Meta-analysis of gene expression in the mouse liver reveals biomarkers associated with inflammation increased early during aging

Mechanisms of Ageing and Development

Volumn 133, Issue 7, 2012, Pages 467-478

  Lee, Janice S ^a   Ward, William O ^a   Ren, Hongzu ^a   Vallanat, Beena ^a   Darlington, Gretchen J ^b   Han, Eun Soo ^c   Laguna, Juan C ^d   DeFord, James H ^e   Papaconstantinou, John ^e   Selman, Colin ^f   Corton, J Christopher ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TULSA   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

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

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Aging; Inflammation; Liver; Longevity; Meta analysis; Microarrays; Xenobiotic metabolism

Indexed keywords

BIOLOGICAL MARKER; RNA;

AGING; ARTICLE; BRAIN; GENE EXPRESSION; INFLAMMATION; LIVER; LONGEVITY; LUNG; METABOLISM; MICROARRAY ANALYSIS; MOUSE; MUSCLE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROGERIA; RNA ISOLATION; WILD TYPE;

AGING; ANIMALS; BIOLOGICAL MARKERS; GENE EXPRESSION REGULATION; INFLAMMATION; LIVER; MALE; MICE; TRANSCRIPTOME;

MUS;

EID: 84864040434     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2012.05.006     Document Type: Article

References (79)

