Skip to main content
SpringerLink
Log in

Nonspecific esterases of mammalian testis

Comparative studies on the mouse (Mus musculus) and rat (Rattus norvegicus)

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

Ten different nonspecific esterases in both mouse (Mus musculus) and rat (Rattus norvegicus) testis were identified following the analysis of electrophoretic patterns using genetic, developmental, and biochemical criteria. None of the enzymes were unique to testis, although the pattern of activity was testis specific. The enzymes comprised, in each species, six carboxylesterases (EC 3.1.1.1), one arylesterase (EC 3.1.1.2), one acetylesterase (EC 3.1.1.6), and two butyrylesterases (tentative designation). Cholinesterase (EC 3.1.1.8) was not detected. Individual homology relationships were recognized between the two species for all of these activities, except three of the carboxylesterases; however, these were coded for by homologous gene clusters. Similarities between the two species extended to the developmental course of expression and the modulation of the pattern of activity by the testicular feminization (Tfm) mutation. We describe the effects of the sex reversal (Sxr) mutation in the mouse, as well as the distribution of individual activities between Leydig cells and seminiferous tubules. The results of earlier histochemical studies are interpreted in the light of the present investigation. The correspondence between mouse- and rat-testis esterases suggests that the results could serve as a basis for mammalian testis esterase systems in general.

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

Similar content being viewed by others

References

  • Antonucci TK, Deimling O von, Rosenblum BB, Skow LC, Meisler MH (1984) Conserved linkage within a 4-cM region of mouse chromosome 9 and human chromosome 11. Genetics 107: 463–475

    Google Scholar 

  • Anselmi E, Arata L, Severi MA, Pecora P (1962) Effetto della radiazione roentgen sull'attività esterasica del testicolo di ratto. Boll Soc Ital Biol Sper 38: 360–362

    Google Scholar 

  • Arata L, Santoro R, Severi MA, Pecora P (1962) Il contenuto on esterasi delle gonadi di ratto posto a dieta carente di vitamina E. Boll Soc Ital Biol Sper 38: 212–214

    Google Scholar 

  • Arndt R, Heymann E, Junge W, Krisch K, Hollandt H (1973) Purification and molecular properties of an unspecific carboxylesterase (E1) from rat liver microsomes. Eur J Biochem 36: 120–128

    Google Scholar 

  • Arvy L (1962) Action de l'hormone gonadotrope choriale sur quelques activités enzymatiques testiculaires chez le rat. C R Acad Sci 255: 1532–1534

    Google Scholar 

  • Augustinsson KB, Henricson B (1966) A genetically controlled esterase in rat plasma. Biochim Biophys Acta 124: 323–331

    Google Scholar 

  • Baillie AH (1964) Esterase substrate specificity in the testis of the growing mouse. Qu J Microse Sci 105: 247–256

    Google Scholar 

  • Barrnett RJ (1952) The distribution of esterolytic activities in the tissue of the rat as demonstrated with indoxyl acetate. Anat Rec 114: 577–599

    Google Scholar 

  • Baust P, Goslar HG, Tonutti E (1966) Das Verhalten der Esterasen im Hoden von Ratte, Maus und Meerschweinchen nach Oestrogenbehandlung. Z Zellforsch 69: 686–698

    Google Scholar 

  • Bender K, Günther E (1978) Screening of inbred rat strains for electrophoretic protein polymorphisms. Biochem Genet 16: 387–398

    Google Scholar 

  • Bender K, Nagel M, Günther E (1982) Es-6, a further polymorphic esterase in the rat. Biochem Genet 20:221–228

    Google Scholar 

  • Bender K, Adams M, Baverstock PR, Bieman M den, Bissbort S, Brdicka R, Butcher GW, Cramer DV, Deimling O von, Festing MFW, Günther E, Guttmann RD, Hedrich HJ, Kendall PB, Kluge R, Moutier R, Simon B, Womack JE, Yamada J, Van Zutphen B (1984) Biochemical markers in inbred strains of rat. Immunogenetics 19:257–266

    Google Scholar 

  • Berning W, de Looze SM, Deimling O von (1985) Identification and development of a genetically closely linked carboxylesterase family of mouse liver. Comp Biochem Physiol (in the press)

  • Böcking A (1976) Ultrastrukturelle Lokalisation der unspezifischen Carboxylester-Hydrolase in präpubertalen und adulten Mäusehoden. Verh Anat Ges 70:869–874

    Google Scholar 

  • Britton-Davidian J, Bonhomme F (1979) Deux nouveaux locus d'estérases Es-14 et ES-15 chez les souris (genre Mus L): charactérisation par différents substrats et inhibiteurs. C R Acad Sci Sér D 288:1419–1422

    Google Scholar 

  • Bryan JHD, Unnithan RR (1973) Cytochemical localization of non-specific esterase and acid phosphatase in spermatozoa of the mouse (Mus musculus). Histochemie 33:169–180

    Google Scholar 

  • Cattanach BM, Pollard CE, Hawkes SG (1971) Sex-revesed mice XX and XO males. Cytogenetics 10:318–337

    Google Scholar 

  • Cavallero C, Martinazzi M, Baroni C, Magrini U (1963) Pituitary control of mouse testis in hereditary dwarfism, histological and cytochemical observations. Gen Comp Endocrinol 3:636–643

    Google Scholar 

  • Chakraborty J, Nelson L (1976) Comparative study of cholinesterases distribution in the spermatozoa of some mammalian species. Biol Reproduct 15:579–585

    Google Scholar 

  • Chapman V (1973) Private communication. Mouse News Lett 48:45

    Google Scholar 

  • Chessick RD (1953) Histochemical distribution of esterases. J. Histochem Cytochem 1:471–485

    Google Scholar 

  • Choudhury SR (1972) The nature of nonspecific esterases. A subunit concept. J Histochem Cytochem 20:507–517

    Google Scholar 

  • Choudhury SR (1974) Isolation and properties of an esterase isozyme of rat serum. Histochem J 6:369–382

    Google Scholar 

  • Deimling O von, de Looze SM (1983) Human red cell butyrylesterase, and its homologies in thirteen other mammalian species. Hum Genet 63:241–246

    Google Scholar 

  • Deimling O von, Müller M, Eisenhardt E (1983) The non-specific esterases of mouse lung. Histochemistry 78:271–284

    Google Scholar 

  • de Looze SM, Ronai A, Deimling O von (1982) Organ-specific expression of esterase-6 in the house mouse, Mus musculus. Histochemistry 74:553–561

    Google Scholar 

  • de Looze SM, Ronai A, Deimling O von (1985) Biochemistry and genetics of esterase-20 (ES-20), a second trimeric carboxylesterase of the house mouse (Mus musculus). I — Purification and characterization of ES-20C1 from male kidney. Biochem Genet (in press)

  • George JC, Ambadkar PM (1963) Histochemical demonstration of lipids and lipase activity in rat testis. J Histochem Cytochem 11:420–425

    Google Scholar 

  • Goldberg E (1977) Isozymes in testes and spermatozoa. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes: current topics in biological and medical research, vol 1. Alan R Liss, New York, pp 79–124

    Google Scholar 

  • Göppinger A, Riebschläger M, Ronai A, Deimling O von (1978) Esterase XXVII. Purification and characterization of esterase-9A of mouse kidney. Biochim Biophys Acta 525:74–86

    Google Scholar 

  • Gomori G (1946) Distribution of lipase in the tissues under normal and pathologic conditions. Arch Pathol 41:121–129

    Google Scholar 

  • Hayashi M, Ogata K, Shiraogawa T, Murakami Z, Tuneishi S (1958) The effect of unilateral and bilateral cryptorchidisms upon the activites of β-glucuronidase, lipase and esterase in the rat testis. Acta Pathol Jpn 8:113–126

    Google Scholar 

  • Hermes B, Riebschläger M Deimling O von (1975) Esterase XX. Diskelektrophoretische Untersuchungen zum Polymorphismus der Esterasen der Hausmaus. Histochemistry 43:81–96

    Google Scholar 

  • Hitzeman JW (1962) Development of enzyme activity in the Leydig cells of the mouse testis. Anat Rec 143:351–361

    Google Scholar 

  • Holmes RS, Masters CJ (1967) The developmental multiplicity and isoenzyme status of rat esterases. Biochim Biophys Acta 146:138–150

    Google Scholar 

  • Huggins JG, Moulton SH (1948) Esterases of testis and other tissues. J Exp Med 88:169–179

    Google Scholar 

  • IUB (International Union of Biochemistry) Nomenclature Committee (1979) Enzyme nomenclature 1978. Academic Press, New York

    Google Scholar 

  • Jimenez-Marin D (1974) Enzyme inheritance in the laboratory rat. J Hered 65:235–237

    Google Scholar 

  • Kendall PB (1983) The genetics of esterase 12 and esterase 13 polymorphisms in the Norway rat. Lab Anim 17:221–224

    Google Scholar 

  • Lagnado JR, Hardy M (1967) Brain esterases during development. Nature 214:1207–1210

    Google Scholar 

  • Lexow U, Ronai A, Deimling O von (1980) Purification and characterization of esterase-2B of the house mouse, Mus musculus. Eur J Biochem 107:123–130

    Google Scholar 

  • Lipps A, Ronai A, Deimling O von (1979) Esterase-7, a common constituent of numerous mouse tissues. Comp Biochem Physiol 62B:201–226

    Google Scholar 

  • Lyon MF, Hawkes SG (1970) X-linked gene for testicular feminization in the mouse. Nature 227:1217–1219

    Google Scholar 

  • Markert CM, Hunter RL, (1959) The distribution of esterases in mouse tissue J Histochem Cytochem 7:42–49

    Google Scholar 

  • Masters J, Holmes S (1972) Isoenzymes and ontogeny. Bio Rev 47:309–361

    Google Scholar 

  • Matsumoto K (1980) New polymorphisms of esterase 7 and esterase 8 in inbred strains of rats tissue expression and linkage studies Biochem Genet 18:887–879

    Google Scholar 

  • Mentlein R, Heiland S, Heymann E (1980) Simultaneous purification and comparative characterization of six serine hydrolases from rat liver microsomes. Arch Biochem Biophys 200:547–559

    Google Scholar 

  • Meyer EHH, Forsgren K, Deimling, O von, Engel W (1974) Esterase XVI. Induction of nonspecific carboxyl esterase in the immature rat testis by human chorionic gonatrophin. Endocrinology 95:1737–1739

    Google Scholar 

  • Moutier R, Toyama K Charrier MF (1973a) Evidence for linkage between four esterase loci in the rat (Rattus norvegicus). Biochem Genet 9:109–115

    Google Scholar 

  • Moutier R, Toyama K, Charrier MF (1973b) Biochemical polymorphism in the rat Rattus norvegicus: Genetic study of four markers. Biochem Genet 8:321–328

    Google Scholar 

  • Münz M, Deimling O von (1985) Electrophoretic characterization of esterase-19 (ES-19) a new arylesterase of the house mouse (Mus musculus). Electrophoresis (in press)

  • Nachlas MM, Seligman AM (1949) The comparative distribution of esterase in the tissues of 5 mammals by a histochemical technique. Anat Rec 105:677–695

    Google Scholar 

  • Nash HR, Deimling O von (1982) Kidney esterase of Mus musculus: Further polymorphism of esterase-6, esterase-9, and a new esterase, esterase-20. Biochem Genet 20:537–554

    Google Scholar 

  • Niemi M, Kormano M (1965) Histochemical demonstration of a C-esterase activity in the seminiferous tubules of the rat testis. J Reprod Fertil 10:49–54

    Google Scholar 

  • Niemi M, Härkönen M, Kokko A (1962) Localization and identification of testicular esterases in the rat. J Histochem Cytochem 10:186–193

    Google Scholar 

  • Niemi M, Härkönen M, Ikonen M (1966) A chemical and histochemical study on the significance of the nonspecific esterase activity in the adult rat testis. Endocrinology 79:294–300

    Google Scholar 

  • Ochm HC, de Looze S, Ronai A, Deimling O von (1982) Purification and characterization of esterase 6A, a trimeric esterase of the house mouse (Mus musculus). Eur J Biochem 129: 157–163

    Google Scholar 

  • Otto J, Deimling O von (1983) Esterase-17 (ES-17): Characterization and linkage to chromosome 9 of a new bis-p-nitrophenyl phosphate resistant esterase of the house mouse (Mus musculus). Biochem Genet 21:37–48

    Google Scholar 

  • Otto J, Ronai A, Deimling O von (1981) Purification and characterization of esterase-1F, the albumin esterase of the house mouse (Mus musculus). Eur J Biochem 116:285–291

    Google Scholar 

  • Peters J (1982) Nonspecific esterases of Mus musculus. Biochem Genet 20:585–606

    Google Scholar 

  • Petras ML (1963) Genetic control of a serum esterase component in Mus musculus. Proc Natl Acad Sci USA 50:112–116

    Google Scholar 

  • Petras ML, Sinclair P (1969) Another esterase variant in the kidney of the house mouse, Mus musculus. Can J Genet Cytol 11:97–102

