Longitudinal epigenetic and gene expression profiles analyzed by three-component analysis reveal down-regulation of genes involved in protein translation in human aging

Nucleic Acids Research

Volumn 43, Issue 15, 2015, Pages

  Jung, Marc ^a   Jin, Seung Gi ^a   Zhang, Xiaoying ^a   Xiong, Wenying ^a   Gogoshin, Grigoriy ^b   Rodin, Andrei S ^b   Pfeifer, Gerd P ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 5; COLLAGEN TYPE 6; DNA; GELATINASE A; HISTONE H3; HOX PROTEIN; INITIATION FACTOR; TRANSCRIPTION FACTOR FOXO; FORKHEAD TRANSCRIPTION FACTOR; HISTONE;

ADULT; AGED; AGING; ARTICLE; COL3A1 GENE; COL5A1 GENE; COL6A1 GENE; DNA METHYLATION; ELN GENE; EPIGENETICS; FIBROBLAST CULTURE; FOXO GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC CODE; GENETIC TRANSCRIPTION; HISTONE METHYLATION; HOXB GENE; HOXD GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; LONGITUDINAL STUDY; MMP14 GENE; MMP2 GENE; PRIORITY JOURNAL; RIBOSOME; RNA TRANSLATION; SCORING SYSTEM; SKIN FIBROBLAST; ALGORITHM; CELL CULTURE; CLUSTER ANALYSIS; DOWN REGULATION; GENETIC EPIGENESIS; GENETICS; MALE; METABOLISM; METHYLATION; MIDDLE AGED; NONPARAMETRIC TEST; PROTEIN SYNTHESIS; SKIN;

ADULT; AGED; AGING; ALGORITHMS; CELLS, CULTURED; CLUSTER ANALYSIS; DNA METHYLATION; DOWN-REGULATION; EPIGENESIS, GENETIC; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; HISTONES; HUMANS; MALE; METHYLATION; MIDDLE AGED; PROTEIN BIOSYNTHESIS; SKIN; STATISTICS, NONPARAMETRIC;

EID: 84941213500     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv473     Document Type: Article

References (72)

