{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2023,9,24]],"date-time":"2023-09-24T15:04:23Z","timestamp":1695567863858},"reference-count":32,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Reprod Biol Endocrinol"],"published-print":{"date-parts":[[2009,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>Placental and fetal growth requires high rates of cellular turnover and differentiation, which contributes to conceptus development. The trophoblast has unique properties and a wide range of metabolic, endocrine and angiogenic functions, but the proliferative profile of the bovine placenta characterized by flow cytometry analysis and its role in fetal development are currently uncharacterized. Complete understanding of placental apoptotic and proliferative rates may be relevant to development, especially if related to the pathogenesis of pregnancy losses and placental abnormalities.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>In this study, the proliferation activity and apoptosis in different regions of normal bovine placenta (central and boundary regions of placentomes, placentomal fusion, microplacentomes, and interplacentomal regions), from distinct gestation periods (Days 70 to 290 of pregnancy), were analyzed by flow cytometry.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Our results indicated that microplacentomes presented a lower number of apoptotic cells throughout pregnancy, with a higher proliferative activity by the end of gestation, suggesting that such structures do not contribute significantly to normal of placental functions and conceptus development during pregnancy. The placentome edges revealed a higher number of apoptotic cells from Day 170 on, which suggests that placentome detachment may well initiate in this region.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Variations involving proliferation and apoptotic rates may influence placental maturation and detachment, compromising placental functions and leading to fetal stress, abnormalities in development and abortion, as frequently seen in bovine pregnancies from in vitro fertilization and cloning procedures. Our findings describing the pattern of cell proliferation and apoptosis in normal bovine pregnancies may be useful for unraveling some of the developmental deviations seen in nature and after in vitro embryo manipulations.<\/jats:p><\/jats:sec>","DOI":"10.1186\/1477-7827-7-25","type":"journal-article","created":{"date-parts":[[2009,3,31]],"date-time":"2009-03-31T06:14:37Z","timestamp":1238480077000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Patterns of cell proliferation and apoptosis by topographic region in normal Bos taurus vs. Bos indicus crossbreeds bovine placentae during pregnancy"],"prefix":"10.1186","volume":"7","author":[{"given":"Patricia R","family":"Facciotti","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rose EG","family":"Rici","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Durvanei A","family":"Maria","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marcelo","family":"Bertolini","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carlos E","family":"Ambr\u00f3sio","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria A","family":"Miglino","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2009,3,30]]},"reference":[{"key":"497_CR1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1159\/000142118","volume":"22","author":"N Bjorkman","year":"1954","unstructured":"Bjorkman N: Morphological and histochemical studies on the bovine placenta. Acta Anat. 1954, 22: 1-91.","journal-title":"Acta Anat"},{"key":"497_CR2","first-page":"63","volume":"4","author":"R Leiser","year":"1975","unstructured":"Leiser R: Development of contact between trophoblast and uterine epithelium during the early stages on implantation in the cow. Zentralbl Veterinarmed. 