{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,6]],"date-time":"2026-09-06T04:03:39Z","timestamp":1788667419473,"version":"build-2803163510"},"reference-count":42,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-017"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-012"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-004"}],"funder":[{"DOI":"10.13039\/501100004663","name":"Taiwan Ministry of Science and Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002811","name":"Cathay General Hospital","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002811","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Reproductive Immunology"],"published-print":{"date-parts":[[2021,6]]},"DOI":"10.1016\/j.jri.2021.103311","type":"journal-article","created":{"date-parts":[[2021,3,20]],"date-time":"2021-03-20T16:44:58Z","timestamp":1616258698000},"page":"103311","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":17,"special_numbering":"C","title":["TGF\u03b21 induces in-vitro and ex-vivo angiogenesis through VEGF production in human ovarian follicular fluid-derived granulosa cells during in-vitro fertilization cycle"],"prefix":"10.1016","volume":"145","author":[{"given":"Tsung-Hsuan","family":"Lai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hsuan-Ting","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9248-5030","authenticated-orcid":false,"given":"Wen-Bin","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.jri.2021.103311_bib0005","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1177\/1933719113503411","article-title":"Bone morphogenetic protein 7 increased vascular endothelial growth factor (vegf)-a expression in human granulosa cells and vegf receptor expression in endothelial cells","volume":"21","author":"Akiyama","year":"2014","journal-title":"Reprod. Sci."},{"key":"10.1016\/j.jri.2021.103311_bib0010","doi-asserted-by":"crossref","first-page":"19431","DOI":"10.1074\/jbc.M401235200","volume":"279","author":"Alam","year":"2004","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.jri.2021.103311_bib0015","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.jprot.2013.05.017","article-title":"Proteomic analysis of human follicular fluid: a new perspective towards understanding folliculogenesis","volume":"87","author":"Ambekar","year":"2013","journal-title":"J. Proteomics"},{"key":"10.1016\/j.jri.2021.103311_bib0020","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1016\/j.fertnstert.2014.04.032","article-title":"Follicular-phase ovarian follicular fluid and plasma cytokine profiling of natural cycle in vitro fertilization patients","volume":"102","author":"Baskind","year":"2014","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.jri.2021.103311_bib0025","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1210\/en.2017-00739","article-title":"Placental growth factor is required for ovulation, luteinization, and angiogenesis in primate ovulatory follicles","volume":"159","author":"Bender","year":"2018","journal-title":"Endocrinology"},{"key":"10.1016\/j.jri.2021.103311_bib0030","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1042\/CS20140278","article-title":"Pericytes at the intersection between tissue regeneration and pathology","volume":"128","author":"Birbrair","year":"2015","journal-title":"Clin. Sci."},{"key":"10.1016\/j.jri.2021.103311_bib0035","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1016\/j.theriogenology.2009.10.011","article-title":"The expression of angiogenic growth factors and their receptors in ovarian follicles throughout the estrous cycle in the ewe","volume":"73","author":"Chowdhury","year":"2010","journal-title":"Theriogenology"},{"key":"10.1016\/j.jri.2021.103311_bib0040","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1530\/jrf.0.0370189","article-title":"Follicular fluid","volume":"37","author":"Edwards","year":"1974","journal-title":"J. Reprod. Fertil."},{"key":"10.1016\/j.jri.2021.103311_bib0045","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1038\/s12276-020-0396-y","article-title":"Tgf-\u03b21 induces vegf expression in human granulosa-lutein cells: a potential mechanism for the pathogenesis of ovarian hyperstimulation syndrome","volume":"52","author":"Fang","year":"2020","journal-title":"Exp. Mol. Med."},{"key":"10.1016\/j.jri.2021.103311_bib0050","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/1477-7827-4-18","article-title":"Regulation of the ovarian follicular vasculature","volume":"4","author":"Fraser","year":"2006","journal-title":"Reprod. Biol. Endocrinol."},{"key":"10.1016\/j.jri.2021.103311_bib0055","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.repbio.2018.06.001","article-title":"Follicular fluid vascular endothelial growth factor is associated with type of infertility and interferon alpha correlates with endometrial thickness in natural cycle in vitro fertilization","volume":"18","author":"Hafner","year":"2018","journal-title":"Reprod. Biol."},{"key":"10.1016\/j.jri.2021.103311_bib0060","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1093\/molehr\/5.12.1115","article-title":"Vascular endothelial growth factor (vegf) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the peri-ovulatory interval","volume":"5","author":"Hazzard","year":"1999","journal-title":"Mol. Hum. Reprod."