Skip to main content
SpringerLink
Log in

Disorder of sexual development in a Yorkshire terrier (78, XY; SRY-positive)

  • Animal Genetics • Original Paper
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

A 9-month-old Yorkshire terrier was admitted to the clinic because of abnormal sexual behaviour and clitoral hypertrophy. External examination confirmed standard development of caudal genital organs: vagina, vulva and cervix uteri. Serum profile of gonadotropin hormones 17 β-estradiol (<10.0 pg.ml−1) and testosterone (9.1 ng.ml−1) revealed the presence of testicular tissue. A midline laparotomy was performed to detect the cranial parts of the genital system. Gonads resembling testicles, structures indicating epididymis and rudimentary deferent ducts were resected, along with adherent part of the uterus. Cytogenetic analysis showed a male chromosomal complement 78, XY in all metaphases of the studied Yorkshire terrier dog. The chromosomal constitution was confirmed by fluorescence in situ hybridisation (FISH) with whole-chromosome painting probes specific for chromosomes X and Y, as well as by polymerase chain reaction (PCR) amplification of the 271-bp Y-linked fragment of SRY (the sex-determining region on the Y chromosome) gene. Sequencing of the dog’s SRY gene coding region did not reveal any mutation. To search for potential mutation in the SOX9 gene (Sry-box containing gene 9), which is considered to be one of the key genes involved in the sex determination process, the PCR fragments of exons 1, 2 and 3 originating from the canine patient were sequenced in order to compare with both male and female healthy control dogs. In the analysed regions of the SOX9 gene, no mutation was found.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adelsberger ME, Smeak DD (2009) Repair of extensive perineal hypospadias in a Boston terrier using tubularized incised plate urethroplasty. Can Vet J 50:937–942

    PubMed  Google Scholar 

  • Ader PL, Hobson HP (1978) Hypospadias: a review of the veterinary literature and a report of three cases in the dog. J Am Anim Hosp Assoc 14:721–727

    Google Scholar 

  • Alam MR, Cho YG, Cho SJ, Lee JI, Lee HB, Tae HJ, Kim IS, Kim NS (2007) Male pseudohermaphroditism in dogs: three case reports. Vet Med 52:74–78

    Google Scholar 

  • Barasc H, Mary N, Letron R, Calgaro A, Dudez AM, Bonnet N, Lahbib-Mansais Y, Yerle M, Ducos A, Pinton A (2012) Y-autosome translocation interferes with meiotic sex inactivation and expression of autosomal genes: a case study in the pig. Sex Dev 6:143–150

    Article  PubMed  CAS  Google Scholar 

  • Bigliardi E, Parma P, Peressotti P, De Lorenzi L, Wohlsein P, Passeri B, Jottini S, Cantoni AM (2011) Clinical, genetic, and pathological features of male pseudohermaphroditism in dog. Reprod Biol Endocrinol 9:12

    Article  PubMed  Google Scholar 

  • Brown TT, Burek JD, McEntee K (1976) Male pseudohermaphroditism, cryptorchism, and Sertoli cell neoplasia in three miniature Schnauzers. J Am Vet Med Assoc 169:821–825

    PubMed  CAS  Google Scholar 

  • Christensen BW (2012) Disorders of sexual development in dogs and cats. Vet Clin North Am Small Anim Pract 42:515–526

    Article  PubMed  Google Scholar 

  • De Lorenzi L, Groppetti D, Arrighi S, Pujar S, Nicoloso L, Molteni L, Pecile A, Cremonesi F, Parma P, Meyers-Wallen V (2008) Mutations in the RSPO1 coding region are not the main cause of canine SRY-negative XX sex reversal in several breeds. Sex Dev 2:84–95

    Article  PubMed  Google Scholar 

  • Hagel T, Baade S, Kirchhoff A, Kuiper H, Perk A (2010) Persistent Mullerian duct syndrome in a Yorkshire terrier. Kleintierpraxis 55:547

    Google Scholar 

  • Hayes HM Jr, Wilson GP, Pendergrass TW, Cox VS (1985) Canine cryptorchism and subsequent testicular neoplasia: case–control study with epidemiologic update. Teratology 32:51–56

    Article  PubMed  Google Scholar 

  • Jurka P, Galanty M, Zielinska P, Max A, Sysa P (2009) Hypospadias in six dogs. Vet Rec 164:331–333

