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Zebrafish age-dependent tissue degeneration occurs in a time- and tissue-dependent manner, and, for most tissues, it is anticipated and exacerbated in the absence of telomerase. There are critical tissues that age before others, such as the intestine and muscle, and this is tightly linked to telomere shortening and DNA damage in natural, wild type (WT) aging fish (Carneiro et al., 2016b). Importantly, this is reminiscent of the human scenario, where telomerase loss-of-function mutations, or mutations affecting telomere stability, lead to premature aging syndromes (termed progeria, Hofer et al., 2005; Alter et al., 2012).
Given the relatively large number of genes involved in monogenic aging disorders it is striking that up to date only a handful of bona fide mutations have been characterized in zebrafish: brca2/fancd1, fancl and rad51/fancr (Rodríguez-Marí et al., 2010, 2011; Botthof et al., 2017). Synthetic antisense morpholino (MO) knockdown of ercc6 (Wei et al., 2015) and fancd2 (Liu et al., 2003) have been also described, and TALEN and CRISPR mutants for atm (Thomas et al., 2014) and ercc5/xpg (China Zebrafish Resource Center [CZRC], 2017) have been reported, but not characterized in detail. As for almost all other genes, insertional and ENU mutants already exist at ZIRC and EZRC. Given how straightforward it is to generate novel alleles with CRISPR, it is likely that this apparent dearth of zebrafish aging disorder models will change soon.
While during the previous decades of zebrafish research, MOs have been the tool of choice for creating loss-of-function phenotypes (Nasevicius and Ekker, 2000), recently, several studies have highlighted the limitations of this approach (Schulte-Merker and Stainier, 2014; Kok et al., 2015; Stainier et al., 2017). MOs are extremely stable and can be easily delivered into embryos at early stages, where they interfere with translation or splicing. However, the effect of MOs is only transient, therefore they are usually injected in molar excess to have a longer lasting effect. The injection of large amounts of synthetic molecules could be the reason why MOs often elicit strong, specific p53-dependent effects (Robu et al., 2007) and the activation of an innate immune response (Gentsch et al., 2018). Given that DNA damage repair is inseparably linked to p53 activation, it is not surprising that MOs have not been widely adopted in areas of research where DNA damage responses (DDR) play a central role, such as cancer and aging.
During aging, short telomeres are deprotected and recognized as DNA damage. As a consequence, both WT and tert-/- mutants zebrafish accumulate γH2AX foci at telomeres with aging, mainly in gut and muscle (Carneiro et al., 2016b). The formation of γH2AX telomeric foci correlates with telomere shortening, supporting the idea that short telomeres are sensed as DNA damage and activate the DDR. Damaged DNA is recognized by the MRN complex, which recruits the kinases ATM and ATR mediating H2AX phosphorylation. In addition to γH2AX foci, gut and muscles of both aged WT and tert-/- animals showed a significant reduction of proliferating cell nuclear antigen (PCNA) staining and an increase of senescence markers (e.g., senescence-associated β-galactosidase staining), indicating that telomere shortening leads also to reduction of proliferation and induction of senescence (Anchelin et al., 2013; Henriques et al., 2013; Carneiro et al., 2016b). Decrease of proliferation and accumulation of senescent cells cooperate to the disruption of tissues homeostasis with aging. These effects are mediated by the activation of p53, as the combination of tert-/- and tp53-/- mutations rescues the replication rate and partially abolish senescence in the gut (Anchelin et al., 2013; Henriques et al., 2013).
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