},{"key":"10.1016\/j.jri.2021.103311_bib0065","series-title":"National Report of the Assisted Reproductive Technology Summary in Taiwan","author":"Health Promotion Administration, M.O.H.a.W","year":"2017"},{"key":"10.1016\/j.jri.2021.103311_bib0070","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1387\/ijdb.120133cc","article-title":"The antral follicle: a microenvironment for oocyte differentiation","volume":"56","author":"Hennet","year":"2012","journal-title":"Int. J. Dev. Biol."},{"key":"10.1016\/j.jri.2021.103311_bib0075","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1160\/TH06-08-0470","article-title":"Signal transduction induced in endothelial cells by growth factor receptors involved in angiogenesis","volume":"97","author":"Hofer","year":"2007","journal-title":"Thromb. Haemost."},{"key":"10.1016\/j.jri.2021.103311_bib0080","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.1136\/bmj.291.6510.1693","article-title":"Population study of causes, treatment, and outcome of infertility","volume":"291","author":"Hull","year":"1985","journal-title":"Br. Med. J. Clin. Res. Ed (Clin Res Ed)"},{"key":"10.1016\/j.jri.2021.103311_bib0085","doi-asserted-by":"crossref","first-page":"1608","DOI":"10.1002\/jcp.22491","article-title":"Potential role of follicle-stimulating hormone (fsh) and transforming growth factor (tgfbeta1) in the regulation of ovarian angiogenesis","volume":"226","author":"Kuo","year":"2011","journal-title":"J. Cell. Physiol."},{"key":"10.1016\/j.jri.2021.103311_bib0090","first-page":"5925","article-title":"Gold nanoparticles induce heme oxygenase-1 expression through nrf2 activation and bach1 export in human vascular endothelial cells","volume":"10","author":"Lai","year":"2015","journal-title":"Int. J. Nanomedicine"},{"key":"10.1016\/j.jri.2021.103311_bib0095","doi-asserted-by":"crossref","first-page":"2185","DOI":"10.1166\/jbn.2016.2315","article-title":"Gold nanoparticles compromise tnf-\u03b1-induced endothelial cell adhesion molecule expression through nf-\u03bab and protein degradation pathways and reduce neointima formation in a rat carotid balloon injury model","volume":"12","author":"Lai","year":"2016","journal-title":"J. Biomed. Nanotechnol."},{"key":"10.1016\/j.jri.2021.103311_bib0100","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1002\/1097-0029(20010215)52:4<437::AID-JEMT1029>3.0.CO;2-G","article-title":"Angiogenesis in breast cancer: the role of transforming growth factor beta and cd105","volume":"52","author":"Li","year":"2001","journal-title":"Microsc. Res. Tech."},{"key":"10.1016\/j.jri.2021.103311_bib0105","first-page":"673","article-title":"Revisiting oocyte\u2013somatic cell interactions: in search of novel intrafollicular predictors and regulators of oocyte developmental competence","volume":"14","author":"Li","year":"2008","journal-title":"MHR: Basic Sci. Reproductive Med."},{"key":"10.1016\/j.jri.2021.103311_bib0110","doi-asserted-by":"crossref","first-page":"4650","DOI":"10.1210\/jc.2012-1440","article-title":"Serum anti-m\u00fcllerian hormone levels in healthy females: a nomogram ranging from infancy to adulthood","volume":"97","author":"Lie Fong","year":"2012","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"10.1016\/j.jri.2021.103311_bib0115","first-page":"397","volume":"159","author":"Mattar","year":"2020"},{"key":"10.1016\/j.jri.2021.103311_bib0120","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1016\/j.fertnstert.2015.07.001","article-title":"Follicular fluid and mural granulosa cells microrna profiles vary in in vitro fertilization patients depending on their age and oocyte maturation stage","volume":"104","author":"Moreno","year":"2015","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.jri.2021.103311_bib0125","doi-asserted-by":"crossref","first-page":"1378","DOI":"10.1016\/j.fertnstert.2011.09.031","article-title":"Angiopoietin 1 and angiopoietin 2 in follicular fluid of women undergoing a long protocol","volume":"96","author":"Nishigaki","year":"2011","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.jri.2021.103311_bib0130","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1002\/rmb2.12229","article-title":"Evaluation of antioxidant status and oxidative stress markers in follicular fluid for human in vitro fertilization outcome","volume":"17","author":"Nishihara","year":"2018","journal-title":"Reprod. Med. Biol."},{"key":"10.1016\/j.jri.2021.103311_bib0135","series-title":"Prevalence of Moderate and Severe Disability (in Millions), by Leading Health Condition Associated With Disability, and by Age and Income Status of Countries","author":"Organization","year":"2017"},{"key":"10.1016\/j.jri.2021.103311_bib0140","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1016\/j.domaniend.2005.04.008","article-title":"Follicular fluid concentration of transforming growth factor-\u03b21 is negatively correlated with estradiol and follicle size at the early stage of development of the first-wave cohort of bovine ovarian follicles","volume":"29","author":"Ouellette","year":"2005","journal-title":"Domest. Anim. Endocrinol."},{"key":"10.1016\/j.jri.2021.103311_bib0145","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/1477-7827-7-40","article-title":"Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics","volume":"7","author":"Revelli","year":"2009","journal-title":"Reprod. Biol. Endocrinol."