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Published in: Brain Structure and Function 3/2006

01-06-2006 | Original Article

Mitotic activity of Sertoli cells in adult human testis: an immunohistochemical study to characterize Sertoli cells in testicular cords from patients showing testicular dysgenesis syndrome

Authors: Ralph Brehm, Rodolfo Rey, Sabine Kliesch, Klaus Steger, Alexander Marks, Martin Bergmann

Published in: Brain Structure and Function | Issue 3/2006

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Abstract

During puberty, normal somatic Sertoli cells undergo dramatic morphological changes due to the differentiation of immature pre-Sertoli cells in functionally active adult Sertoli cells. Sertoli cell maturation is accompanied with loss of their mitotic activity before onset of spermatogenesis and loss of pre-pubertal and occurrence of adult immunohistochemical Sertoli cell differentiation markers. Testes of infertile adult patients often exhibit numerous histological signs of testicular dysgenesis syndrome (TDS) such as microliths, Sertoli cell only (SCO) tubules, tubules containing carcinoma in situ and immature seminiferous tubules (Sertoli cell nodules). Sertoli cell tumours, however, are very rare neoplasms possibly due to the fact that the mechanism and temporal origin of neoplastic Sertoli cells underlying Sertoli cell tumourigenesis still remain unknown. To clarify the state of Sertoli cell differentiation in both immature seminiferous tubules of adult patients with TDS and Sertoli cell tumour, we compared the expression of the Sertoli cell differentiation markers vimentin, inhibin-α, anti-Muellerian-hormone, cytokeratin 18, M2A-antigen, androgen receptor and connexin43 with that of SCO tubules with hyperplasia. In addition, we demonstrated for the first time the existence of proliferating Sertoli cells by Ki67- and PCNA-immunostaining in Sertoli cell nodules of the adult human testis. Our data indicate that mitotically active Sertoli cells in Sertoli cell nodules will be arrested prior to puberty and, contrary to dogma, do not represent foetal or neonatal cells. Since all markers in Sertoli cell nodules revealed a staining pattern identical to that in neoplastic Sertoli cells, but different to that in Sertoli cells of SCO tubules with hyperplasia, it may be speculated that Sertoli cell tumours in adult men may originate from Sertoli cell nodules.
Literature
go back to reference Al-Attar L, Noel K, Dutertre M, Belville C, Forrest MG, Burgoyne PS, Josso N, Rey R (1997) Hormonal and cellular regulation of Sertoli cell anti-Mullerian hormone production in the postnatal mouse. J Clin Invest 100:1335–1343PubMedCrossRef Al-Attar L, Noel K, Dutertre M, Belville C, Forrest MG, Burgoyne PS, Josso N, Rey R (1997) Hormonal and cellular regulation of Sertoli cell anti-Mullerian hormone production in the postnatal mouse. J Clin Invest 100:1335–1343PubMedCrossRef
go back to reference Anderson RA, Cambray N, Hartley PS, McNeilly AS (2002) Expression and localization of inhibin-α, inhibin/activin βA and βB and the activin type II inhibin β-glycan receptors in the developing human testis. Reproduction 123:779–788CrossRefPubMed Anderson RA, Cambray N, Hartley PS, McNeilly AS (2002) Expression and localization of inhibin-α, inhibin/activin βA and βB and the activin type II inhibin β-glycan receptors in the developing human testis. Reproduction 123:779–788CrossRefPubMed
