{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,13]],"date-time":"2026-08-13T16:58:55Z","timestamp":1786640335275,"version":"build-2736575974"},"reference-count":110,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2019,3,1]],"date-time":"2019-03-01T00:00:00Z","timestamp":1551398400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":["rep.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2019,3,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The multimodular matricellular protein thrombospondin-1 (THBS1) was among the first identified endogenous antiangiogenic molecules. Recent studies have shown THBS1-mediated suppression of angiogenesis and other critical activities for corpus luteum (CL) regression. THBS1 is specifically induced by prostaglandin F2alpha in mature CL undergoing regression, whereas luteinizing signals such as luteinizing hormone and insulin reduced its expression. THBS1 interacts both synergistically and antagonistically with other essential luteal factors, such as fibroblast growth factor 2, transforming growth factor beta1 and serpin family E member 1, to promote vascular instability, apoptosis and matrix remodeling during luteal regression. Expression of THBS1 is also downregulated by pregnancy recognition signals to maintain the CL during early pregnancy. This dynamic pattern of luteal expression, the extensive interactivity with other luteal factors and strong antiangiogenic and proapoptotic activities indicate that THBS1 is a major determinant of CL fate.<\/jats:p>","DOI":"10.1530\/rep-18-0530","type":"journal-article","created":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T10:43:11Z","timestamp":1545216191000},"page":"R73-R83","update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-1","source":"Crossref","is-referenced-by-count":28,"title":["Thrombospondin-1 at the crossroads of corpus luteum fate decisions"],"prefix":"10.1093","volume":"157","author":[{"given":"Svetlana","family":"Farberov","sequence":"first","affiliation":[{"name":"Department of Animal Sciences , The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raghavendra","family":"Basavaraja","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rina","family":"Meidan","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,3,1]]},"reference":[{"key":"2026010712184961300_bib1","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/0960-9822(93)90270-X","article-title":"The thrombospondin family","volume":"3","author":"Adams","year":"1993","journal-title":"Current Biology"},{"key":"2026010712184961300_bib2","doi-asserted-by":"publisher","first-page":"961","DOI":"10.1016\/j.biocel.2004.01.004","article-title":"The thrombospondins","volume":"36","author":"Adams","year":"2004","journal-title":"International Journal of Biochemistry and Cell Biology"},{"key":"2026010712184961300_bib3","doi-asserted-by":"publisher","first-page":"a009712","DOI":"10.1101\/cshperspect.a009712","article-title":"The thrombospondins","volume":"3","author":"Adams","year":"2011","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"2026010712184961300_bib4","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1006\/bbrc.1994.2262","article-title":"Thrombospondin (TSP) and transforming growth factor beta 1 (TGF-beta) promote human A549 lung carcinoma cell plasminogen activator inhibitor type 1 (PAI-1) production and stimulate tumor cell attachment in vitro","volume":"203","author":"Albo","year":"1994","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2026010712184961300_bib5","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/S1091-255X(99)80058-4","article-title":"Thrombospondin-1 and transforming growth factor beta-1 upregulate plasminogen activator inhibitor type 1 in pancreatic cancer","volume":"3","author":"Albo","year":"1999","journal-title":"Journal of Gastrointestinal Surgery"},{"key":"2026010712184961300_bib6","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1006\/bbrc.1993.1418","article-title":"Recombinant truncated thrombospondin-1 monomer modulates endothelial cell plasminogen activator inhibitor 1 accumulation and proliferation in vitro","volume":"192","author":"Bagavandoss","year":"1993","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2026010712184961300_bib7","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1177\/002215549804600908","article-title":"Secreted protein, acidic and rich in cysteine (SPARC) and thrombospondin in the developing follicle and corpus luteum of the rat","volume":"46","author":"Bagavandoss","year":"1998","journal-title":"Journal of Histochemistry and Cytochemistry"},{"key":"2026010712184961300_bib8","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1530\/REP-17-0290","article-title":"Interferon-tau promotes luteal endothelial cell