1975, 4: 63-86.","journal-title":"Zentralbl Veterinarmed"},{"key":"497_CR3","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1055\/s-0029-1211275","volume":"102","author":"R Leiser","year":"1994","unstructured":"Leiser R, Kaufmann P: Placental structure: in a comparative aspect. Exp Clin Endocrinol. 1994, 102: 122-134.","journal-title":"Exp Clin Endocrinol"},{"key":"497_CR4","first-page":"391","volume":"31","author":"M Bertolini","year":"2007","unstructured":"Bertolini M, Bertolini LR, Gerger RPC, Batchelder CA, Anderson GB: Developmental problems during pregnancy after in vitro embryo manipulations. Rev Bras Reprod Anim. 2007, 31: 391-405.","journal-title":"Rev Bras Reprod Anim"},{"key":"497_CR5","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1530\/jrf.0.0890213","volume":"89","author":"LP Reynolds","year":"1990","unstructured":"Reynolds LP, Millaway DS, Kirsch JD, Infeld JE, Redmer DA: Growth and in vitro metabolism of placental tissues of cows from day 100 to day 250 of gestation. J Reprod Fertil. 1990, 89: 213-222.","journal-title":"J Reprod Fertil"},{"key":"497_CR6","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1046\/j.1439-0531.2001.00297.x","volume":"36","author":"RA Laven","year":"2001","unstructured":"Laven RA, Peters RA: Gross morphometry of the bovine placentome during gestation. Reprod Dom Anim. 2001, 36: 289-296. 10.1046\/j.1439-0531.2001.00297.x.","journal-title":"Reprod Dom Anim"},{"key":"497_CR7","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1111\/j.1439-0442.1966.tb00042.x","volume":"13","author":"M Abdel-Raouf","year":"1965","unstructured":"Abdel-Raouf M, Badawi HM: Morphological study of uterine caruncles in Egyptian buffalo cows. Zbl Vet Med. 1965, 13: 252-263.","journal-title":"Zbl Vet Med"},{"key":"497_CR8","first-page":"586","volume":"34","author":"FTV Pereira","year":"2006","unstructured":"Pereira FTV, Barreto RSN, Miglino MA, Silva SM, Burioli KC: Fus\u00e3o caruncular em vacas prenhes. Acta Sci Vet. 2006, 34: 586-","journal-title":"Acta Sci Vet"},{"key":"497_CR9","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1590\/S0100-736X2007000600002","volume":"27","author":"SMM Cazerta","year":"2007","unstructured":"Cazerta SMM, Miglino MA, Marques RS, Vulcano M, Pereira FTV: Caracteriza\u00e7\u00e3o das \u00e1reas hem\u00f3fagas da placenta bovina. Pesq Vet Bras. 2007, 27: 229-235. 10.1590\/S0100-736X2007000600002.","journal-title":"Pesq Vet Bras"},{"key":"497_CR10","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1016\/j.theriogenology.2007.04.060","volume":"68","author":"M Miglino","year":"2007","unstructured":"Miglino M, Pereira F, Visintin J, Garcia J, Meirelles F, Rumpf R, Ambrosio C, Papa P, Santos T, Carvalho A: Placentation in cloned cattle: Structure and microvascular architecture. Theriogenology. 2007, 68: 604-617. 10.1016\/j.theriogenology.2007.04.060.","journal-title":"Theriogenology"},{"key":"497_CR11","first-page":"410","volume":"57","author":"A Andresen","year":"1927","unstructured":"Andresen A: Die plazentome der wiederkauer. Morphologisches Jahrbuch. 1927, 57: 410-485.","journal-title":"Morphologisches Jahrbuch"},{"key":"497_CR12","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.2527\/jas1979.4861546x","volume":"48","author":"RL Prior","year":"1979","unstructured":"Prior RL, Laster DB: Development of the bovine foetus. J Anim Sci. 1979, 48: 1546-1553.","journal-title":"J Anim Sci"},{"key":"497_CR13","doi-asserted-by":"crossref","first-page":"1945","DOI":"10.2527\/1991.6951945x","volume":"69","author":"CL Ferrel","year":"1991","unstructured":"Ferrel CL: Maternal and fetal influences on uterine and conceptus development in the cow: growth of tissues of the gravid uterus. J Anim Sci. 1991, 69: 1945-1953.","journal-title":"J Anim Sci"},{"key":"497_CR14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1432-1033.1996.00001.x","volume":"236","author":"AJ Hale","year":"1996","unstructured":"Hale AJ, Smith CA, Sutherland LC, Stoneman VEA, Longthorne VL, Culhane AC, Williams GT: Apoptosis: molecular regulation of cell death. Eur J Biochem. 