genetic factors predisposing to HIV-associated neurocognitive disorder. Curr HIV/AIDS Rep. doi:10.1007/s11904-014-0222-z
41. Kazantsev AG, Thompson LM (2008) Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov 7(10):854–868. doi:10.1038/nrd2681
42. Kirk GD, Mehta SH, Astemborski J, Galai N, Washington J, Higgins Y … Thomas DL (2013) HIV, age, and the severity of hepatitis C virus–related liver disease A cohort study. Ann Intern Med. doi:10.7326/0003-4819-158-9-201305070-00604
43. Kraft-Terry SD, Buch SJ, Fox HS, Gendelman HE (2009) A coat of many colors: neuroimmune crosstalk in human immunodeficiency virus infection. Neuron 64(1):133–145. doi:10.1016/j.neuron.2009.09.042
44. Letendre S (2011) Central nervous system complications in HIV disease: HIV-associated neurocognitive disorder. Top Antivir Med 19(4):137–142
45. Levine AJ, Horvath S, Miller EN, Singer EJ, Shapshak P, Baldwin GC, Martínez-Maza O, Witt MD, Langfelder P (2013a) Transcriptome analysis of HIV-infected peripheral blood monocytes: gene transcripts and networks associated with neurocognitive functioning. J Neuroimmunol 265(1–2):96–105. doi:10.1016/j.jneuroim.2013.09.016
46. Levine AJ, Miller JA, Shapshak P, Gelman B, Singer EJ, Hinkin CH, Commins D, Morgello S, Grant I, Horvath S (2013b) Systems analysis of human brain gene expression: mechanisms for HIV-associated neurocognitive impairment and common pathways with Alzheimer’s disease. BMC Med Genomics 6(1):4. doi:10.1186/1755-8794-6-4
47. Levine AJ, Panos SE, Horvath S (2014) Genetic, transcriptomic, and epigenetic studies of HIV-associated neurocognitive disorder. J Acquir Immune Defic Syndr 65(4):481–503. doi:10.1097/QAI.0000000000000069
48. Lucas GM, Mehta SH, Atta MG, Kirk GD, Galai N, Vlahov D, Moore RD (2007) End-stage renal disease and chronic kidney disease in a cohort of African-American HIV-infected and at-risk HIV-seronegative participants followed between 1988 and 2004. AIDS 21(18):2435–2443
49. Malan-Muller S, Hemmings SM, Spies G, Kidd M, Fennema-Notestine C, Seedat S (2013) Shorter telomere length–a potential susceptibility factor for HIV-associated neurocognitive impairments in South African women [corrected]. PLoS One 8(3):e58351. doi:10.1371/journal.pone.0058351
50. Marioni RE, Shah S, McRae AF, Chen BH, Colicino E, Harris SE … Deary IJ (2015a) DNA methylation age of blood predicts all-cause mortality in later life. Genome Biol 16:25. doi:10.1186/s13059-015-0584-6
51. Marioni RE, Shah S, McRae AF, Ritchie SJ, Muniz-Terrera G, Harris SE … Deary IJ (2015b) The epigenetic clock is correlated with physical and cognitive fitness in the Lothian Birth Cohort 1936. Int J Epidemiol. doi:10.1093/ije/dyu277
52. Martin J, Volberding P (2010) HIV and premature aging: a field still in its infancy. Ann Intern Med 153(7):477–479. doi:10.7326/0003-4819-153-7-201010050-00013
53. Migliore L, Coppede F (2009) Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutat Res 667(1–2):82–97. doi:10.1016/j.mrfmmm.2008.10.011
54. Morgello S, Gelman B, Kozlowski P, Vinters H, Masliah E, Cornford M … Singer E (2001) The national neuroAIDS tissue consortium: a new paradigm in brain banking with an emphasis on infectious disease. Neuropathol Appl Neurobiol 27(4):326–335
55. Mukerjee R, Chang JR, Del Valle L, Bagashev A, Gayed MM, Lyde RB … Sawaya BE (2011) Deregulation of microRNAs by HIV-1 Vpr protein leads to the development of neurocognitive disorders. J Biol Chem 286(40):34976–34985. doi:10.1074/jbc.M111.241547
56. Narasipura SD, Kim S, Al-Harthi L (2014) Epigenetic regulation of HIV-1 latency in astrocytes. J Virol 88(5):3031–3038. doi:10.1128/JVI.03333-13
57. Numata S, Ye T, Hyde, Thomas M, Guitart-Navarro X, Tao R, Wininger M … Lipska, Barbara K (2012) DNA methylation signatures in development and aging of the human prefrontal cortex. Am J Hum Genet 90(2):260–272. doi:10.1016/j.ajhg.2011.12.020
58. Ojeda D, Lopez-Costa JJ, Sede M, Lopez EM, Berria MI, Quarleri J (2014) Increased in vitro glial fibrillary acidic protein expression, telomerase activity, and telomere length after productive human immunodeficiency virus-1 infection in murine astrocytes. J Neurosci Res 92(2):267–274. doi:10.1002/jnr.23294
59. Palmer S, Wiegand AP, Maldarelli F, Bazmi H, Mican JM, Polis M, Coffin JM (2003) New real-time reverse transcriptase-initiated PCR assay with single-copy sensitivity for human immunodeficiency virus type 1 RNA in plasma. J Clin Microbiol 41(10):4531–4536
60. Pendyala G, Fox HS (2010) Proteomic and metabolomic strategies to investigate HIV-associated neurocognitive disorders. Genome Med 2(3):22. doi:10.1186/gm143