},{"issue":"135","key":"10.1016\/j.jri.2021.103311_bib0150","first-page":"1","article-title":"Hif1 activity in granulosa cells is required for fsh-regulated vegfa expression and follicle survival in mice1","volume":"90","author":"Rico","year":"2014","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.jri.2021.103311_bib0155","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1186\/s12958-017-0277-y","article-title":"Proteomic analysis of human follicular fluid associated with successful in vitro fertilization","volume":"15","author":"Shen","year":"2017","journal-title":"Reprod. Biol. Endocrinol."},{"key":"10.1016\/j.jri.2021.103311_bib0160","doi-asserted-by":"crossref","first-page":"1794","DOI":"10.1016\/j.fertnstert.2009.05.004","article-title":"Bone morphogenetic protein-6 stimulates gene expression of follicle-stimulating hormone receptor, inhibin\/activin beta subunits, and anti-mullerian hormone in human granulosa cells","volume":"92","author":"Shi","year":"2009","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.jri.2021.103311_bib0165","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1016\/j.fertnstert.2008.11.014","article-title":"Bone morphogenetic protein 7 (bmp-7) increases the expression of follicle-stimulating hormone (fsh) receptor in human granulosa cells","volume":"93","author":"Shi","year":"2010","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.jri.2021.103311_bib0170","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1111\/j.1600-0897.2010.00917.x","article-title":"Bone morphogenetic protein-2 (bmp-2) increases gene expression of fsh receptor and aromatase and decreases gene expression of lh receptor and star in human granulosa cells","volume":"65","author":"Shi","year":"2011","journal-title":"Am. J. Reprod. Immunol."},{"key":"10.1016\/j.jri.2021.103311_bib0175","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1262\/jrd.18088","article-title":"Differential effect of follicle-stimulating hormone and estradiol on expressions of vascular endothelial growth factor (vegf) 120, vegf164 and their receptors in bovine granulosa cells","volume":"53","author":"Shimizu","year":"2007","journal-title":"J. Reprod. Dev."},{"key":"10.1016\/j.jri.2021.103311_bib0180","article-title":"Comparison of different stimulation protocols used in in vitro fertilization: a review","volume":"3","author":"Shrestha","year":"2015","journal-title":"Ann. Transl. Med."},{"key":"10.1016\/j.jri.2021.103311_bib0185","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1016\/j.fertnstert.2007.03.080","article-title":"Anti-m\u00fcllerian hormone substance from follicular fluid is positively associated with success in oocyte fertilization during in vitro fertilization","volume":"89","author":"Takahashi","year":"2008","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.jri.2021.103311_bib0190","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1093\/molehr\/gam056","article-title":"Effects of inhibition of vascular endothelial growth factor at time of selection on follicular angiogenesis, expansion, development and atresia in the marmoset","volume":"13","author":"Taylor","year":"2007","journal-title":"Mol. Hum. Reprod."},{"key":"10.1016\/j.jri.2021.103311_bib0195","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.1210\/jc.2005-2457","article-title":"Regulation of vascular endothelial growth factor synthesis and release by human luteal cells in vitro","volume":"91","author":"Tropea","year":"2006","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"10.1016\/j.jri.2021.103311_bib0200","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1093\/humrep\/deu044","article-title":"Gonadotrophin stimulation for in vitro fertilization significantly alters the hormone milieu in follicular fluid: a comparative study between natural cycle ivf and conventional ivf","volume":"29","author":"Von Wolff","year":"2014","journal-title":"Hum. Reprod."},{"key":"10.1016\/j.jri.2021.103311_bib0205","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1093\/fampra\/cmp029","article-title":"Epidemiology and management of infertility: a population-based study in uk primary care","volume":"26","author":"Wilkes","year":"2009","journal-title":"Fam. Pract."},{"key":"10.1016\/j.jri.2021.103311_bib0210","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1039\/c2fo30051f","article-title":"Anti-inflammatory and anti-angiogenic effects of flavonoids isolated from lycium barbarum linnaeus on human umbilical vein endothelial cells","volume":"3","author":"Wu","year":"2012","journal-title":"Food Funct."}],"container-title":["Journal of Reproductive Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0165037821000413?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0165037821000413?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,28]],"date-time":"2025-09-28T04:30:26Z","timestamp":1759033826000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0165037821000413"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6]]},"references-count":42,"alternative-id":["S0165037821000413"],"URL":"https:\/\/doi.org\/10.1016\/j.jri.2021.103311","relation":{},"ISSN":["0165-0378"],"issn-type":[{"value":"0165-0378","type":"print"}],"subject":[],"published":{"date-parts":[[2021,6]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"TGF\u03b21 induces in-vitro and ex-vivo angiogenesis through VEGF production in human ovarian follicular fluid-derived granulosa cells during in-vitro fertilization cycle","name":"articletitle","label":"Article Title"},{"value":"Journal of Reproductive Immunology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.jri.2021.103311","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 Elsevier B.V. All rights reserved.","name":"copyright","label":"Copyright"}],"article-number":"103311"}}