1996, 236: 1-26. 10.1111\/j.1432-1033.1996.00001.x.","journal-title":"Eur J Biochem"},{"key":"497_CR15","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1046\/j.1439-0531.2000.d01-12.x","volume":"35","author":"G Schuler","year":"2000","unstructured":"Schuler G, Wirth C, Klisch K, Failing K, Hoffmann B: Characterization of Proliferative Activity in Bovine Placentomes Between Day 150 and Parturition by Quantitative Immunohistochemical Detection of Ki67-Antigen. Reprod Dom Anim. 2000, 35: 157-162.","journal-title":"Reprod Dom Anim"},{"key":"497_CR16","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1530\/rep.0.1260469","volume":"126","author":"A Boos","year":"2003","unstructured":"Boos A, Janssen V, M\u00fclling C: Proliferation and apoptosis in bovine placentomes during pregnancy and around induced and spontaneous parturition as well as in cows retaining the fetal membranes. Reproduction. 2003, 126: 469-480. 10.1530\/rep.0.1260469.","journal-title":"Reproduction"},{"key":"497_CR17","doi-asserted-by":"publisher","first-page":"1919","DOI":"10.1095\/biolreprod.104.031427","volume":"71","author":"JR Miles","year":"2004","unstructured":"Miles JR, Farin CE, Rodriguez KF, Alexander JE, Farin PW: Angiogenesis and morphometry of bovine placentas in late gestation from embryos produced in vivo or in vitro. Biol Reprod. 2004, 71: 1919-1926. 10.1095\/biolreprod.104.031427.","journal-title":"Biol Reprod"},{"key":"497_CR18","doi-asserted-by":"publisher","first-page":"1128","DOI":"10.1016\/j.theriogenology.2007.08.012","volume":"68","author":"P Lonergan","year":"2007","unstructured":"Lonergan P, Evans ACO, Boland E, Rizos D, Fair T, Duffy P, Sung LY, Duc F, Chaubal S, Xu J, Yang X, Tian XC: Pregnancy and fetal characteristics after transfer of vitrified in vivo and cloned bovine embryos. Theriogenology. 2007, 68: 1128-1137. 10.1016\/j.theriogenology.2007.08.012.","journal-title":"Theriogenology"},{"key":"497_CR19","volume-title":"Anim Reprod Sci","author":"REG Rici","year":"2008","unstructured":"Rici REG, Facciotti PR, Ambr\u00f3sio CE, Maria DA, Kfoury JR, Bertolini M, Miglino MA: Cell cycle and apoptosis in normal and cloned bovine near-term placentae. Anim Reprod Sci. 2008, 2008 Nov 27,"},{"key":"497_CR20","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1530\/ror.0.0030155","volume":"3","author":"LE Young","year":"1998","unstructured":"Young LE, Sinclair KD, Wilmut I: Large offspring syndrome in cattle and sheep. Rev Reprod. 1998, 3: 155-163. 10.1530\/ror.0.0030155.","journal-title":"Rev Reprod"},{"key":"497_CR21","volume-title":"Veterinary reproduction and obstetrics","author":"C Richardson","year":"1989","unstructured":"Richardson C: Veterinary reproduction and obstetrics. Edited by: Arthur GH. Noakes DE, Pearson H. 1989, London: Bailli\u00e9re Tindal, 6","edition":"6"},{"key":"497_CR22","volume-title":"Reprod Domest Anim","author":"AC Assis Neto","year":"2009","unstructured":"Assis Neto AC, Pereira FTV, Santos TC, Ambrosio CE, Leiser R, Miglino MA: Morpho-physical Recording of Bovine Conceptus (Bos indicus) and Placenta from Days 20 to 70 of Pregnancy. Reprod Domest Anim. 2009, 2009 Feb 25,"},{"key":"497_CR23","first-page":"247","volume-title":"Textbook of Veterinary Histology","author":"J Priedklns","year":"1998","unstructured":"Priedklns J, Leiser R: Female Reproductive System. Textbook of Veterinary Histology. Edited by: Dellmann HD, Eurell J. 1998, Philadelphia: Lippincott Williams & Williams, 247-286. 5","edition":"5"},{"key":"497_CR24","first-page":"106","volume-title":"Histology and cell biology. An introduction to pathology","author":"AL Kierszenbaum","year":"2002","unstructured":"Kierszenbaum AL: Histology and cell biology. An introduction to pathology. 2002, Mosby: St Louis, 106-108."},{"key":"497_CR25","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1002\/cyto.990030503","volume":"3","author":"LL Vindelov","year":"1983","unstructured":"Vindelov LL, Christensen IJ, Nissen NI: A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry. 1983, 3: 323-327. 