survival and inhibits specific luteolytic genes in bovine corpus luteum","volume":"154","author":"Basavaraja","year":"2017","journal-title":"Reproduction"},{"key":"2026010712184961300_bib9","doi-asserted-by":"publisher","first-page":"32167","DOI":"10.1074\/jbc.M003834200","article-title":"Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity","volume":"275","author":"Bein","year":"2000","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712184961300_bib10","doi-asserted-by":"publisher","first-page":"C1012","DOI":"10.1152\/ajpcell.00101.2004","article-title":"Role of TGF-beta1 and JNK signaling in capillary tube patterning","volume":"287","author":"Bein","year":"2004","journal-title":"American Journal of Physiology: Cell Physiology"},{"key":"2026010712184961300_bib11","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1262\/jrd.2016-056","article-title":"Expression and localization of members of the thrombospondin family during final follicle maturation and corpus luteum formation and function in the bovine ovary","volume":"62","author":"Berisha","year":"2016","journal-title":"Journal of Reproduction and Development"},{"key":"2026010712184961300_bib12","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1002\/(SICI)1097-4652(199910)181:1&lt;96::AID-JCP10&gt;3.0.CO;2-I","article-title":"Growth state-dependent regulation of plasminogen activator inhibitor type-1 gene expression during epithelial cell stimulation by serum and transforming growth factor-\u03b21","volume":"181","author":"Boehm","year":"1999","journal-title":"Journal of Cellular Physiology"},{"key":"2026010712184961300_bib13","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1172\/JCI12749","article-title":"Thrombospondins as matricellular modulators of cell function","volume":"107","author":"Bornstein","year":"2001","journal-title":"Journal of Clinical Investigation"},{"key":"2026010712184961300_bib14","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1007\/s12079-009-0060-8","article-title":"Thrombospondins function as regulators of angiogenesis","volume":"3","author":"Bornstein","year":"2009","journal-title":"Journal of Cell Communication and Signaling"},{"key":"2026010712184961300_bib15","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1095\/biolreprod.109.079467","article-title":"Uterine vein infusion of interferon tau (IFNT) extends luteal life span in ewes","volume":"82","author":"Bott","year":"2010","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib16","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1016\/S0962-8924(00)01906-1","article-title":"Integrin-associated protein (CD47) and its ligands","volume":"11","author":"Brown","year":"2001","journal-title":"Trends in Cell Biology"},{"key":"2026010712184961300_bib17","first-page":"757","article-title":"Thrombospondin-1 (TSP-1) and TSP-1-derived heparin-binding peptides induce promyelocytic leukemia cell differentiation and apoptosis","volume":"25","author":"Bruel","year":"2005","journal-title":"Anticancer Research"},{"key":"2026010712184961300_bib18","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1007\/s00109-006-0075-z","article-title":"The proangiogenic phenotype of human tumor-derived endothelial cells depends on thrombospondin-1 downregulation via phosphatidylinositol 3-kinase\/Akt pathway","volume":"84","author":"Bussolati","year":"2006","journal-title":"Journal of Molecular Medicine"},{"key":"2026010712184961300_bib19","doi-asserted-by":"publisher","first-page":"41734","DOI":"10.1074\/jbc.M406267200","article-title":"Identification of novel beta1 integrin binding sites in the type 1 and type 2 repeats of thrombospondin-1","volume":"279","author":"Calzada","year":"2004","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712184961300_bib20","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1007\/s00018-007-7484-1","article-title":"Structures of thrombospondins","volume":"65","author":"Carlson","year":"2008","journal-title":"Cellular and Molecular Life Sciences"},{"key":"2026010712184961300_bib21","doi-asserted-by":"publisher","first-page":"2885","DOI":"10.1091\/mbc.11.9.2885","article-title":"Cell contact-dependent activation of \u03b13\u03b21 integrin modulates endothelial cell responses to thrombospondin-1","volume":"11","author":"Chandrasekaran","year":"2000","journal-title":"Molecular Biology of the Cell"},{"key":"2026010712184961300_bib22","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1016\/S0945-053X(00)00107-4","article-title":"The cell biology of thrombospondin-1","volume":"19","author":"Chen","year":"2000","journal-title":"Matrix Biology"},{"key":"2026010712184961300_bib23","doi-asserted-by":"publisher","first-page":"1227","DOI":"10.1158\/1535-7163.MCT-08-0051","article-title":"Plasminogen activator