go back to reference Andersson AM, Toppari J, Haavisto AM, Petersen JH, Simell T, Simell O, Skakkebaek NE (1998) Longitudinal reproductive hormone profiles in infants: peak of inhibin B Levels in infant boys exceeds levels in adult men. J Clin Endocrinol Metab 83:675–681CrossRefPubMed Andersson AM, Toppari J, Haavisto AM, Petersen JH, Simell T, Simell O, Skakkebaek NE (1998) Longitudinal reproductive hormone profiles in infants: peak of inhibin B Levels in infant boys exceeds levels in adult men. J Clin Endocrinol Metab 83:675–681CrossRefPubMed
go back to reference Aumüller G, Steinbrück M, Krause W, Wagner HJ (1988) Distribution of vimentin-type intermediate filaments in Sertoli cells of the human testis, normal and pathologic. Anat Embryol 178:129–136PubMedCrossRef Aumüller G, Steinbrück M, Krause W, Wagner HJ (1988) Distribution of vimentin-type intermediate filaments in Sertoli cells of the human testis, normal and pathologic. Anat Embryol 178:129–136PubMedCrossRef
go back to reference Aumüller G, Schulze C, Viehbahn C (1992) Intermediate filaments in Sertoli cells. Micros Res Tech 20:50–72CrossRef Aumüller G, Schulze C, Viehbahn C (1992) Intermediate filaments in Sertoli cells. Micros Res Tech 20:50–72CrossRef
go back to reference Bailey D, Baumal R, Law J, Sheldon K, Kannampuzha P, Stratis M, Kahn H, Marks A (1986) Production of a monoclonal antibody specific for seminomas and dysgerminomas. Proc Natl Acad Sci USA 83:5291–5295PubMedCrossRef Bailey D, Baumal R, Law J, Sheldon K, Kannampuzha P, Stratis M, Kahn H, Marks A (1986) Production of a monoclonal antibody specific for seminomas and dysgerminomas. Proc Natl Acad Sci USA 83:5291–5295PubMedCrossRef
go back to reference Baumal R, Bailey D, Giwercman A, Skakkebaek NE, Stratis M, Marks A (1989) A novel maturation marker for human Sertoli cells. Int J Androl 12:354–359PubMedCrossRef Baumal R, Bailey D, Giwercman A, Skakkebaek NE, Stratis M, Marks A (1989) A novel maturation marker for human Sertoli cells. Int J Androl 12:354–359PubMedCrossRef
go back to reference Behringer RR, Finegold MJ, Cate RL (1994) Mullerian-inhibiting substance function during mammalian sexual development. Cell 79:415–425CrossRefPubMed Behringer RR, Finegold MJ, Cate RL (1994) Mullerian-inhibiting substance function during mammalian sexual development. Cell 79:415–425CrossRefPubMed
go back to reference Berensztein EB, Sciara MI, Rivarola MA, Belgorosky A (2002) Apoptosis and proliferation of human testicular somatic and germ cells during prepuberty: high rate of testicular growth in newborns mediated by decreased apoptosis. J Clin Endocrinol Metab 87:5113–5118CrossRefPubMed Berensztein EB, Sciara MI, Rivarola MA, Belgorosky A (2002) Apoptosis and proliferation of human testicular somatic and germ cells during prepuberty: high rate of testicular growth in newborns mediated by decreased apoptosis. J Clin Endocrinol Metab 87:5113–5118CrossRefPubMed
go back to reference Bergmann M, Kliesch S (1998) Hodenbiopsie. In: Krause W, Weidner W (eds) Andrologie: Krankheiten der männlichen Geschlechtsorgane. Enke Verlag, Stuttgart, pp 66–71 Bergmann M, Kliesch S (1998) Hodenbiopsie. In: Krause W, Weidner W (eds) Andrologie: Krankheiten der männlichen Geschlechtsorgane. Enke Verlag, Stuttgart, pp 66–71
