{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T11:48:29Z","timestamp":1790768909974,"version":"4.1.0"},"reference-count":29,"publisher":"Wiley","issue":"12","license":[{"start":{"date-parts":[[2016,10,20]],"date-time":"2016-10-20T00:00:00Z","timestamp":1476921600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Molecular Reproduction Devel"],"published-print":{"date-parts":[[2016,12]]},"abstract":"<jats:title>SUMMARY<\/jats:title><jats:sec><jats:label\/><jats:p>Sialylation creates a negative charge on the cell surface that can interfere with blastocyst implantation. For example, \u03b12,6\u2010sialylation on terminal galactose, catalyzed by the sialyltransferase ST6GAL1, inhibits the binding of galectin\u20101, a <jats:italic>\u03b2<\/jats:italic>\u2010galactoside\u2010binding lectin. We recently reported the potential involvement of galectin\u20101 and \u20103 in the pathogenesis of tubal ectopic pregnancy; however, the precise role of galectins and their ligand glycoconjugates remain unclear. Here, we investigated the expression of the genes encoding \u03b12,3\u2010 and \u03b12,6\u2010galactoside sialyltransferases (<jats:italic>ST3GAL1\u22126<\/jats:italic> and <jats:italic>ST6GAL1\u22122<\/jats:italic>) and the localization of sialic acids in the Fallopian tube of women with or without ectopic implantation. <jats:italic>ST6GAL1<\/jats:italic> expression was higher in the mid\u2010secretory phase than the proliferative phase of non\u2010pregnant women (<jats:italic>P\u2009<\/jats:italic>&lt;\u20090.0001), whereas <jats:italic>ST6GAL1<\/jats:italic> (<jats:italic>P\u2009<\/jats:italic>&lt;\u20090.0001), <jats:italic>ST3GAL3<\/jats:italic> (<jats:italic>P<\/jats:italic>\u2009=\u20090.0029), <jats:italic>ST3GAL5<\/jats:italic> (<jats:italic>P<\/jats:italic>\u2009=\u20090.0089), and <jats:italic>ST3GAL6<\/jats:italic> (<jats:italic>P<\/jats:italic>\u2009=\u20090.0018) were all lower in Fallopian tubes with ectopic implantations. \u03b12,3\u2010 and \u03b12,6\u2010sialic acids, however, both remained enriched on the surface of Fallopian tube epithelium. Cigarette smoking, a major risk factor for tubal ectopic pregnancy, was associated with reduced mid\u2010secretory\u2010phase expression of <jats:italic>ST6GAL1<\/jats:italic> (<jats:italic>P<\/jats:italic>\u2009=\u20090.0298), but elevated expression of <jats:italic>ST3GAL5<\/jats:italic> (<jats:italic>P<\/jats:italic>\u2009=\u20090.0006), an enzyme known to be involved in ciliogenesis. Indeed, sialic acid\u2010containing ciliated inclusion cysts, which are associated with abnormal ciliogenesis, were observed within the epithelium at a higher frequency in women who smoked (<jats:italic>P<\/jats:italic>\u2009=\u20090.0177), suggesting that abnormal ciliogenesis is associated with smoking. Thus, cigarette smoking alters sialylation in the Fallopian tube epithelium, and is potentially a source of decreased tubal transport and increased receptivity for blastocyst in the human Fallopian tube. <jats:italic>Mol. Reprod. Dev. 83: 1083\u20131091, 2016. \u00a9 2016 Wiley Periodicals, Inc<\/jats:italic>.<\/jats:p><\/jats:sec>","DOI":"10.1002\/mrd.22747","type":"journal-article","created":{"date-parts":[[2016,10,12]],"date-time":"2016-10-12T18:25:18Z","timestamp":1476296718000},"page":"1083-1091","source":"Crossref","is-referenced-by-count":11,"title":["Cigarette smoking alters sialylation in the Fallopian tube of women, with implications for the pathogenesis of ectopic pregnancy"],"prefix":"10.1002","volume":"83","author":[{"given":"Junko","family":"Nio\u2010Kobayashi","sequence":"first","affiliation":[{"name":"Laboratory of Histology and Cytology Hokkaido University Graduate School of Medicine Sapporo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hazirah B.Z.","family":"Abidin","sequence":"additional","affiliation":[{"name":"MRC Centre for Reproductive Health The Queen's Medical Research Institute, The University of Edinburgh Edinburgh United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeremy K.","family":"Brown","sequence":"additional","affiliation":[{"name":"MRC Centre for Reproductive Health The Queen's Medical Research Institute, The University of Edinburgh Edinburgh United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Toshihiko","family":"Iwanaga","sequence":"additional","affiliation":[{"name":"Laboratory of Histology and Cytology Hokkaido University Graduate School of Medicine Sapporo Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew W.","family":"Horne","sequence":"additional","affiliation":[{"name":"MRC Centre for Reproductive Health The Queen's Medical Research Institute, The University of Edinburgh Edinburgh United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"W. Colin","family":"Duncan","sequence":"additional","affiliation":[{"name":"MRC Centre for Reproductive Health The Queen's Medical Research Institute, The University of Edinburgh Edinburgh United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2016,10,20]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1093\/humrep\/dep233"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001710308"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod34.4.701"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.1042\/bst0290153"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01740770"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod32.5.1135"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0023595"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(05)67103-6"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.1007\/s007950000009"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0300-9084(01)01301-3"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod21.3.691"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0089400"},{"key":"e_1_2_7_14_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.273.48.31652"},{"key":"e_1_2_7_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4827(77)90185-9"},{"key":"e_1_2_7_16_1","doi-asserted-by":"publisher","DOI":"10.1369\/jhc.2009.952085"},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2010.04.011"},{"key":"e_1_2_7_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(17)42271-X"},{"key":"e_1_2_7_19_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1432-1033.2003.03458.x"},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M115.651489"},{"key":"e_1_2_7_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/0010-7824(75)90006-2"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1159\/000439166"},{"key":"e_1_2_7_23_1","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1093\/biolreprod\/6.2.204","article-title":"Changes in uterine sialic acid and glycogen during early pregnancy in the rat","volume":"6","author":"Rajalakshmi M","year":"1972","journal-title":"Biol Reprod"},{"key":"e_1_2_7_24_1","doi-asserted-by":"publisher","DOI":"10.1530\/jrf.0.0350203"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.fertnstert.2007.04.036"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1093\/humupd\/dmp057"},{"key":"e_1_2_7_27_1","first-page":"1406","article-title":"Tubal ectopic pregnancy","volume":"10","author":"Varma R","year":"2012","journal-title":"BMJ Clin Evid"},{"key":"e_1_2_7_28_1","doi-asserted-by":"publisher","DOI":"10.1097\/GRF.0b013e31802f4f79"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0903279106"},{"key":"e_1_2_7_30_1","doi-asserted-by":"publisher","DOI":"10.1002\/path.4375"}],"container-title":["Molecular Reproduction and Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fmrd.22747","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fmrd.22747","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/mrd.22747","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,4]],"date-time":"2023-10-04T00:21:52Z","timestamp":1696378912000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/mrd.22747"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,20]]},"references-count":29,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2016,12]]}},"alternative-id":["10.1002\/mrd.22747"],"URL":"https:\/\/doi.org\/10.1002\/mrd.22747","archive":["Portico"],"relation":{},"ISSN":["1040-452X","1098-2795"],"issn-type":[{"value":"1040-452X","type":"print"},{"value":"1098-2795","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,20]]}}}