inhibitor-1 inhibits prostate tumor growth through endothelial apoptosis","volume":"7","author":"Chen","year":"2008","journal-title":"Molecular Cancer Therapeutics"},{"key":"2026010712184961300_bib24","first-page":"129","article-title":"MicroRNA control of ovarian function","volume":"7","author":"Christenson","year":"2010","journal-title":"Animal Reproduction"},{"key":"2026010712184961300_bib25","doi-asserted-by":"publisher","first-page":"8733","DOI":"10.1074\/jbc.M109.085605","article-title":"Non-peptidic thrombospondin-1 mimics as fibroblast growth factor-2 inhibitors: an integrated strategy for the development of new antiangiogenic compounds","volume":"285","author":"Colombo","year":"2010","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712184961300_bib26","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1016\/j.cytogfr.2005.01.007","article-title":"Mechanisms underlying differential responses to FGF signaling","volume":"16","author":"Dailey","year":"2005","journal-title":"Cytokine and Growth Factor Reviews"},{"key":"2026010712184961300_bib27","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1089\/nat.2013.0467","article-title":"Multiple microRNAs derived from chemically synthesized precursors regulate thrombospondin 1 expression","volume":"24","author":"Dogar","year":"2014","journal-title":"Nucleic Acid Therapeutics"},{"key":"2026010712184961300_bib28","doi-asserted-by":"publisher","first-page":"2565","DOI":"10.1210\/endo.130.5.1374008","article-title":"Differentiation-controlled synthesis and binding of thrombospondin to granulosa cells","volume":"130","author":"Dreyfus","year":"1992","journal-title":"Endocrinology"},{"key":"2026010712184961300_bib29","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1095\/biolreprod.114.121020","article-title":"Functions and transcriptional regulation of thrombospondins and their interrelationship with fibroblast growth factor-2 in bovine luteal cells","volume":"91","author":"Farberov","year":"2014","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib30","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1095\/biolreprod.115.135822","article-title":"Thrombospondin-1 affects bovine luteal function via transforming growth factor-beta1-dependent and independent actions","volume":"94","author":"Farberov","year":"2016","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib31","doi-asserted-by":"publisher","first-page":"366","DOI":"10.1093\/biolre\/iox167","article-title":"Fibroblast growth factor-2 and transforming growth factor-beta1 oppositely regulate miR-221 that targets thrombospondin-1 in bovine luteal endothelial cells","volume":"98","author":"Farberov","year":"2018","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.neulet.2015.02.002","article-title":"miR-487b promotes human umbilical vein endothelial cell proliferation, migration, invasion and tube formation through regulating THBS1","volume":"591","author":"Feng","year":"2015","journal-title":"Neuroscience Letters"},{"key":"2026010712184961300_bib33","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1016\/j.exer.2004.07.005","article-title":"Thrombospondin-1 in the trabecular meshwork: localization in normal and glaucomatous eyes, and induction by TGF-beta1 and dexamethasone in vitro","volume":"79","author":"Flugel-Koch","year":"2004","journal-title":"Experimental Eye Research"},{"key":"2026010712184961300_bib34","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1006\/bbrc.2000.2678","article-title":"Integrin-associated protein and thrombospondin-1 as endothelial mechanosensitive death mediators","volume":"271","author":"Freyberg","year":"2000","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2026010712184961300_bib35","doi-asserted-by":"publisher","first-page":"1280","DOI":"10.1210\/en.2009-0686","article-title":"Thrombospondin-1 inhibits angiogenesis and promotes follicular atresia in a novel in vitro angiogenesis assay","volume":"151","author":"Garside","year":"2010","journal-title":"Endocrinology"},{"key":"2026010712184961300_bib36","doi-asserted-by":"publisher","first-page":"5905","DOI":"10.1210\/en.2010-0283","article-title":"A thrombospondin-mimetic peptide, ABT-898, suppresses angiogenesis and promotes follicular atresia in pre- and early-antral follicles in vivo","volume":"151","author":"Garside","year":"2010","journal-title":"Endocrinology"},{"key":"2026010712184961300_bib37","doi-asserted-by":"publisher","first-page":"213","DOI":"10.3389\/fgene.2017.00213","article-title":"The dynamics of microRNA transcriptome in bovine corpus luteum during its formation, function, and regression","volume":"8","author":"Gecaj","year":"2017","journal-title":"Frontiers in