Reduced Expression of MYC Increases Longevity and Enhances Healthspan

Cell - Tập 160 - Trang 477-488 - 2015
Jeffrey W. Hofmann1, Xiaoai Zhao2, Marco De Cecco1, Abigail L. Peterson1, Luca Pagliaroli1, Jayameenakshi Manivannan1, Gene B. Hubbard3, Yuji Ikeno3, Yongqing Zhang4, Bin Feng5, Xiaxi Li6, Thomas Serre6, Wenbo Qi3, Holly Van Remmen3, Richard A. Miller7, Kevin G. Bath6, Rafael de Cabo4, Haiyan Xu5, Nicola Neretti1, John M. Sedivy1
1Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, RI 02912 USA
2Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, RI 02912, USA
3Department of Cellular and Structural Biology, Barshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA
4Translational Gerontology Branch, National Institute on Aging, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA
5Hallett Center for Diabetes and Endocrinology, Rhode Island Hospital, Warren Alpert Medical School of Brown University, Providence, RI 02903, USA
6Department of Cognitive, Linguistic, and Psychological Sciences, Brown University, Providence, RI 02912, USA
7Department of Pathology and Geriatrics Center, University of Michigan, Ann Arbor, MI 48109, USA

Tài liệu tham khảo

Akbar, 2011, Are senescence and exhaustion intertwined or unrelated processes that compromise immunity?, Nat. Rev. Immunol., 11, 289, 10.1038/nri2959 Anisimov, 2004, Body weight is not always a good predictor of longevity in mice, Exp. Gerontol., 39, 305, 10.1016/j.exger.2003.12.007 Bartke, 2012, Metabolic characteristics of long-lived mice, Front. Genet., 3, 288, 10.3389/fgene.2012.00288 Brown, 2008, Evolution of the holozoan ribosome biogenesis regulon, BMC Genomics, 9, 442, 10.1186/1471-2164-9-442 Brown-Borg, 2012, Expression of oxidative phosphorylation components in mitochondria of long-living Ames dwarf mice, Age (Dordr.), 34, 43, 10.1007/s11357-011-9212-x Cho, 2008, A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells, Blood, 111, 5553, 10.1182/blood-2007-11-123547 Dai, 2009, Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging, Circulation, 119, 2789, 10.1161/CIRCULATIONAHA.108.822403 Dang, 2012, MYC on the path to cancer, Cell, 149, 22, 10.1016/j.cell.2012.03.003 de Alboran, 2001, Analysis of C-MYC function in normal cells via conditional gene-targeted mutation, Immunity, 14, 45, 10.1016/S1074-7613(01)00088-7 Dey, 2013, PERK-ing up autophagy during MYC-induced tumorigenesis, Autophagy, 9, 612, 10.4161/auto.23486 Eilers, 2008, Myc’s broad reach, Genes Dev., 22, 2755, 10.1101/gad.1712408 Fujimoto, 2011, Not just fat: the structure and function of the lipid droplet, Cold Spring Harb. Perspect. Biol., 3, 3, 10.1101/cshperspect.a004838 Gems, 2013, Genetics of longevity in model organisms: debates and paradigm shifts, Annu. Rev. Physiol., 75, 621, 10.1146/annurev-physiol-030212-183712 Gomes, 2013, Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging, Cell, 155, 1624, 10.1016/j.cell.2013.11.037 Goronzy, 2005, T cell development and receptor diversity during aging, Curr. Opin. Immunol., 17, 468, 10.1016/j.coi.2005.07.020 Greer, 2013, Myc-dependent genome instability and lifespan in Drosophila, PLoS ONE, 8, e74641, 10.1371/journal.pone.0074641 Heiman, 2003, Body composition of prolactin-, growth hormone, and thyrotropin-deficient Ames dwarf mice, Endocrine, 20, 149, 10.1385/ENDO:20:1-2:149 Herkert, 2010, Transcriptional repression: the dark side of myc, Genes Cancer, 1, 580, 10.1177/1947601910379012 Hoeijmakers, 2009, DNA damage, aging, and cancer, N. Engl. J. Med., 361, 1475, 10.1056/NEJMra0804615 Ikeno, 2003, Delayed occurrence of fatal