{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,7]],"date-time":"2026-06-07T20:15:24Z","timestamp":1780863324391,"version":"3.54.1"},"reference-count":38,"publisher":"CSIRO Publishing","issue":"12","license":[{"start":{"date-parts":[[2025,5,27]],"date-time":"2025-05-27T00:00:00Z","timestamp":1748304000000},"content-version":"vor","delay-in-days":1331,"URL":"https:\/\/doi.org\/10.1071\/journalslicense"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,10,8]]},"abstract":"<jats:p>The long-term storage of spermatozoa in the female reproductive tract is limited by the innate immune system. Oestrogen plays a role in regulating the innate immune system. Thus, exploring the expression of genes in the Toll-like receptor (TLR) 2\/4 pathway and oestrogen receptors in the oviduct of Mauremys reevesii could contribute to our understanding of the mechanism of sperm storage. In this study, three parts of the oviduct (isthmus, uterus and vagina) in three mated and unmated female turtles were used to perform immunohistochemistry and real-time quantitative polymerase chain reaction (qPCR). Immunohistochemistry revealed that the TLR2\/4 protein was mainly distributed in epithelial tissues and glandular cell membranes, and that TLR2\/4 levels in the oviduct were significantly decreased in mated compared with unmated turtles. Real-time qPCR indicated that TLR2\/4, myeloid differentiation factor 88 (MyD88), interleukin 1 receptor associated kinase 4 (IRAK4), TNF receptor associated factor 6 (TRAF6), interferon regulatory factor 3 (IRF3) and interleukin 6 (IL6) mRNA expression was significantly higher in the oviduct of unmated than mated turtles, whereas the opposite was true for the expression of oestrogen receptor 1 (ESR1) and progesterone receptor (PGR). These results indicate that when spermatozoa are stored in the oviduct, an increase in oestrogen suppresses the immune response induced by the TLR2\/4 pathway so that spermatozoa are not removed as a foreign substance, but stored until fertilisation. The findings of this study are relevant to our understanding of the relationship between sperm storage and the innate immune system in the oviduct of reptiles.<\/jats:p>","DOI":"10.1071\/rd20341","type":"journal-article","created":{"date-parts":[[2021,10,3]],"date-time":"2021-10-03T21:39:55Z","timestamp":1633297195000},"page":"736-745","source":"Crossref","is-referenced-by-count":4,"title":["Sperm storage in the oviduct of the Chinese pond turtle Mauremys reevesii depends on oestrogen-based suppression of the TLR2\/4 immune pathway"],"prefix":"10.1071","volume":"33","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8679-4291","authenticated-orcid":true,"given":"Wenlong","family":"Cai","sequence":"first","affiliation":[{"name":"AAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, Anhui, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Chen","sequence":"additional","affiliation":[{"name":"AAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, Anhui, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yajie","family":"Wang","sequence":"additional","affiliation":[{"name":"AAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, Anhui, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9365-1379","authenticated-orcid":true,"given":"Xingjiang","family":"Bu","sequence":"additional","affiliation":[{"name":"AAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, Anhui, China."},{"name":"BCorresponding author. Email: buxingjiang@163.com"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingquan","family":"Xia","sequence":"additional","affiliation":[{"name":"AAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, Anhui, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liuwang","family":"Nie","sequence":"additional","affiliation":[{"name":"AAnhui Provincial Key Laboratory of the Conservation and Exploitation of Biological Resources, College of Life Sciences, Anhui Normal University, Wuhu 241000, Anhui, China."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"67","published-online":{"date-parts":[[2021,10,4]]},"reference":[{"issue":"4","key":"2025102820242661400_R1","doi-asserted-by":"publisher","first-page":"275","DOI":"10.30906\/1026-2296-2019-24-4-275-290","article-title":"Comparison of the modern reproductive technologies for amphibians and reptiles.","volume":"24","author":"Ananjeva","year":"2017","journal-title":"Russ. J. Herpetol."},{"issue":"4","key":"2025102820242661400_R2","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1093\/MOLEHR\/4.4.309","article-title":"Sperm survival in the female reproductive tract: presence of immunosuppression or absence of recognition?","volume":"4","author":"Barratt","year":"1998","journal-title":"Mol. Hum. Reprod."},{"issue":"4","key":"2025102820242661400_R3","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1111\/J.1095-8312.1993.TB00933.X","article-title":"Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals.","volume":"50","author":"Birkhead","year":"1993","journal-title":"Biol. J. Linn. Soc. Lond."},{"issue":"15","key":"2025102820242661400_R4","doi-asserted-by":"publisher","first-page":"3023","DOI":"10.1002\/ECE3.1575","article-title":"Sperm storage and spermatozoa interaction with epithelial cells in oviduct of Chinese soft-shelled turtle, Pelodiscus sinensis.","volume":"5","author":"Chen","year":"2015","journal-title":"Ecol. Evol."