Apoptotic Cell Death in Ewe Endometrium during the Oestrous Cycle


Keywords:
ewes endometrium apoptosis proliferation oestrous cycle
S. BENBIA
Y. BELKHIRI
M. YAHIA
Abstract

We hypothesized that endometrial tissues from ewes undergo spatial and temporal changes. Thus, two regulatory events were investigated in this study: cell death (apoptosis) and cell proliferation. Uteri were obtained from healthy ewes at Batna abattoir (Algeria). Based on macroscopic observation of the ovaries and plasma progesterone, uteri were assigned to follicular, early and active luteal phases. Apoptosis and proliferation were assessed by detection of cleaved caspase-3 and Ki-67, respectively. Ki-67 and cleaved caspase-3 (CCP-3) were expressed in both phases of the oestrous cycle and all endometrium cells types [luminal epithelia (LE), superficial gland epithelia (SG) and deep gland epithelia (DG)]. Immunohistochemistry for cleaved caspase-3 revealed few or no apoptotic stained cells in all endometrium locations during the entire oestrous cycle. However, Ki-67 was significantly higher in the follicular phase than in the early and active luteal phase. Besides, expression of CCP-3 in LE was higher than in SG and DG at the follicular phase and early luteal phase. However, Ki -67 and CCP-3 levels in all endometrium cells types did not significantly change at active luteal phase. Therefore, it is concluded that apoptosis and proliferation were occurred in ewe endometrium in a cyclic pattern and under the influence of the endocrine profile.