1. Adler A.S., Sinha S., Kawahara T.L., Zhang J.Y., Segal E., Chang H.Y. Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes and Development 2007, 21:3244-3257.
2. Amador-Noguez D., Dean A., Huang W., Setchell K., Moore D., Darlington G. Alterations in xenobiotic metabolism in the long-lived Little mice. Aging Cell 2007, 6:453-470.
3. Amador-Noguez D., Yagi K., Venable S., Darlington G. Gene expression profile of long-lived Ames dwarf mice and Little mice. Aging Cell 2004, 3:423-441.
4. Amador-Noguez D., Zimmerman J., Venable S., Darlington G. Gender-specific alterations in gene expression and loss of liver sexual dimorphism in the long-lived Ames dwarf mice. Biochemical and Biophysical Research Communications 2005, 332:1086-1100.
5. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:7915-7922.
6. Barger J.L., Kayo T., Vann J.M., Arias E.B., Wang J., Hacker T.A., Wang Y., Raederstorff D., Morrow J.D., Leeuwenburgh C., Allison D.B., Saupe K.W., Cartee G.D., Weindruch R., Prolla T.A. A low dose of dietary resveratrol partially mimics caloric restriction and retards aging parameters in mice. PLoS One 2008, 3:e2264.
7. Bartke A., Brown-Borg H. Life extension in the dwarf mouse. Current Topics in Developmental Biology 2004, 63:189-225.
8. Boffoli D., Scacco S.C., Vergari R., Solarino G., Santacroce G., Papa S. Decline with age of the respiratory chain activity in human skeletal muscle. Biochimica et Biophysica Acta 1994, 1226:73-82.
9. Bowling A.C., Mutisya E.M., Walker L.C., Price D.L., Cork L.C., Beal M.F. Age-dependent impairment of mitochondrial function in primate brain. Journal of Neurochemistry 1993, 60:1964-1967.
10. Boylston W.H., DeFord J.H., Papaconstantinou J. Identification of longevity-associated genes in long-lived Snell and Ames dwarf mice. Age 2006, 28:125-144.
11. Boylston W.H., Gerstner A., DeFord J.H., Madsen M., Flurkey K., Harrison D.E., Papaconstantinou J. Altered cholesterologenic and lipogenic transcriptional profile in livers of aging Snell dwarf (Pit1dw/dwJ) mice. Aging Cell 2004, 3:283-296.
12. Butler R.N., Sprott R., Warner H., Bland J., Feuers R., Forster M., Fillit H., Harman S.M., Hewitt M., Hyman M., Johnson K., Kligman E., McClearn G., Nelson J., Richardson A., Sonntag W., Weindruch R., Wolf N. Biomarkers of aging: from primitive organisms to humans. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 2004, 59:B560-B567.
13. Cahan P., Rovegno F., Mooney D., Newman J.C., St Laurent G., McCaffrey T.A. Meta-analysis of microarray results: challenges, opportunities, and recommendations for standardization. Gene 2007, 401:12-18.
14. Chitturi S., Farrell G.C. Etiopathogenesis of nonalcoholic steatohepatitis. Seminars in Liver Disease 2001, 21:27-41.
15. Choi J.K., Yu U., Kim S., Yoo O.J. Combining multiple microarray studies and modeling interstudy variation. Bioinformatics 2003, 19(Suppl. 1):i84-i90.
16. Christensen K., Doblhammer G., Rau R., Vaupel J.W. Ageing populations: the challenges ahead. The Lancet 2009, 374:1196-1208.
17. Cooper J.D., Smyth D.J., Smiles A.M., Plagnol V., Walker N.M., Allen J.E., Downes K., Barrett J.C., Healy B.C., Mychaleckyj J.C., Warram J.H., Todd J.A. Meta-analysis of genome-wide association study data identifies additional type 1 diabetes risk loci. Nature Genetics 2008, 40:1399-1401.
18. Crimmins E., Vasunilashorn S., Kim J.K., Alley D. Biomarkers related to aging in human populations. Advances in Clinical Chemistry 2008, 46:161-216.
19. de Magalhaes J.P., Curado J., Church G.M. Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics 2009, 25:875-881.
20. Dolle M.E., Busuttil R.A., Garcia A.M., Wijnhoven S., van Drunen E., Niedernhofer L.J., van der Horst G., Hoeijmakers J.H., van Steeg H., Vijg J. Increased genomic instability is not a prerequisite for shortened lifespan in DNA repair deficient mice. Mutation Research 2006, 596:22-35.
21. Dozmorov I., Galecki A., Chang Y., Krzesicki R., Vergara M., Miller R.A. Gene expression profile of long-lived snell dwarf mice. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 2002, 57:B99-B108.
22. Edamatsu R., Mori A., Packer L. The spin-trap N-tert-alpha-phenyl-butylnitrone prolongs the life span of the senescence accelerated mouse. Biochemical and Biophysical Research Communications 1995, 211:847-849.
23. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:14863-14868.
24. Elsharkawy A.M., Mann D.A. Nuclear factor-kappaB and the hepatic inflammation-fibrosis-cancer axis. Hepatology 2007, 46:590-597.
25. Engler M.M., Engler M.B., Nguyen H. Age-related changes in plasma and tissue fatty acid composition in Fischer 344 rats. Biochemistry and Molecular Biology International 1998, 46:1117-1126.
26. Estep P.W., Warner J.B., Bulyk M.L. Short-term calorie restriction in male mice feminizes gene expression and alters key regulators of conserved aging regulatory pathways. PLoS One 2009, 4:e5242.
27. Fischer P., Hoek G., Brunekreef B., Verhoeff A., van Wijnen J. Air pollution and mortality in The Netherlands: are the elderly more at risk?. European Respiratory Journal - Supplements 2003, 40:34s-38s.
