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Infertility in the hyperplasic ovary of freshwater planarians: the role of programmed cell death

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Abstract

Ex-fissiparous planarians produce infertile cocoons or, in very rare cases, cocoons with very low fertility. Here, we describe the features of programmed cell death (PCD) occurring in the hyperplasic ovary of the ex-fissiparous freshwater planarian Dugesia arabica that may explain this infertility. Based on TEM results, we demonstrate a novel extensive co-clustering of cytoplasmic organelles, such as lysosomes and microtubules, and their fusion with autophagosomes during the early stage of oocyte cell death occurring through an autophagic pattern. During a later stage of cell death, the generation of apoptotic vesicles in the cytoplasm can be observed. The immunohistochemical labeling supports the ultrastructural results because it has been shown that the proapoptotic protein bax was more highly expressed in the hyperplasic ovary than in the normal one, whereas the anti-apoptotic protein bcl2 was slightly more highly expressed in the normal ovary compared to the hyperplasic one. TUNEL analysis of the hyperplasic ovary confirmed that the nuclei of the majority of differentiating oocytes were TUNEL-positive, whereas the nuclei of oogonia and young oocytes were TUNEL-negative; in the normal ovary, oocytes are TUNEL-negative. Considering all of these data, we suggest that the cell death mechanism of differentiating oocytes in the hyperplasic ovary of freshwater planarians is one of the most important factors that cause ex-fissiparous planarian infertility. We propose that autophagy precedes apoptosis during oogenesis, whereas apoptotic features can be observed later.

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Acknowledgments

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through the research group project NoRGP-VPP-254. We thank Dr. Cristina González-Estévez, Department of Developmental Genetics and Gene Control, Institute of Genetics, Queen’s Medical Centre, The University of Nottingham, for her constructive criticism on an earlier draft of the manuscript.

Conflict of Interest

The authors declare no conflict of interest.

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Authors and Affiliations

  1. Zoology Department College of Science, King Saud University, P. O. Box 2455, Riyadh, 11451, Saudi Arabia

    Abdel Halim Harrath, Lamjed Mansour, Mukhtar Ahmed, Alexander V. Sirotkin, Suliman Y. Al Omar, Ibrahim M. Alhazza & Saleh Alwasel

  2. Genome Research Chair- Department of Biochemistry College of Science, King Saud University, Riyadh, 12372, Saudi Arabia

    Abdelhabib Semlali & Mohamed S. Al Anazi

  3. Animal Production Research Center Nitra, Luzianky, Slovakia

    Alexander V. Sirotkin

  4. Constantine the Philosopher University, Nitra, Slovakia

    Alexander V. Sirotkin

  5. Pathology Department, College of Medicine, King Saud University, Riyadh, 12372, Saudi Arabia

    Maha Arfah

  6. Stereology and Electron Microscopy Laboratory Centre for Stochastic Geometry and Advanced Bioimaging Department of Clinical Medicine, Aarhus University, Aarhus, Denmark

    Jens R. Nyengaard

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  1. Abdel Halim Harrath
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Correspondence to Abdel Halim Harrath.

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Harrath, A.H., Semlali, A., Mansour, L. et al. Infertility in the hyperplasic ovary of freshwater planarians: the role of programmed cell death. Cell Tissue Res 358, 607–620 (2014). https://doi.org/10.1007/s00441-014-1971-0

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