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References
Alan E and Liman N (2016) Involution Dependent Changes in Distribution and Localization of Bax , Survivin , Caspase-3 , and Calpain-1 in the Rat Endometrium. Microscopy Research And Technique. 297(79):285–297.
Antsiferova YS and Sotnikova NY (2016) Apoptosis and endometrial receptivity: Relationship with in vitro fertilization treatment outcome. World Journal of Obstetrics and Gynecology. 5(1):87.
Arai M, Yoshioka S, Nishimura R and Okuda K (2014) FAS / FASL-mediated cell death in the bovine endometrium. Animal Reproduction Science. 151(3–4):97–104, Elsevier B.V. Arai M, Yoshioka S, Tasaki Y and Okuda K (2013) Remodeling of bovine endometrium throughout the estrous cycle. Animal Reproduction Science. 1–9, Elsevier B.V.
Armstrong GM et al. (2017) Endometrial apoptosis and neutrophil infiltration during menstruation exhibits spatial and temporal dynamics that are recapitulated in a mouse model. Scientific Reports. 717416.
Bazer FW (2013) Pregnancy recognition signaling mechanisms in ruminants and pigs. Journal of animal science and biotechnology. 4(1):.
Benbia S, Yahia M, Letron IR and Benounne O (2017) Endometrial Cells Morphology Depending on Estrous Cycle and Histologic Layers in Cows: Morphometric Study Biotechnology’s Laboratory of the Bioactive Molecules and the. Global Veterinaria. 18(1):68–73.
Brenner D and Mak TW (2009) Mitochondrial cell death effectors. Current Opinion in Cell Biology. 21871–877.
Costa RPR da et al. (2007) Caspase-3 mediated apoptosis and cell proliferation in the equine endometrium during the estrous cycle. Reproduction, Fertility and Development. 19925–932.
García-Palencia P et al. (2007) Sex steroid receptor expression in the oviduct and uterus of sheep with estrus synchronized with progestagen or prostaglandin analogues. Animal Reproduction Science. 97(1–2):25–35.
Harada T et al. (2004) Apoptosis in human endometrium and endometriosis. Human Reproduction Update,. 10(1):29–38.
Jin Z and El-Deiry WS (2005) Overview of Cell Death Signaling Pathways ND ES SC. Cancer Biology & Therapy. 4(2):147–171.
Johnson ML, Redmer D a and Reynolds LP (1997a) Uterine growth, cell proliferation, and c-fos proto-oncogene expression throughout the estrous cycle in ewes. Biology of reproduction. 56(2):393–401.
Johnson ML, Redmer D a and Reynolds LP (1997b) Effects of ovarian steroids on uterine growth, morphology, and cell proliferation in ovariectomized, steroid-treated ewes. Biology of reproduction. 57(January 2017):588–596.
Li H, Zhu H, Xu CJ and Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94(4):491–501.
Li P et al. (1997) Cytochrome c and dATP-Dependent Formation of Apaf- 1 / Caspase-9 Complex Initiates an Apoptotic Protease Cascade. 91479–489.
Lonergan P and Forde N (2014) Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle. Animal. 8(s1):64–69.
Mcilwain DR, Berger T and Mak TW (2013) Caspase Functions in Cell Death and Disease. Cold Spring Harb Perspect Biol. 51–27.
Md. Rashedul Islam, Yamagami K, Yoshii Y and Yamauchi N (2016) Growth factor induced proliferation, migration, and lumen formation of rat endometrial epithelial cells. Journal of Reproduction and Development. 62(3):271–278.
Okano A, Ogawa H, Takahashi H and Geshi M (2007) Apoptosis in the porcine uterine endometrium during the estrous cycle, early pregnancy and Post partum. Journal of Reproduction and Development. 53(4):923–930.
Öner H, Öner J and Demir R (2010) Distributions of PCNA and Cas-3 in rat uterus during early pregnancy. Folia Histochemica Et Cytobiologica. 48(1):71–77.
Park HJ et al. (2017) Integrins functioning in uterine endometrial stromal and epithelial cells in estrus. Reproduction. 153351–360 Introduction. Robinson RS,
Mann GE, Lamming GE and Wathes DC (2001) Expression of oxytocin, oestrogen and progesterone receptors in uterine biopsy samples throughout the oestrous cycle and early pregnancy in cows. Reproduction. 122(6):965–979.
Sağsöz H, Akbalik ME, Saruhan BG and Ketani M a (2011) Localization of estrogen receptor α and progesterone receptor B in bovine cervix and vagina during the follicular and luteal phases of the sexual cycle. Biotechnic & histochemistry. 86(4):262–71.
Shiozawa T et al. (2001) Up-Regulation of p27Kip1 by Progestins Is Involved in the Growth Suppression of the Normal and Malignant Human Endometrial Glandular Cells. Endocrinology. 142(4):4182–4188.
Simmons RM et al. (2009) Insulin-like growth factor binding protein-1 in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation. Endocrinology. 150(9):4295–4305.
Stevenson KR, Gilmour RS and Wathes DC (1994) Localization of insulin- like growth factor-I (IGF-I) and -II messenger ribonucleic acid and type 1 IGF receptors in the ovine uterus during the estrous cycle and early pregnancy. Endocrinology. 134(4):1655–1664.
Stewart CJR, Critchley HOD and Farquharson MA (1999) Endometrial apoptosis in patients with dysfunctional uterine bleeding. Histopathology. 3499–105.
Verheijen R, Kuijpers HJH, Driel R Van, et al. (1989a) Ki-67 detects a nuclear matrix-associated proliferation-related antigen II . Localization in mitotic cells and association with chromosomes. Journal of Cell Science 92,. 92531–540.
Verheijen R, Kuijpers HJH, Schlingemann RO, et al. (1989b) Ki-67 detects a nuclear matrix-associated proliferation-related antigen I . Intracellular localization during interphase. J Cell Sci. 92(( Pt 1)):123–30.
Yuan D -z. et al. (2014) Progesterone-Induced Cyclin G1 Inhibits the Proliferation of Endometrial Epithelial Cell and its Possible Molecular Mechanism. Endocrine Research. 46761–767.
Zhang L et al. (2018) MiR-26a promoted endometrial epithelium cells (EECs) proliferation and induced stromal cells (ESCs) apoptosis via the PTEN-PI3K/AKT pathway in dairy goats. Journal of Cellular Physiology. 233(6):4688–4706.
Zhang L et al. (2019) Endometrial Epithelial Cell Apoptosis Is Inhibited by a ciR8073-miR181a-Neurotensis Pathway during Embryo Implantation. Molecular Therapy: Nucleic Acid. 14(22):262–273, Elsevier Ltd.
Zheng J, Johnson ML, Redmer DA and Reynolds LP (1996) Estrogen and progesterone receptors, cell proliferation, and c-fos expression in the ovine uterus during early pregnancy. Endocrinology. 137(1):340–348.