{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T23:45:31Z","timestamp":1791848731267,"version":"4.3.4"},"reference-count":53,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2022,5,31]],"date-time":"2022-05-31T00:00:00Z","timestamp":1653955200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science Centre","award":["2017\/25\/N\/NZ4\/01965"],"award-info":[{"award-number":["2017\/25\/N\/NZ4\/01965"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Oxygen balance is crucial for angiogenesis, immunity, and tissue repair. The human oviduct is essential for reproductive function, and any imbalance in homeostasis leads to fertility disturbances and might be a reason for ectopic pregnancy development. Uterine myoma is a widespread benign tumour, which is often accompanied by infertility. Telocytes have been discussed in the contexts of motility, fibrosis development, and angiogenesis. We observed the oviducts from patients with and without uterine myoma, comparing the expression of HIF-1, HO, VEGF and its receptor, NOS, oestrogen, and progesterone receptors by immunolabeling. The myometrial and oviductal telocytes were also compared in both groups. Biochemical analyses were conducted for FSH, LH, AMH, sFlt, oestrogen, and progesterone in blood samples. Patients with uterine myoma have different expressions of sex steroid receptors and an increased number of telocytes. The decreasing VEFG expression was compensated by the rise in the HIF-1 and NOS expression. Blood biochemical analyses revealed a higher progesterone level and lower AMH in patients with uterine myoma. No differences in sFlt, FSH, and LF were observed. Uterine myoma impacts oviduct oxygen homeostasis and might cause fertility disturbances (uterine and oviductal infertility factors).<\/jats:p>","DOI":"10.3390\/ijms23116155","type":"journal-article","created":{"date-parts":[[2022,5,31]],"date-time":"2022-05-31T05:25:42Z","timestamp":1653974742000},"page":"6155","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Oviductal Oxygen Homeostasis in Patients with Uterine Myoma: Correlation between Hypoxia and Telocytes"],"prefix":"10.3390","volume":"23","author":[{"given":"Anna","family":"Wrona","sequence":"first","affiliation":[{"name":"Gynecology and Obstetrics Ward with Gynecologic Oncology Subdivision, J. \u015aniadecki\u2019s Specialistic Hospital, 33-300 Nowy S\u0105cz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9850-6269","authenticated-orcid":false,"given":"Veronika","family":"Aleksandrovych","sequence":"additional","affiliation":[{"name":"Department of Pathophysiology, Jagiellonian University Medical College, 31-121 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomasz","family":"Bereza","sequence":"additional","affiliation":[{"name":"Department of Anatomy, Jagiellonian University Medical College, 31-034 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pawe\u0142","family":"Basta","sequence":"additional","affiliation":[{"name":"Department of Gynecology and Oncology, Jagiellonian University Medical College, 30-688 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Gil","sequence":"additional","affiliation":[{"name":"Department of Anatomy, Jagiellonian University Medical College, 31-034 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magdalena","family":"Ulatowska-Bia\u0142as","sequence":"additional","affiliation":[{"name":"Department of Pathomorphology, Jagiellonian University Medical College, 31-531 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ma\u0142gorzata","family":"Mazur-Laskowska","sequence":"additional","affiliation":[{"name":"Diagnostic Department of University Hospital, Jakubowskiego 2 St., 30-688 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kazimierz","family":"Pity\u0144ski","sequence":"additional","affiliation":[{"name":"Department of Gynecology and Oncology, Jagiellonian University Medical College, 30-688 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4732-7698","authenticated-orcid":false,"given":"Krzysztof","family":"Gil","sequence":"additional","affiliation":[{"name":"Department of Pathophysiology, Jagiellonian University Medical College, 31-121 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1590","DOI":"10.4187\/respcare.03357","article-title":"Tissue hypoxia: Implications for the respiratory clinician","volume":"59","author":"Maclntyre","year":"2014","journal-title":"Respir. Care"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1058","DOI":"10.1002\/ijc.29519","article-title":"HIF-1 at the crossroads of hypoxia, inflammation, and cancer","volume":"138","author":"Balamurugan","year":"2016","journal-title":"Int. J. Cancer"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.freeradbiomed.2018.03.042","article-title":"Hypoxia, oxidative stress and inflammation","volume":"125","author":"McGarry","year":"2018","journal-title":"Free Radic. Biol. