Telomere lengthening early in development
Lin Liu1, 4, Susan M. Bailey2, Maja Okuka1, Purificación Muñoz3, Chao Li4, Lingjun Zhou4, Chao Wu4, Eva Czerwiec5, Laurel Sandler6, Andreas Seyfang6, Maria A. Blasco3 & David L. Keefe1
1 Laboratory for Reproductive Medicine, Department of Obstetrics and Gynecology, University of South Florida College of Medicine, Tampa, Florida 33612, USA.
2 Environmental & Radiological Health Sciences, Colorado State University, Fort Collins, Colorado 80523, USA.
3 Telomeres and Telomerase Group, Molecular Oncology Program, Spanish National Cancer Centre (CNIO), Madrid 28029, Spain.
4 College of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, China.
5 Women and Infants Hospital, Brown Medical School, Providence, RI 02905, USA.
6 Departments of Molecular Medicine and Neurosurgery, University of South Florida College of Medicine, Tampa, Florida 33612, USA.
Correspondence should be addressed to Lin Liu liutelom@yahoo.com or David L. Keefe dkeefe@health.usf.edu
Stem cells and cancer cells maintain telomere length mostly through telomerase1, 2, 3. Telomerase activity is high in male germ line and stem cells, but is low or absent in mature oocytes and cleavage stage embryos, and then high again in blastocysts3. How early embryos reset telomere length remains poorly understood. Here, we show that oocytes actually have shorter telomeres than somatic cells, but their telomeres lengthen remarkably during early cleavage development. Moreover, parthenogenetically activated oocytes also lengthen their telomeres, thus the capacity to elongate telomeres must reside within oocytes themselves. Notably, telomeres also elongate in the early cleavage embryos of telomerase-null mice, demonstrating that telomerase is unlikely to be responsible for the abrupt lengthening of telomeres in these cells. Coincident with telomere lengthening, extensive telomere sister-chromatid exchange (T-SCE) and colocalization of the DNA recombination proteins Rad50 and TRF1 were observed in early cleavage embryos. Both T-SCE and DNA recombination proteins decrease in blastocyst stage embryos, whereas telomerase activity increases and telomeres elongate only slowly. We suggest that telomeres lengthen during the early cleavage cycles following fertilization through a recombination-based mechanism, and that from the blastocyst stage onwards, telomerase only maintains the telomere length established by this alternative mechanism.
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