Global genome splicing analysis reveals an increased number of alternatively spliced genes with aging

Aging Cell

Volumn 15, Issue 2, 2016, Pages 267-278

  Rodríguez, Sofía A ^a   Grochová, Diana ^a   Mckenna, Tomás ^a   Borate, Bhavesh ^b   Trivedi, Niraj S ^b   Erdos, Michael R ^b   Eriksson, Maria ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

HGPS; Aging; Alternative splicing; NF B; Progeria; Spliceosome; Transcriptome

Indexed keywords

MUTANT PROTEIN; PROGERIN; UNCLASSIFIED DRUG;

AGING; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE; CONTROLLED STUDY; EXON; GENE; GENOME; MALE; MOUSE; NONHUMAN; PREMATURE AGING; PRIORITY JOURNAL; PROGERIA; SKELETAL MUSCLE; SKIN; THYMUS; WHITE ADIPOSE TISSUE; WILD TYPE; ANIMAL; C57BL MOUSE; FUNCTIONS OF THE SKIN AND ITS APPENDAGES; GENETICS; PATHOLOGY;

AGING; AGING, PREMATURE; ALTERNATIVE SPLICING; ANIMALS; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; SKIN; SKIN PHYSIOLOGICAL PHENOMENA;

EID: 84959933210     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12433     Document Type: Article

References (43)