},{"issue":"1","key":"2025102820242661400_R5","first-page":"1","article-title":"Advances in understanding mechanisms of long-term sperm storage-the soft-shelled turtle model.","volume":"35","author":"Chen","year":"2020","journal-title":"Histol. Histopathol."},{"issue":"11","key":"2025102820242661400_R6","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1016\/J.IT.2018.09.006","article-title":"Extracellular DAMPs in plants and mammals: immunity, tissue damage and repair.","volume":"39","author":"De Lorenzo","year":"2018","journal-title":"Trends Immunol."},{"issue":"10","key":"2025102820242661400_R7","doi-asserted-by":"publisher","first-page":"2797","DOI":"10.1093\/HUMREP\/13.10.2797","article-title":"Human sperm function in co-culture with human, macaque or bovine oviduct epithelial cell monolayers.","volume":"13","author":"Ellington","year":"1998","journal-title":"Hum. Reprod."},{"issue":"4","key":"2025102820242661400_R8","doi-asserted-by":"publisher","DOI":"10.1371\/JOURNAL.PONE.0214516","article-title":"TLR2\/4 signaling pathway mediates sperm-induced inflammation in bovine endometrial epithelial cells in vitro.","volume":"14","author":"Ezz","year":"2019","journal-title":"PLoS One"},{"issue":"1","key":"2025102820242661400_R9","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1196\/ANNALS.1443.012","article-title":"Toll-like receptors in autoimmunity.","volume":"1143","author":"Fischer","year":"2008","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"2025102820242661400_R10","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/J.LFS.2017.11.047","article-title":"Lycium barbarum polysaccharides improve CCl4-induced liver fibrosis, inflammatory response and TLRs\/NF-kB signaling pathway expression in wistar rats.","volume":"192","author":"Gan","year":"2018","journal-title":"Life Sci."},{"issue":"3","key":"2025102820242661400_R11","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1002\/JMOR.1051990311","article-title":"Sperm storage within the oviduct of turtles.","volume":"199","author":"Gist","year":"1989","journal-title":"J. Morphol."},{"issue":"15","key":"2025102820242661400_R12","doi-asserted-by":"publisher","first-page":"5365","DOI":"10.3390\/IJMS21155365","article-title":"Bovine follicular fluid and extracellular vesicles derived from follicular fluid alter the bovine oviductal epithelial cells transcriptome.","volume":"21","author":"Hasan","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"2025102820242661400_R13","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1146\/ANNUREV-ANIMAL-021815-111350","article-title":"Sperm storage in the female reproductive tract.","volume":"4","author":"Holt","year":"2016","journal-title":"Annu. Rev. Anim. Biosci."},{"issue":"6","key":"2025102820242661400_R14","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1016\/J.THERIOGENOLOGY.2009.07.002","article-title":"Sperm storage in the vertebrate female reproductive tract: how does it work so well?","volume":"73","author":"Holt","year":"2010","journal-title":"Theriogenology"},{"key":"2025102820242661400_R15","doi-asserted-by":"publisher","first-page":"674","DOI":"10.1016\/0003-3472(89)90046-8","article-title":"The effectiveness of competitive male inseminations in golden hamsters, Mesocricetus auratus, depends on an interaction of mating order, time delay between males, and the time of mating relative to ovulation.","volume":"37","author":"Huck","year":"1989","journal-title":"Anim. Behav."},{"issue":"4","key":"2025102820242661400_R16","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1038\/NI.3123","article-title":"Control of adaptive immunity by the innate immune system.","volume":"16","author":"Iwasaki","year":"2015","journal-title":"Nat. Immunol."},{"key":"2025102820242661400_R17"},{"issue":"14","key":"2025102820242661400_R18","doi-asserted-by":"publisher","first-page":"2905","DOI":"10.1093\/NAR\/29.14.2905","article-title":"Estrogen receptor interaction with estrogen response elements.","volume":"29","author":"Klinge","year":"2001","journal-title":"Nucleic Acids Res."},{"issue":"1","key":"2025102820242661400_R19","doi-asserted-by":"publisher","first-page":"16","DOI":"10.3109\/08830185.2010.529976","article-title":"Pathogen recognition by the innate immune system.","volume":"30","author":"Kumar","year":"2011","journal-title":"Int. Rev. Immunol."},{"key":"2025102820242661400_R20","doi-asserted-by":"publisher","first-page":"33296","DOI":"10.1038\/SREP33296","article-title":"Global analysis of differential gene expression related to long-term sperm storage in oviduct of Chinese Soft-Shelled Turtle Pelodiscus sinensis.","volume":"6","author":"Liu","year":"2016","journal-title":"Sci. Rep."},{"key":"2025102820242661400_R21","doi-asserted-by":"publisher","first-page":"S204","DOI":"10.1016\/J.DOMANIEND.2016.02.005","article-title":"Local immune system in oviduct physiology and pathophysiology: attack or tolerance?","volume":"56","author":"Marey","year":"2016","journal-title":"Domest. Anim. Endocrinol."