go back to reference Blagosklonova O, Joanne C, Roux C, Bittard H, Fellmann F, Bresson JL (2002) Absence of anti-Müllerian hormone (AMH) and M2A immunoreactivities in Sertoli cell-only syndrome and maturation arrest with and without AZF microdeletions. Hum Reprod 17:2062–2065CrossRefPubMed Blagosklonova O, Joanne C, Roux C, Bittard H, Fellmann F, Bresson JL (2002) Absence of anti-Müllerian hormone (AMH) and M2A immunoreactivities in Sertoli cell-only syndrome and maturation arrest with and without AZF microdeletions. Hum Reprod 17:2062–2065CrossRefPubMed
go back to reference Brehm R, Marks A, Rey R, Kliesch S, Bergmann M, Steger K (2002) Altered expression of connexins 26 and 43 in Sertoli cells in seminiferous tubules infiltrated with carcinoma-in-situ or seminoma. J Pathol 197:647–653CrossRefPubMed Brehm R, Marks A, Rey R, Kliesch S, Bergmann M, Steger K (2002) Altered expression of connexins 26 and 43 in Sertoli cells in seminiferous tubules infiltrated with carcinoma-in-situ or seminoma. J Pathol 197:647–653CrossRefPubMed
go back to reference Cazorla O, Seck M, Pisselet C, Perreau C, Saumande J, Fontaine J, de Reviers M, Hochereau-de Reviers MT (1998) Anti-Mullerian hormone (AMH) secretion in prepubertal and adult rams. J Reprod Fertil 112:259–266PubMedCrossRef Cazorla O, Seck M, Pisselet C, Perreau C, Saumande J, Fontaine J, de Reviers M, Hochereau-de Reviers MT (1998) Anti-Mullerian hormone (AMH) secretion in prepubertal and adult rams. J Reprod Fertil 112:259–266PubMedCrossRef
go back to reference Cheville JC (1999) Classification and pathology of testicular germ cell and sex cord-stromal tumours. Urol Clin North Am 26:595–609CrossRefPubMed Cheville JC (1999) Classification and pathology of testicular germ cell and sex cord-stromal tumours. Urol Clin North Am 26:595–609CrossRefPubMed
go back to reference Comperat E, Tissier F, Boye K, de Pinieux G, Vieillefond A (2004) Non-Leydig sex-cord tumours of the testis. The place of immunohistochemistry in diagnosis and prognosis. A study of twenty cases. Virchows Arch 444:567–571PubMedCrossRef Comperat E, Tissier F, Boye K, de Pinieux G, Vieillefond A (2004) Non-Leydig sex-cord tumours of the testis. The place of immunohistochemistry in diagnosis and prognosis. A study of twenty cases. Virchows Arch 444:567–571PubMedCrossRef
go back to reference Cortes D, Müller J, Skakkebaek NE (1987) Proliferation of Sertoli cells during development of the human testis assessed by stereological methods. Int J Androl 10:589–596PubMedCrossRef Cortes D, Müller J, Skakkebaek NE (1987) Proliferation of Sertoli cells during development of the human testis assessed by stereological methods. Int J Androl 10:589–596PubMedCrossRef
go back to reference Costa MJ, Morris RJ, Wilson R, Judd R (1992) Utility of immunohistochemistry in distinguishing ovarian sertoli-stromal cell tumours from carcinosarcomas. Hum Pathol 23:787–797CrossRefPubMed Costa MJ, Morris RJ, Wilson R, Judd R (1992) Utility of immunohistochemistry in distinguishing ovarian sertoli-stromal cell tumours from carcinosarcomas. Hum Pathol 23:787–797CrossRefPubMed
go back to reference Dutertre M, Rey R, Porteu A, Josso N, Picard JY (1997) A mouse Sertoli cell line expressing anti-Müllerian hormone and its type II receptor. Mol Cell Endocrinol 136:57–65CrossRefPubMed Dutertre M, Rey R, Porteu A, Josso N, Picard JY (1997) A mouse Sertoli cell line expressing anti-Müllerian hormone and its type II receptor. Mol Cell Endocrinol 136:57–65CrossRefPubMed
go back to reference Fenichel P, Rey R, Poggioli S, Donzeau M, Chevallier D, Pointis G (1999) Anti-Mullerian hormone as a seminal marker for spermatogenesis in non-obstructive azoospermia. Hum Reprod 14:2020–2024CrossRefPubMed Fenichel P, Rey R, Poggioli S, Donzeau M, Chevallier D, Pointis G (1999) Anti-Mullerian hormone as a seminal marker for spermatogenesis in non-obstructive azoospermia. Hum Reprod 14:2020–2024CrossRefPubMed