    Article  PubMed  CAS  Google Scholar 

  • Klein OD, Backstrand K, Cotter PD, Marco E, Sherr E, Slavotinek A (2005) Case report: Y;6 translocation with deletion of 6p. Clin Dysmorphol 14:93–96

    Article  PubMed  Google Scholar 

  • Kubíčková S, Černohorská H, Musilová P, Rubeš J (2002) The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res 10:571–577

    Article  PubMed  Google Scholar 

  • Lyle SK (2007) Disorders of sexual development in the dog and cat. Theriogenology 68:338–343

    Article  PubMed  CAS  Google Scholar 

  • Marshall LS, Oehlert ML, Haskins ME, Selden JR, Patterson DF (1982) Persistent Müllerian duct syndrome in miniature schnauzers. J Am Vet Med Assoc 181:798–801

    PubMed  CAS  Google Scholar 

  • Meyers-Wallen VN (2003) Sry and Sox9 expression during canine gonadal sex determination assayed by quantitative reverse transcription-polymerase chain reaction. Mol Reprod Dev 65:373–381

    Article  PubMed  CAS  Google Scholar 

  • Meyers-Wallen VN (2006) Genetics, genomics, and molecular biology of sex determination in small animals. Theriogenology 66:1655–1658

    Article  PubMed  CAS  Google Scholar 

  • Meyers-Wallen VN (2012) Gonadal and sex differentiation abnormalities of dogs and cats. Sex Dev 6:46–60

    Article  PubMed  CAS  Google Scholar 

  • Meyers-Wallen VN, Bowman L, Acland GM, Palmer VL, Schlafer D, Fajt V (1995) Sry-negative XX sex reversal in the German shorthaired pointer dog. J Hered 86:369–374

    PubMed  CAS  Google Scholar 

  • Ninomiya S, Yokoyama Y, Teraoka M, Mori R, Inoue C, Yamashita S, Tamai H, Funato M, Seino Y (2000) A novel mutation (296 del G) of the SOX90 gene in a patient with campomelic syndrome and sex reversal. Clin Genet 58:224–227

    Article  PubMed  CAS  Google Scholar 

  • Nowacka J, Nizanski W, Klimowicz M, Dzimira S, Switonski M (2005) Lack of the SOX9 gene polymorphism in sex reversal dogs (78, XX; SRY negative). J Hered 96:797–802

    Article  PubMed  CAS  Google Scholar 

  • Nowacka-Woszuk J, Switonski M (2009) Differentiated evolutionary conservatism and lack of polymorphism of crucial sex determination genes (SRY and SOX9) in four species of the family Canidae. Folia Biol (Krakow) 57:171–176

    Article  CAS  Google Scholar 

  • Nowacka-Woszuk J, Switonski M (2010) Comparative cytogenetic mapping of three genes involved in sex determination in four species of the family Canidae. J Anim Feed Sci 19:5–12

    Google Scholar 

  • Nowacka-Woszuk J, Nizanski W, Klimowicz M, Switonski M (2007) Normal male chromosome complement and a lack of the SRY and SOX9 gene mutations in a male pseudohermaphrodite dog. Anim Reprod Sci 98:371–376

    Article  PubMed  CAS  Google Scholar 

  • Poth T, Breuer W, Walter B, Hecht W, Hermanns W (2010) Disorders of sex development in the dog—adoption of a new nomenclature and reclassification of reported cases. Anim Reprod Sci 121:197–207

    Article  PubMed  CAS  Google Scholar 

  • Preiss S, Argentaro A, Clayton A, John A, Jans DA, Ogata T, Nagai T, Barroso I, Schafer AJ, Harley VR (2001) Compound effects of point mutations causing campomelic dysplasia/autosomal sex reversal upon SOX9 structure, nuclear transport, DNA binding, and transcriptional activation. J Biol Chem 276:27864–27872

    Article  PubMed  CAS  Google Scholar 

  • Pujar S, Meyers-Wallen VN (2009) A molecular diagnostic test for persistent Müllerian duct syndrome in miniature schnauzer dogs. Sex Dev 3:326–328

    Article  PubMed  CAS  Google Scholar 

  • Pujar S, Kothapalli KS, Kirkness E, Van Wormer RH, Meyers-Wallen VN (2005) Exclusion of Lhx9 as a candidate gene for Sry-negative XX sex reversal in the American cocker spaniel model. J Hered 96:452–454