    Google Scholar 

  • Popp RA, Popp DM (1962) Inheritance of serum esterases having different electrophoretic patterns. J Hered 53:111–114

    Google Scholar 

  • Popp RA, Heddel JG, Canning RE, Allen RC (1966) Some physical and chemical properties of albumin esterase and albumin from mouse serum. Biochim Biophys Acta 115:113–120

    Google Scholar 

  • Reissenweber NJ (1970) Histochemical study of isolated intratubular cells of the rat testis. I. Hydrolases and phosphorylase. Histochemie 21:73–83

    Google Scholar 

  • Risley PL, Skrepetos CN (1964) Histochemical distribution of cholin-esterase in the testis, epididymis and vas deferens of the rat. Anat Rec 148:231–241

    Google Scholar 

  • Rommerts FFG, Doorn LG van, Galjaard H, Cooke BA, Molen HJ van der (1973) Dissection of wet tissue and of freeze-dried sections in the investigation of seminiferous tubules and interstitial tissue from rat testis. J Histochem Cytochem 21:572–579

    Google Scholar 

  • Ruddle FH, Harrington L (1967) Tissue specific esterase isozymes of the mouse (Mus musculus). J Exp Zool 166:51–64

    Google Scholar 

  • Ruddle F, Roderick T (1965) The genetic control of three kidney esterase in C57BL/6J and RF/J mice. Genetics 51:445–454

    Google Scholar 

  • Sakai Y, Yamamoto N, Yasuda K (1979) Localization of nonspecific esterase in the testis. Acta Histochem Cytochem (Kyoto) 12:620–621

    Google Scholar 

  • Santamaria L, Nistal M (1983) Las esterasas inspecificas del testiculo de rata: Localization y patrones histoquimicos frente a diversos sustratos e inhibidores. Morfologia Normal y Patológica Sec A 7:417–425

    Google Scholar 

  • Schnelle V, Madden R, Rivenson A (1983) Demonstration on non-specific esterase activity in normal and neoplastic mouse Leydig cells. Histochem J 15:715–719

    Google Scholar 

  • Schollen J, Bender K, Deimling O von (1975) Esterase XXI. ES-9, a possibly new polymorphic esterase in Mus musculus genetically linked to Es-2. Biochem Genet 13:369–377

    Google Scholar 

  • Scholze M, Günther E, Deimling O von (1984) Esterase-13 of the rat (Rattus norvegicus) and its homology with esterase-3 of the house mouse (Mus musculus). Comp Biochem Physiol 78B:713–718

    Google Scholar 

  • Schumacher M, Schäfer G, Holstein AF, Hilz H (1978) Rapid isolation of mouse Leydig cells by centrifugation in Percoll density gradients with complete retention of morphological and biochemical intergrity. FEBS Lett 91:333–338

    Google Scholar 

  • Simon B (1985) personal communication

  • Van Zutphen B (1983) Revision of the genetic nomenclature of esterase loci in the rat (Rattus norvegicus). Transplant Proceed 15:1687–1688

    Google Scholar 

  • Verne J, Hebert S (1952) L'activité estérasique des cellules interstitielle du testicule et de l'épididyme chez le rat. Ann Endocrinol 13:924–930

    Google Scholar 

  • Wachstein M, Meisel E, Falcon C (1961) Histochemistry of thiolacetic acid esterase: a comparison with nonspecific esterase with special regard to the effect of fixatives and inhibitors on intracellular localization. J Histochem 9:325–339

    Google Scholar 

  • Womack JE (1972) Genetic control of the major electrophoretic component of rat plasma esterase. J Hered 63:41–42

    Google Scholar 

  • Womack JE, Sharp M (1976) Comparative autosomal linkage in mammals: genetics of esterases in Mus musculus and Rattus norvegicus. Genetics 82:665–675

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemical Pathology, University of Freiburg, Albertstrasse 19, D-7800, Freiburg im Breisgau, Federal Republic of Germany

    O. von Deimling, A. Ronai & S. de Looze

Authors
  1. O. von Deimling
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Ronai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. de Looze
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This is communication no. 47 of a research program devoted to the cellular distribution, genetics, and regulation of nonspeific esterases. This work was supported by the Dcutsche Forschungsgemeinschaft

Rights and permissions

Reprints and permissions

About this article

Cite this article

von Deimling, O., Ronai, A. & de Looze, S. Nonspecific esterases of mammalian testis. Histochemistry 82, 547–555 (1985). https://doi.org/10.1007/BF00489976

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00489976

Keywords

Search

Navigation