{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T16:15:17Z","timestamp":1785428117629,"version":"3.56.0"},"reference-count":44,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2026,5,16]],"date-time":"2026-05-16T00:00:00Z","timestamp":1778889600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100014434","name":"Polish National Agency for Academic Exchange","doi-asserted-by":"publisher","award":["PPI\/APM\/2019\/1\/00044\/U\/00001"],"award-info":[{"award-number":["PPI\/APM\/2019\/1\/00044\/U\/00001"]}],"id":[{"id":"10.13039\/501100014434","id-type":"DOI","asserted-by":"publisher"}]},{"award":["PPI\/APM\/2019\/1\/00044\/U\/00001"],"award-info":[{"award-number":["PPI\/APM\/2019\/1\/00044\/U\/00001"]}],"id":[{"id":"https:\/\/ror.org\/02jf81j23","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Veterinary Sciences"],"abstract":"<jats:p>Heat shock proteins (HSPs) fulfil protective tasks in the whole organism; in pregnant dogs, they are expressed in the ovary, placenta and preimplantation embryo. Our objective was to compare the expression of HSP60 and -70, along with indicators of proliferation and apoptosis, in the non-pregnant and pregnant uterus\/placenta and ovaries. Tissues were obtained after ovariohysterectomy and examined by means of immunohistochemistry. There were differences between pregnant and non-pregnant tissues: the expression level of HSP70 during preimplantation in superficial cells was significantly lower than that in early diestrus, with similar results observed for Ki67. The immunosignal for HSP70 was significantly decreased during the postimplantation stage in almost all cell types, whilst the number of HSP60-positive cells did not change. In pregnant animals, the number of Ki67-positive cells significantly increased until the postimplantation stage. In the placenta and trophoblast, the expression of HSP60 and -70 was strong, while no HSP70 signal was detected in endometrial epithelial cells. The caspase 3 immunosignal in the uterus and placenta was generally weak. In the corpora lutea, HSP60, HSP70 and caspase 3 were mainly detected in theca lutein cells, while no signal for KI67 was seen. In follicles, caspase 3 and KI67 expression was low, except in granulosa cells of tertiary follicles and oocytes. We conclude that the different expression of HSPs in pregnant and non-pregnant animals may point towards different regulatory and\/or protective tasks.<\/jats:p>","DOI":"10.3390\/vetsci13050482","type":"journal-article","created":{"date-parts":[[2026,5,19]],"date-time":"2026-05-19T07:35:43Z","timestamp":1779176143000},"page":"482","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Heat Shock Proteins 60 and 70, Ki67 and Caspase 3 Are Differentially Expressed in the Canine Pregnant and Non-Pregnant Uterus and Ovaries"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5676-7644","authenticated-orcid":false,"given":"Sch\u00e4fer-Somi","family":"Sabine","sequence":"first","affiliation":[{"name":"Department of Small Animals and Horses, Clinical Center for Reproduction, University of Veterinary Medicine Vienna, 1210 Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Binli","family":"Firdevs","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ondokuz May\u0131s University, 55139 Samsun, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9052-5924","authenticated-orcid":false,"given":"Kaya","family":"Duygu","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Dokuz Eyl\u00fcl University, Kiraz, 35210 \u0130zmir, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1791-9588","authenticated-orcid":false,"given":"Karadag","family":"Muhammed Ali","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Kafkas University, 36100 Kars, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ay","family":"Serhan","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ondokuz May\u0131s University, 55139 Samsun, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1408-2548","authenticated-orcid":false,"given":"Findik","family":"Murat","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ondokuz May\u0131s University, 55139 Samsun, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6411-5489","authenticated-orcid":false,"given":"Aslan","family":"Selim","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Near East University, 99138 Nicosia, Cyprus"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,5,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/3-540-29717-0_1","article-title":"Chaperones