{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,9]],"date-time":"2026-02-09T20:50:47Z","timestamp":1770670247737,"version":"3.49.0"},"reference-count":54,"publisher":"American Veterinary Medical Association (AVMA)","issue":"7","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["ajvr"],"published-print":{"date-parts":[[2020,7]]},"abstract":"Abstract<\/jats:title>\n\nOBJECTIVE<\/jats:title>\nTo determine whether luteinizing hormone receptors (LHRs) are expressed in canine femoral head subchondral bone (FHSB), hip joint round ligament (RL), cranial cruciate ligament (CCL), and femorotibial joint synovium (FJS) specimens.<\/jats:p>\n<\/jats:sec>\n\nSAMPLE<\/jats:title>\n1 specimen each of the FHSB, RL, CCL, and FJS obtained from the left hind limbs of 19 fresh canine cadavers.<\/jats:p>\n<\/jats:sec>\n\nPROCEDURES<\/jats:title>\n1 section of each FHSB, RL, CCL, and FJS specimen was processed with rabbit polyclonal IgG anti-human LHR antibody, and 1 section was treated with negative control reagents. Percentage immunoexpression of LHRs in FHSB and FJS sections was analyzed by assessment of 100 bone marrow cells or synoviocytes in 3 adjacent hpf (400\u00d7). In each RL and CCL section, immunoexpression of LHRs in fibrocytes was semiquantitatively analyzed on the basis of the mean of the product of percentage staining score (from 0 [no staining] to 3 [> 50% of cells stained]) and staining intensity score (from 0 [no staining] to 2 [moderate to strong staining]) for 3 adjacent hpf.<\/jats:p>\n<\/jats:sec>\n\nRESULTS<\/jats:title>\nAll tissues examined had variable LHR expression. Expression of LHRs in FHSB, CCL, or FJS specimens did not differ between sexes or between sexually intact and gonadectomized dogs. However, RL specimens from female dogs had significantly greater LHR expression scores, compared with findings for male dogs.<\/jats:p>\n<\/jats:sec>\n\nCONCLUSIONS AND CLINICAL RELEVANCE<\/jats:title>\nResults indicated that LHRs are expressed in structural support tissues of canine hip and femorotibial joints. Further research is required to determine the LHRs' function, mechanism of action, and potential contribution to the pathogenesis of hip dysplasia or CCL rupture in dogs.<\/jats:p>\n<\/jats:sec>","DOI":"10.2460\/ajvr.81.7.565","type":"journal-article","created":{"date-parts":[[2020,6,25]],"date-time":"2020-06-25T15:27:12Z","timestamp":1593098832000},"page":"565-571","source":"Crossref","is-referenced-by-count":5,"title":["Assessment of luteinizing hormone receptor expression in structural support tissues of canine hip and femorotibial joints"],"prefix":"10.2460","volume":"81","author":[{"given":"Claire A.","family":"Kiefel","sequence":"first","affiliation":[{"name":"1Department of Integrative Biology, College of Science, Oregon State University, Corvallis, OR 97331."},{"name":"2Department of Clinical Sciences, Carlson College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michelle A.","family":"Kutzler","sequence":"additional","affiliation":[{"name":"3Department of Animal and Rangeland Sciences, College of Agricultural Sciences, Oregon State University, Corvallis, OR 97331."}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1272","reference":[{"key":"ref1","series-title":"Theriogenology","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.1016\/j.theriogenology.2006.12.003","article-title":"Basal and GnRH-induced secretion of FSH and LH in anestrous versus ovariectomized bitches","volume":"67","author":"Beijerink","year":"2007"},{"key":"ref2","series-title":"Annu Rev Physiol","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1146\/annurev.physiol.60.1.461","article-title":"The luteinizing hormone receptor","volume":"60","author":"Dufau","year":"1998"},{"key":"ref3","series-title":"Vet J","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.tvjl.2004.01.002","article-title":"Nongonadal LH receptors, their involvement in female