neoplastic diseases in Ames dwarf mice: correlation to extended longevity, J. Gerontol. A Biol. Sci. Med. Sci., 58, 291, 10.1093/gerona/58.4.B291 Jang, 2011, Skeletal muscle stem cells: effects of aging and metabolism on muscle regenerative function, Cold Spring Harb. Symp. Quant. Biol., 76, 101, 10.1101/sqb.2011.76.010652 Jhuang, 2010, Automated home-cage behavioural phenotyping of mice, Nat. Commun., 1, 68, 10.1038/ncomms1064 Johnson, 2013, mTOR is a key modulator of ageing and age-related disease, Nature, 493, 338, 10.1038/nature11861 Kujoth, 2005, Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging, Science, 309, 481, 10.1126/science.1112125 Ladiges, 2009, Lifespan extension in genetically modified mice, Aging Cell, 8, 346, 10.1111/j.1474-9726.2009.00491.x Lanza, 2012, Chronic caloric restriction preserves mitochondrial function in senescence without increasing mitochondrial biogenesis, Cell Metab., 16, 777, 10.1016/j.cmet.2012.11.003 Lee, 2011, Fasting vs dietary restriction in cellular protection and cancer treatment: from model organisms to patients, Oncogene, 30, 3305, 10.1038/onc.2011.91 Li, 2013, Direct and indirect effects of growth hormone receptor ablation on liver expression of xenobiotic metabolizing genes, Am. J. Physiol. Endocrinol. Metab., 305, E942, 10.1152/ajpendo.00304.2013 Martin-Montalvo, 2013, Metformin improves healthspan and lifespan in mice, Nat. Commun., 4, 2192, 10.1038/ncomms3192 Mateyak, 1997, Phenotypes of c-Myc-deficient rat fibroblasts isolated by targeted homologous recombination, Cell Growth Differ., 8, 1039 Matheu, 2004, Increased gene dosage of Ink4a/Arf results in cancer resistance and normal aging, Genes Dev., 18, 2736, 10.1101/gad.310304 Meyer, 2008, Reflecting on 25 years with MYC, Nat. Rev. Cancer, 8, 976, 10.1038/nrc2231 Neff, 2013, Rapamycin extends murine lifespan but has limited effects on aging, J. Clin. Invest., 123, 3272, 10.1172/JCI67674 Pearson, 2008, Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span, Cell Metab., 8, 157, 10.1016/j.cmet.2008.06.011 Peck, 2013, Antagonism between FOXO and MYC regulates cellular powerhouse, Front. Oncol., 3, 96, 10.3389/fonc.2013.00096 Salmon, 2010, Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging?, Free Radic. Biol. Med., 48, 642, 10.1016/j.freeradbiomed.2009.12.015 Syed, 2011, Rodent models of aging bone: an update, Curr. Osteoporos. Rep., 9, 219, 10.1007/s11914-011-0074-z Teleman, 2008, Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila, Cell Metab., 7, 21, 10.1016/j.cmet.2007.11.010 Trumpp, 2001, c-Myc regulates mammalian body size by controlling cell number but not cell size, Nature, 414, 768, 10.1038/414768a Tsuchiya, 2004, Additive regulation of hepatic gene expression by dwarfism and caloric restriction, Physiol. Genomics, 17, 307, 10.1152/physiolgenomics.00039.2004 Vafa, 2002, c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability, Mol. Cell, 9, 1031, 10.1016/S1097-2765(02)00520-8 Wang, 2011, Immunoaging induced by hematopoietic stem cell aging, Curr. Opin. Immunol., 23, 532, 10.1016/j.coi.2011.05.004 Wang, 2011, The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation, Immunity, 35, 871, 10.1016/j.immuni.2011.09.021 Whitfield, 2012, Tumor microenvironment: becoming sick of Myc, Cell. Mol. Life Sci., 69, 931, 10.1007/s00018-011-0860-x Wu, 2013, Increased mammalian lifespan and a segmental and tissue-specific slowing of aging after genetic reduction of mTOR expression, Cell Rep., 4, 913, 10.1016/j.celrep.2013.07.030 Yuan, 2009, Aging in inbred strains of mice: study design and