10.1002\/cyto.990030503.","journal-title":"Cytometry"},{"key":"497_CR26","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.anireprosci.2005.03.012","volume":"91","author":"A Boos","year":"2006","unstructured":"Boos A, Kohtes J, Janssen V, M\u00fclling C, Stelljes A, Zerbe H, H\u00e4ssig M, Thole HH: Pregnancy effects on distribution of progesterone receptors, oestrogen receptor, glucocorticoid receptors, Ki-67 antigen and apoptosis in the bovine interplacentomal uterine wall and foetal membranes. Anim Reprod Sci. 2006, 91: 55-76. 10.1016\/j.anireprosci.2005.03.012.","journal-title":"Anim Reprod Sci"},{"key":"497_CR27","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1095\/biolreprod.105.040808","volume":"73","author":"JR Miles","year":"2005","unstructured":"Miles JR, Farin CE, Rodriguez KF, Alexander JE, Farin PW: Effects of embryo culture on angiogenesis and morphometry of bovine placentas during early gestation. Biol Reprod. 2005, 73: 663-671. 10.1095\/biolreprod.105.040808.","journal-title":"Biol Reprod"},{"key":"497_CR28","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/j.domaniend.2004.06.006","volume":"3","author":"DA Redmer","year":"2004","unstructured":"Redmer DA, Wallace JM, Reynolds LP: Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development. Domest Anim Endocrinol. 2004, 3: 199-217. 10.1016\/j.domaniend.2004.06.006.","journal-title":"Domest Anim Endocrinol"},{"key":"497_CR29","doi-asserted-by":"publisher","first-page":"3111","DOI":"10.1210\/jc.81.8.3119","volume":"81","author":"R Runic","year":"1996","unstructured":"Runic R, Lockwood CJ, Ma Y, DiPasquale B, Guller S: Expression of Fas ligand by human cytotrophoblast: implications in placentation and foetal survival. J Clin Endocrinol Metabol. 1996, 81: 3111-3122. 10.1210\/jc.81.8.3119.","journal-title":"J Clin Endocrinol Metabol"},{"key":"497_CR30","doi-asserted-by":"crossref","first-page":"4122","DOI":"10.4049\/jimmunol.158.9.4122","volume":"158","author":"JS Hunt","year":"1997","unstructured":"Hunt JS, Vassmer D, Ferguson TA, Miller L: Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol. 1997, 158: 4122-4128.","journal-title":"J Immunol"},{"key":"497_CR31","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1093\/molehr\/3.8.655","volume":"3","author":"D Uckan","year":"1997","unstructured":"Uckan D, Steele A, Cherry A: Trophoblasts express Fas ligand: a proposed mechanism for immune privilege in placenta and maternal invasion. Mol Hum Reprod. 1997, 3: 655-662. 10.1093\/molehr\/3.8.655.","journal-title":"Mol Hum Reprod"},{"key":"497_CR32","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1055\/s-2007-1016210","volume":"17","author":"S Guller","year":"1999","unstructured":"Guller S, Lachapelle L: The role of placental Fas ligand in maintaining immune privilege at maternal-foetal interfaces. Semin Reprod Endocrinol. 1999, 17: 39-44. 10.1055\/s-2007-1016210.","journal-title":"Semin Reprod Endocrinol"}],"container-title":["Reproductive Biology and Endocrinology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1477-7827-7-25.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,24]],"date-time":"2023-05-24T18:06:18Z","timestamp":1684951578000},"score":1,"resource":{"primary":{"URL":"https:\/\/rbej.biomedcentral.com\/articles\/10.1186\/1477-7827-7-25"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,3,30]]},"references-count":32,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2009,12]]}},"alternative-id":["497"],"URL":"https:\/\/doi.org\/10.1186\/1477-7827-7-25","relation":{},"ISSN":["1477-7827"],"issn-type":[{"value":"1477-7827","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,3,30]]},"assertion":[{"value":"29 October 2008","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 March 2009","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 March 2009","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"25"}}