Meta-analysis on blood transcriptomic studies identifies consistently coexpressed protein-protein interaction modules as robust markers of human aging

Aging Cell

Volumn 13, Issue 2, 2014, Pages 216-225

  Van den Akker, Erik B ^a,b   Passtoors, Willemijn M ^a   Jansen, Rick ^c,d   van Zwet, Erik W ^a   Goeman, Jelle J ^a   Hulsman, Marc ^b   Emilsson, Valur ^e   Perola, Markus ^f   Willemsen, Gonneke ^g   Penninx, Brenda W J H ^c,d   Heijmans, Bas T ^a   Maier, Andrea B ^c   Boomsma, Dorret I ^d,g   Kok, Joost N ^a,h   Slagboom, Pieternella E ^a   Reinders, Marcel J T ^b   Beekman, Marian ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e ICELANDIC HEART ASSOCIATION   (Iceland)

^f NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^g VU UNIVERSITY AMSTERDAM   (Netherlands)

^h LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Aging; Blood transcriptomics; Meta analysis; Network based analysis; Protein protein interactions

Indexed keywords

BIOLOGICAL MARKER; DNA; PROTEIN; TRANSCRIPTOME;

ADOLESCENT; ADULT; AGE; AGED; ARTICLE; BLOOD ANALYSIS; BLOOD SAMPLING; CELL AGING; CYTOLYSIS; DNA METABOLISM; FEMALE; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; GENETIC DATABASE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; LONGEVITY; LYMPHOCYTE COUNT; MALE; META ANALYSIS (TOPIC); MIDDLE AGED; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SURVIVAL RATE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTOMICS; VERY ELDERLY; YOUNG ADULT;

AGING; BLOOD TRANSCRIPTOMICS; META-ANALYSIS; NETWORK-BASED ANALYSIS; PROTEIN-PROTEIN INTERACTIONS;

AGED, 80 AND OVER; AGING; BIOLOGICAL MARKERS; CELL CYCLE PROTEINS; DATABASES, GENETIC; GENE EXPRESSION REGULATION; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; PROTEIN INTERACTION MAPS; REPRODUCIBILITY OF RESULTS; SURVIVAL ANALYSIS; T-LYMPHOCYTES; TRANSCRIPTOME;

EID: 84895812671     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12160     Document Type: Article

References (45)