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1177\/1933719118776793","article-title":"Hypoxia Induces Hypoxia-Inducible Factor 1\u03b1 and Potential HIF-Responsive Gene Expression in Uterine Leiomyoma","volume":"26","author":"Ishikawa","year":"2019","journal-title":"Reprod. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s00441-016-2461-3","article-title":"Hypoxia in tissue repair and fibrosis","volume":"365","author":"Darby","year":"2016","journal-title":"Cell Tissue Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1146\/annurev-pathol-012615-044231","article-title":"Hypoxia and Mucosal Inflammation","volume":"11","author":"Colgan","year":"2016","journal-title":"Annu. Rev. Pathol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1038\/nri.2017.103","article-title":"Regulation of immunity and inflammation by hypoxia in immunological niches","volume":"17","author":"Taylor","year":"2017","journal-title":"Nat. Rev. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1152\/physiol.00031.2008","article-title":"Inflammation and stem cells in gastrointestinal carcinogenesis","volume":"23","author":"Quante","year":"2008","journal-title":"Physiology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3806","DOI":"10.1038\/s41388-018-0189-0","article-title":"Hypoxia-induced exosomes contribute to a more aggressive and chemoresistant ovarian cancer phenotype: A novel mechanism linking STAT3\/Rab proteins","volume":"37","author":"Dorayappan","year":"2018","journal-title":"Oncogene"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Kawanishi, S., Ohnishi, S., Ma, N., Hiraku, Y., and Murata, M. (2017). Crosstalk between DNA Damage and Inflammation in the Multiple Steps of Carcinogenesis. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18081808"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1124\/mol.106.027029","article-title":"Hypoxia-inducible factor-1 (HIF-1)","volume":"70","author":"Ke","year":"2006","journal-title":"Mol. Pharmacol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3661","DOI":"10.1172\/JCI84426","article-title":"Hypoxia-inducible factors: Key regulators of myeloid cells during inflammation","volume":"126","author":"Lin","year":"2016","journal-title":"J. Clin. Investig."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1515\/hsz-2012-0320","article-title":"Role of hypoxia inducible factor-1\u03b1 for interferon synthesis in mouse dendritic cells","volume":"394","author":"Wobben","year":"2013","journal-title":"Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1038\/nature20165","article-title":"S-2-hydroxyglutarate regulates CD8+ T-lymphocyte fate","volume":"540","author":"Tyrakis","year":"2016","journal-title":"Nature"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1038\/nature19334","article-title":"Germinal centre hypoxia and regulation of antibody qualities by a hypoxia response system","volume":"537","author":"Cho","year":"2016","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"944","DOI":"10.2741\/4526","article-title":"Alpha-Enolase (ENO1), a potential target in novel immunotherapies","volume":"22","author":"Cappello","year":"2017","journal-title":"Front. Biosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.canlet.2015.07.028","article-title":"Classical and non-classical proangiogenic factors as a target of antiangiogenic therapy in tumor microenvironment","volume":"380","author":"Marech","year":"2016","journal-title":"Cancer Lett."},{"key":"ref_18","first-page":"55","article-title":"mRNA expression of VEGF and its receptors in fallopian tubes of women with ectopic pregnancies","volume":"9","author":"Zarezade","year":"2015","journal-title":"Int. J. Fertil. Steril."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.theriogenology.2017.01.028","article-title":"Expression of the vascular endothelial growth factor system (VEGF) in the porcine oviduct during the estrous cycle","volume":"93","author":"Olsson","year":"2017","journal-title":"Theriogenology"},{"key":"ref_20","unstructured":"Aleksandrovych, V., Bereza, T., Ulatowska-Bia\u0142as, M., Pasternak, A., Walocha, J.A., Pity\u0144ski, K., and Gil, K. (2022). Identification of PDGFR\u03b1 + cells in uterine fibroids\u2013link between angiogenesis and uterine telocytes. Arch. Med. Sci., 18."