reproductive function and a new applicable approach","volume":"169","author":"Ziecik","year":"2005"},{"key":"ref4","series-title":"Semin Reprod Med","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1055\/s-2001-13906","article-title":"An overview of the past, present, and future of nongonadal LH\/hCG action in reproductive biology and medicine","volume":"19","author":"Rao","year":"2001"},{"key":"ref5","series-title":"Endocrinology","doi-asserted-by":"publisher","first-page":"1159","DOI":"10.1210\/endo-119-3-1159","article-title":"Evidence for the presence of luteinizing hormone\/human chorionic gonadotropin-binding sites in the porcine uterus","volume":"119","author":"Ziecik","year":"1986"},{"key":"ref6","series-title":"J Clin Endocrinol Metab","first-page":"863","article-title":"Novel co-expression of human chorionic gonadotropin (hCG)\/human luteinizing hormone receptors and their ligand hCG in human fallopian tubes","volume":"77","author":"Lei","year":"1993"},{"key":"ref7","series-title":"J Physiol Pharmacol","first-page":"77","article-title":"Cycle dependent LH\/hCG receptor gene expression in porcine non-gonadal reproductive tissues","volume":"46","author":"Derecka","year":"1995"},{"key":"ref8","series-title":"J Clin Endocrinol Metab","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1210\/jcem-70-2-421","article-title":"The presence of gonadotropin receptors in non-pregnant human uterus, human placenta, fetal membranes, and decidua","volume":"70","author":"Reshef","year":"1990"},{"key":"ref9","series-title":"Biol Reprod","doi-asserted-by":"publisher","first-page":"1020","DOI":"10.1095\/biolreprod52.5.1020","article-title":"Bovine cyclic endometrium contains high-affinity luteinizing hormone, human chorionic gonadotropin binding sites","volume":"52","author":"Freidman","year":"1995"},{"key":"ref10","series-title":"Exp Clin Endocrinol Diabetes","first-page":"44","article-title":"Distribution and cycle phase dependency of gonadotropin receptors in musculature and blood vessels of the porcine broad ligament","volume":"103","author":"Ziecik","year":"1995"},{"key":"ref11","series-title":"J Physiol Pharmacol","first-page":"917","article-title":"LH\/hCG receptors in the porcine uterus: a new evidence of their presence in the uterus","volume":"51","author":"Stepien","year":"2000"},{"key":"ref12","series-title":"Biol Reprod","doi-asserted-by":"publisher","first-page":"1202","DOI":"10.1095\/biolreprod57.5.1202","article-title":"Presence of functional luteinizing hormone\/chorionic gonadotropin (hCG) receptors in human breast cell lines: implication supporting the premise that hCG protects women against breast cancer","volume":"57","author":"Lojun","year":"1997"},{"key":"ref13","series-title":"J Clin Endocrinol Metab","first-page":"307","article-title":"Expression of functional human chorionic gonadotropin\/human luteinizing hormone receptor gene in human uterine arteries","volume":"79","author":"Toth","year":"1994"},{"key":"ref14","series-title":"Theriogenology","doi-asserted-by":"publisher","first-page":"1391","DOI":"10.1016\/j.theriogenology.2004.02.011","article-title":"Changes in plasma gonadotropin concentrations and urethral closure pressure in the bitch during the 12 months following ovariectomy","volume":"62","author":"Reichler","year":"2004"},{"key":"ref15","series-title":"Theriogenology","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/j.theriogenology.2006.08.007","article-title":"Luteinizing hormone and follicle-stimulating hormone receptors and their transcribed genes (mRNA) are present in the lower urinary tract of intact male and female dogs","volume":"67","author":"Ponglowhapan","year":"2007"},{"key":"ref16","series-title":"Reprod Domest Anim","first-page":"350","article-title":"Influence of spaying in the expression of GnRH-, FSH- and LH- receptors of the urinary tract in the bitch","volume":"40","author":"Reichler","year":"2005"},{"key":"ref17","series-title":"J