1. Kenyon, C., Chang, J., Gensch, E., Rudner, A., and Tabtiang, R. (1993). A C. elegans mutant that lives twice as long as wild type. Nature, 366, 461-464.
2. Valdes, A.M., Glass, D., and Spector, T.D. (2013). Omics technologies and the study of human ageing. Nat. Rev. Genet., 14, 601-607.
3. Jung, M., and Pfeifer, G.P. (2015). Aging and DNA methylation. BMC Biol., 13, 7.
4. Magalhães, J.P.D., Curado, J., and Church, G.M. (2009). Meta-Analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics, 25, 875-881.
5. Horvath, S., Zhang, Y., Langfelder, P., Kahn, R.S., Boks, M.P., Eijk, K.v., van den Berg, L.H., and Ophoff, R.A. (2012). Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol., 13, R97.
6. Glass, D., Viñuela, A., Davies, M.N., Ramasamy, A., Parts, L., Knowles, D., Brown, A.A., Hedman, Å .K., Small, K.S., Buil, A., et al. (2013). Gene expression changes with age in skin, adipose tissue, blood and brain. Genome Biol., 14, R75.
7. Thompson, R.F., Atzmon, G., Gheorghe, C., Liang, H.Q., Lowes, C., Greally, J.M., and Barzilai, N. (2010). Tissue-specific dysregulation of DNA methylation in aging. Aging Cell, 9, 506-518.
8. Berchtold, N.C., Coleman, P.D., Cribbs, D.H., Rogers, J., Gillen, D.L., and Cotman, C.W. (2013). Synaptic genes are extensively downregulated across multiple brain regions in normal human aging and Alzheimer's disease. Neurobiol. Aging, 34, 1653-1661.
9. Johansson, A., Enroth, S., and Gyllensten, U. (2013). Continuous aging of the human DNA methylome throughout the human lifespan. PloS One, 8, e67378.
10. McClay, J.L., Aberg, K.A., Clark, S.L., Nerella, S., Kumar, G., Xie, L.Y., Hudson, A.D., Harada, A., Hultman, C.M., Magnusson, P.K., et al. (2014). A methylome-wide study of aging using massively parallel sequencing of the methyl-CpG-enriched genomic fraction from blood in over 700 subjects. Hum. Mol. Genet., 23, 1175-1185.
11. Swindell, W.R., Johnston, A., Sun, L., Xing, X., Fisher, G.J., Bulyk, M.L., Elder, J.T., and Gudjonsson, J.E. (2012). Meta-profiles of gene expression during aging: limited similarities between mouse and human and an unexpectedly decreased inflammatory signature. PloS One, 7, e33204.
12. Fraga, M.F., Ballestar, E., Paz, M.F., Ropero, S., Setien, F., Ballestar, M.L., Heine-Suner, D., Cigudosa, J.C., Urioste, M., Benitez, J., et al. (2005). Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. U.S.A., 102, 10604-10609.
13. Kerkel, K., Spadola, A., Yuan, E., Kosek, J., Jiang, L., Hod, E., Li, K., Murty, V.V., Schupf, N., Vilain, E., et al. (2008). Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation. Nat. Genet., 40, 904-908.
14. Rawlings, J.O., Pantula, S.G., and Dickey, D.A. (1998). Applied regression analysis: a research tool. Springer, NY.
15. Bjornsson, H.T., Sigurdsson, M.I., Fallin, M.D., Irizarry, R.A., Aspelund, T., Cui, H., Yu, W., Rongione, M.A., Ekstrom, T.J., Harris, T.B., et al. (2008). Intra-individual change over time in DNA methylation with familial clustering. JAMA, 299, 2877-2883.
16. Hannum, G., Guinney, J., Zhao, L., Zhang, L., Hughes, G., Sadda, S., Klotzle, B., Bibikova, M., Fan, J.B., Gao, Y., et al. (2013). Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol. Cell, 49, 359-367.
17. Issa, J.P. (2014). Aging and epigenetic drift: a vicious cycle. J. Clin. Invest., 124, 24-29.
18. Maegawa, S., Hinkal, G., Kim, H.S., Shen, L., Zhang, L., Zhang, J., Zhang, N., Liang, S., Donehower, L.A., and Issa, J.-P. (2010). Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res., 20, 332-340.
19. Teschendorff, A.E., West, J., and Beck, S. (2013). Age-Associated epigenetic drift: implications, and a case of epigenetic thrift? Hum. Mol. Genet., 22, R7-R15.
20. Lu, J.-Y., Lin, Y.-Y., Zhu, H., Chuang, L.-M., and Boeke, J.D. (2011). Protein acetylation and aging. Aging, 3, 911-912.
21. Liu, L., Cheung, T.H., Charville, G.W., Hurgo, B.M., Leavitt, T., Shih, J., Brunet, A., and Rando, T.A. (2013). Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep., 4, 189-204.
22. Greer, E.L., Maures, T.J., Hauswirth, A.G., Green, E.M., Leeman, D.S., Maro, G.S., Han, S., Banko, M.R., Gozani, O., and Brunet, A. (2010). Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature, 466, 383-387.