go back to reference Franke WW, Grund C, Schmidt E (1979) Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 19:269–275PubMed Franke WW, Grund C, Schmidt E (1979) Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 19:269–275PubMed
go back to reference Franke FE, Pauls K, Rey R, Marks A, Bergmann M, Steger K (2004) Differentiation markers of Sertoli cells and germ cells in fetal and early postnatal human testis. Anat Embryol 209:169–177PubMed Franke FE, Pauls K, Rey R, Marks A, Bergmann M, Steger K (2004) Differentiation markers of Sertoli cells and germ cells in fetal and early postnatal human testis. Anat Embryol 209:169–177PubMed
go back to reference Froland A, Skakkebaek NE (1971) Dimorphism in sex chromatin pattern of Sertoli cells in adults with Klinefelter’s syndrome: correlation with two types of “Sertoli-cell-only” tubules. J Clin Endocrinol Metab 33:683–687PubMedCrossRef Froland A, Skakkebaek NE (1971) Dimorphism in sex chromatin pattern of Sertoli cells in adults with Klinefelter’s syndrome: correlation with two types of “Sertoli-cell-only” tubules. J Clin Endocrinol Metab 33:683–687PubMedCrossRef
go back to reference Gaskell TL, Esnal A, Robinson LL, Anderson RA, Saunders PT (2004) Immunohistochemical profiling of germ cells within the human fetal testis: identification of three subpopulations. Biol Reprod 71:2012–2021CrossRefPubMed Gaskell TL, Esnal A, Robinson LL, Anderson RA, Saunders PT (2004) Immunohistochemical profiling of germ cells within the human fetal testis: identification of three subpopulations. Biol Reprod 71:2012–2021CrossRefPubMed
go back to reference Gilcrease MZ, Delgado R, Albores-Saavedra J (1998) Testicular Sertoli cell tumour with a heterologous sarcomatous component: immunohistochemical assessment of Sertoli cell differentiation. Arch Pathol Lab Med 122:907–911PubMed Gilcrease MZ, Delgado R, Albores-Saavedra J (1998) Testicular Sertoli cell tumour with a heterologous sarcomatous component: immunohistochemical assessment of Sertoli cell differentiation. Arch Pathol Lab Med 122:907–911PubMed
go back to reference Giwercman A, Kledal T, Schwartz M, Giwercman YL, Leffers H, Zazzi H, Wedell A, Skakkebaek NE (2000) Preserved male fertility despite decreased androgen sensitivity caused by a mutation in the ligand-binding domain of the androgen receptor gene. J Clin Endocrinol Metab 85:2253–2259CrossRefPubMed Giwercman A, Kledal T, Schwartz M, Giwercman YL, Leffers H, Zazzi H, Wedell A, Skakkebaek NE (2000) Preserved male fertility despite decreased androgen sensitivity caused by a mutation in the ligand-binding domain of the androgen receptor gene. J Clin Endocrinol Metab 85:2253–2259CrossRefPubMed
go back to reference Gondos B, Berndston WE (1993) Postnatal, pubertal development In: Griswold MD, Russell LD (eds) The Sertoli cell. Cache River Press, Clearwater, pp 115–154 Gondos B, Berndston WE (1993) Postnatal, pubertal development In: Griswold MD, Russell LD (eds) The Sertoli cell. Cache River Press, Clearwater, pp 115–154
go back to reference Govender D, Sing Y, Chetty R (2004) Sertoli cell nodules in the undescended testis: a histochemical, immunohistochemical, and ultrastructural study of hyaline deposits. J Clin Pathol 57:802–806CrossRefPubMed Govender D, Sing Y, Chetty R (2004) Sertoli cell nodules in the undescended testis: a histochemical, immunohistochemical, and ultrastructural study of hyaline deposits. J Clin Pathol 57:802–806CrossRefPubMed