Small Anim Pract","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1111\/j.1748-5827.1985.tb02099.x","article-title":"Urinary incontinence in the bitch due to sphincter incompetence: prevalence in referred dogs and retrospective analysis of sixty cases","volume":"26","author":"Holt","year":"1985"},{"key":"ref18","series-title":"Domest Anim Endocrinol","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/j.domaniend.2007.09.005","article-title":"Differences in the expression of luteinizing hormone and follicle-stimulating hormone receptors in the lower urinary tract between intact and gonadectomised male and female dogs","volume":"34","author":"Ponglowhapan","year":"2008"},{"key":"ref19","series-title":"Thai J Vet Med","first-page":"259","article-title":"Canine urinary incontinence post-neutering: a review of associated factors, pathophysiology and treatment options","volume":"42","author":"Ponglowhapan","year":"2012"},{"key":"ref20","series-title":"J Reprod Fertil Suppl","first-page":"227","article-title":"Comparison of long-term effects of ovariectomy versus ovariohysterectomy in bitches","volume":"51","author":"Okkens","year":"1997"},{"key":"ref21","series-title":"Am J Vet Res","first-page":"1990","article-title":"Joint laxity and its association with hip dysplasia in Labrador Retrievers","volume":"54","author":"Lust","year":"1993"},{"key":"ref22","series-title":"Theriogenology","doi-asserted-by":"publisher","first-page":"1207","DOI":"10.1016\/S0093-691X(02)01368-7","article-title":"The effect of GnRH analogs on urinary incontinence after ablation of the ovaries in dogs","volume":"60","author":"Reichler","year":"2003"},{"key":"ref23","series-title":"Theriogenology","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1016\/j.theriogenology.2013.08.013","article-title":"Gonadotropin-releasing hormone immunization for the treatment of urethral sphincter mechanism incompetence in ovariectomized bitches","volume":"81","author":"Donovan","year":"2014"},{"key":"ref24","series-title":"J Vet Sci Med Diagn","first-page":"1","article-title":"Gonadotropin-releasing hormone immunization to treat urethral sphincter mechanism incompetence in a bitch that experienced an adverse reaction to phenylpropanolamine","volume":"2","author":"Donovan","year":"2013"},{"key":"ref25","series-title":"Am J Vet Res","doi-asserted-by":"publisher","first-page":"307","DOI":"10.2460\/ajvr.2005.66.307","article-title":"Incidence, risk factors, and heritability estimates of hind limb lameness caused by hip dysplasia in a birth cohort of Boxers","volume":"66","author":"van Hagen","year":"2005"},{"key":"ref26","series-title":"J Am Vet Med Assoc","doi-asserted-by":"publisher","first-page":"1818","DOI":"10.2460\/javma.232.12.1818","article-title":"Prevalence of and risk factors for hip dysplasia and cranial cruciate ligament deficiency in dogs","volume":"232","author":"Witsberger","year":"2008"},{"key":"ref27","series-title":"PLoS One","doi-asserted-by":"publisher","first-page":"e55937","DOI":"10.1371\/journal.pone.0055937","article-title":"Neutering dogs: effects of joint disorders and cancers in Golden Retrievers","volume":"8","author":"Torres de la Riva","year":"2013"},{"key":"ref28","series-title":"Body condition scoring systems (BCS)","year":"2018"},{"key":"ref29","series-title":"Anim Reprod Sci","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.anireprosci.2017.10.002","article-title":"Oxytocin is not involved in luteolysis and early maternal recognition of pregnancy (MRP) in alpacas","volume":"187","author":"Ciccarelli","year":"2017"},{"key":"ref30","series-title":"Vet Dermatol","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1111\/j.1365-3164.2008.00652.x","article-title":"Spaying-induced coat changes: the role of gonadotropins, GnRH and GnRH treatment on the hair cycle of female