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Abstract:

The aim of this study was to determine the effect of the local inhibition of ANGPT1 on steroid production, proliferation and apoptosis of ovarian follicular cells and on the PI3K/AKT pathway. We also examined the effect of ANGPTs on follicular cell apoptosis and proliferation in early antral follicles (EAFs) in culture. Follicular cells expressing PCNA decreased after ANGPT1 Ab treatment. Moreover, ANGPT1 inhibition increased the levels of active caspase 3 and androsterone, but decreased estradiol, AKT phosphorylation and the area of smooth muscle cell actin. In cultured EAFs from prepubertal rats treated with diethylstilbestrol (DES), ANGPT1 increased PCNA and decreased apoptosis while ANGPT2 reversed these effects. These results show that ANGPT1 alters steroidogenesis, reduces ovarian apoptosis, and stimulates cell proliferation in antral follicles. ANGPT1 may exert these roles by regulating ovarian vascular stability and/or by a direct effect on follicular cells, possibly involving the PI3K/AKT pathway. © 2011 Elsevier Ireland Ltd.

Registro:

Documento: Artículo
Título:Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway
Autor:Parborell, F.; Abramovich, D.; Irusta, G.; Tesone, M.
Filiación:Instituto de Biología y Medicina Experimental (IByME) - CONICET, Buenos Aires, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Angiogenesis; Angiopoietins; Apoptosis; Follicular development; Ovary; actin; androsterone; angiopoietin 1; angiopoietin 2; antibody; caspase 3; cycline; diethylstilbestrol; estradiol; phosphatidylinositol 3 kinase; protein kinase B; animal cell; animal experiment; animal tissue; antigen expression; apoptosis; article; cell proliferation; controlled study; enzyme phosphorylation; female; nonhuman; ovary follicle atresia; ovary follicle cell; prepuberty; priority journal; protein function; rat; steroidogenesis; Angiopoietin-1; Animals; Apoptosis; Caspase 3; Cell Proliferation; Cells, Cultured; Female; Follicular Atresia; Humans; Ovarian Follicle; Phosphatidylinositol 3-Kinases; Proto-Oncogene Proteins c-akt; Rats; Rats, Sprague-Dawley; Signal Transduction; Steroids
Año:2011
Volumen:343
Número:1-2
Página de inicio:79
Página de fin:87
DOI: http://dx.doi.org/10.1016/j.mce.2011.06.009
Título revista:Molecular and Cellular Endocrinology
Título revista abreviado:Mol. Cell. Endocrinol.
ISSN:03037207
CODEN:MCEND
CAS:androsterone, 53-41-8; angiopoietin 1, 186270-49-5; angiopoietin 2, 194368-66-6; caspase 3, 169592-56-7; diethylstilbestrol, 30498-85-2, 56-53-1; estradiol, 50-28-2; phosphatidylinositol 3 kinase, 115926-52-8; protein kinase B, 148640-14-6; Angiopoietin-1; Caspase 3, 3.4.22.-; Phosphatidylinositol 3-Kinases, 2.7.1.-; Proto-Oncogene Proteins c-akt, 2.7.11.1; Steroids
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03037207_v343_n1-2_p79_Parborell

Referencias:

  • Abramovich, D., Parborell, F., Tesone, M., Effect of a vascular endothelial growth factor (VEGF) inhibitory treatment on the folliculogenesis and ovarian apoptosis in gonadotropin-treated prepubertal rats (2006) Biol. Reprod., 75 (3), pp. 434-441
  • Abramovich, D., Rodriguez, C.A., Hernandez, F., Tesone, M., Parborell, F., Spatiotemporal analysis of the protein expression of angiogenic factors and their related receptors during folliculogenesis in rats with and without hormonal treatment (2009) Reproduction, 137 (2), pp. 309-320