interim report on median lifespans and circulating IGF1 levels, Aging Cell, 8, 277, 10.1111/j.1474-9726.2009.00478.x Zahn, 2007, AGEMAP: a gene expression database for aging in mice, PLoS Genet., 3, e201, 10.1371/journal.pgen.0030201 Algire, 2012, Metformin reduces endogenous reactive oxygen species and associated DNA damage, Cancer Prev. Res. (Phila.), 5, 536, 10.1158/1940-6207.CAPR-11-0536 Arum, 2013, Prevention of neuromusculoskeletal frailty in slow-aging Ames dwarf mice: longitudinal investigation of interaction of longevity genes and caloric restriction, PLoS ONE, 8, e72255, 10.1371/journal.pone.0072255 Bartke, 2004, Life extension in the dwarf mouse, Curr. Top. Dev. Biol., 63, 189, 10.1016/S0070-2153(04)63006-7 Bartke, 2013, Somatotropic signaling: trade-offs between growth, reproductive development, and longevity, Physiol. Rev., 93, 571, 10.1152/physrev.00006.2012 Bokov, 2011, Does reduced IGF-1R signaling in Igf1r+/- mice alter aging?, PLoS ONE, 6, e26891, 10.1371/journal.pone.0026891 Bonkowski, 2006, Long-lived growth hormone receptor knockout mice show a delay in age-related changes of body composition and bone characteristics, J. Gerontol. A Biol. Sci. Med. Sci., 61, 562, 10.1093/gerona/61.6.562 Cheadle, 2003, Analysis of microarray data using Z score transformation, J. Mol. Diagn., 5, 73, 10.1016/S1525-1578(10)60455-2 Conover, 2007, Loss of pregnancy-associated plasma protein A extends lifespan in mice, Aging Cell, 6, 727, 10.1111/j.1474-9726.2007.00328.x Conover, 2004, Metalloproteinase pregnancy-associated plasma protein A is a critical growth regulatory factor during fetal development, Development, 131, 1187, 10.1242/dev.00997 Coschigano, 2003, Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span, Endocrinology, 144, 3799, 10.1210/en.2003-0374 Cufí, 2012, Metformin lowers the threshold for stress-induced senescence: a role for the microRNA-200 family and miR-205, Cell Cycle, 11, 1235, 10.4161/cc.11.6.19665 Dai, 2014, Rapamycin drives selection against a pathogenic heteroplasmic mitochondrial DNA mutation, Hum. Mol. Genet., 23, 637, 10.1093/hmg/ddt450 Danilovich, 1999, Deficits in female reproductive function in GH-R-KO mice; role of IGF-I, Endocrinology, 140, 2637, 10.1210/endo.140.6.6992 Debacq-Chainiaux, 2009, Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo, Nat. Protoc., 4, 1798, 10.1038/nprot.2009.191 Donato, 2013, Life-long caloric restriction reduces oxidative stress and preserves nitric oxide bioavailability and function in arteries of old mice, Aging Cell, 12, 772, 10.1111/acel.12103 Ecarot-Charrier, 1983, Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture, J. Cell Biol., 96, 639, 10.1083/jcb.96.3.639 Folch, 1957, A simple method for the isolation and purification of total lipides from animal tissues, J. Biol. Chem., 226, 497, 10.1016/S0021-9258(18)64849-5 Garcia, 2008, Effect of Ames dwarfism and caloric restriction on spontaneous DNA mutation frequency in different mouse tissues, Mech. Ageing Dev., 129, 528, 10.1016/j.mad.2008.04.013 Garcia-Cao, 2012, Systemic elevation of PTEN induces a tumor-suppressive metabolic state, Cell, 149, 49, 10.1016/j.cell.2012.02.030 Garlick, 1980, A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of [3H]phenylalanine, Biochem. J., 192, 719, 10.1042/bj1920719 Hamrick, 2008, Caloric restriction decreases cortical bone mass but spares trabecular bone in the mouse skeleton: implications for the regulation of bone mass by body weight, J. Bone Miner. Res., 23, 870, 10.1359/jbmr.080213 Harper, 2007, Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone, Aging