dogs","volume":"19","author":"Reichler","year":"2008"},{"key":"ref31","series-title":"Arthroscopy","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/S0749-8063(98)70125-2","article-title":"Transient laxity of an anterior cruciate ligament-reconstructed knee related to pregnancy","volume":"14","author":"Blecher","year":"1998"},{"key":"ref32","series-title":"Knee","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.knee.2008.09.005","article-title":"The effect of relaxin on the female anterior cruciate ligament: analysis of mechanical properties in an animal model","volume":"16","author":"Dragoo","year":"2009"},{"key":"ref33","series-title":"PLoS One","doi-asserted-by":"publisher","first-page":"e0160984","DOI":"10.1371\/journal.pone.0160984","article-title":"Changes in knee laxity and relaxin receptor isoforms expression (RXFP1\/RXFP2) in the knee throughout estrous cycle phases in rodents","volume":"11","author":"Dehghan","year":"2016"},{"key":"ref34","series-title":"Am J Physiol Regul Integr Comp Physiol","doi-asserted-by":"publisher","first-page":"R15","DOI":"10.1152\/ajpregu.00829.2004","article-title":"Effect of testosterone on the female anterior cruciate ligament","volume":"289","author":"Lovering","year":"2005"},{"key":"ref35","series-title":"Knee","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.knee.2003.12.003","article-title":"Examination of the failure properties of the anterior cruciate ligament during the estrous cycle","volume":"12","author":"Rau","year":"2005"},{"key":"ref36","series-title":"Am J Sports Med","doi-asserted-by":"publisher","first-page":"614","DOI":"10.1177\/03635465980260050301","article-title":"Association between the menstrual cycle and anterior cruciate ligament injuries in female athletes","volume":"26","author":"Wojtys","year":"1998"},{"key":"ref37","series-title":"J Womens Health (Larchmt)","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1089\/154099903321667627","article-title":"The correlations between estradiol, estrone, estriol, progesterone, and sex hormone-binding globulin and anterior cruciate ligament stiffness in healthy, active females","volume":"12","author":"Romani","year":"2003"},{"key":"ref38","series-title":"Knee Surg Sports Traumatol Arthrosc","doi-asserted-by":"publisher","first-page":"2742","DOI":"10.1007\/s00167-014-3077-3","article-title":"The influence of sex hormones on anterior cruciate ligament rupture: female study","volume":"23","author":"Stijak","year":"2015"},{"key":"ref39","series-title":"Knee Surg Sports Traumatol Arthrosc","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1007\/s00167-006-0237-0","article-title":"Reproductive hormone effects on strength of the rat anterior cruciate ligament","volume":"15","author":"Woodhouse","year":"2007"},{"key":"ref40","series-title":"Clin Orthop Relat Res","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1097\/00003086-200106000-00022","article-title":"Correlation of estradiol in pregnancy and anterior cruciate ligament laxity","volume":"387","author":"Charlton","year":"2001"},{"key":"ref41","series-title":"J Orthop Res","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1002\/jor.1100170316","article-title":"Estrogen level alters the failure load of the rabbit anterior cruciate ligament","volume":"17","author":"Slauterbeck","year":"1999"},{"key":"ref42","series-title":"Biochem Biophys Res Commun","doi-asserted-by":"publisher","first-page":"1221","DOI":"10.1016\/j.bbrc.2004.03.174","article-title":"Tensile forces attenuate estrogen stimulated collagen synthesis in the ACL","volume":"317","author":"Lee","year":"2004"},{"key":"ref43","series-title":"Am J Sports Med","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1177\/03635465020300020601","article-title":"The effect of the menstrual cycle on anterior cruciate ligament injuries in women as determined by hormone levels","volume":"30","author":"Wojtys","year":"2002"},{"key":"ref44","series-title":"J Athl Train","first-page":"275","article-title":"The