Skip to main content
Log in

Expression of KiSS-1 in rat oviduct: possible involvement in prevention of ectopic implantation?

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The mammalian oviduct is a crucial site for essential postovulatory events in the female reproductive system. These events are, in part, accomplished by clear-cut oviductal segmentation, which helps to provide appropriate epithelial and fluid microenvironments. Early embryonic development and the timely transport of the embryo to the uterus must be promoted, but implantation within the oviduct itself must be avoided. Indeed, the rarity of extra-uterine pregnancies in laboratory animals strongly suggests that active mechanisms operate to prevent ectopic implantation. Kisspeptins, products of the KiSS-1 gene, have been proposed as physiological regulators of uterine implantation by limiting the invasion of the trophoblast into the maternal decidua. We describe here the patterns of expression of the KiSS-1 gene and of kisspeptin immunoreactivity (IR) in the rat oviduct. KiSS-1 mRNA is readily detectable in oviduct samples from all phases of the estrous cycle, whereas kisspeptin-IR is detected in rat oviduct with a regionalized pattern of distribution, viz., strong expression in the isthmus, faint signals in the proximal ampulla, and a lack of immunostaining in the fimbriated infundibulum and interstitial portion. When positive, IR has been localized at the adluminal surface and the cytoplasmic domain of secretory cells. Of note, KiSS-1 expression (at the mRNA and protein levels) shows cycle-related changes with peak expression in proestrus/estrus and lower levels at metestrus/diestrus. This knowledge of the regional- and cycle-specific pattern of expression of KiSS-1 in rat oviduct should open up the possibility of a physiological role of kisspeptins in the prevention of ectopic (tubal) implantation.

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

Access this article

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
Fig. 4

Similar content being viewed by others

References

  • Bai SX, Wang YL, Qin L, Xiao ZJ, Herva R, Piao YS (2005) Dynamic expression of matrix metalloproteinases (MMP-2, -9 and -14) and tissue inhibitors of MMPs (TIMP-1, -2 and -3) at the implantation site during tubal pregnancy. Reproduction 129:103–113

    Article  PubMed  CAS  Google Scholar 

  • Bilban M, Ghaffari-Tabrizi N, Hintermann E, Bauer S, Molzer S, Zoratti C, Malli R, Sharabi A, Hiden U, Graier W, Knofler M, Andreae F, Wagner O, Quaranta V, Desoye G (2004) Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci 117:1319–1328

    Article  PubMed  CAS  Google Scholar 

  • Bouyer J, Coste J, Fernandez H, Pouly JL, Job-Spira N (2002) Sites of ectopic pregnancy: a 10-year population-based study of 1800 cases. Human Reprod 17:3224–3230

    Article  CAS  Google Scholar 

  • Buhi WC (2002) Characterization and biological roles of oviducvt-specific, oestrogen-dependent glycoprotein. Reproduction 123:355–362

    Article  PubMed  CAS  Google Scholar 

  • Castellano JM, Gaytán M, Roa J, Vigo E, Navarro VM, Bellido C, Dieguez C, Aguilar E, Sanchez-Criado JE, Pellicer A, Pinilla L, Gaytán F, Tena-Sempere M (2006) Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology 147:4852–4862

    Article  PubMed  CAS  Google Scholar 

  • Corpa JM (2006) Ectopic pregnancy in animals and humans. Reproduction 131:631–640

    Article  PubMed  CAS  Google Scholar 

  • Gaytán F, Morales C, Garcia-Pardo L, Reymundo C, Bellido C, Sanchez-Criado JE (1998) Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod 59:417–425

    Article  PubMed  Google Scholar 

  • Gaytán F, Barreiro ML, Caminos JE, Chopin LK, Herington AC, Morales C, Pinilla L, Paniagua R, Nistal M, Casanueva FF, Aguilar E, Dieguez C, Tena-Sempere M (2004) Expression of ghrelin and its functional receptor, the type 1a growth hormone secretagogue receptor, in normal human testis and testicular tumors. J Clin Endocrinol Metab 89:400–409

    Article  PubMed  Google Scholar 

  • Hunter RHF (2005) The Fallopian tubes in domestic animals: how vital is their physiological activity? Reprod Nutr Dev 45:281–290

    Article  PubMed  Google Scholar 

  • Killian GJ (2004) Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim Reprod Sci 82:141–153