  • Andreone, L., Velasquez, E.V., Abramovich, D., Ambao, V., Loreti, N., Croxatto, H.B., Parborell, F., Campo, S., Regulation of inhibin/activin expression in rat early antral follicles (2009) Mol. Cell Endocrinol., 309 (1-2), pp. 48-54
  • Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., Ito, K., Suda, T., Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche (2004) Cell, 118 (2), pp. 149-161
  • Basilico, C., Moscatelli, D., The FGF family of growth factors and oncogenes (1992) Adv. Cancer Res., 59, pp. 115-165
  • Billig, H., Furuta, I., Hsueh, A.J., Gonadotropin-releasing hormone directly induces apoptotic cell death in the rat ovary: biochemical and in situ detection of deoxyribonucleic acid fragmentation in granulosa cells (1994) Endocrinology, 134 (1), pp. 245-252
  • Boone, D.L., Tsang, B.K., Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression (1998) Biol. Reprod., 58 (6), pp. 1533-1539
  • Carmeliet, P., Fibroblast growth factor-1 stimulates branching and survival of myocardial arteries: a goal for therapeutic angiogenesis? (2000) Circ. Res., 87 (3), pp. 176-178
  • Chun, S.Y., Eisenhauer, K.M., Minami, S., Billig, H., Perlas, E., Hsueh, A.J., Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor (1996) Endocrinology, 137 (4), pp. 1447-1456
  • Chun, S.Y., Eisenhauer, K.M., Minami, S., Hsueh, A.J., Growth factors in ovarian follicle atresia (1996) Semin. Reprod. Endocrinol., 14 (3), pp. 197-202
  • Cortvrindt, R., Smitz, J., Van Steirteghem, A.C., A morphological and functional study of the effect of slow freezing followed by complete in-vitro maturation of primary mouse ovarian follicles (1996) Hum. Reprod., 11 (12), pp. 2648-2655
  • Cortvrindt, R., Smitz, J., Van Steirteghem, A.C., In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system (1996) Hum. Reprod., 11 (12), pp. 2656-2666
  • Davis, S., Aldrich, T.H., Jones, P.F., Acheson, A., Compton, D.L., Jain, V., Ryan, T.E., Yancopoulos, G.D., Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning (1996) Cell, 87 (7), pp. 1161-1169
  • Eppig, J.J., Wigglesworth, K., Factors affecting the developmental competence of mouse oocytes grown in vitro: oxygen concentration (1995) Mol. Reprod. Dev., 42 (4), pp. 447-456
  • Folkman, J., Angiogenesis: initiation and control (1982) Ann. NY Acad. Sci., 401, pp. 212-227
  • Fujikawa, K., de Aos Scherpenseel, I., Jain, S.K., Presman, E., Christensen, R.A., Varticovski, L., Role of PI 3-kinase in angiopoietin-1-mediated migration and attachment-dependent survival of endothelial cells (1999) Exp. Cell Res., 253 (2), pp. 663-672
  • Goede, V., Schmidt, T., Kimmina, S., Kozian, D., Augustin, H.G., Analysis of blood vessel maturation processes during cyclic ovarian angiogenesis (1998) Lab. Invest., 78 (11), pp. 1385-1394
  • Gougeon, A., Regulation of ovarian follicular development in primates: facts and hypotheses (1996) Endocr. Rev., 17 (2), pp. 121-155
  • Hanahan, D., Christofori, G., Naik, P., Arbeit, J., Transgenic mouse models of tumour angiogenesis: the angiogenic switch, its molecular controls, and prospects for preclinical therapeutic models (1996) Eur. J. Cancer, 32 A (14), pp. 2386-2393
  • Harfouche, R., Hassessian, H.M., Guo, Y., Faivre, V., Srikant, C.B., Yancopoulos, G.D., Hussain, S.N., Mechanisms which mediate the antiapoptotic effects of angiopoietin-1 on endothelial cells (2002) Microvasc. Res., 64 (1), pp. 135-147