Genetics"},{"key":"2026010712184961300_bib38","doi-asserted-by":"publisher","first-page":"1071","DOI":"10.1095\/biolreprod.104.031120","article-title":"Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development","volume":"72","author":"Greenaway","year":"2005","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib39","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1095\/biolreprod66.1.144","article-title":"Coordinate expression of anticoagulant heparan sulfate proteoglycans and serine protease inhibitors in the rat ovary: a potent system of proteolysis control","volume":"66","author":"Hasan","year":"2002","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib40","doi-asserted-by":"publisher","first-page":"920","DOI":"10.1093\/molehr\/5.10.920","article-title":"Co-expression of integrin-associated protein (IAP\/CD47) and its ligand thrombospondin-1 on human granulosa and large luteal cells","volume":"5","author":"Higuchi","year":"1999","journal-title":"Molecular Human Reproduction"},{"key":"2026010712184961300_bib41","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1186\/1471-2164-10-443","article-title":"Identification and characterization of miRNAs expressed in the bovine ovary","volume":"10","author":"Hossain","year":"2009","journal-title":"BMC Genomics"},{"key":"2026010712184961300_bib42","doi-asserted-by":"publisher","first-page":"e0158160","DOI":"10.1371\/journal.pone.0158160","article-title":"Circulating microRNA profiles during the bovine oestrous cycle","volume":"11","author":"Ioannidis","year":"2016","journal-title":"PLoS ONE"},{"key":"2026010712184961300_bib43","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1038\/71517","article-title":"Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1","volume":"6","author":"Jimenez","year":"2000","journal-title":"Nature Medicine"},{"key":"2026010712184961300_bib44","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1210\/endo.132.1.8419126","article-title":"Apoptosis during luteal regression in cattle","volume":"132","author":"Juengel","year":"1993","journal-title":"Endocrinology"},{"key":"2026010712184961300_bib45","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1038\/emm.2004.41","article-title":"Weakening of the repressive YY-1 site on the thrombospondin-1 promoter via c-Jun\/YY-1 interaction","volume":"36","author":"Kang","year":"2004","journal-title":"Experimental and Molecular Medicine"},{"key":"2026010712184961300_bib46","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1562\/2005-09-29-RA-702","article-title":"Ultraviolet radiation attenuates thrombospondin 1 expression via PI3K-Akt activation in human keratinocytes","volume":"82","author":"Kim","year":"2006","journal-title":"Photochemistry and Photobiology"},{"key":"2026010712184961300_bib47","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1530\/REP-06-0172","article-title":"Expression and localisation of extracellular matrix degrading proteases and their inhibitors during the oestrous cycle and after induced luteolysis in the bovine corpus luteum","volume":"134","author":"Kliem","year":"2007","journal-title":"Reproduction"},{"key":"2026010712184961300_bib48","doi-asserted-by":"publisher","first-page":"1223","DOI":"10.1038\/sj.emboj.7600166","article-title":"Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats","volume":"23","author":"Kvansakul","year":"2004","journal-title":"EMBO Journal"},{"key":"2026010712184961300_bib49","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1083\/jcb.140.2.419","article-title":"Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis","volume":"140","author":"Kyriakides","year":"1998","journal-title":"Journal of Cell Biology"},{"key":"2026010712184961300_bib50","doi-asserted-by":"publisher","first-page":"801","DOI":"10.2527\/jas.2008-1407","article-title":"ASAS centennial paper: contributions in the Journal of Animal Science to the development of protocols for breeding management of cattle through synchronization of estrus and ovulation","volume":"87","author":"Lauderdale","year":"2009","journal-title":"Journal of Animal Science"},{"key":"2026010712184961300_bib51","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1016\/S0955-0674(00)00143-5","article-title":"The functions of thrombospondin-1 and-2","volume":"12","author":"Lawler","year":"2000","journal-title":"Current Opinion in Cell Biology"},{"key":"2026010712184961300_bib53","doi-asserted-by":"publisher","first-page":"982","DOI":"10.1172\/JCI1684","article-title":"Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia","volume":"101","author":"Lawler","year":"1998","journal-title":"Journal of Clinical Investigation"},{"key":"2026010712184961300_bib52","doi-asserted-by":"publisher","first-page":"1949","DOI":"10.1016\/S0002-9440(10)63042-8","article-title":"Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice","volume":"159","author":"Lawler","year":"2001","journal-title":"American