in preventing protein denaturation in living cells and protecting against cellular stress","volume":"Volume 172","author":"Kampinga","year":"2006","journal-title":"Molecular Chaperones in Health and Disease; Handbook of Experimental Pharmacology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/3-540-29717-0_8","article-title":"Heat shock proteins: Endogenous modulators of apoptotic cell death","volume":"Volume 172","author":"Didelot","year":"2006","journal-title":"Molecular Chaperones in Health and Disease; Handbook of Experimental Pharmacology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1006\/scdb.1999.0347","article-title":"Roles of molecular chaperones in cytoplasmic protein folding","volume":"11","author":"Agashe","year":"2000","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1038\/355033a0","article-title":"Protein folding in the cell","volume":"355","author":"Gething","year":"1992","journal-title":"Nature"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1002\/jcb.240510206","article-title":"Mechanisms of transcriptional activation by steroid hormone receptors","volume":"51","author":"Baniahmad","year":"1993","journal-title":"J. Cell. Biochem."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Campanella, C., Bavisotto, C.C., Gammazza, A.M., Nikolic, D., Rappa, F., David, S., Cappello, F., Bucchieri, F., and Fais, S. (2014). Exosomal Heat Shock Proteins as New Players in Tumour Cell-to-Cell Communication. J. Circ. Biomark., 3.","DOI":"10.33393\/jcb.2014.2046"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/S0006-291X(03)00623-5","article-title":"Heat shock proteins, cellular chaperones that modulate mitochondrial cell death pathways","volume":"304","author":"Parcellier","year":"2003","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1016\/S0741-5214(99)70329-0","article-title":"Heat shock proteins: A review of the molecular chaperones","volume":"29","author":"Whitley","year":"1999","journal-title":"J. Vasc. Surg."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.theriogenology.2020.01.082","article-title":"Canine conceptus-maternal communication during maintenance and termination of pregnancy, including the role of species-specific decidualization","volume":"150","author":"Kowalewski","year":"2020","journal-title":"Theriogenology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1007\/978-3-319-15856-3_11","article-title":"The Dog: Nonconformist, Not Only in Maternal Recognition Signaling","volume":"216","author":"Kowalewski","year":"2015","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1111\/j.1439-0531.2007.00966.x","article-title":"Expression of genes in the canine pre-implantation uterus and embryo: Implications for an active role of the embryo before and during invasion","volume":"43","author":"Beceriklisoy","year":"2008","journal-title":"Reprod. Domest. Anim."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1111\/rda.12063","article-title":"Is apoptosis a regulatory mechanism during early canine pregnancy?","volume":"47","author":"Sabitzer","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1016\/j.theriogenology.2020.02.019","article-title":"Embryo-maternal communication in dogs: Immune system related factors","volume":"150","author":"Gabriel","year":"2020","journal-title":"Theriogenology"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"117644","DOI":"10.1016\/j.theriogenology.2025.117644","article-title":"Modulation of uterine responses in dogs: The divergent effects of semen and embryonal signals on steroidogenic receptors and selected immune system-related factors","volume":"250","author":"Mushati","year":"2026","journal-title":"Theriogenology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1530\/REP-13-0648","article-title":"Expression of genes involved in the embryo-maternal interaction in the early-pregnant canine uterus","volume":"147","author":"Kautz","year":"2014","journal-title":"Reproduction"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/978-3-319-51409-3_6","article-title":"The Role of Hsp70 in the Regulation of Autophagy in Gametogenesis, Pregnancy, and Parturition","volume":"222","author":"Witkin","year":"2017","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1556\/004.2019.044","article-title":"First detection of heat shock protein 60 and 70 in the serum of early pregnant bitches","volume":"67","author":"Aksoy","year":"2019","journal-title":"Acta Vet. Hung."