  • Hashiramoto, A., Sakai, C., Yoshida, K., Tsumiyama, K., Miura, Y., Shiozawa, K., Nose, M., Shiozawa, S., Angiopoietin 1 directly induces destruction of the rheumatoid joint by cooperative, but independent, signaling via ERK/MAPK and phosphatidylinositol 3-kinase/Akt (2007) Arthritis Rheum., 56 (7), pp. 2170-2179
  • Hayashi, K.G., Acosta, T.J., Tetsuka, M., Berisha, B., Matsui, M., Schams, D., Ohtani, M., Miyamoto, A., Involvement of angiopoietin-tie system in bovine follicular development and atresia: messenger RNA expression in theca interna and effect on steroid secretion (2003) Biol. Reprod., 69 (6), pp. 2078-2084
  • Hazzard, T.M., Christenson, L.K., Stouffer, R.L., Changes in expression of vascular endothelial growth factor and angiopoietin-1 and -2 in the macaque corpus luteum during the menstrual cycle (2000) Mol. Hum. Reprod., 6 (11), pp. 993-998
  • Hazzard, T.M., Molskness, T.A., Chaffin, C.L., Stouffer, R.L., Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the peri-ovulatory interval (1999) Mol. Hum. Reprod., 5 (12), pp. 1115-1121
  • Irusta, G., Parborell, F., Peluffo, M., Manna, P.R., Gonzalez-Calvar, S.I., Calandra, R., Stocco, D.M., Tesone, M., Steroidogenic acute regulatory protein in ovarian follicles of gonadotropin-stimulated rats is regulated by a gonadotropin-releasing hormone agonist (2003) Biol. Reprod., 68 (5), pp. 1577-1583
  • Kaipia, A., Chun, S.Y., Eisenhauer, K., Hsueh, A.J., Tumor necrosis factor-alpha and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles (1996) Endocrinology, 137 (11), pp. 4864-4870
  • Kim, I., Kim, H.G., So, J.N., Kim, J.H., Kwak, H.J., Koh, G.Y., Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway (2000) Circ. Res., 86 (1), pp. 24-29
  • Koos, R.D., Increased expression of vascular endothelial growth/permeability factor in the rat ovary following an ovulatory gonadotropin stimulus: potential roles in follicle rupture (1995) Biol. Reprod., 52 (6), pp. 1426-1435
  • Kwak, H.J., So, J.N., Lee, S.J., Kim, I., Koh, G.Y., Angiopoietin-1 is an apoptosis survival factor for endothelial cells (1999) FEBS Lett., 448 (2-3), pp. 249-253
  • Lee, H.J., Cho, C.H., Hwang, S.J., Choi, H.H., Kim, K.T., Ahn, S.Y., Kim, J.H., Koh, G.Y., Biological characterization of angiopoietin-3 and angiopoietin-4 (2004) FASEB J., 18 (11), pp. 1200-1208
  • Li, J., Kim, J.M., Liston, P., Li, M., Miyazaki, T., Mackenzie, A.E., Korneluk, R.G., Tsang, B.K., Expression of inhibitor of apoptosis proteins (IAPs) in rat granulosa cells during ovarian follicular development and atresia (1998) Endocrinology, 139 (3), pp. 1321-1328
  • Maga, G., Hubscher, U., Proliferating cell nuclear antigen (PCNA): a dancer with many partners (2003) J. Cell Sci., 116 (PART 15), pp. 3051-3060
  • Maisonpierre, P.C., Suri, C., Jones, P.F., Bartunkova, S., Wiegand, S.J., Radziejewski, C., Compton, D., Yancopoulos, G.D., Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis (1997) Science, 277 (5322), pp. 55-60
  • Mizunuma, H., Liu, X., Andoh, K., Abe, Y., Kobayashi, J., Yamada, K., Yokota, H., Hasegawa, Y., Activin from secondary follicles causes small preantral follicles to remain dormant at the resting stage (1999) Endocrinology, 140 (1), pp. 37-42