1. Adler AS, Sinha S, Kawahara TL, Zhang JY, Segal E, Chang HY (2007) Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes Dev. 21, 3244-3257.
2. Baker PB, Baba N, Boesel CP (1981) Cardiovascular abnormalities in progeria. Case report and review of the literature. Arch. Pathol. Lab. Med. 105, 384-386.
3. Black DL, Grabowski PJ (2003) Alternative pre-mRNA splicing and neuronal function. Prog. Mol. Subcell. Biol. 31, 187-216.
4. Brow DA (2002) Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36, 333-360.
5. Cao K, Capell BC, Erdos MR, Djabali K, Collins FS (2007) A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc. Natl Acad. Sci. USA 104, 4949-4954.
6. Cao K, Blair CD, Faddah DA, Kieckhaefer JE, Olive M, Erdos MR, Nabel EG, Collins FS (2011) Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest. 121, 2833-2844.
7. Chen M, Manley JL (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol. 10, 741-754.
8. Csoka AB, English SB, Simkevich CP, Ginzinger DG, Butte AJ, Schatten GP, Rothman FG, Sedivy JM (2004) Genome-scale expression profiling of Hutchinson-Gilford progeria syndrome reveals widespread transcriptional misregulation leading to mesodermal/mesenchymal defects and accelerated atherosclerosis. Aging Cell 3, 235-243.
9. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FS (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298.
10. Ferguson VL, Ayers RA, Bateman TA, Simske SJ (2003) Bone development and age-related bone loss in male C57BL/6J mice. Bone 33, 387-398.
11. Gaidatzis D, Jacobeit K, Oakeley EJ, Stadler MB (2009) Overestimation of alternative splicing caused by variable probe characteristics in exon arrays. Nucleic Acids Res. 37, e107.
12. Glatt V, Canalis E, Stadmeyer L, Bouxsein ML (2007) Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J. Bone Miner. Res. 22, 1197-1207.
13. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, Collins FS (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 101, 8963-8968.
14. Guo Z, Karunatilaka KS, Rueda D (2009) Single-molecule analysis of protein-free U2-U6 snRNAs. Nat. Struct. Mol. Biol. 16, 1154-1159.
15. Hanif M, Rosengardten Y, Sagelius H, Rozell B, Eriksson M (2009) Differential expression of A type and B-type lamins during hair cycling. PLoS ONE 4, e4114.
16. 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.
17. Holly AC, Melzer D, Pilling LC, Fellows AC, Tanaka T, Ferrucci L, Harries LW (2013) Changes in splicing factor expression are associated with advancing age in man. Mech. Ageing Dev. 134, 356-366.
18. Hsia N, Cornwall GA (2004) DNA microarray analysis of region-specific gene expression in the mouse epididymis. Biol. Reprod. 70, 448-457.
19. Huang TT, Wuerzberger-Davis SM, Wu ZH, Miyamoto S (2003) Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell 115, 565-576.
20. Lazuardi L, Herndler-Brandstetter D, Brunner S, Laschober GT, Lepperdinger G, Grubeck-Loebenstein B (2009) Microarray analysis reveals similarity between CD8+CD28- T cells from young and elderly persons, but not of CD8+CD28+ T cells. Biogerontology 10, 191-202.
21. Ly DH, Lockhart DJ, Lerner RA, Schultz PG (2000) Mitotic misregulation and human aging. Science 287, 2486-2492.
22. Maniatis T, Tasic B (2002) Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418, 236-243.
23. Martin GM (2005) Genetic modulation of senescent phenotypes in Homo sapiens. Cell 120, 523-532.
24. Mazin P, Xiong J, Liu X, Yan Z, Zhang X, Li M, He L, Somel M, Yuan Y, Phoebe Chen YP, Li N, Hu Y, Fu N, Ning Z, Zeng R, Yang H, Chen W, Gelfand M, Khaitovich P (2013) Widespread splicing changes in human brain development and aging. Mol. Syst. Biol. 9, 633.
25. McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, Collins FS, Djabali K (2007) The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS ONE 2, e1269.
26. McCord RP, Nazario-Toole A, Zhang H, Chines PS, Zhan Y, Erdos MR, Collins FS, Dekker J, Cao K (2013) Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res. 23, 260-269.
27. McKenna T, Rosengardten Y, Viceconte N, Baek JH, Grochova D, Eriksson M (2014) Embryonic expression of the common progeroid lamin A splice mutation arrests postnatal skin development. Aging Cell 13, 292-302.
28. Meshorer E, Soreq H (2002) Pre-mRNA splicing modulations in senescence. Aging Cell 1, 10-16.
29. Modrek B, Lee C (2002) A genomic view of alternative splicing. Nat. Genet. 30, 13-19.
30. Rodriguez S, Coppedè F, Sagelius H, Eriksson M (2009) Increased expression of the Hutchinson Gilford progeria syndrome truncated lamin A transcript during cell aging. Eur. J. Hum. Genet. 17, 928-937.
31. Rosengardten Y, McKenna T, Grochova D, Eriksson M (2011) Stem cell depletion in Hutchinson-Gilford progeria syndrome. Aging Cell 10, 1011-1020.
32. Sagelius H, Rosengardten Y, Hanif M, Erdos MR, Rozell B, Collins FS, Eriksson M (2008a) Targeted transgenic expression of the mutation causing Hutchinson-Gilford progeria syndrome leads to proliferative and degenerative epidermal disease. J. Cell Sci. 121, 969-978.
33. Sagelius H, Rosengardten Y, Schmidt E, Sonnabend C, Rozell B, Eriksson M (2008b) Reversible phenotype in a mouse model of Hutchinson-Gilford progeria syndrome. J. Med. Genet. 45, 794-801.
34. Scaffidi P, Misteli T (2006) Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063.
35. Scaffidi P, Misteli T (2008) Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat. Cell Biol. 10, 452-459.
36. Singh RK, Cooper TA (2012) Pre-mRNA splicing in disease and therapeutics. Trends Mol. Med. 18, 472-482.
37. Sohal RS, Ferguson M, Sohal BH, Forster MJ (2009) Life span extension in mice by food restriction depends on an energy imbalance. J. Nutr. 139, 533-539.
38. Tollervey JR, Wang Z, Hortobagyi T, Witten JT, Zarnack K, Kayikci M, Clark TA, Schweitzer AC, Rot G, Curk T, Zupan B, Rogelj B, Shaw CE, Ule J (2011) Analysis of alternative splicing associated with aging and neurodegeneration in the human brain. Genome Res. 21, 1572-1582.
39. Wang J, Duncan D, Shi Z, Zhang B (2013) WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res. 41, W77-W83.
40. Wu ZH, Shi Y, Tibbetts RS, Miyamoto S (2006) Molecular linkage between the kinase ATM and NF-kappaB signaling in response to genotoxic stimuli. Science 311, 1141-1146.
41. Yannarell A, Schumm DE, Webb TE (1977) Age-dependence of nuclear RNA processing. Mech. Ageing Dev. 6, 259-264.
42. Zahn JM, Poosala S, Owen AB, Ingram DK, Lustig A, Carter A, Weeraratna AT, Taub DD, Gorospe M, Mazan-Mamczarz K, Lakatta EG, Boheler KR, Xu X, Mattson MP, Falco G, Ko MS, Schlessinger D, Firman J, Kummerfeld SK, Wood WH 3rd, Zonderman AB, Kim SK, Becker KG (2007) AGEMAP: a gene expression database for aging in mice. PLoS Genet. 3, e201.
43. Zhang B, Kirov S, Snoddy J (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 33, W741-W748.