61. Perez-Santiago J, Plongthongkum N, Letendre S, Ellis R, Gouaux B, Moore D, LeBlanc S, Rajagopal N, Zhang K, Woelk C (2012) DNA methylation correlates with neurological decline in HIV-infected individuals. Paper presented at the 19th conference on retroviruses and opportunistic infections. Seattle, Washington
62. Pulliam L, Rempel H, Sun B, Abadjian L, Calosing C, Meyerhoff DJ (2011) A peripheral monocyte interferon phenotype in HIV infection correlates with a decrease in magnetic resonance spectroscopy metabolite concentrations. AIDS 25(14):1721–1726. doi:10.1097/QAD.0b013e328349f022
63. Rakyan VK, Down TA, Maslau S, Andrew T, Yang TP, Beyan H … Spector TD (2010) Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 20(4):434–439. doi:10.1101/gr.103101.109
64. Saiyed ZM, Gandhi N, Agudelo M, Napuri J, Samikkannu T, Reddy PV … Nair MP (2011) HIV-1 Tat upregulates expression of histone deacetylase-2 (HDAC2) in human neurons: implication for HIV-associated neurocognitive disorder (HAND). Neurochem Int 58(6):656–664. doi:10.1016/j.neuint.2011.02.004
65. Silverberg M, Chao C, Leyden W, Xu L, Tang B, Horberg M … Abrams D (2009) HIV infection and the risk of cancers with and without a known infectious cause. AIDS 23(17):2337–2345. doi:10.1097/QAD.0b013e3283319184
66. Silverberg MJ, Chao C, Leyden WA, Xu L, Horberg MA, Klein D … Abrams DI (2011) HIV infection, immunodeficiency, viral replication, and the risk of cancer. Cancer Epidemiol Biomarkers Prev 20(12):2551–2559. doi:10.1158/1055-9965.epi-11-0777
67. Soontornniyomkij V, Risbrough VB, Young JW, Wallace CK, Soontornniyomkij B, Jeste DV, Achim CL (2010) Short-term recognition memory impairment is associated with decreased expression of FK506 binding protein 51 in the aged mouse brain. Age (Dordr) 32(3):309–322. doi:10.1007/s11357-010-9145-9
68. Soontornniyomkij V, Moore DJ, Gouaux B, Soontornniyomkij B, Tatro ET, Umlauf A, Masliah E, Levine AJ, Singer EJ, Vinters HV, Gelman BB, Morgello S, Cherner M, Grant I, Achim CL (2012a) Cerebral beta-amyloid deposition predicts HIV-associated neurocognitive disorders in APOE epsilon4 carriers. AIDS 26(18):2327–2335. doi:10.1097/QAD.0b013e32835a117c
69. Soontornniyomkij V, Soontornniyomkij B, Moore DJ, Gouaux B, Masliah E, Tung S, Vinters HV, Grant I, Achim CL (2012b) Antioxidant sestrin-2 redistribution to neuronal soma in human immunodeficiency virus-associated neurocognitive disorders. J Neuroimmune Pharmacol 7(3):579–590. doi:10.1007/s11481-012-9357-0
70. Sun JM, Spencer VA, Chen HY, Li L, Davie JR (2003) Measurement of histone acetyltransferase and histone deacetylase activities and kinetics of histone acetylation. Methods 31(1):12–23
71. Tatro ET, Scott ER, Nguyen TB, Salaria S, Banerjee S, Moore DJ … Everall IP (2010) Evidence for alteration of gene regulatory networks through microRNAs of the HIV-infected brain: novel analysis of retrospective cases. PLoS One 5(4):e10337. doi:10.1371/journal.pone.0010337
72. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H … Widschwendter M (2010) Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res 20(4):440–446. doi:10.1101/gr.103606.109
73. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, Beck S (2013) A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics 29(2):189–196. doi:10.1093/bioinformatics/bts680
74. Thomas J (1999) Doherty SM (2003) HIV infection–a risk factor for osteoporosis. J Acquir Immune Defic Syndr 33(3):281–291
75. Toggas SM, Mucke L (1996) Transgenic models in the study of AIDS dementia complex. Curr Top Microbiol Immunol 206:223–241
76. Triant VA, Lee H, Hadigan C, Grinspoon SK (2007) Increased acute myocardial infarction rates and cardiovascular risk factors among patients with human immunodeficiency virus disease. J Clin Endocrinol Metab 92(7):2506–2512. doi:10.1210/jc.2006-2190
77. Wendelken L, Valcour V (2012) Impact of HIV and aging on neuropsychological function. J Neurovirol 18(4):256–263. doi:10.1007/s13365-012-0094-1
78. Winkler JM, Chaudhuri AD, Fox HS (2012) Translating the brain transcriptome in neuroAIDS: from non-human primates to humans. J Neuroimmune Pharm 7(2):372–379. doi:10.1007/s11481-012-9344-5
79. Womack JA, Goulet JL, Gibert C, Brandt C, Chang CC, Gulanski B … for the Veterans Aging Cohort Study Project T (2011) Increased risk of fragility fractures among HIV infected compared to uninfected male veterans. PLoS One 6(2):e17217. doi:10.1371/journal.pone.0017217
80. Yuan T, Jiao Y, de Jong S, Ophoff RA, Beck S, Teschendorff AE (2015) An integrative multi-scale analysis of the dynamic DNA methylation landscape in aging. PLoS Genet 11(2):e1004996. doi:10.1371/journal.pgen.1004996