Atypical senescent states: Experimental induction of cyclin-dependent kinase inhibitors (e.g. p16, p21)

For many researchers, irreversible cell cycle arrest is the canonical trait of senescent cells.   Such growth arrest can be induced experimentally by the up-regulation or over-expression of cyclin dependent kinase inhibitors (CDKi).  Thus valuable models are, at least potentially, available in which to study the physiological effect of growth arrest distinct from the DDR or any other upstream response.   Unfortunately there has been little characterization of the phenotype of cells rendered ‘senescent’ by this means.

Blagosklonny and co-workers (Korotchkina et al. 2009) used an isopropyl-thio-galactosidase (IPTG)-inducible p21 expression construct to induce a senescence-like state in an HT1080-derived cell line (HT-p21-9).   Characterisation of the phenotype of these cells does not appear to have been attempted beyond observing irreversible growth arrest and the presence of increased SA-β-Gal activity.  Given that HT1080 is a highly tumorigenic fibrosarcoma carrying an activated N-ras oncogene (Benedict et al. 1984), it probably represents a poor genetic background in which to assess whether markers of immunogenic conversion or resistance to cell death can be induced by CDKi overexpression alone.  However, the basic principle of using such a construct for that purpose is sound.

Tokarsky-Amiel et al (2013) showed that overexpression of p14ARF in the epidermis of the skin of mice (using a tetracyclin-inducible construct) resulted in mass apoptosis and cell cycle arrest.  As measured by SA-β-Gal activity, the p14ARF transgene drove senescence in up to 8% of the surviving cells in the epithelium by a p53-dependent mechanism (demonstrated by ablation of p53 through co-expression of a specific shRNA directed against it).  These senescent cells were viable within the epidermis for several weeks consistent with lack of clearance.  Unfortunately, minimal analysis of their phenotype was conducted (beyond assessment of the message levels for the senescence-associated genes Pai-1 and Dcr2).  Thus, the immune state of the p14ARF-senescent cells is currently unclear and the picture is complicated by the fact that senescent rodent cells do not display a senescent secretome under some conditions.  However, given that alopecia and follical stem cell dysfunction were observed in the animals, it is clear that cells rendered ‘senescent’ in this manner can exert phenotypic effects.  Thus, there is some evidence that cell cycle arrest alone may be sufficient to cause problems in highly mitotic tissues such as the epidermis, but large amounts of work remain to be done.  

CDKi overexpression systems clearly have the potential to be valuable tools.  However the extent to which these are physiologically reflective can legitimately be challenged.  This can be understood in two ways (i) the mechanism by which the growth arrest is induced has not been reported in vivo and (ii) cells do not become senescent en mass but gradually as a result of tissue turnover throughout life.  Thus, findings made with these systems could be considered ‘artefactual’

By way of addressing these concerns, it is worth remembering that for many years replicative senescence was dismissed as a ‘tissue culture artefact’ because senescent cells had not been observed in vivo (evidence for their existence in tissue remained severely limited until the late 1990s).  By the same token, elevation of CDKi alone in cells in vivo is not impossible.  Absence of evidence is never evidence of absence.   Similarly, many over-expression systems model systems can be said to be non-physiological.  However, valuable data is routinely gathered using them and in this instance could allow researchers to gage the maximum physiological impact that irreversible growth arrest can have on tissue function.  Thus, if these limits are recognized, such models are potentially utile, especially when combined with detailed analysis of phenotypes known to exist in other ‘senescent cells’ (e.g. apoptosis resistance, immune ligand presentation and the secretory response) 



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