  • Nahum, R., Beyth, Y., Chun, S.Y., Hsueh, A.J., Tsafriri, A., Early onset of deoxyribonucleic acid fragmentation during atresia of preovulatory ovarian follicles in rats (1996) Biol. Reprod., 55 (5), pp. 1075-1080
  • Nayudu, P.L., Osborn, S.M., Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro (1992) J. Reprod. Fertil., 95 (2), pp. 349-362
  • Neufeld, G., Cohen, T., Gengrinovitch, S., Poltorak, Z., Vascular endothelial growth factor (VEGF) and its receptors (1999) FASEB J., 13 (1), pp. 9-22
  • Otrock, Z.K., Mahfouz, R.A., Makarem, J.A., Shamseddine, A.I., Understanding the biology of angiogenesis: review of the most important molecular mechanisms (2007) Blood Cells Mol. Dis., 39 (2), pp. 212-220
  • Palumbo, A., Yeh, J., In situ localization of apoptosis in the rat ovary during follicular atresia (1994) Biol. Reprod., 51 (5), pp. 888-895
  • Papapetropoulos, A., Fulton, D., Mahboubi, K., Kalb, R.G., O'Connor, D.S., Li, F., Altieri, D.C., Sessa, W.C., Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway (2000) J. Biol. Chem., 275 (13), pp. 9102-9105
  • Papapetropoulos, A., Garcia-Cardena, G., Dengler, T.J., Maisonpierre, P.C., Yancopoulos, G.D., Sessa, W.C., Direct actions of angiopoietin-1 on human endothelium: evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors (1999) Lab. Invest., 79 (2), pp. 213-223
  • Parborell, F., Abramovich, D., Tesone, M., Intrabursal administration of the antiangiopoietin 1 antibody produces a delay in rat follicular development associated with an increase in ovarian apoptosis mediated by changes in the expression of BCL2 related genes (2008) Biol. Reprod., 78 (3), pp. 506-513
  • Parborell, F., Dain, L., Tesone, M., Gonadotropin-releasing hormone agonist affects rat ovarian follicle development by interfering with FSH and growth factors on the prevention of apoptosis (2001) Mol. Reprod. Dev., 60 (2), pp. 241-247
  • Parborell, F., Irusta, G., Vitale, A.M., Gonzalez, O., Pecci, A., Tesone, M., GnRH antagonist Antide inhibits apoptosis of preovulatory follicle cells in rat ovary (2005) Biol. Reprod., 72, pp. 659-666
  • Phillips, H.S., Hains, J., Leung, D.W., Ferrara, N., Vascular endothelial growth factor is expressed in rat corpus luteum (1990) Endocrinology, 127 (2), pp. 965-967
  • Rasband, W.S., (1997), http://www.rsb.info.nih.gov/ij/, ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA, Available from: <>; Sato, T.N., Tozawa, Y., Deutsch, U., Wolburg-Buchholz, K., Fujiwara, Y., Gendron-Maguire, M., Gridley, T., Qin, Y., Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation (1995) Nature, 376 (6535), pp. 70-74
  • Suri, C., Jones, P.F., Patan, S., Bartunkova, S., Maisonpierre, P.C., Davis, S., Sato, T.N., Yancopoulos, G.D., Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis (1996) Cell, 87 (7), pp. 1171-1180
  • Tanaka, J., Acosta, T.J., Berisha, B., Tetsuka, M., Matsui, M., Kobayashi, S., Schams, D., Miyamoto, A., Relative changes in mRNA expression of angiopoietins and receptors tie in bovine corpus luteum during estrous cycle and prostaglandin F2alpha-induced luteolysis: a possible mechanism for the initiation of luteal regression (2004) J. Reprod. Dev., 50 (6), pp. 619-626
  • Testa, J.R., Tsichlis, P.N., AKT signaling in normal and malignant cells (2005) Oncogene, 24 (50), pp. 7391-7393
  • Tilly, J.L., Molecular and genetic basis of normal and toxicant-induced apoptosis in female germ cells (1998) Toxicol. Lett., pp. 497-501