    Article  PubMed  CAS  Google Scholar 

  • Rijnberk A, Kooistra HS (2010) Clinical endocrinology of dogs and cats. Schlutersche Verlagsgesellschaft mbH & Co, Hannover

    Google Scholar 

  • Rota A, Cucuzza AS, Iussich S, DeLorenzi L, Parma P (2010) The case of an Sry-negative XX male Pug with an inguinal gonad. Reprod Domest Anim 45:743–745

    Article  PubMed  CAS  Google Scholar 

  • Schelling C, Pieńkowska A, Arnold S, Hauser B, Switoński M (2001) A male to female sex-reversed dog with a reciprocal translocation. J Reprod Fertil Suppl 57:435–438

    PubMed  CAS  Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972

    Article  PubMed  CAS  Google Scholar 

  • Switoński M, Reimann N, Bosma AA, Long S, Bartnitzke S, Pieńkowska A, Moreno-Milan MM, Fischer P (1996) Report on the progress of standardization of the G-banded canine (Canis familiaris) karyotype. Committee for the Standardized Karyotype of the Dog (Canis familiaris). Chromosome Res 4:306–309

    Article  PubMed  Google Scholar 

  • Switonski M, Szczerbal I, Nizanski W, Kociucka B, Bartz M, Dzimira S, Mikolajewska N (2011) Robertsonian translocation in a sex reversal dog (XX, SRY negative) may indicate that the causative mutation for this intersexuality syndrome resides on canine chromosome 23 (CFA23). Sex Dev 5:141–146

    Article  PubMed  CAS  Google Scholar 

  • Switonski M, Payan-Carreira R, Bartz M, Nowacka-Woszuk J, Szczerbal I, Colaço B, Pires MA, Ochota M, Nizanski W (2012) Hypospadias in a male (78,XY; SRY-positive) dog and sex reversal female (78,XX; SRY-negative) dogs: clinical, histological and genetic studies. Sex Dev 6:128–134

    Article  PubMed  CAS  Google Scholar 

  • Volpe P, Izzo B, Di Meo GP, Perucatti A, Iannuzzi L (2000) Male pseudo-hermaphroditism in a dog: a clinical case. Vet Rec 146:532–533

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Wan S, Pujar S, Haskins ME, Schlafer DH, Lee MM, Meyers-Wallen VN (2009) A single base pair mutation encoding a premature stop codon in the MIS type II receptor is responsible for canine persistent Müllerian duct syndrome. J Androl 30:46–56

    Article  PubMed  CAS  Google Scholar 

  • Yates D, Hayes G, Heffernan M, Beynon R (2003) Incidence of cryptorchidism in dogs and cats. Vet Rec 152:502–504

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Petra Musilová and Dr. Svatava Kubíčková (Department of Genetics and Reproduction, Veterinary Research Institute, Brno, Czech Republic) for their kind personal communication in relation to the dog FISH probes and Dr. Ľudmila Tkáčiková (Department of Microbiology and Immunology, University of Veterinary Medicine and Pharmacy, Košice, Slovak Republic) for the PCR consultations, as well as Dr. Mangesh Bhide and Dr. Stanislav Hreško (Laboratory of Biomedical Microbiology and Immunology, University of Veterinary Medicine and Pharmacy, Košice, Slovak Republic) for their helpful advice and evaluation of the DNA sequencing results.

Funding

This work was supported by VEGA grants 1/0125/11 and 1/0117/13.

Author information

Authors and Affiliations

  1. Department of Biology and Genetics, University of Veterinary Medicine and Pharmacy, Komenského 73, 041 81, Košice, Slovak Republic

    Ján Dianovský, Beáta Holečková & Katarina Šiviková

  2. Clinics of Small Animals, University of Veterinary Medicine and Pharmacy, Komenského 73, 041 81, Košice, Slovak Republic

    Jaroslav Hajurka

  3. Department of Anatomy, Histology and Physiology, University of Veterinary Medicine and Pharmacy, Komenského 73, 041 81, Košice, Slovak Republic

    Viera Cigánková

Authors
  1. Ján Dianovský
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beáta Holečková
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaroslav Hajurka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Katarina Šiviková
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Viera Cigánková
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Beáta Holečková.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dianovský, J., Holečková, B., Hajurka, J. et al. Disorder of sexual development in a Yorkshire terrier (78, XY; SRY-positive). J Appl Genetics 54, 193–199 (2013). https://doi.org/10.1007/s13353-013-0137-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-013-0137-1

Keywords

Search

Navigation