Journal of Pathology"},{"key":"2026010712184961300_bib54","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/S0741-5214(02)75468-2","article-title":"Thrombospondin-1 induces matrix metalloproteinase-2 activation in vascular smooth muscle cells","volume":"38","author":"Lee","year":"2003","journal-title":"Journal of Vascular Surgery"},{"key":"2026010712184961300_bib55","doi-asserted-by":"publisher","first-page":"1003","DOI":"10.1071\/RD9961003","article-title":"Effects of local growth factors on the secretory function of bovine corpus luteum during the oestrous cycle and pregnancy in vitro","volume":"8","author":"Liebermann","year":"1996","journal-title":"Reproduction, Fertility and Development"},{"key":"2026010712184961300_bib56","doi-asserted-by":"publisher","first-page":"64","DOI":"10.3389\/fgene.2013.00064","article-title":"miR-221 affects multiple cancer pathways by modulating the level of hundreds messenger RNAs","volume":"4","author":"Lupini","year":"2013","journal-title":"Frontiers in Genetics"},{"key":"2026010712184961300_bib57","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1095\/biolreprod.115.135053","article-title":"Changes in microRNA expression during maturation of the bovine corpus luteum: regulation of luteal cell proliferation and function by microRNA-34a","volume":"94","author":"Maalouf","year":"2016","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib58","doi-asserted-by":"publisher","first-page":"2501","DOI":"10.1242\/jcs.084558","article-title":"TGFB1 disrupts the angiogenic potential of microvascular endothelial cells of the corpus luteum","volume":"124","author":"Maroni","year":"2011","journal-title":"Journal of Cell Science"},{"key":"2026010712184961300_bib59","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1038\/35043051","article-title":"How cells read TGF-beta signals","volume":"1","author":"Massague","year":"2000","journal-title":"Nature Reviews Molecular Cell Biology"},{"key":"2026010712184961300_bib60","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.mce.2006.04.007","article-title":"Androgen and fibroblast growth factor 8 (FGF8) downregulation of thrombospondin 1 (TSP1) in mouse breast cancer cells","volume":"253","author":"Mattila","year":"2006","journal-title":"Molecular and Cellular Endocrinology"},{"key":"2026010712184961300_bib61","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1530\/REP-12-0025","article-title":"Identification of miRNAs associated with the follicular-luteal transition in the ruminant ovary","volume":"144","author":"McBride","year":"2012","journal-title":"Reproduction"},{"key":"2026010712184961300_bib62","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1152\/physrev.1999.79.2.263","article-title":"Luteolysis: a neuroendocrine-mediated event","volume":"79","author":"McCracken","year":"1999","journal-title":"Physiological Reviews"},{"key":"2026010712184961300_bib63","first-page":"159","author":"Meidan","year":"2017","journal-title":"Luteolysis in Ruminants: Past Concepts, New Insights, and Persisting Challenges, The Life Cycle of the Corpus Luteum"},{"key":"2026010712184961300_bib64","first-page":"289","article-title":"Regulation of corpus luteum development and maintenance: specific roles of angiogenesis and action of prostaglandin F2alpha","volume":"67","author":"Miyamoto","year":"2010","journal-title":"Society of Reproduction and Fertility Supplement"},{"key":"2026010712184961300_bib65","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1152\/physiolgenomics.00155.2010","article-title":"Deciphering the luteal transcriptome: potential mechanisms mediating stage-specific luteolytic response of the corpus luteum to prostaglandin F(2)alpha","volume":"43","author":"Mondal","year":"2011","journal-title":"Physiological Genomics"},{"key":"2026010712184961300_bib66","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/S1359-6101(99)00029-5","article-title":"Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology","volume":"11","author":"Murphy-Ullrich","year":"2000","journal-title":"Cytokine and Growth Factor Reviews"},{"key":"2026010712184961300_bib67","doi-asserted-by":"publisher","first-page":"404","DOI":"10.1006\/excr.1995.1103","article-title":"Transforming growth factors beta stimulate both thrombospondin-1 and CISP\/thrombospondin-2 synthesis by bovine adrenocortical cells","volume":"217","author":"Negoescu","year":"1995","journal-title":"Experimental Cell Research"},{"key":"2026010712184961300_bib68","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1111\/j.1749-6632.2001.tb03944.x","article-title":"Role of CD36, the macrophage class B scavenger receptor, in atherosclerosis","volume":"947","author":"Nicholson","year":"2001","journal-title":"Annals