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Birbrair, A. (2021). Telocytes in the Tumor Microenvironment. Tumor Microenvironment. Advances in Experimental Medicine and Biology, Springer.","DOI":"10.1007\/978-3-030-73119-9"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1111\/jcmm.12427","article-title":"Telocytes damage in endometriosis-affected rat oviduct and potential impact on fertility","volume":"19","author":"Yang","year":"2015","journal-title":"J. Cell Mol. Med."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Aleksandrovych, V., Wrona, A., Bereza, T., Pity\u0144ski, K., and Gil, K. (2021). Oviductal Telocytes in Patients with Uterine Myoma. Biomedicines, 9.","DOI":"10.3390\/biomedicines9081060"},{"key":"ref_24","first-page":"81","article-title":"Sex steroid hormone receptors of telocytes-potential key role in leiomyoma development","volume":"60","author":"Aleksandrovych","year":"2020","journal-title":"Folia Med. Cracov."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/978-981-10-1061-3_18","article-title":"Telocytes in Inflammatory Gynaecologic Diseases and Infertility","volume":"913","author":"Yang","year":"2016","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1093\/humrep\/deg213","article-title":"Vascular system of intramural leiomyomata revealed by corrosion casting and scanning electron microscopy","volume":"18","author":"Walocha","year":"2003","journal-title":"Hum. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1007\/978-981-10-1061-3_17","article-title":"Roles of Telocytes in the Development of Angiogenesis","volume":"913","author":"Zheng","year":"2016","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_28","first-page":"5","article-title":"Telocytes: Facts, speculations and myths (Review article)","volume":"57","author":"Aleksandrovych","year":"2017","journal-title":"Folia Med. Cracov."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/978-981-10-1061-3_22","article-title":"Immunohistochemistry of Telocytes in the Uterus and Fallopian Tubes","volume":"913","author":"Cretoiu","year":"2016","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_30","first-page":"37","article-title":"Angiogenesis and pro-angiogenic factors in uterine fibroids-facts and myths","volume":"56","author":"Konarska","year":"2016","journal-title":"Folia Med. Cracov."},{"key":"ref_31","unstructured":"Duffy, A.M., Bouchier-Hayes, D.J., and Harmey, J.H. (2021, December 20). Vascular Endothelial Growth Factor (VEGF) and Its Role in Non-Endothelial Cells: Autocrine Signalling by VEGF, Madame Curie Bioscience Database [Internet], Available online: https:\/\/www.ncbi.nlm.nih.gov\/books\/NBK6482\/."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1289\/ehp.00108s5785","article-title":"Regulation of Vascular Endothelial Growth Factor Expression by Estrogens and Progestins","volume":"108","author":"Hyder","year":"2000","journal-title":"Environ. Health Perspect."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3802","DOI":"10.7150\/jca.29233","article-title":"Oestrogen Inhibits VEGF Expression and Angiogenesis In Triple-Negative Breast Cancer By Activating GPER-1","volume":"9","author":"Wang","year":"2018","journal-title":"J. Cancer"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1095\/biolreprod.116.144733","article-title":"Vascular endothelial growth factors C and D may promote angiogenesis in the primate ovulatory follicle","volume":"96","author":"Kim","year":"2017","journal-title":"Biol. Reprod."},{"key":"ref_35","first-page":"1537","article-title":"New markers for regulation of transcription and macromolecule metabolic process in porcine oocytes during in vitro maturation","volume":"21","author":"Kranc","year":"2020","journal-title":"Mol. Med. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1530\/REP-11-0091","article-title":"Ovarian VEGF(165)b expression regulates follicular development, corpus luteum function and fertility","volume":"143","author":"Qiu","year":"2012","journal-title":"Reproduction"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1093\/abbs\/gmy066","article-title":"Telocytes promote VEGF expression and alleviate ventilator-induced lung injury in mice","volume":"50","author":"Ma","year":"2018","journal-title":"Acta Biochim. Biophys. Sin."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"9697","DOI":"10.1111\/jcmm.16919","article-title":"Telocytes in the human ascending aorta: Characterization and exosome-related KLF-4\/VEGF-A expression","volume":"25","author":"Aschacher","year":"2021","journal-title":"J. Cell Mol. