Molecular anatomy of tunicate senescence: reversible function of mitochondrial and nuclear genes associated with budding cycles

Abstract

SUMMARYZooids of the asexual strain of Polyandrocarpa misakiensis have a lifespan of 4-5 months; before dying, they produce many buds, enabling continuation of the strain. This study was designed to investigate the nature of gene inactivation and reactivation during this continuous process of senescence and budding. During senescence, the zooidal epidermis showed acid -galactosidase activity, lost proliferating cell nuclear antigen immunoreactivity and became ultrastructurally worn, indicating that the epidermis is a major tissue affected by the ageing process. Semi-quantitative PCR analysis showed that the genes encoding mitochondrial respiratory chains (MRCs) engaged in decreased transcriptional activity in senescent adults compared with younger adults. The results of in situ hybridization showed that the epidermis dramatically attenuates MRC expression during ageing but restores gene activity when budding commences. During budding and ageing, the nuclear gene Eed (a polycomb group component) was activated and inactivated in a pattern similar to that observed in MRCs. In buds, RNA interference (RNAi) of Eed attenuated Eed transcripts but did not affect the gene expression of pre-activated MRCs. A tunicate humoral factor, TC14-3, could induce Eed, accompanying the reactivation of MRC in adult zooids. When RNAi of Eed and Eed induction were performed simultaneously, zooidal cells and tissues failed to engage in MRC reactivation, indicating the involvement of Eed in MRC activation. Results of this study provide evidence that the mitochondrial gene activities of Polyandrocarpa can be reversed during senescence and budding, suggesting that they are regulated by nuclear polycomb group genes.

Chorioamniotic membrane senescence: a signal for parturition?

“…This change in mitochondrial structure has been previously reported as senescence-related change. [61][62][63][64][65][66] In amnion, in the term labor group, profiles of rough endoplasmic reticulum were often dilated, as was the nuclear envelope ( Figure 3, A). This change was not seen in most sections in the term not in labor group (Figure 3, B).…”

Histone methylation codes involved in stemness, multipotency, and senescence in budding tunicates

“…The specimens were prefixed with the fixative for 2 h on ice, and then postfixed with 1% osmium tetroxide in the same buffer for 1 h on ice. The specimens were rinsed, dehydrated, and embedded, as described previously (Kawamura et al, 2012a). The samples were observed with a Jeol JEM-1400 transmission electron microscope (JEOL, Tokyo, Japan).…”

“…After thorough washing with chilled PBS, specimens were preincubated in 20 mM citrate-phosphate buffer (pH 6.0) for 10 min and then incubated in a staining solution (3 mM K-ferrocyanide, 3 mM K-ferricyanide, 150 mM NaCl, 1 mM MgCl 2 , 0.1% x-gal in the same buffer) overnight at 37 • C (Kawamura et al, 2012a).…”

“…Zooids of this species live for 4-5 months, and before dying, they produce many longer-lived buds, thereby enabling a prolonged lifespan of the asexual strain for more than 4 decades (Kawamura et al, 2012a). The zooidal senescence in P. misakiensis involves the attenuation of proliferating cell nuclear antigen and gene activities of PmEed, superoxide dismutase 1, and mitochondrial respiratory complex (MRC), and inversely it accompanies the increasing enzyme activity of senescence-associated acid ␤-galactosidase (SA-gal) (Kawamura et al, 2012a;Kawamura and Sunanaga, 2013). These progressive events are indeed stopped by budding and cells resume rejuvenescent condition (Kawamura et al, 2012a).…”

“…The zooidal senescence in P. misakiensis involves the attenuation of proliferating cell nuclear antigen and gene activities of PmEed, superoxide dismutase 1, and mitochondrial respiratory complex (MRC), and inversely it accompanies the increasing enzyme activity of senescence-associated acid ␤-galactosidase (SA-gal) (Kawamura et al, 2012a;Kawamura and Sunanaga, 2013). These progressive events are indeed stopped by budding and cells resume rejuvenescent condition (Kawamura et al, 2012a). A buddingspecific humoral factor TC14-3 could activate both PmEed and MRC (Kawamura et al, 2012b), although the signaling pathways remain elusive.…”