Cell, 6, 1, 10.1111/j.1474-9726.2006.00255.x Harrison, 2009, Rapamycin fed late in life extends lifespan in genetically heterogeneous mice, Nature, 460, 392, 10.1038/nature08221 Harvey, 2013, Decreased systemic IGF-1 in response to calorie restriction modulates murine tumor cell growth, nuclear factor-κB activation, and inflammation-related gene expression, Mol. Carcinog., 52, 997, 10.1002/mc.21940 Holzenberger, 2003, IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice, Nature, 421, 182, 10.1038/nature01298 Hsieh, 2009, Dermal fibroblasts from long-lived Ames dwarf mice maintain their in vivo resistance to mitochondrial generated reactive oxygen species (ROS), Aging (Albany, N.Y. Online), 1, 784 Jeyapalan, 2013, How to measure RNA expression in rare senescent cells expressing any specific protein such as p16Ink4a, Aging (Albany, N.Y. Online), 5, 120 Jeyapalan, 2007, Accumulation of senescent cells in mitotic tissue of aging primates, Mech. Ageing Dev., 128, 36, 10.1016/j.mad.2006.11.008 Kaeberlein, 2013, mTOR inhibition: from aging to autism and beyond, Scientifica (Cairo), 2013, 849186 Kamentsky, 2011, Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software, Bioinformatics, 27, 1179, 10.1093/bioinformatics/btr095 Kendziorski, 2005, On the utility of pooling biological samples in microarray experiments, Proc. Natl. Acad. Sci. USA, 102, 4252, 10.1073/pnas.0500607102 Kreiling, 2011, Age-associated increase in heterochromatic marks in murine and primate tissues, Aging Cell, 10, 292, 10.1111/j.1474-9726.2010.00666.x Kristan, 2007, Chronic calorie restriction increases susceptibility of laboratory mice (Mus musculus) to a primary intestinal parasite infection, Aging Cell, 6, 817, 10.1111/j.1474-9726.2007.00345.x Kurki, 2012, Distinct effects of calorie restriction on adipose tissue cytokine and angiogenesis profiles in obese and lean mice, Nutr. Metab. (Lond), 9, 64, 10.1186/1743-7075-9-64 Lee, 2012, Fasting cycles retard growth of tumors and sensitize a range of cancer cell types to chemotherapy, Sci. Transl. Med., 4, 124, 10.1126/scitranslmed.3003293 Ma, 2006, Suppression of insulin receptor substrate 1 (IRS-1) promotes mammary tumor metastasis, Mol. Cell. Biol., 26, 9338, 10.1128/MCB.01032-06 Masternak, 2012, Metabolic effects of intra-abdominal fat in GHRKO mice, Aging Cell, 11, 73, 10.1111/j.1474-9726.2011.00763.x Mercken, 2012, Of mice and men: the benefits of caloric restriction, exercise, and mimetics, Ageing Res. Rev., 11, 390, 10.1016/j.arr.2011.11.005 Miller, 2007, An Aging Interventions Testing Program: study design and interim report, Aging Cell, 6, 565, 10.1111/j.1474-9726.2007.00311.x Miller, 2011, Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice, J. Gerontol. A Biol. Sci. Med. Sci., 66, 191, 10.1093/gerona/glq178 Miyoshi, 2013, Effect of the anti-diabetic drug metformin in hepatocellular carcinoma in vitro and in vivo, Int. J. Oncol. Müller, 2013, Concurrent inhibition of PI3K and mTORC1/mTORC2 overcomes resistance to rapamycin induced apoptosis by down-regulation of Mcl-1 in mantle cell lymphoma, Int. J. Cancer, 133, 1813, 10.1002/ijc.28206 Murasko, 2005, Response of aged mice to primary virus infections, Immunol. Rev., 205, 285, 10.1111/j.0105-2896.2005.00273.x Nagy, 1998, Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles, Curr. Biol., 8, 661, 10.1016/S0960-9822(98)70254-4 Nyegaard, 2010, Lack of functional pregnancy-associated plasma protein-A (PAPPA) compromises mouse ovarian steroidogenesis and female fertility, Biol. Reprod., 82, 1129, 