28. Fu C., Hickey M., Morrison M., McCarter R., Han E.S. Tissue specific and non-specific changes in gene expression by aging and by early stage CR. Mechanisms of Ageing and Development 2006, 127:905-916.
29. Gems D., McElwee J.J. Broad spectrum detoxification: the major longevity assurance process regulated by insulin/IGF-1 signaling?. Mechanisms of Ageing and Development 2005, 126:381-387.
30. Gouveia N., Fletcher T. Time series analysis of air pollution and mortality: effects by cause, age and socioeconomic status. Journal of Epidemiology and Community Health 2000, 54:750-755.
31. Green C.B., Douris N., Kojima S., Strayer C.A., Fogerty J., Lourim D., Keller S.R., Besharse J.C. Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:9888-9893.
32. Guo M., Gong L., He L., Lehman-McKeeman L., Wan Y.J. The expression of cancer-related genes in aging mouse liver is RXRα and gender dependent. Advanced Studies in Biology 2009, 1:61-83.
33. Hayflick L. Biological aging is no longer an unsolved problem. Annals of the New York Academy of Sciences 2007, 1100:1-13.
34. Hayflick L. Entropy explains aging, genetic determinism explains longevity, and undefined terminology explains misunderstanding both. PLoS Genetics 2007, 3:e220.
35. He, W., Sengupta, M., Velkoff, V.A., DeBarros, K.A., 2005. 65+ in the United States: 2005. U.S. Census Bureau.
36. Henthorn P., Kiledjian M., Kadesch T. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. Science 1990, 247:467-470.
37. Hiratsuka S., Watanabe A., Aburatani H., Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nature Cell Biology 2006, 8:1369-1375.
38. Hjelmstrom P. Lymphoid neogenesis: de novo formation of lymphoid tissue in chronic inflammation through expression of homing chemokines. Journal of Leukocyte Biology 2001, 69:331-339.
39. Hong F., Breitling R. A comparison of meta-analysis methods for detecting differentially expressed genes in microarray experiments. Bioinformatics 2008, 24:374-382.
40. Kawai M., Green C.B., Lecka-Czernik B., Douris N., Gilbert M.R., Kojima S., Ackert-Bicknell C., Garg N., Horowitz M.C., Adamo M.L., Clemmons D.R., Rosen C.J. A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-gamma nuclear translocation. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:10508-10513.
41. Kirkwood T.B. Evolution of ageing. Nature 1977, 270:301-304.
42. Kirkwood T.B., Rose M.R. Evolution of senescence: late survival sacrificed for reproduction. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 1991, 332:15-24.
43. Klotz U. Pharmacokinetics and drug metabolism in the elderly. Drug Metabolism Reviews 2009, 41:67-76.
44. Landis G.N., Abdueva D., Skvortsov D., Yang J., Rabin B.E., Carrick J., Tavare S., Tower J. Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:7663-7668.
45. Lee C.K., Weindruch R., Prolla T.A. Gene-expression profile of the ageing brain in mice. Nature Genetics 2000, 25:294-297.
46. Lee J.S., Ward W.O., Wolf D.C., Allen J.W., Mills C., DeVito M.J., Corton J.C. Coordinated changes in xenobiotic metabolizing enzyme gene expression in aging male rats. Toxicological Sciences 2008, 106:263-283.
47. Lee J.S., Ward W.O., Liu J., Ren H., Vallanat B., Delker D., Corton J.C. Hepatic xenobiotic metabolizing enzyme and transporter gene expression through the life stages of the mouse. PLoS One 2011, 6:e24381.
48. McCarroll S.A., Murphy C.T., Zou S., Pletcher S.D., Chin C.S., Jan Y.N., Kenyon C., Bargmann C.I., Li H. Comparing genomic expression patterns across species identifies shared transcriptional profile in aging. Nature Genetics 2004, 36:197-204.
49. McElwee J.J., Schuster E., Blanc E., Piper M.D., Thomas J.H., Patel D.S., Selman C., Withers D.J., Thornton J.M., Partridge L., Gems D. Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biology 2007, 8:R132.
50. Misra V., Lee H., Singh A., Huang K., Thimmulappa R.K., Mitzner W., Biswal S., Tankersley C.G. Global expression profiles from C57BL/6J and DBA/2J mouse lungs to determine aging-related genes. Physiological Genomics 2007, 31:429-440.
51. Mori K., Blackshear P.E., Lobenhofer E.K., Parker J.S., Orzech D.P., Roycroft J.H., Walker K.L., Johnson K.A., Marsh T.A., Irwin R.D., Boorman G.A. Hepatic transcript levels for genes coding for enzymes associated with xenobiotic metabolism are altered with age. Toxicologic Pathology 2007, 35:242-251.
52. Nemeth J., Stein I., Haag D., Riehl A., Longerich T., Horwitz E., Breuhahn K., Gebhardt C., Schirmacher P., Hahn M., Ben-Neriah Y., Pikarsky E., Angel P., Hess J. S100A8 and S100A9 are novel nuclear factor kappa B target genes during malignant progression of murine and human liver carcinogenesis. Hepatology 2009, 50:1251-1262.
53. Oberdoerffer P., Michan S., McVay M., Mostoslavsky R., Vann J., Park S.K., Hartlerode A., Stegmuller J., Hafner A., Loerch P., Wright S.M., Mills K.D., Bonni A., Yankner B.A., Scully R., Prolla T.A., Alt F.W., Sinclair D.A. SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell 2008, 135:907-918.
54. Pagano M.B., Bartoli M.A., Ennis T.L., Mao D., Simmons P.M., Thompson R.W., Pham C.T. Critical role of dipeptidyl peptidase I in neutrophil recruitment during the development of experimental abdominal aortic aneurysms. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:2855-2860.