of the New York Academy of Sciences"},{"key":"2026010712184961300_bib69","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1016\/j.devcel.2012.01.008","article-title":"miR-221 is required for endothelial tip cell behaviors during vascular development","volume":"22","author":"Nicoli","year":"2012","journal-title":"Developmental Cell"},{"key":"2026010712184961300_bib70","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1152\/physrev.2000.80.1.1","article-title":"Mechanisms controlling the function and life span of the corpus luteum","volume":"80","author":"Niswender","year":"2000","journal-title":"Physiological Reviews"},{"key":"2026010712184961300_bib71","doi-asserted-by":"publisher","first-page":"e36990","DOI":"10.1371\/journal.pone.0036990","article-title":"Direct and allosteric inhibition of the FGF2\/HSPGs\/FGFR1 ternary complex formation by an antiangiogenic, thrombospondin-1-mimic small molecule","volume":"7","author":"Pagano","year":"2012","journal-title":"PLoS ONE"},{"key":"2026010712184961300_bib72","doi-asserted-by":"publisher","first-page":"1763","DOI":"10.1002\/jcp.22505","article-title":"Induction of Id-1 by FGF-2 involves activity of EGR-1 and sensitizes neuroblastoma cells to cell death","volume":"226","author":"Passiatore","year":"2011","journal-title":"Journal of Cellular Physiology"},{"key":"2026010712184961300_bib73","doi-asserted-by":"publisher","first-page":"1104","DOI":"10.1161\/hq0701.093685","article-title":"Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis","volume":"21","author":"Pepper","year":"2001","journal-title":"Arteriosclerosis, Thrombosis and Vascular Biology"},{"key":"2026010712184961300_bib74","doi-asserted-by":"publisher","first-page":"1522","DOI":"10.1095\/biolreprod.102.007153","article-title":"Expression and localization of thrombospondin-1 and -2 and their cell-surface receptor, CD36, during rat follicular development and formation of the corpus luteum","volume":"67","author":"Petrik","year":"2002","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib75","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1016\/j.bbcan.2005.11.002","article-title":"Regulation of tumor angiogenesis by thrombospondin-1","volume":"1765","author":"Ren","year":"2006","journal-title":"Biochimica et Biophysica Acta (BBA): Reviews on Cancer"},{"key":"2026010712184961300_bib76","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/j.matbio.2014.01.012","article-title":"Current understanding of the thrombospondin-1 interactome","volume":"37","author":"Resovi","year":"2014","journal-title":"Matrix Biology"},{"key":"2026010712184961300_bib77","doi-asserted-by":"publisher","first-page":"13586","DOI":"10.1074\/jbc.274.19.13586","article-title":"The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta","volume":"274","author":"Ribeiro","year":"1999","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712184961300_bib78","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/j.cytogfr.2013.06.003","article-title":"Unchaining the beast; insights from structural and evolutionary studies on TGFbeta secretion, sequestration, and activation","volume":"24","author":"Robertson","year":"2013","journal-title":"Cytokine and Growth Factor Reviews"},{"key":"2026010712184961300_bib80","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1095\/biolreprod.106.055434","article-title":"Fibroblast growth factor 2 is more dynamic than vascular endothelial growth factor A during the follicle-luteal transition in the cow","volume":"77","author":"Robinson","year":"2007","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib79","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1093\/jas\/skx069","article-title":"MicroRNA 221 expression in theca and granulosa cells: hormonal regulation and function","volume":"96","author":"Robinson","year":"2018","journal-title":"Journal of Animal Science"},{"key":"2026010712184961300_bib81","doi-asserted-by":"publisher","first-page":"12485","DOI":"10.1073\/pnas.171460498","article-title":"Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor","volume":"98","author":"Rodriguez-Manzaneque","year":"2001","journal-title":"PNAS"},{"key":"2026010712184961300_bib83","doi-asserted-by":"publisher","first-page":"1095","DOI":"10.1152\/physiolgenomics.00082.2013","article-title":"Pregnancy-associated genes contribute to antiluteolytic mechanisms in ovine corpus luteum","volume":"45","author":"Romero","year":"2013","journal-title":"Physiological Genomics"},{"key":"2026010712184961300_bib82","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1095\/biolreprod.115.132860","article-title":"Temporal release, paracrine and endocrine actions of ovine conceptus-derived interferon-tau during early