1. van den Akker EB, Verbruggen B, Heijmans BT, Beekman M, Kok JN, Slagboom PE, Reinders MJ (2011) Integrating protein-protein interaction networks with gene-gene co-expression networks improves gene signatures for classifying breast cancer metastasis. J. Integr. Bioinform. 8, 188.
2. Baker DJ, Jeganathan KB, Malureanu L, Perez-Terzic C, Terzic A, van Deursen JM (2006) Early aging-associated phenotypes in Bub3/Rae1 haploinsufficient mice. J. Cell Biol. 172, 529-540.
3. Bell R, Hubbard A, Chettier R, Chen D, Miller JP, Kapahi P, Tarnopolsky M, Sahasrabuhde S, Melov S, Hughes RE (2009) A human protein interaction network shows conservation of aging processes between human and invertebrate species. PLoS Genet. 5, e1000414.
4. Boomsma DI, Willemsen G, Sullivan PF, Heutink P, Meijer P, Sondervan D, Kluft C, Smit G, Nolen WA, Zitman FG, Smit JH, Hoogendijk WJ, van Dyck R, de Geus EJ, Penninx BW (2008) Genome-wide association of major depression: description of samples for the GAIN Major Depressive Disorder Study: NTR and NESDA biobank projects. Eur. J. Hum. Genet. 16, 335-342.
5. Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573, 83-92.
6. Calnan DR, Brunet A (2008) The FoxO code. Oncogene 27, 2276-2288.
7. Chen Y, Liu W, McPhie DL, Hassinger L, Neve RL (2003) APP-BP1 mediates APP-induced apoptosis and DNA synthesis and is increased in Alzheimer's disease brain. J. Cell Biol. 163, 27-33.
8. Chi H (2012) Regulation and function of mTOR signalling in T cell fate decisions. Nat. Rev. Immunol. 12, 325-338.
9. Clemens MJ (2001) Initiation factor eIF2 alpha phosphorylation in stress responses and apoptosis. Prog. Mol. Subcell. Biol. 27, 57-89.
10. Curran SP, Ruvkun G (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 3, e56.
11. Dall'olio F, Vanhooren V, Chen CC, Slagboom PE, Wuhrer M, Franceschi C (2013) N-glycomic biomarkers of biological aging and longevity: a link with inflammaging. Ageing Res. Rev. 12, 685-698.
12. Derhovanessian E, Maier AB, Beck R, Jahn G, Hahnel K, Slagboom PE, de Craen AJ, Westendorp RG, Pawelec G (2010) Hallmark features of immunosenescence are absent in familial longevity. J. Immunol. 185, 4618-4624.
13. Emilsson V, Thorleifsson G, Zhang B, Leonardson AS, Zink F, Zhu J, Carlson S, Helgason A, Walters GB, Gunnarsdottir S, Mouy M, Steinthorsdottir V, Eiriksdottir GH, Bjornsdottir G, Reynisdottir I, Gudbjartsson D, Helgadottir A, Jonasdottir A, Jonasdottir A, Styrkarsdottir U, Gretarsdottir S, Magnusson KP, Stefansson H, Fossdal R, Kristjansson K, Gislason HG, Stefansson T, Leifsson BG, Thorsteinsdottir U, Lamb JR, Gulcher JR, Reitman ML, Kong A, Schadt EE, Stefansson K (2008) Genetics of gene expression and its effect on disease. Nature 452, 423-428.
14. Fan AC, Kozlov G, Hoegl A, Marcellus RC, Wong MJ, Gehring K, Young JC (2011) Interaction between the human mitochondrial import receptors Tom20 and Tom70 in vitro suggests a chaperone displacement mechanism. J. Biol. Chem. 286, 32208-32219.
15. Goring HH, Curran JE, Johnson MP, Dyer TD, Charlesworth J, Cole SA, Jowett JB, Abraham LJ, Rainwater DL, Comuzzie AG, Mahaney MC, Almasy L, MacCluer JW, Kissebah AH, Collier GR, Moses EK, Blangero J (2007) Discovery of expression QTLs using large-scale transcriptional profiling in human lymphocytes. Nat. Genet. 39, 1208-1216.
16. Grube K, Burkle A (1992) Poly(ADP-ribose) polymerase activity in mononuclear leukocytes of 13 mammalian species correlates with species-specific life span. Proc. Natl Acad. Sci. USA 89, 11759-11763.
17. Harries LW, Hernandez D, Henley W, Wood AR, Holly AC, Bradley-Smith RM, Yaghootkar H, Dutta A, Murray A, Frayling TM, Guralnik JM, Bandinelli S, Singleton A, Ferrucci L, Melzer D (2011) Human aging is characterized by focused changes in gene expression and deregulation of alternative splicing. Aging Cell 10, 868-878.
18. Hitt R, Young-Xu Y, Silver M, Perls T (1999) Centenarians: the older you get, the healthier you have been. Lancet 354, 652.
19. Hong MG, Myers AJ, Magnusson PK, Prince JA (2008) Transcriptome-wide assessment of human brain and lymphocyte senescence. PLoS ONE 3, e3024.