go back to reference Hadziselimovic F (1977) Cryptorchidism. Ultrastructure of normal and cryptorchid testis development. Adv Anat Embryol Cell Biol 53:3–71PubMed Hadziselimovic F (1977) Cryptorchidism. Ultrastructure of normal and cryptorchid testis development. Adv Anat Embryol Cell Biol 53:3–71PubMed
go back to reference Halley JBW (1963) The growth of Sertoli cell tumours: a positive index of differential gonadotropin activity in the male. J Urol 90:220–229PubMed Halley JBW (1963) The growth of Sertoli cell tumours: a positive index of differential gonadotropin activity in the male. J Urol 90:220–229PubMed
go back to reference Hedinger CE, Huber R, Weber E (1967) Frequency of so-called hypoplastic or dysgenetic zones in scrotal and otherwise normal human testes. Virchows Arch Path Anat 342:165–168CrossRef Hedinger CE, Huber R, Weber E (1967) Frequency of so-called hypoplastic or dysgenetic zones in scrotal and otherwise normal human testes. Virchows Arch Path Anat 342:165–168CrossRef
go back to reference Henley JD, Young RH, Ulbright TM (2002) Malignant Sertoli cell tumours of the testis: a study of 13 examples of a neoplasm frequently misinterpreted as seminoma. Am J Surg Pathol 26:541–550CrossRefPubMed Henley JD, Young RH, Ulbright TM (2002) Malignant Sertoli cell tumours of the testis: a study of 13 examples of a neoplasm frequently misinterpreted as seminoma. Am J Surg Pathol 26:541–550CrossRefPubMed
go back to reference Hoei-Hansen CE, Holm M, Rajpert-De Meyts E, Skakkebaek NE (2003) Histological evidence of testicular dysgenesis in contralateral biopsies of 218 patients with testicular germ cell cancer. J Pathol 200:370–374CrossRefPubMed Hoei-Hansen CE, Holm M, Rajpert-De Meyts E, Skakkebaek NE (2003) Histological evidence of testicular dysgenesis in contralateral biopsies of 218 patients with testicular germ cell cancer. J Pathol 200:370–374CrossRefPubMed
go back to reference Hofmann MC, Narisawa S, Hess RA, Millan JL (1992) Immortalization of germ cells and somatic testicular cells using the SV40 large T Antigen. Exp Cell Res 201:417–435CrossRefPubMed Hofmann MC, Narisawa S, Hess RA, Millan JL (1992) Immortalization of germ cells and somatic testicular cells using the SV40 large T Antigen. Exp Cell Res 201:417–435CrossRefPubMed
go back to reference Iczkowski KA, Bostwick DG, Roche PC, Cheville JC (1998) Inhibin A is a sensitive and specific marker for testicular sex cord-stromal tumours. Mod Pathol 11:774–779PubMed Iczkowski KA, Bostwick DG, Roche PC, Cheville JC (1998) Inhibin A is a sensitive and specific marker for testicular sex cord-stromal tumours. Mod Pathol 11:774–779PubMed
go back to reference Jorgensen N, Rajpert-De Meyts E, Graem N, Muller J, Giwercman A, Skakkebaek NE (1995) Expression of immunohistochemical markers for testicular carcinoma in situ by normal human fetal germ cells. Lab Invest 72:223–231PubMed Jorgensen N, Rajpert-De Meyts E, Graem N, Muller J, Giwercman A, Skakkebaek NE (1995) Expression of immunohistochemical markers for testicular carcinoma in situ by normal human fetal germ cells. Lab Invest 72:223–231PubMed
go back to reference Josso N, Lamarre I, Picard JY, Berta P, Davies N, Morichon N, Peschanski M, Jeny R (1993) Anti-Müllerian hormone in early human development. Early Hum Dev 33:91–99CrossRefPubMed Josso N, Lamarre I, Picard JY, Berta P, Davies N, Morichon N, Peschanski M, