Tissue kallikrein and bradykinin B2 receptors in the reproductive tract of the male rat
Corresponding Author
T. K. Monsees
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Centre of Dermatology and Andrology, Justus Liebig University, Gafikystr. 14, 35385 Giessen, Germany. Tel.: +49 641 99 43372; fax:+49 641 99 43379; e-mail: [email protected]Search for more papers by this authorS. Blöcher
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Institute for Veterinary Anatomy, Giessen, Germany
Search for more papers by this authorC. Loddo
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Search for more papers by this authorW.-B. Schill
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Search for more papers by this authorCorresponding Author
T. K. Monsees
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Centre of Dermatology and Andrology, Justus Liebig University, Gafikystr. 14, 35385 Giessen, Germany. Tel.: +49 641 99 43372; fax:+49 641 99 43379; e-mail: [email protected]Search for more papers by this authorS. Blöcher
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Institute for Veterinary Anatomy, Giessen, Germany
Search for more papers by this authorC. Loddo
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Search for more papers by this authorW.-B. Schill
Centre of Dermatology and Andrology, Justus Liebig University, Giessen, Germany
Search for more papers by this authorAbstract
Summary. The setting of a local tissue kallikrein kinin system (tKKS) within the reproductive organs of the male rat was investigated by analysing bradykinin subtype 2 receptor (B2R) gene expression and cellular distribution of B2R protein and the kinin-liberating protease tissue kallikrein (tK). Reverse transcription—polymerase chain reaction showed B2R expression in testis, epididymis and prostate from prepubertal and sexually mature rats. In mature testis, in situ hybridization and immunohistochemistry localized B2R mRNA and protein besides endothelial cells of blood vessels exclusively on pachytene spermatocytes and round and elongated spermatids. B2R expression within the seminiferous tubules was found to be dependent on the stage of the spermatogenic cycle. In prepubertal rat testis, B2R mRNA and protein were additionally located in peritubular cells. In the testis, specific staining for tK occurred in addition to endothelial cells of blood vessels on the acrosomal cap of round and elongated spermatids. This immunostaining was also stage-dependent. In the epididymis, tK was detected on epithelial cells near the apical surface. The stage-dependent specific expression of tK and bradykinin B2Rs in developing germ cells and peritubular cells suggests a potential role of the tKKS in the local regulation of spermatogenesis and seminiferous tubule function.
References
- Alla, Abd S., Quitterer U., Grigiriev S., Maidhof A., Haasemann M., Jarnagin K., Müller-Ersterl W. (1996) Extracellular domains of the bradykinin B2 receptor involved in ligand binding and agonist sensing defined by anti-peptide antibodies. J Biol Chem 271: 1748 – 1755.
- Atanassova N., Kancheva L., Somlev B. (1998) Bradykinin stimulates prepubertal germ cell proliferation in vitro. Immunopharmacology 40: 173 – 178.
- Blasini R., Schmeller ML, Pfeiffer C., Wriedt-Lübbe I., Huber P., Blümel G. (1980) Experimentelle Untersuchungen über die organspezifische Anreicherung von Kininogenasen im Hoden-Nebenhodenbereich. Andrologia 12: 199 – 205.
- Blöcher S., Miska W., Schill WB, Monsees TK (2000) Development-dependent changes in the expression of tissue kallikrein and bradykinin B2 receptor in rat seminiferous tubules. Reprod Dom Anim 35: 35.
-
Clements JA (1997) Molecular biology of the kallikreins. In: The Kinin System. SG Farmer (ed). The Handbook of Immunopharmacology. Academic Press,
San Diego
, pp 71
–
97.
10.1016/B978-012249340-9/50007-3 Google Scholar
- Clements JA, Mukhtar A. (1997) Tissue kallikrein and the bradykinin B2 receptor are expressed in endometrial and prostate cancers. Immunopharmacology 36: 217 – 220.
-
Clements JA,
Mukthar A.,
Ehrlich A.,
Fuller P. (1992) A re-evaluation of the tissue-specific pattern of the expression of the rat kallikrein gene family. In: Recent Progress on Kinins, Agents and Actions. Suppl. Vol. 38/I. H. Fritz,
W. Müller-Esterl,
M. Jochum,
A. Roscher,
K. Luppertz (eds). Birkhauser-Verlag,
Basel
, pp 34
–
41.
10.1007/978-3-0348-7321-5_5 Google Scholar
- El-Dahr S., Chao J. (1992) Spatial and temporal expression of kallikrein and its mRNA during nephron maturation. Am J Phys 262: F705 – F711.
- Erdös EG, Skidgel RA (1997) Metabolism of bradykinin by peptidases in health and disease. In: The Kinin System. SG Farmer (Ed.) Academic Press, San Diego , pp 112 – 141.
- Figueroa CD, Caorsi I., Subiabre J., Vio CP (1984) Immunoreactive kallikrein localization in the rat kidney: an immuno-electron-microscopic study. J Histochem Cytochem 32: 117 – 121.
- Figueroa CD, Gonzales CB, Grigoriev S., Alla SA, Haasemann M., Jarnagin K., Mueller-Esterl W. (1995) Probing for the bradykinin B2 receptor in rat kidney by anti-peptide and anti-ligand antibodies. J Histochem Cytochem 43: 137 – 148.
- Fink E., Schill WB, Miska W. (1989) Kinin-containing kininogen is present in human seminal plasma. Adv Exp Med Biol 247B:311 – 315.
- Hess JF (1997) Molecular pharmacology of kinin receptors. In: The kinin System. SG Farmer (eds). Academic Press, San Diego , pp 45 – 56.
- Lewis FA, Wells M. (1992) Detection of virus infected human tissue by in-situ hybridization. In: In-Situ Hybridization, A Practical Approach. DG Wilkinson (Ed.). Oxford University Press, Oxford , pp 121 – 135.
-
Marceau F. (1997) Kinin B1 receptor induction and inflammation. In: The Kinin System. SG Farmer (Ed.). Academic Press,
San Diego
, pp 143
–
156.
10.1016/B978-012249340-9/50010-3 Google Scholar
- McEachern AE, Shelton ER, Bhakta S., Obernolte R., Bach C., Zuppan P., Fujisaki J., Aldrich RW, Jarnagin K. (1991) Expression cloning of a rat B2 bradykinin receptor. PNAS 88: 7724 – 7728.
- Miska W., Croseck H., Schill WB (1988) Kininase II from human seminal plasma. Biol Chem Hoppe-Seyler 369: 493 – 496.
- Miska W., Schill WB (1990) Enhancement of sperm motility by bradykinin and kinin analogs. Arch Androl 25: 63 – 67.
- Miska W., Schill WB (1994) Influence of bradykinin antagonists on the motility of human spermatozoa enhanced by bradykinin. Arch Androl 33: 1 – 5.
- Monsees TK, Miska W., Schill WB (1996a) Enzymatic digestion of bradykinin by rat Sertoli cell cultures. J Androl 17: 375 – 381.
- Monsees TK, Miska W., Schill WB (1996b) Characterization of kininases in testicular cells. Immunopharmacology 32: 169 – 171.
- Monsees TK, Görnig M., Schill WB, Miska W. (1998) Possible involvement of proteases in the regulation of spermatogenesis. Andrologia 30: 185 – 191.
- Monsees TK, Miska W., Blöcher S., Schill WB, Winkler A., Siems WE (1999) Elements of the kallikrein kinin system are present in rat seminiferous epithelium. Immunopharmacology 45: 107 – 114.
- Monsees TK, Kos P., Schill WB, Henkel R. (2002a) Identification of protease activities in testicular rat peritubular cells. Andrologia 34: 279.
- Monsees TK, Blöcher S., Heidorn F., Winkler A., Siems WE, Müller-Esterl W., Hayatpour J., Miska W., Schill WB (2002b) Expression and location of the bradykinin B2 receptor in rat testis. Biol Reprod 67: 1832 – 1839.