55. Paradies G., Ruggiero F.M. Age-related changes in the activity of the pyruvate carrier and in the lipid composition in rat-heart mitochondria. Biochimica et Biophysica Acta 1990, 1016:207-212.
56. Park S.K., Page G.P., Kim K., Allison D.B., Meydani M., Weindruch R., Prolla T.A. Alpha- and gamma-tocopherol prevent age-related transcriptional alterations in the heart and brain of mice. Journal of Nutrition 2008, 138:1010-1018.
57. -/- mice. EMBO Journal 2005, 24:861-871.
58. Rossi D.J., Bryder D., Zahn J.M., Ahlenius H., Sonu R., Wagers A.J., Weissman I.L. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:9194-9199.
59. Sandstrom T., Frew A.J., Svartengren M., Viegi G. The need for a focus on air pollution research in the elderly. European Respiratory Journal - Supplements 2003, 40:92s-95s.
60. Schumacher B., van der Pluijm I., Moorhouse M.J., Kosteas T., Robinson A.R., Suh Y., Breit T.M., van Steeg H., Niedernhofer L.J., van Ijcken W., Bartke A., Spindler S.R., Hoeijmakers J.H., van der Horst G.T., Garinis G.A. Delayed and accelerated aging share common longevity assurance mechanisms. PLoS Genetics 2008, 4:e1000161.
61. Selman C., Kerrison N.D., Cooray A., Piper M.D., Lingard S.J., Barton R.H., Schuster E.F., Blanc E., Gems D., Nicholson J.K., Thornton J.M., Partridge L., Withers D.J. Coordinated multitissue transcriptional and plasma metabonomic profiles following acute caloric restriction in mice. Physiological Genomics 2006, 27:187-200.
62. Selman C., Lingard S., Gems D., Partridge L., Withers D.J. Comment on " Brain IRS2 signaling coordinates life span and nutrient homeostasis" Science 2008, 320:1012. (author reply).
63. Singh P., Coskun Z.Z., Goode C., Dean A., Thompson-Snipes L., Darlington G. Lymphoid neogenesis and immune infiltration in aged liver. Hepatology 2008, 47:1680-1690.
64. Swindell W.R. Gene expression profiling of long-lived dwarf mice: longevity-associated genes and relationships with diet, gender and aging. BMC Genomic 2007, 8:353.
65. Thomas R.P., Guigneaux M., Wood T., Evers B.M. Age-associated changes in gene expression patterns in the liver. Journal of Gastrointestinal Surgery 2002, 6:445-453. (discussion 454).
66. Torii K., Sugiyama S., Takagi K., Satake T., Ozawa T. Age-related decrease in respiratory muscle mitochondrial function in rats. American Journal of Respiratory Cell and Molecular Biology 1992, 6:88-92.
67. van der Pluijm I., Garinis G.A., Brandt R.M., Gorgels T.G., Wijnhoven S.W., Diderich K.E., de Wit J., Mitchell J.R., van Oostrom C., Beems R., Niedernhofer L.J., Velasco S., Friedberg E.C., Tanaka K., van Steeg H., Hoeijmakers J.H., van der Horst G.T. Impaired genome maintenance suppresses the growth hormone-insulin-like growth factor 1 axis in mice with Cockayne syndrome. PLoS Biology 2007, 5:e2.
68. Vasto S., Carruba G., Lio D., Colonna-Romano G., Di Bona D., Candore G., Caruso C. Inflammation, ageing and cancer. Mechanisms of Ageing and Development 2009, 130:40-45.
69. Vaupel J.W. Biodemography of human ageing. Nature 2010, 464:536-542.
70. Vila L., Roglans N., Alegret M., Camins A., Pallas M., Sanchez R.M., Vazquez-Carrera M., Laguna J.C. Hepatic gene expression changes in an experimental model of accelerated senescence: the SAM-P8 mouse. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 2008, 63:1043-1052.
71. Waghray A., Keppler D., Sloane B.F., Schuger L., Chen Y.Q. Analysis of a truncated form of cathepsin H in human prostate tumor cells. Journal of Biological Chemistry 2002, 277:11533-11538.
72. Weindruch R., Kayo T., Lee C.K., Prolla T.A. Microarray profiling of gene expression in aging and its alteration by caloric restriction in mice. Journal of Nutrition 2001, 131:918S-923S.
73. Wendt W., Lubbert H., Stichel C.C. Upregulation of cathepsin S in the aging and pathological nervous system of mice. Brain Research 2008, 1232:7-20.
74. Wennmalm K., Wahlestedt C., Larsson O. The expression signature of in vitro senescence resembles mouse but not human aging. Genome Biology 2005, 6:R109.
75. Wilson C.L., Miller C.J. Simpleaffy: a BioConductor package for Affymetrix quality control and data analysis. Bioinformatics 2005, 21:3683-3685.
76. Wu D., Ren Z., Pae M., Guo W., Cui X., Merrill A.H., Meydani S.N. Aging up-regulates expression of inflammatory mediators in mouse adipose tissue. Journal of Immunology 2007, 179:4829-4839.
77. Ye S.M., Johnson R.W. Increased interleukin-6 expression by microglia from brain of aged mice. Journal of Neuroimmunology 1999, 93:139-148.
78. Yuan Q., Bromley S.K., Means T.K., Jones K.J., Hayashi F., Bhan A.K., Luster A.D. CCR4-dependent regulatory T cell function in inflammatory bowel disease. Journal of Experimental Medicine 2007, 204:1327-1334.
79. Zahn J.M., Poosala S., Owen A.B., Ingram D.K., Lustig A., Carter A., Weeraratna A.T., Taub D.D., Gorospe M., Mazan-Mamczarz K., Lakatta E.G., Boheler K.R., Xu X., Mattson M.P., Falco G., Ko M.S., Schlessinger D., Firman J., Kummerfeld S.K., Wood W.H., Zonderman A.B., Kim S.K., Becker K.G. AGEMAP: a gene expression database for aging in mice. PLoS Genetics 2007, 3:e201.