23. Jin, C., Li, J., Green, C.D., Yu, X., Tang, X., Han, D., Xian, B., Wang, D., Huang, X., Cao, X., et al. (2011). Histone demethylase UTX-1 regulates C. elegans life span by targeting the Insulin/IGF-1 signaling pathway. Cell Metab., 14, 161-172.
24. Siebold, A.P., Banerjee, R., Tie, F., Kiss, D.L., Moskowitz, J., and Harte, P.J. (2010). Polycomb repressive complex 2 and trithorax modulate Drosophila longevity and stress resistance. Proc. Natl Acad. Sci. U.S.A., 107, 169-174.
25. Jolliffe, I.T. (2002). Principal component analysis. Springer Series in Statistics. 2nd edn, Springer, NY.
26. Kononenko, I., and Kukar, M. (2007). Machine Learning and Data Mining. 1st edn. Hardwood Publishing Ltd, West Sussex
27. Fozard, J.L., Metter, E.J., and Brant, L.J. (1990). Next steps in describing aging and disease in longitudinal studies. J. Gerontol., 45, P116-P127.
28. Jaffe, A.E., and Irizarry, R.A. (2014). Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol., 15, R31.
29. Rauch, T.A., and Pfeifer, G.P. (2010). DNA methylation profiling using the methylated-CpG island recovery assay (MIRA). Methods, 52, 213-217.
30. Xiong, Z., and Laird, P.W. (1997). COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res., 25, 2532-2534.
31. Singh, P., and Szab, P.E. (2012). Chromatin immunoprecipitation to characterize the epigenetic profiles of imprinted domains. Meth. Mol. Biol., 925, 159-172.
32. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., and Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28, 511-515.
33. Hansen, K.D., Irizarry, R.A., and Wu, Z. (2012). Removing technical variability in RNA-seq data using conditional quantile normalization. Biostatistics, 13, 204-216.
34. Harrow, J., Frankish, A., Gonzalez, J.M., Tapanari, E., Diekhans, M., Kokocinski, F., Aken, B.L., Barrell, D., Zadissa, A., Searle, S., et al. (2012). GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res., 22, 1760-1774.
35. Shanley, T.P., Cvijanovich, N., Lin, R., Allen, G.L., Thomas, N.J., Doctor, A., Kalyanaraman, M., Tofil, N.M., Penfil, S., Monaco, M., et al. (2007). Genome-level longitudinal expression of signaling pathways and gene networks in pediatric septic shock. Mol. Med., 13, 495-508.
36. Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2008). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
37. Jiao, X., Sherman, B.T., Huang, D.W., Stephens, R., Baseler, M.W., Lane, H.C., and Lempicki, R.A. (2012). DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics, 28, 1805-1806.
38. McLean, C.Y., Bristor, D., Hiller, M., Clarke, S.L., Schaar, B.T., Lowe, C.B., Wenger, A.M., and Bejerano, G. (2010). GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol., 28, 495-501.
39. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B, 57, 289-300.
40. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. U.S.A., 102, 15545-15550.
41. Sephel, G.C., Buckley, A., and Davidson, J.M. (1987). Developmental initiation of elastin gene expression by human fetal skin fibroblasts. J. Invest. Dermatol., 88, 732-735.
42. Uitto, J. (2008). The role of elastin and collagen in cutaneous aging: intrinsic aging versus photoexposure. J. Drugs Dermatol., 7, S12-S16.
43. Jung, H.-J., Tu, Y., Yang, S.H., Tatar, A., Nobumori, C., Wu, D., Young, S.G., and Fong, L.G. (2014). New Lmna knock-in mice provide a molecular mechanism for the 'segmental aging' in Hutchinson-Gilford progeria syndrome. Hum. Mol. Genet., 23, 1506-1515.
44. Przybilla, J., Galle, J., and Rohlf, T. (2012). Is adult stem cell aging driven by conflicting modes of chromatin remodeling? BioEssays, 34, 841-848.
45. Raddatz, G., Hagemann, S., Aran, D., Sohle, J., Kulkarni, P.P., Kaderali, L., Hellman, A., Winnefeld, M., and Lyko, F. (2013). Aging is associated with highly defined epigenetic changes in the human epidermis. Epigenetics Chromatin, 6, 36.
46. Rauch, T., Li, H., Wu, X., and Pfeifer, G.P. (2006). MIRA-Assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res., 66, 7939-7947.
47. Rauch, T., Wang, Z., Zhang, X., Zhong, X., Wu, X., Lau, S.K., Kernstine, K.H., Riggs, A.D., and Pfeifer, G.P. (2007). Homeobox gene methylation in lung cancer studied by genome-wide analysis with a microarray-based methylated CpG island recovery assay. Proc. Natl Acad. Sci. U.S.A., 104, 5527-5532.
48. Guyon, I., and Elisseeff, A. (2003). An introduction to variable and feature selection. J. Mach. Learn. Res., 3, 1157-1182.