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1016\/j.fertnstert.2005.10.023","article-title":"Hypoxia regulates vascular endothelial growth factor and soluble fms-like tyrosine kinase-1 secretion by human oviductal epithelial cells and stromal fibroblasts","volume":"85","author":"Itoh","year":"2006","journal-title":"Fertil. Steril."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1007\/s00011-018-1151-x","article-title":"A review on heme oxygenase-1 induction: Is it a necessary evil","volume":"67","author":"Waza","year":"2018","journal-title":"Inflamm. Res."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Yachie, A. (2021). Heme Oxygenase-1 Deficiency and Oxidative Stress: A Review of 9 Independent Human Cases and Animal Models. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22041514"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1111\/aji.12366","article-title":"The Stress-responsive Heme Oxygenase (HO)-1 Isoenzyme is Increased in Labouring Myometrium where it Regulates Contraction-associated Proteins","volume":"74","author":"Liong","year":"2015","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"4589214","DOI":"10.1155\/2017\/4589214","article-title":"Modulation of Progesterone Receptor Isoform Expression in Pregnant Human Myometrium","volume":"2017","author":"Ilicic","year":"2017","journal-title":"Biomed. Res. Int."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"994","DOI":"10.1111\/jcmm.12843","article-title":"Telocytes in female reproductive system (human and animal)","volume":"20","author":"Aleksandrovych","year":"2016","journal-title":"J. Cell Mol. Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1097\/01.EHX.0000425654.68291.c8","article-title":"Immunohistochemical characterization of telocytes in rat uterus in different reproductive stages","volume":"36","author":"Salama","year":"2013","journal-title":"Egypt. J. Histol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1177\/0963689719833303","article-title":"The Autonomic Innervation and Uterine Telocyte Interplay in Leiomyoma Formation","volume":"28","author":"Aleksandrovych","year":"2019","journal-title":"Cell Transplant."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/s00404-012-2220-y","article-title":"c-kit\/CD 117 positive cells in the myometrium of pregnant women and those with uterine endometriosis","volume":"286","author":"Horn","year":"2012","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"978","DOI":"10.3389\/fimmu.2018.00978","article-title":"Targeting VEGF\/VEGFR to Modulate Antitumor Immunity","volume":"9","author":"Yang","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1016\/j.cmet.2020.08.002","article-title":"The Role of HIF in Immunity and Inflammation","volume":"32","author":"McGettrick","year":"2020","journal-title":"Cell Metab."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Dom\u00e8nech, M., Hern\u00e1ndez, A., Plaja, A., Mart\u00ednez-Balibrea, E., and Bala\u00f1\u00e0, C. (2021). Hypoxia: The Cornerstone of Glioblastoma. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222212608"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1007\/s10735-011-9338-2","article-title":"Immunohistochemical assessment of intrinsic and extrinsic markers of hypoxiain reproductive tissue: Differential expression of HIF1\u03b1 and HIF2\u03b1 in rat oviduct and endometrium","volume":"42","author":"Gillies","year":"2011","journal-title":"J. Mol. Histol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1292\/jvms.64.803","article-title":"Effect of vascular endothelial growth factor on maturation, fertilization and developmental competence of bovine oocytes","volume":"64","author":"Luo","year":"2002","journal-title":"J. Vet. Med. Sci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1080\/10495398.2019.1588128","article-title":"Adaptive response of reproduction to high-altitude hypoxic stress by altering mRNA expression of hypoxia-inducible factors in female yaks (Bos grunniens)","volume":"31","author":"He","year":"2020","journal-title":"Anim. Biotechnol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/11\/6155\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:22:26Z","timestamp":1760138546000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/11\/6155"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,31]]},"references-count":53,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2022,6]]}},"alternative-id":["ijms23116155"],"URL":"https:\/\/doi.org\/10.3390\/ijms23116155","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,31]]}}}