},{"issue":"6","key":"2025102820242661400_R22","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1016\/J.IMMUNI.2006.04.008","article-title":"Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment.","volume":"24","author":"Nagai","year":"2006","journal-title":"Immunity"},{"issue":"1","key":"2025102820242661400_R23","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1016\/J.RESP.2011.04.003","article-title":"Physiological responses to acute changes in temperature and oxygenation in bird and reptile embryos.","volume":"178","author":"Nechaeva","year":"2011","journal-title":"Respir. Physiol. Neurobiol."},{"issue":"1","key":"2025102820242661400_R24","doi-asserted-by":"publisher","first-page":"R8","DOI":"10.1016\/J.CUB.2011.11.003","article-title":"Sperm storage.","volume":"22","author":"Orr","year":"2012","journal-title":"Curr. Biol."},{"issue":"1737","key":"2025102820242661400_R25","doi-asserted-by":"publisher","first-page":"2299","DOI":"10.1098\/RSPB.2012.0100","article-title":"Arrested embryonic development: a review of strategies to delay hatching in egg-laying reptiles.","volume":"279","author":"Rafferty","year":"2012","journal-title":"Proc. R. Soc. B."},{"key":"2025102820242661400_R26"},{"issue":"2","key":"2025102820242661400_R27","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1002\/JEZ.1154","article-title":"Female sperm storage in reptiles.","volume":"292","author":"Sever","year":"2002","journal-title":"J. Exp. Zool."},{"key":"2025102820242661400_R28"},{"issue":"1","key":"2025102820242661400_R29","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1095\/BIOLREPROD56.1.83","article-title":"Role of direct contact between spermatozoa and oviductal epithelial cells in maintaining rabbit sperm viability.","volume":"56","author":"Smith","year":"1997","journal-title":"Biol. Reprod."},{"issue":"4","key":"2025102820242661400_R30","doi-asserted-by":"publisher","first-page":"730","DOI":"10.1093\/BIOLINNEAN\/BLY153","article-title":"Cold and isolated ectotherms: drivers of reptilian longevity.","volume":"125","author":"Stark","year":"2018","journal-title":"Biol. J. Linn. Soc. Lond."},{"issue":"10","key":"2025102820242661400_R31","doi-asserted-by":"publisher","first-page":"6303","DOI":"10.4049\/JIMMUNOL.175.10.6303","article-title":"Essential role of the MyD88 pathway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoimmunity.","volume":"175","author":"Su","year":"2005","journal-title":"J. Immunol."},{"issue":"5\u20136","key":"2025102820242661400_R32","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1387\/ijdb.072527ss","article-title":"Regulation of sperm storage and movement in the mammalian oviduct.","volume":"52","author":"Suarez","year":"2008","journal-title":"Int. J. Dev. Biol."},{"issue":"5","key":"2025102820242661400_R33","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1007\/S10753-010-9254-8","article-title":"Baicalin inhibits TLR2\/4 signaling pathway in rat brain following permanent cerebral ischemia.","volume":"34","author":"Tu","year":"2011","journal-title":"Inflammation"},{"issue":"9","key":"2025102820242661400_R34","doi-asserted-by":"publisher","first-page":"712","DOI":"10.1007\/S00109-006-0084-Y","article-title":"Toll-like receptors and innate immunity.","volume":"84","author":"Uematsu","year":"2006","journal-title":"J. Mol. Med."},{"issue":"11","key":"2025102820242661400_R35","doi-asserted-by":"publisher","first-page":"2566","DOI":"10.1111\/J.1365-294X.2008.03772.X","article-title":"Multiple paternity in reptiles: patterns and processes.","volume":"17","author":"Uller","year":"2008","journal-title":"Mol. Ecol."},{"issue":"1","key":"2025102820242661400_R36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/S00011-007-6093-7","article-title":"Toll-like receptor signalling and the clinical benefits that lie within.","volume":"56","author":"Verstak","year":"2007","journal-title":"Inflamm. Res."},{"issue":"4","key":"2025102820242661400_R37","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1038\/NRI3819","article-title":"The role of sex hormones in immune protection of the female reproductive tract.","volume":"15","author":"Wira","year":"2015","journal-title":"Nat. Rev. Immunol."},{"issue":"9","key":"2025102820242661400_R38","doi-asserted-by":"publisher","DOI":"10.1371\/JOURNAL.PONE.0162309","article-title":"Sperm binding to oviduct epithelial cells enhances TGFB1 and IL10 expressions in epithelial cells as well as neutrophils in vitro: prostaglandin E2 as a main regulator of anti-inflammatory response in the bovine oviduct.","volume":"11","author":"Yousef","year":"2016","journal-title":"PLoS One"}],"container-title":["Reproduction, Fertility and Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/connectsci.au\/rd\/article-pdf\/33\/12\/736\/319036\/rd20341.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/connectsci.au\/rd\/article-pdf\/33\/12\/736\/319036\/rd20341.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,29]],"date-time":"2025-10-29T00:24:37Z","timestamp":1761697477000},"score":1,"resource":{"primary":{"URL":"https:\/\/connectsci.au\/rd\/article\/33\/12\/736\/50918\/Sperm-storage-in-the-oviduct-of-the-Chinese-pond"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,4]]},"references-count":38,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2021,10,8]]}},"URL":"https:\/\/doi.org\/10.1071\/rd20341","relation":{},"ISSN":["1031-3613","1448-5990"],"issn-type":[{"value":"1031-3613","type":"print"},{"value":"1448-5990","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,4]]}}}