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.theriogenology.2011.01.019","article-title":"The intravaginal application of misoprostol improves induction of abortion with aglepristone","volume":"76","author":"Agaoglu","year":"2011","journal-title":"Theriogenology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.anireprosci.2010.08.028","article-title":"Reproductive cycles of the domestic bitch","volume":"124","author":"Concannon","year":"2011","journal-title":"Anim. Reprod. Sci."},{"key":"ref_20","first-page":"107","article-title":"Ultrasonographic appearance of the ovary and uterus of the bitch during oestrus, ovulation and early pregnancy","volume":"47","author":"England","year":"1993","journal-title":"J. Reprod. Fertil. Suppl."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"8065830","DOI":"10.1155\/2016\/8065830","article-title":"Expression of Progesterone Receptor Membrane Component 1 (PGRMC1), Progestin and AdipoQ Receptor 7 (PAQPR7), and Plasminogen Activator Inhibitor 1 RNA-Binding Protein (PAIRBP1) in Glioma Spheroids In Vitro","volume":"2016","author":"Hlavaty","year":"2016","journal-title":"Biomed Res. Int."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1023\/A:1003259907014","article-title":"Differential localization of heat shock proteins 90, 70, 60 and 27 in human decidua and placenta during pregnancy","volume":"30","author":"Shah","year":"1998","journal-title":"Histochem. J."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0021-9975(08)80313-1","article-title":"Proliferative activity assessed by anti-PCNA and Ki67 monoclonal antibodies in canine testicular tumours","volume":"110","author":"Sarli","year":"1994","journal-title":"J. Comp. Pathol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e20","DOI":"10.1097\/PAI.0000000000000853","article-title":"A Scoring Method for Immunohistochemical Staining on Ki67","volume":"29","author":"Guo","year":"2021","journal-title":"Appl. Immunohistochem. Mol. Morphol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"101667","DOI":"10.1016\/j.tice.2021.101667","article-title":"Hesperetin may alleviate the development of doxorubicin-induced pulmonary toxicity by decreasing oxidative stress and apoptosis in male rats","volume":"73","author":"Guzel","year":"2021","journal-title":"Tissue Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1267\/ahc.20-00032","article-title":"Comparative Analysis of Immunohistochemical Staining Intensity Determined by Light Microscopy, ImageJ and QuPath in Placental Hofbauer Cells","volume":"54","author":"Cizkova","year":"2021","journal-title":"Acta Histochem. Cytochem."},{"key":"ref_27","unstructured":"Sch\u00e4fer-Somi, S., Gabriel, C., and Aslan, S. (2021, January 10\u201312). Heat shock protein 60 and 70 are expressed in the early canine placenta and fetal syncytiotrophoblast. Proceedings of the 54th Annual Conference Physiology and Pathology of Reproduction and Simultaneously 46th Joint Congress of Veterinary and Human Medicine, Zurich, Switzerland."},{"key":"ref_28","unstructured":"Sch\u00e4fer-Somi, S., Ay, S.S., Kaya, D., Karada\u011f, M.A., and Aslan, S. (2024, January 25\u201329). Protein expression of HSP60,70, Ki67 and caspase3 in the pregnant and non-pregnant canine uterus. Proceedings of the 25TH International EVSSAR Congress-European Veterinary Society for Small Animal Reproduction, Barcelona, Spain."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"skac129","DOI":"10.1093\/jas\/skac129","article-title":"Porcine endometrial heat shock proteins are differentially influenced by pregnancy status, heat stress, and altrenogest supplementation during the peri-implantation period","volume":"100","author":"Adur","year":"2022","journal-title":"J. Anim. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1264","DOI":"10.1095\/biolreprod64.4.1264","article-title":"X-linked inhibitor of apoptosis protein expression and the regulation of apoptosis during human placental development","volume":"64","author":"Gruslin","year":"2001","journal-title":"Biol. Reprod."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1210\/er.2005-0003","article-title":"The role of apoptosis in the regulation of trophoblast survival and differentiation during pregnancy","volume":"26","author":"Abrahams","year":"2005","journal-title":"Endocr. Rev."