pregnancy","volume":"93","author":"Romero","year":"2015","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib84","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1095\/biolreprod60.5.1087","article-title":"Accumulation of caspase-3 messenger ribonucleic acid and induction of caspase activity in the ovine corpus luteum following prostaglandin F2\u03b1 treatment in vivo","volume":"60","author":"Rueda","year":"1999","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib85","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.cytogfr.2004.11.002","article-title":"Dual role for TGF-beta1 in apoptosis","volume":"16","author":"Sanchez-Capelo","year":"2005","journal-title":"Cytokine and Growth Factor Reviews"},{"key":"2026010712184961300_bib86","doi-asserted-by":"publisher","first-page":"41143","DOI":"10.1074\/jbc.M104913200","article-title":"Induction of the transcriptional repressor yin yang-1 by vascular cell injury autocrine\/paracrine role of endogenous fibroblast growth factor-2","volume":"276","author":"Santiago","year":"2001","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712184961300_bib87","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1111\/j.1439-0531.2004.00509.x","article-title":"Regulation of corpus luteum function in cattle \u2013 an overview","volume":"39","author":"Schams","year":"2004","journal-title":"Reproduction in Domestic Animals"},{"key":"2026010712184961300_bib88","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/j.domaniend.2012.03.007","article-title":"Vascular and immune regulation of corpus luteum development, maintenance, and regression in the cow","volume":"43","author":"Shirasuna","year":"2012","journal-title":"Domestic Animal Endocrinology"},{"key":"2026010712184961300_bib89","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.matbio.2004.11.005","article-title":"The antiangiogenic effect of thrombospondin-2 is mediated by CD36 and modulated by histidine-rich glycoprotein","volume":"24","author":"Simantov","year":"2005","journal-title":"Matrix Biology"},{"key":"2026010712184961300_bib90","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/S0303-7207(02)00054-0","article-title":"Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors","volume":"191","author":"Smith","year":"2002","journal-title":"Molecular and Cellular Endocrinology"},{"key":"2026010712184961300_bib91","doi-asserted-by":"publisher","first-page":"6556","DOI":"10.1021\/bbib240a028","article-title":"Synthesis of truncated amino-terminal trimers of thrombospondin","volume":"30","author":"Sottile","year":"1991","journal-title":"Biochemistry"},{"key":"2026010712184961300_bib92","doi-asserted-by":"publisher","first-page":"1308","DOI":"10.1161\/01.RES.0000266662.98355.66","article-title":"Interaction of alpha9beta1 integrin with thrombospondin-1 promotes angiogenesis","volume":"100","author":"Staniszewska","year":"2007","journal-title":"Circulation Research"},{"key":"2026010712184961300_bib93","doi-asserted-by":"publisher","first-page":"2319","DOI":"10.1159\/000475651","article-title":"Up-regulated expression of matrix metalloproteinases in endothelial cells mediates platelet microvesicle-induced angiogenesis","volume":"41","author":"Sun","year":"2017","journal-title":"Cellular Physiology and Biochemistry"},{"key":"2026010712184961300_bib94","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1016\/j.matbio.2012.01.006","article-title":"Thrombospondin1 in tissue repair and fibrosis: TGF-beta-dependent and independent mechanisms","volume":"31","author":"Sweetwyne","year":"2012","journal-title":"Matrix Biology"},{"key":"2026010712184961300_bib95","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.str.2005.09.017","article-title":"The structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin","volume":"14","author":"Tan","year":"2006","journal-title":"Structure"},{"key":"2026010712184961300_bib96","doi-asserted-by":"publisher","first-page":"1674","DOI":"10.1096\/fj.99-0931fje","article-title":"The heparin binding 25 kDa fragment of thrombospondin-1 promotes angiogenesis and modulates gelatinase and TIMP-2 production in endothelial cells","volume":"14","author":"Taraboletti","year":"2000","journal-title":"FASEB Journal"},{"key":"2026010712184961300_bib97","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1210\/en.2007-0835","article-title":"Thrombospondin-1 expression is increased during follicular atresia in the primate ovary","volume":"149","author":"Thomas","year":"2008","journal-title":"Endocrinology"},{"key":"2026010712184961300_bib98","doi-asserted-by":"publisher","first-page":"44","DOI":"10.7150\/ijbs.5.44","article-title":"Non-classical p38 map kinase functions: cell cycle checkpoints and survival","volume":"5","author":"Thornton","year":"2009","journal-title":"International