  • Tilly, J.L., Billig, H., Kowalski, K.I., Hsueh, A.J., Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a tyrosine kinase-dependent mechanism (1992) Mol. Endocrinol., 6 (11), pp. 1942-1950
  • Tilly, J.L., Kowalski, K.I., Johnson, A.L., Hsueh, A.J., Involvement of apoptosis in ovarian follicular atresia and postovulatory regression (1991) Endocrinology, 129 (5), pp. 2799-2801
  • Tilly, J.L., Kowalski, K.I., Schomberg, D.W., Hsueh, A.J., Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase (1992) Endocrinology, 131 (4), pp. 1670-1676
  • Valable, S., Bellail, A., Lesne, S., Liot, G., Mackenzie, E.T., Vivien, D., Bernaudin, M., Petit, E., Angiopoietin-1-induced PI3-kinase activation prevents neuronal apoptosis (2003) FASEB J., 17 (3), pp. 443-445
  • Valenzuela, D.M., Griffiths, J.A., Rojas, J., Aldrich, T.H., Jones, P.F., Zhou, H., McClain, J., Yancopoulos, G.D., Angiopoietins 3 and 4: diverging gene counterparts in mice and humans (1999) Proc. Natl. Acad. Sci. USA, 96 (5), pp. 1904-1909
  • Vitale, A.M., Gonzalez, O.M., Parborell, F., Irusta, G., Campo, S., Tesone, M., Inhibin a increases apoptosis in early ovarian antral follicles of diethylstilbestrol-treated rats (2002) Biol. Reprod., 67 (6), pp. 1989-1995
  • Wang, Z., Cui, M., Sun, L., Jia, Z., Bai, Y., Ma, K., Chen, F., Zhou, C., Angiopoietin-1 protects H9c2 cells from H2O2-induced apoptosis through AKT signaling (2007) Biochem. Biophys. Res. Commun., 359 (3), pp. 685-690
  • Woodruff, T.K., Lyon, R.J., Hansen, S.E., Rice, G.C., Mather, J.P., Inhibin and activin locally regulate rat ovarian folliculogenesis (1990) Endocrinology, 127 (6), pp. 3196-3205
  • Wulff, C., Wilson, H., Largue, P., Duncan, W.C., Armstrong, D.G., Fraser, H.M., Angiogenesis in the human corpus luteum: localization and changes in angiopoietins, tie-2, and vascular endothelial growth factor messenger ribonucleic acid (2000) J. Clin. Endocrinol. Metab., 85 (11), pp. 4302-4309
  • Xu, M., West, E., Shea, L.D., Woodruff, T.K., Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development (2006) Biol. Reprod., 75 (6), pp. 916-923
  • Yacobi, K., Wojtowicz, A., Tsafriri, A., Gross, A., Gonadotropins enhance caspase-3 and -7 activity and apoptosis in the theca-interstitial cells of rat preovulatory follicles in culture (2004) Endocrinology, 145 (4), pp. 1943-1951

Citas:

---------- APA ----------
Parborell, F., Abramovich, D., Irusta, G. & Tesone, M. (2011) . Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway. Molecular and Cellular Endocrinology, 343(1-2), 79-87.
http://dx.doi.org/10.1016/j.mce.2011.06.009
---------- CHICAGO ----------
Parborell, F., Abramovich, D., Irusta, G., Tesone, M. "Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway" . Molecular and Cellular Endocrinology 343, no. 1-2 (2011) : 79-87.
http://dx.doi.org/10.1016/j.mce.2011.06.009
---------- MLA ----------
Parborell, F., Abramovich, D., Irusta, G., Tesone, M. "Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway" . Molecular and Cellular Endocrinology, vol. 343, no. 1-2, 2011, pp. 79-87.
http://dx.doi.org/10.1016/j.mce.2011.06.009
---------- VANCOUVER ----------
Parborell, F., Abramovich, D., Irusta, G., Tesone, M. Angiopoietin 1 reduces rat follicular atresia mediated by apoptosis through the PI3K/Akt pathway. Mol. Cell. Endocrinol. 2011;343(1-2):79-87.
http://dx.doi.org/10.1016/j.mce.2011.06.009