- Müller K., Heder G., Nehring H., Siems WE, Wolf R. (1991) Investigations on the influence of bradykinin upon the motility of ram spermatozoa. Andrologia 23: 357 – 362.
-
Müller-Esterl W. (1997) Immunological probes for the bradykinin B2 receptor. A toolbox. In: The Kinin System. SG Farmer (Ed.). Academic Press,
San Diego
, pp 99
–
110.
10.1016/B978-012249340-9/50008-5 Google Scholar
- Oza NB, Amin VM, McGregor RK, Scicli AG, Carretero OA (1976) Isolation of rat urinary kallikrein and properties of its antibodies. Biochem Pharmacol 25: 1607 – 1612.
- Regoli D. (1984) Neurohumoral regulation of precapillary vessels: the kallikrein-kinin system. J Cardiovasc Pharmacol 6: S401 – S410.
- Rohen JW, Stuttman R. (1977) The early postnatal development of the germinative epithelium of the testis in the albino rat under the influence of kallikrein. In: Kininogen. Kallikrein 4. GL Haberland, JW Rohen, T. Suzuki (eds). Schattauer, Stuttgart , pp 217 – 223.
- Saed GM, Carretero OA, McDonald R., Scili AG (1990) Kallikrein mRNA in rat arteries and veins. Circ Res 67: 510 – 516.
- Saitoh S., Kumamoto Y., Shimamato K., Iimura O. (1987) Kallikrein in the male reproductive system. Arch Androl 19: 133 – 147.
- Saitoh S., Mikuma N., Kumamoto Y. (1989) Effect of kallikrein on the Sertoli cell function. Urol Int 44: 87 – 89.
- Siems WE, Maul B., Wiesner B., Becker M., Walther T., Rothe L., Winkler A. (2003) Effects of kinins on mammalian spermatozoa and the impact of peptidolytic enzymes. Andrologia 35: 44 – 54.
- Somlev B., Helili K. (1996) Kinin-induced stimulation of bovine sperm motility and its relation to seminal plasma kallikrein. Immunopharmacology 33: 137 – 139.
- Steger K., Klonisch T., Gavenis K., Drabant B., Doenecke D., Bergmann M. (1998) Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol Hum Reprod 4: 939 – 945.
- Takano M., Kondo J., Yayama K., Sano K., Okamoto H. (1997) Molecular cloning of cDNAs for mouse low molecular-weight and high molecular-weight prekininogens. Biochim Biophys Acta. 30: 222 – 230.
- Tung PS, Fritz IB (1990) Characterization of rat testicular peritubular myoid cells in culture: alpha-smooth muscle isoactin is a specific differentiation marker. Biol Reprod 42: 351 – 360.
- Valdes G., Figueroa CD, Corthorn J. (1996) Temporospatial changes of the kallikrein-like enzymes during the estrous cycle and pregnancy in the rat uterus. Biol Reprod 55: 236 – 245.
-
Walsh DA,
Fan TPD (1997) Bradykinin as a growth factor. In: The Kinin System. SG Farmer (Ed.). Academic Press,
San Diego
, pp 301
–
314.
10.1016/B978-012249340-9/50020-6 Google Scholar
- Wennemuth G., Aumüller G., Bacher M., Meinhardt A. (2000) Macrophage migration inhibitory factor-induced Ca2+ response in rat testicular peritubular cells. Biol Reprod 62: 1632 – 1639.
- Wennemuth G., Blöcher S., Schill WB, Aumüller G., Monsees TK (2002) Bradykinin increases intracellular calcium levels in rat testis peritubular cells via the B2 receptor subtype. Br J Pharmacol, in press, doi: 10.1038/sj.bjp.0705039.
- Wolf WC, Harley RA, Sluce D., Chao, Chao J. (1999) Localization and expression of tissue kallikrein and kallistatin in human blood vessels. J Histochem Cytochem 47: 221 – 228.