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1538","DOI":"10.1136\/bmj.322.7301.1538","article-title":"How apoptosis is regulated, and what goes wrong in cancer","volume":"322","author":"Bergh","year":"2001","journal-title":"BMJ"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1536","DOI":"10.1136\/bmj.322.7301.1536","article-title":"What is apoptosis, and why is it important?","volume":"322","author":"Renehan","year":"2001","journal-title":"BMJ"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"71","DOI":"10.2478\/v10042-008-0088-2","article-title":"Distributions of PCNA and Cas-3 in rat uterus during early pregnancy","volume":"48","author":"Oner","year":"2010","journal-title":"Folia Histochem. Cytobiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2157","DOI":"10.1096\/fj.201600910RR","article-title":"Role of HSP60 (HSPD1) in diabetes-induced renal tubular dysfunction: Regulation of intracellular protein aggregation, ATP production, and oxidative stress","volume":"31","author":"Aluksanasuwan","year":"2017","journal-title":"FASEB J."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1111\/vco.12113","article-title":"Immunohistochemical expression of heat shock proteins, p63 and androgen receptor in benign prostatic hyperplasia and prostatic carcinoma in the dog","volume":"14","author":"Romanucci","year":"2016","journal-title":"Vet. Comp. Oncol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1007\/s12192-013-0414-2","article-title":"Heat shock protein expression analysis in canine osteosarcoma reveals HSP60 as a potentially relevant therapeutic target","volume":"18","author":"Selvarajah","year":"2013","journal-title":"Cell Stress Chaperones"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1095\/biolreprod.113.108068","article-title":"Lipopolysaccharide drives alternation of heat shock proteins and induces failure of blastocyst implantation in mouse","volume":"88","author":"Jaiswal","year":"2013","journal-title":"Biol. Reprod."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1002\/j.1460-2075.1983.tb01401.x","article-title":"Spontaneous high expression of heat-shock proteins in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo","volume":"2","author":"Bensaude","year":"1983","journal-title":"EMBO J."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1262\/jrd.2019-157","article-title":"Canine decidualization in vitro: Extracellular matrix modification, progesterone mediated effects and selective blocking of prostaglandin E2 receptors","volume":"66","author":"Graubner","year":"2020","journal-title":"J. Reprod. Dev."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1093\/molehr\/gam054","article-title":"Abortion is associated with increased expression of FasL in decidual leukocytes and apoptosis of extravillous trophoblasts: A role for CRH and urocortin","volume":"13","author":"Minas","year":"2007","journal-title":"Mol. Hum. Reprod."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"102532","DOI":"10.1016\/j.jtherbio.2020.102532","article-title":"Effects of heat stress on ovarian development and the expression of HSP genes in mice","volume":"89","author":"Bei","year":"2020","journal-title":"J. Therm. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"152157","DOI":"10.1016\/j.acthis.2024.152157","article-title":"Immunohistochemical localization and expression of heat shock proteins (HSP27, HSP60, HSP70, and HSP90) during the oestrous cycle, pregnancy, and lactation in rat ovaries","volume":"126","author":"Kandil","year":"2024","journal-title":"Acta Histochem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1095\/biolreprod61.4.993","article-title":"Tumor necrosis factor-alpha stimulates proliferation of rat ovarian theca-interstitial cells","volume":"61","author":"Spaczynski","year":"1999","journal-title":"Biol. Reprod."}],"container-title":["Veterinary Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2306-7381\/13\/5\/482\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,21]],"date-time":"2026-05-21T12:59:23Z","timestamp":1779368363000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2306-7381\/13\/5\/482"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,16]]},"references-count":44,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2026,5]]}},"alternative-id":["vetsci13050482"],"URL":"https:\/\/doi.org\/10.3390\/vetsci13050482","relation":{},"ISSN":["2306-7381"],"issn-type":[{"value":"2306-7381","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,16]]}}}