49. Beerman, I., Bock, C., Garrison, B.S., Smith, Z.D., Gu, H., Meissner, A., and Rossi, D.J. (2013). Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging. Cell Stem Cell, 12, 413-425.
50. Teschendorff, A.E., Menon, U., Gentry-Maharaj, A., Ramus, S.J., Weisenberger, D.J., Shen, H., Campan, M., Noushmehr, H., Bell, C.G., Maxwell, A.P., et al. (2010). Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res., 20, 440-446.
51. Rodwell, G.E.J., Sonu, R., Zahn, J.M., Lund, J., Wilhelmy, J., Wang, L., Xiao, W., Mindrinos, M., Crane, E., Segal, E., et al. (2004). A transcriptional profile of aging in the human kidney. PLoS Biol., 2, e427.
52. Zahn, J.M., Sonu, R., Vogel, H., Crane, E., Mazan-Mamczarz, K., Rabkin, R., Davis, R.W., Becker, K.G., Owen, A.B., and Kim, S.K. (2006). Transcriptional profiling of aging in human muscle reveals a common aging signature. PLoS Genet., 2, e115.
53. Eijkelenboom, A., and Burgering, B.M. (2013). FOXOs: signalling integrators for homeostasis maintenance. Nat. Rev. Mol. Cell. Biol., 14, 83-97.
54. Hay, N. (2011). Interplay between FOXO, TOR, and Akt. Biochim. Biophys. Acta, 1813, 1965-1970.
55. Webb, A.E., and Brunet, A. (2014). FOXO transcription factors: key regulators of cellular quality control. Trends Biochem. Sci., 39, 159-169.
56. Lpez-Oti, C., Blasco, M.A., Partridge, L., Serrano, M., and Kroemer, G. (2013). The hallmarks of aging. Cell, 153, 1194-1217.
57. Syntichaki, P., Troulinaki, K., and Tavernarakis, N. (2007). Protein synthesis is a novel determinant of aging in Caenorhabditis elegans. Ann. NY Acad. Sci., 1119, 289-295.
58. Tavernarakis, N. (2008). Ageing and the regulation of protein synthesis: a balancing act? Trends Cell Biol., 18, 228-235.
59. Hansen, M., Taubert, S., Crawford, D., Libina, N., Lee, S.-J., and Kenyon, C. (2007). Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell, 6, 95-110.
60. Hofmann, J.W., Zhao, X., De Cecco, M., Peterson, A.L., Pagliaroli, L., Manivannan, J., Hubbard, G.B., Ikeno, Y., Zhang, Y., Feng, B., et al. (2015). Reduced expression of MYC increases longevity and enhances healthspan. Cell, 160, 477-488.
61. Brown, S.J., Cole, M.D., and Erives, A.J. (2008). Evolution of the holozoan ribosome biogenesis regulon. BMC Genomics, 9, 442.
62. Schrack, J.A., Knuth, N.D., Simonsick, E.M., and Ferrucci, L. (2014). 'IDEAL' aging is associated with lower resting metabolic rate: the Baltimore Longitudinal Study of Aging. J. Am. Geriatr. Soc., 62, 667-672.
63. Hu, F., and Liu, F. (2014). Targeting tissue-specific metabolic signaling pathways in aging: the promise and limitations. Protein Cell, 5, 21-35.
64. Gong, Z., Kennedy, O., Sun, H., Wu, Y., Williams, G.A., Klein, L., Cardoso, L., Matheny, R.W. Jr, Hubbard, G.B., Ikeno, Y., et al. (2014). Reductions in serum IGF-1 during aging impair health span. Aging Cell, 13, 408-418.
65. Vitale, G., Brugts, M.P., Ogliari, G., Castaldi, D., Fatti, L.M., Varewijck, A.J., Lamberts, S.W., Monti, D., Bucci, L., Cevenini, E., et al. (2012). Low circulating IGF-I bioactivity is associated with human longevity: findings in centenarians' offspring. Aging, 4, 580-589.
66. Gems, D., and Partridge, L. (2013). Genetics of longevity in model organisms: debates and paradigm shifts. Annu. Rev. Physiol., 75, 621-644.
67. Sun, D., Luo, M., Jeong, M., Rodriguez, B., Xia, Z., Hannah, R., Wang, H., Le, T., Faull, K.F., Chen, R., et al. (2014). Epigenomic profiling of young and aged HSCs reveals concerted changes during aging that reinforce self-renewal. Cell Stem Cell, 14, 673-688.
68. Le Bot, N. (2014). Tight control of HSC protein synthesis. Nat. Cell Biol., 16, 307-307.
69. Holstege, H., Pfeiffer, W., Sie, D., Hulsman, M., Nicholas, T.J., Lee, C.C., Ross, T., Lin, J., Miller, M.A., Ylstra, B., et al. (2014). Somatic mutations found in the healthy blood compartment of a 115-yr-old woman demonstrate oligoclonal hematopoiesis. Genome Res., 24, 733-742.
70. Salih, D.A.M., and Brunet, A. (2008). FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr. Opin. Cell Biol., 20, 126-136.
71. Schaible, R., and Sussman, M. (2013). FOXO in aging: did evolutionary diversification of FOXO function distract it from prolonging life? BioEssays, 35, 1101-1110.
72. Slack, C., Giannakou, M.E., Foley, A., Goss, M., and Partridge, L. (2011). dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell, 10, 735-748.