    Article  PubMed  Google Scholar 

  • Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M (2001) The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276:34631–34636

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Welch DR (1997) Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1. Cancer Res 57:2384–2387

    PubMed  CAS  Google Scholar 

  • Lee JH, Sugimura M, Kudo N (1976) Segmentation of the rat oviduct. Jpn J Vet Res 24:77–86

    PubMed  CAS  Google Scholar 

  • Moore GD, Eddy CA, Pauerstein CJ (1992) Rabbit endosalpinx inhibits implantation in vitro. Fertil Steril 57:902–907

    PubMed  CAS  Google Scholar 

  • Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CGC, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC (2001) AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276:28969–28975

    Article  PubMed  CAS  Google Scholar 

  • Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M (2004) Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor GPR54 in rat hypothalamus and potent LH releasing activity of KiSS-1 peptide. Endocrinology 145:4565–4574

    Article  PubMed  CAS  Google Scholar 

  • Novak S, Treacy BK, Almeida FR, Mao J, Buhi WC, Dixon WT, Foxcroft GR (2002) Regulation of IGF-I and porcine oviductal secretory protein (pOSP) secretion into the pig oviduct in the peri-ovulatory period, and effects of previous nutrition. Reprod Nutr Dev 42:355–372

    Article  PubMed  CAS  Google Scholar 

  • Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Fujino C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M (2001) Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G protein-coupled receptor. Nature 411:613–617

    Article  PubMed  CAS  Google Scholar 

  • Okada A, Ohta Y, Inoue S, Hiroi H, Muramatsu M, Iguchi T (2003) Expression of estrogen, progesterone and androgen receptors in the oviduct of developing, cycling and pre-implantation rats. J Mol Endocrinol 30:301–315

    Article  PubMed  CAS  Google Scholar 

  • Pauerstein CJ, Eddy CA, Koong MK, Moore GD (1990) Rabbit endosalpinx suppresses ectopic pregnancy. Fertil Steril 54:522–526

    PubMed  CAS  Google Scholar 

  • Roux N de, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E (2003) Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972–10976

    Article  PubMed  Google Scholar 

  • Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O’Rahilly S, Carlton MB, Crowley WF, Aparicio SA, Colledge WH (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614–1627

    Article  PubMed  CAS  Google Scholar 

  • Staun-Ram E, Goldman S, Gabarin D, Shalev E (2004) Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod Biol Endocrinol 2:59

    Article  PubMed  Google Scholar 

  • Tena-Sempere M (2006) GPR54 and kisspeptin in reproduction. Hum Reprod Update 12:631–639

    Article  PubMed  CAS  Google Scholar 

  • Terao Y, Kumano S, Takatsu Y, Hattori M, Nishimura A, Ohtaki T, Shintani Y (2004) Expression of KiSS-1, a metastasis suppressor gene, in trophoblast giant cells of the rat placenta. Biochim Biophys Acta 1678:102–110

    PubMed  CAS  Google Scholar 

  • Yan C, Wang H, Boyd DD (2001) KiSS-1 represses 92-kDa type IV collagenase expression by down-regulating NF-κB binding to the promoter as a consequence of IκBα-induced block of p65/p50 nuclear translocation. J Biol Chem 276:1164–1172

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are indebted to E. Aguilar, C. Bellido, and L. Pinilla (University of Córdoba, Spain), and M. Burrell (University of Navarra, Spain) for assistance and helpful discussions during the reported experimental studies and the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Manuel Tena-Sempere or Francisco Gaytán.

Additional information

This work was supported by grants BFU 2005-01443 and BFU 2005-07446 (Ministerio de Educacion y Ciencia, Spain), by funds from the Instituto de Salud Carlos III (Red de Centros RCMN C03/08 and Project PI042082; Ministerio de Sanidad, Spain), and by EU research contract EDEN QLK4-CT-2002-00603. M.T.-S. is also supported by grants from the CIBER Fisiopatología de la Obesidad y Nutrición (CB06/03/0003; Instituto de Salud Carlos III) of which he is a member.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gaytán, M., Castellano, J.M., Roa, J. et al. Expression of KiSS-1 in rat oviduct: possible involvement in prevention of ectopic implantation?. Cell Tissue Res 329, 571–579 (2007). https://doi.org/10.1007/s00441-007-0426-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-007-0426-2

Keywords

Navigation