20. Inouye M, Silander K, Hamalainen E, Salomaa V, Harald K, Jousilahti P, Mannisto S, Eriksson JG, Saarela J, Ripatti S, Perola M, van Ommen GJ, Taskinen MR, Palotie A, Dermitzakis ET, Peltonen L (2010) An immune response network associated with blood lipid levels. PLoS Genet. 6, e1001113.
21. Johnson SC, Rabinovitch PS, Kaeberlein M (2013) mTOR is a key modulator of ageing and age-related disease. Nature 493, 338-345.
22. Kirkwood TB (1977) Evolution of ageing. Nature 270, 301-304.
23. von Kobbe C, Harrigan JA, May A, Opresko PL, Dawut L, Cheng WH, Bohr VA (2003) Central role for the Werner syndrome protein/poly(ADP-ribose) polymerase 1 complex in the poly(ADP-ribosyl)ation pathway after DNA damage. Mol. Cell. Biol. 23, 8601-8613.
24. Koziol JA (2010) Comments on the rank product method for analyzing replicated experiments. FEBS Lett. 584, 941-944.
25. Laplante M, Sabatini DM (2009) mTOR signaling at a glance. J. Cell Sci. 122, 3589-3594.
26. de Magalhaes JP, Toussaint O (2004) GenAge: a genomic and proteomic network map of human ageing. FEBS Lett. 571, 243-247.
27. de Magalhaes JP, Curado J, Church GM (2009) Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics 25, 875-881.
28. Marbach D, Costello JC, Kuffner R, Vega NM, Prill RJ, Camacho DM, Allison KR, Consortium D, Kellis M, Collins JJ, Stolovitzky G (2012) Wisdom of crowds for robust gene network inference. Nat. Methods 9, 796-804.
29. McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr. Biol. 16, R551-R560.
30. Napoli AM, Fast LD, Gardiner F, Nevola M, Machan JT (2012) Increased granzyme levels in cytotoxic T lymphocytes are associated with disease severity in emergency department patients with severe sepsis. Shock 37, 257-262.
31. Oeppen J, Vaupel JW (2002) Demography. Broken limits to life expectancy. Science 296, 1029-1031.
32. Partridge L, Gems D (2002) Mechanisms of ageing: public or private? Nat. Rev. Genet. 3, 165-175.
33. Passtoors WM, Beekman M, Gunn D, Boer JM, Heijmans BT, Westendorp RG, Zwaan BJ, Slagboom PE (2008) Genomic studies in ageing research: the need to integrate genetic and gene expression approaches. J. Intern. Med. 263, 153-166.
34. Passtoors WM, Boer JM, Goeman JJ, Akker EB, Deelen J, Zwaan BJ, Scarborough A, Breggen R, Vossen RH, Houwing-Duistermaat JJ, Ommen GJ, Westendorp RG, van Heemst D, de Craen AJ, White AJ, Gunn DA, Beekman M, Slagboom PE (2012) Transcriptional profiling of human familial longevity indicates a role for ASF1A and IL7R. PLoS ONE 7, e27759.
35. Passtoors WM, Beekman M, Deelen J, van der Breggen R, Maier AB, Guigas B, Derhovanessian E, van Heemst D, de Craen AJ, Gunn DA, Pawelec G, Slagboom PE (2013) Gene expression analysis of mTOR pathway: association with human longevity. Aging Cell 12, 24-31.
36. Pawelec G, Solana R (1997) Immunosenescence. Immunol. Today 18, 514-516.
37. Smith ED, Tsuchiya M, Fox LA, Dang N, Hu D, Kerr EO, Johnston ED, Tchao BN, Pak DN, Welton KL, Promislow DE, Thomas JH, Kaeberlein M, Kennedy BK (2008) Quantitative evidence for conserved longevity pathways between divergent eukaryotic species. Genome Res. 18, 564-570.
38. Southworth LK, Owen AB, Kim SK (2009) Aging mice show a decreasing correlation of gene expression within genetic modules. PLoS Genet. 5, e1000776.
39. Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302, 249-255.
40. Tacutu R, Shore DE, Budovsky A, de Magalhaes JP, Ruvkun G, Fraifeld VE, Curran SP (2012) Prediction of C. elegans longevity genes by human and worm longevity networks. PLoS ONE 7, e48282.
41. Wilson PW, D'Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB (1998) Prediction of coronary heart disease using risk factor categories. Circulation 97, 1837-1847.
42. Witten TM, Bonchev D (2007) Predicting aging/longevity-related genes in the nematode Caenorhabditis elegans. Chem. Biodivers. 4, 2639-2655.
43. Xue H, Xian B, Dong D, Xia K, Zhu S, Zhang Z, Hou L, Zhang Q, Zhang Y, Han JD (2007) A modular network model of aging. Mol. Syst. Biol. 3, 147.
44. Zahn JM, Sonu R, Vogel H, Crane E, Mazan-Mamczarz K, Rabkin R, Davis RW, Becker KG, Owen AB, Kim SK (2006) Transcriptional profiling of aging in human muscle reveals a common aging signature. PLoS Genet. 2, e115.
45. Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol. 4, Article17.