Journal of Biological Sciences"},{"key":"2026010712184961300_bib99","doi-asserted-by":"publisher","first-page":"pe17","DOI":"10.1126\/stke.2282004pe17","article-title":"Promotion and attenuation of FGF signaling through the Ras-MAPK pathway","volume":"2004","author":"Tsang","year":"2004","journal-title":"Science Signaling"},{"key":"2026010712184961300_bib100","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1667\/RR2200.1","article-title":"HUVEC respond to radiation by inducing the expression of pro-angiogenic microRNAs","volume":"175","author":"Vincenti","year":"2011","journal-title":"Radiation Research"},{"key":"2026010712184961300_bib101","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1002\/jcb.240530109","article-title":"Modulation of endothelial cell proliferation, adhesion, and motility by recombinant heparin-binding domain and synthetic peptides from the type I repeats of thrombospondin","volume":"53","author":"Vogel","year":"1993","journal-title":"Journal of Cellular Biochemistry"},{"key":"2026010712184961300_bib102","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1016\/S1535-6108(02)00209-X","article-title":"Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1","volume":"2","author":"Volpert","year":"2002","journal-title":"Cancer Cell"},{"key":"2026010712184961300_bib103","doi-asserted-by":"publisher","first-page":"630","DOI":"10.1002\/dvdy.10412","article-title":"Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration","volume":"228","author":"Wang","year":"2003","journal-title":"Developmental Dynamics"},{"key":"2026010712184961300_bib104","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1111\/j.1471-4159.2008.05777.x","article-title":"Role of oxidative stress and caspase 3 in CD47-mediated neuronal cell death","volume":"108","author":"Xing","year":"2009","journal-title":"Journal of Neurochemistry"},{"key":"2026010712184961300_bib105","doi-asserted-by":"publisher","first-page":"10357","DOI":"10.1074\/jbc.M409596200","article-title":"Prostaglandin F2alpha-mediated activation of apoptotic signaling cascades in the corpus luteum during apoptosis: involvement of caspase-activated DNase","volume":"280","author":"Yadav","year":"2005","journal-title":"Journal of Biological Chemistry"},{"key":"2026010712184961300_bib106","doi-asserted-by":"publisher","first-page":"1449","DOI":"10.1002\/mrd.20878","article-title":"Effect of local neutralization of basic fibroblast growth factor or vascular endothelial growth factor by a specific antibody on the development of the corpus luteum in the cow","volume":"75","author":"Yamashita","year":"2008","journal-title":"Molecular Reproduction and Development"},{"key":"2026010712184961300_bib107","first-page":"179","article-title":"Proteoglycans and hyaluronan in female reproductive organs","volume":"70","author":"Yanagishita","year":"1994","journal-title":"Exs"},{"key":"2026010712184961300_bib108","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1158\/0008-5472.CAN-09-1474","article-title":"An ets2-driven transcriptional program in tumor-associated macrophages promotes tumor metastasis","volume":"70","author":"Zabuawala","year":"2010","journal-title":"Cancer Research"},{"key":"2026010712184961300_bib109","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1095\/biolreprod.111.095067","article-title":"Regulation of angiogenesis-related prostaglandin f2alpha-induced genes in the bovine corpus luteum","volume":"86","author":"Zalman","year":"2012","journal-title":"Biology of Reproduction"},{"key":"2026010712184961300_bib110","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1038\/cr.2008.328","article-title":"Non-Smad pathways in TGF-beta signaling","volume":"19","author":"Zhang","year":"2009","journal-title":"Cell Research"}],"container-title":["Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/rep.bioscientifica.com\/view\/journals\/rep\/157\/3\/REP-18-0530.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/reproduction\/article-pdf\/157\/3\/R73\/64124257\/rep-18-0530.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/reproduction\/article-pdf\/157\/3\/R73\/64124257\/rep-18-0530.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,7]],"date-time":"2026-01-07T17:19:59Z","timestamp":1767806399000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/reproduction\/article\/157\/3\/R73\/8235318"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,1]]},"references-count":110,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2019,3,1]]}},"URL":"https:\/\/doi.org\/10.1530\/rep-18-0530","relation":{},"ISSN":["1470-1626","1741-7899"],"issn-type":[{"value":"1470-1626","type":"print"},{"value":"1741-7899","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,3,1]]},"published":{"date-parts":[[2019,3,1]]}}}