10.1095/biolreprod.109.079517 Ortega-Molina, 2012, Pten positively regulates brown adipose function, energy expenditure, and longevity, Cell Metab., 15, 382, 10.1016/j.cmet.2012.02.001 Prevel, 2013, Beneficial role of rapamycin in experimental autoimmune myositis, PLoS ONE, 8, e74450, 10.1371/journal.pone.0074450 Sanchez-Alavez, 2011, Sex- and age-specific differences in core body temperature of C57Bl/6 mice, Age (Dordr.), 33, 89, 10.1007/s11357-010-9164-6 Selman, 2008, Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice, FASEB J., 22, 807, 10.1096/fj.07-9261com Selman, 2009, Ribosomal protein S6 kinase 1 signaling regulates mammalian life span, Science, 326, 140, 10.1126/science.1177221 Spindler, 2007, Conserved and tissue-specific genic and physiologic responses to caloric restriction and altered IGFI signaling in mitotic and postmitotic tissues, Annu. Rev. Nutr., 27, 193, 10.1146/annurev.nutr.27.061406.093743 Steinbaugh, 2012, Activation of genes involved in xenobiotic metabolism is a shared signature of mouse models with extended lifespan, Am. J. Physiol. Endocrinol. Metab., 303, E488, 10.1152/ajpendo.00110.2012 Storey, 2003, Statistical significance for genomewide studies, Proc. Natl. Acad. Sci. USA, 100, 9440, 10.1073/pnas.1530509100 Swain, 2009, Key research opportunities in immune system aging, J. Gerontol. A Biol. Sci. Med. Sci., 64, 183, 10.1093/gerona/gln068 Taguchi, 2007, Brain IRS2 signaling coordinates life span and nutrient homeostasis, Science, 317, 369, 10.1126/science.1142179 Vezeridis, 2006, Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation, Biochem. Biophys. Res. Commun., 348, 1082, 10.1016/j.bbrc.2006.07.146 Wang, 2012, Fibroblasts from long-lived mutant mice exhibit increased autophagy and lower TOR activity after nutrient deprivation or oxidative stress, Aging Cell, 11, 668, 10.1111/j.1474-9726.2012.00833.x Wang, 2006, Adipocytokines and lipid levels in Ames dwarf and calorie-restricted mice, J. Gerontol. A Biol. Sci. Med. Sci., 61, 323, 10.1093/gerona/61.4.323 Wang, 2010, Adult-onset, short-term dietary restriction reduces cell senescence in mice, Aging (Albany, N.Y. Online), 2, 555 Ward, 2005, Effects of age and caloric restriction on lipid peroxidation: measurement of oxidative stress by F2-isoprostane levels, J. Gerontol. A Biol. Sci. Med. Sci., 60, 847, 10.1093/gerona/60.7.847 Weindruch, 1988 Westbrook, 2009, Alterations in oxygen consumption, respiratory quotient, and heat production in long-lived GHRKO and Ames dwarf mice, and short-lived bGH transgenic mice, J. Gerontol. A Biol. Sci. Med. Sci., 64, 443, 10.1093/gerona/gln075 Withers, 1998, Disruption of IRS-2 causes type 2 diabetes in mice, Nature, 391, 900, 10.1038/36116 Xiao, 2010, Metformin attenuates cardiac fibrosis by inhibiting the TGFbeta1-Smad3 signalling pathway, Cardiovasc. Res., 87, 504, 10.1093/cvr/cvq066 Xu, 2014, Longevity effect of IGF-1R(+/-) mutation depends on genetic background-specific receptor activation, Aging Cell, 13, 19, 10.1111/acel.12145 Yan, 2013, Calorie restriction can reverse, as well as prevent, aging cardiomyopathy, Age (Dordr.), 35, 10.1007/s11357-012-9508-5 Yang, 2009, Inhibition of thymic adipogenesis by caloric restriction is coupled with reduction in age-related thymic involution, J. Immunol., 183, 3040, 10.4049/jimmunol.0900562 Yoshino, 2011, Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice, Cell Metab., 14, 528, 10.1016/j.cmet.2011.08.014 Zheng, 2014, Metformin induces renal medullary interstitial cell apoptosis in type 2 diabetic mice, J. Diabetes, 6, 132, 10.1111/1753-0407.12105