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. Author manuscript; available in PMC: 2020 Mar 1.
Published in final edited form as: Crit Rev Biochem Mol Biol. 2019 Mar 1;54(1):61–83. doi: 10.1080/10409238.2019.1570075

Table 1.

Studies of age-related epigenetic changes in pre-clinical and clinical models.

Epigenetic change with aging Markers Model(s) References
Reduced global heterochromatin HP1 and H3K9me3 reduced, lamin A changes C. elegans (Haithcock et al. 2005; Ni et al. 2012)
Drosophila (Brandt et al. 2008; Wood et al. 2010; Larson et al. 2012)
Human fibroblasts (Scaffidi and Misteli 2006)
Progeria patient cells (Scaffidi and Misteli 2006; Shumaker et al. 2006; Zhang et al. 2015)
Senescence-associated heterochromatin foci (SAHF) HP1 and H3K9me3 increased, macroH2A and HMGA increased Mice (Kreiling et al. 2012)
Baboons (Herbig et al. 2006; Kreiling et al. 2012)
Human fibroblasts (Narita et al. 2003, 2006; Zhang et al. 2005)
Nucleosome remodeling and loss Loss of core histone proteins Yeast (Dang et al. 2009; Feser et al. 2010; Hu et al. 2014)
Worms (Ni et al. 2012)
Human fibroblasts (O’Sullivan et al. 2010b; Ivanov et al. 2013)
Histone variants increased H3.3, H3.3cs1 Mouse brain (Maze et al. 2015)
Human fibroblasts (Duarte et al. 2015)
Changed histone marks Globally active marks increased (H3K4me3, H4K16ac) and repressive marks decreased (H3K9me3, H3K27me3) Yeast (Dang et al. 2009; Feser et al. 2010)
Drosophila (Wood et al. 2010; Larson et al. 2012)
C. elegans (Ni et al. 2012)
Killifish (Liu, Wang, et al. 2013; Baumgart et al. 2014)
Rats (Sarg et al. 2002)
Mouse brain (Peleg et al. 2010; Ryu et al. 2011)
Mouse stem cells (Sun et al. 2014; Schwoerer et al. 2016)
Mouse fibroblasts (Lyu et al. 2018)
Progeria mouse models (Wang et al. 2010)
Progeria patient cells (Shumaker et al. 2006; Maures et al. 2011; Zhang et al. 2015)
Human fibroblasts (O’Sullivan et al. 2010a; Shah et al. 2013)
Human brain tissue (Nativio et al. 2018)
DNA methylation changes Global DNA hypomethylation, CpG island hypermethylation Salmon (Berdyshev et al. 1967)
Mice (Wilson et al. 1987; Cole et al. 2017; Petkovich et al. 2017; Stubbs et al. 2017; Wang et al. 2017)
Rats (Vanyushin et al. 1973)
Dogs (Thompson et al. 2017)
Rhesus monkeys (Maegawa et al. 2017)
Human fibroblasts (Koch et al. 2012b)
Human stem cells (Fernández and Bayón 2014)
Humans (Christensen et al. 2009; Zampieri et al. 2015; Li et al. 2017; Wagner 2017; Horvath and Raj 2018)
Relocalization of chromatin-modifying factors (RCM) SIRT-1, PARP-1, REST, HDAC-1 Yeast (Kennedy et al. 1997; Sinclair and Guarente 1997; Oberdoerffer et al. 2008)
Mice (Oberdoerffer et al. 2008)
ncRNA changes H19, Dicer, lin-4, lin-14, mir-34 Yeast (Saka et al. 2013)
C. elegans (Boehm and Slack 2005; Ibáñez-ventoso et al. 2006; Mori et al. 2012)
Mice (Fu et al. 2008; Li, Khanna, et al. 2011; Mori et al. 2012)
AD mouse models (Wang et al. 2009)
Humans (Hooten et al. 2010; Wang, Huang, et al. 2011; Zhang et al. 2014)