menstrual cycle, sex hormones, and anterior cruciate ligament injury","volume":"37","author":"Slauterbeck","year":"2002"},{"key":"ref45","series-title":"J Athl Train","doi-asserted-by":"publisher","first-page":"22","DOI":"10.4085\/1062-6050-45.1.22","article-title":"Sex, collagen expression, and anterior cruciate ligament strength in rats","volume":"45","author":"Romani","year":"2010"},{"key":"ref46","series-title":"Knee","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1016\/j.knee.2016.07.004","article-title":"Testosterone may increase rat anterior cruciate ligament strength","volume":"23","author":"Romani","year":"2016"},{"key":"ref47","series-title":"Am J Sports Med","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1177\/03635465030310041701","article-title":"Relaxin receptors in the female anterior cruciate ligament","volume":"31","author":"Dragoo","year":"2003"},{"key":"ref48","series-title":"J Orthop Res","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1002\/jor.1100140405","article-title":"Primary immunolocalization of estrogen and progesterone target cells in the human anterior cruciate ligament","volume":"14","author":"Liu","year":"1996"},{"key":"ref49","series-title":"J Orthop Res","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1002\/jor.1100160513","article-title":"Identification of sex hormone receptors in human and rabbit ligaments of the knee by reverse transcription-polymerase chain reaction: evidence that receptors are present in tissue from both male and female subjects","volume":"16","author":"Sciore","year":"1998"},{"key":"ref50","series-title":"Orthop Clin North Am","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1016\/j.ocl.2006.09.001","article-title":"Anterior cruciate ligament biology and its relationship to injury forces","volume":"37","author":"Slauterbeck","year":"2006"},{"key":"ref51","series-title":"Vet Comp Orthop Traumatol","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1055\/s-0038-1633097","article-title":"Incidence of canine appendicular musculoskeletal disorders in 16 veterinary teaching hospitals from 1980 through 1989","volume":"7","author":"Johnson","year":"1994"},{"key":"ref52","series-title":"J Am Vet Med Assoc","doi-asserted-by":"publisher","first-page":"1688","DOI":"10.2460\/javma.231.11.1688","article-title":"Risk factors for excessive tibial angle plateau in large-breed dogs with cranial cruciate ligament disease","volume":"231","author":"Duerr","year":"2007"},{"key":"ref53","series-title":"Textbook of small animal orthopedics","article-title":"Hip dysplasia","author":"Riser","year":"1985"},{"key":"ref54","series-title":"Vet J","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1016\/j.tvjl.2005.07.003","article-title":"Nitric oxide and metalloproteinases in canine articular ligaments: a comparison between the cranial cruciate, the medial genual collateral and the femoral head ligament","volume":"172","author":"Louis","year":"2006"}],"container-title":["American Journal of Veterinary Research"],"original-title":[],"link":[{"URL":"https:\/\/avmajournals.avma.org\/view\/journals\/ajvr\/81\/7\/ajvr.81.7.565.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/avmajournals.avma.org\/downloadpdf\/journals\/ajvr\/81\/7\/ajvr.81.7.565.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/avmajournals.avma.org\/downloadpdf\/journals\/ajvr\/81\/7\/ajvr.81.7.565.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,5]],"date-time":"2023-10-05T20:44:15Z","timestamp":1696538655000},"score":1,"resource":{"primary":{"URL":"https:\/\/avmajournals.avma.org\/view\/journals\/ajvr\/81\/7\/ajvr.81.7.565.xml"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7]]},"references-count":54,"journal-issue":{"issue":"7"},"URL":"https:\/\/doi.org\/10.2460\/ajvr.81.7.565","relation":{},"ISSN":["0002-9645"],"issn-type":[{"value":"0002-9645","type":"print"}],"subject":[],"published":{"date-parts":[[2020,7]]}}}