C. elegans Germ Cells Show Temperature and Age-Dependent Expression of Cer1, a Gypsy/Ty3-Related Retrotransposon

Abstract

Virus-like particles (VLPs) have not been observed in Caenorhabditis germ cells, although nematode genomes contain low numbers of retrotransposon and retroviral sequences. We used electron microscopy to search for VLPs in various wild strains of Caenorhabditis, and observed very rare candidate VLPs in some strains, including the standard laboratory strain of C. elegans, N2. We identified the N2 VLPs as capsids produced by Cer1, a retrotransposon in the Gypsy/Ty3 family of retroviruses/retrotransposons. Cer1 expression is age and temperature dependent, with abundant expression at 15°C and no detectable expression at 25°C, explaining how VLPs escaped detection in previous studies. Similar age and temperature-dependent expression of Cer1 retrotransposons was observed for several other wild strains, indicating that these properties are common, if not integral, features of this retroelement. Retrotransposons, in contrast to DNA transposons, have a cytoplasmic stage in replication, and those that infect non-dividing cells must pass their genomic material through nuclear pores. In most C. elegans germ cells, nuclear pores are largely covered by germline-specific organelles called P granules. Our results suggest that Cer1 capsids target meiotic germ cells exiting pachytene, when free nuclear pores are added to the nuclear envelope and existing P granules begin to be removed. In pachytene germ cells, Cer1 capsids concentrate away from nuclei on a subset of microtubules that are exceptionally resistant to microtubule inhibitors; the capsids can aggregate these stable microtubules in older adults, which exhibit a temperature-dependent decrease in egg viability. When germ cells exit pachytene, the stable microtubules disappear and capsids redistribute close to nuclei that have P granule-free nuclear pores. This redistribution is microtubule dependent, suggesting that capsids that are released from stable microtubules transfer onto new, dynamic microtubules to track toward nuclei. These studies introduce C. elegans as a model to study the interplay between retroelements and germ cell biology.

Extension of Saccharomyces paradoxus Chronological Lifespan by Retrotransposons in Certain Media Conditions Is Associated with Changes in Reactive Oxygen Species

“…Retrotransposon expression increases with age in gonads of C. elegans, brain tissue of D. melanogaster, normal human cells maintained ex vivo, multiple mouse tissues, and yeast mother cells (Wang et al 2011;Dennis et al 2012;De Cecco et al 2013a,b;Li et al 2013;Hu et al 2014). Increased mobility of retrotransposons occurs at late time points during yeast chronological lifespan and in brains of aged D. melanogaster (Maxwell et al 2011;Li et al 2013).…”

“…Changes in chromatin and genome instability are observed with aging, and recent work is demonstrating that the regulation and mobility of retrotransposons also changes during aging (Moskalev et al 2013;Wood and Helfand 2013). Increased expression of retrotransposons with age has been observed in gonads of Caenorhabditis elegans, brains of Drosophila melanogaster, somatic tissues in mice, normal human cells grown ex vivo, and in yeast mother cells (Wang et al 2011;Dennis et al 2012;De Cecco et al 2013a,b;Li et al 2013;Hu et al 2014). Increased mobility of retrotransposons has been detected at late stages of Saccharomyces cerevisiae chronological lifespan (CLS) and in brains of aged D. melanogaster (Maxwell et al 2011;Li et al 2013).…”

Age‐associated de‐repression of retrotransposons in the Drosophila fat body, its potential cause and consequence

“…Additionally, increased expression of Cer1 , which belongs to the gypsy/Ty3 family of retrotransposons, is observed in old C. elegans (Dennis et al ., 2012). Studies of the old Drosophila brains have also revealed an increased expression of several TEs, including the gypsy retrotransposon (Li et al ., 2013).…”

Chromatin-modifying genetic interventions suppress age-associated transposable element activation and extend life span in Drosophila

“…Overexpressing TE RNAs is sufficient to cause cytotoxicity, and inhibiting expression of these TEs causes reversal of both senescence and cytotoxic phenotypes (10,11). TE activation has been observed with age in mice (8,12), as well as C. elegans (13), yeast (14), Drosophila (15,16), and senescent human tissue culture cells (7).…”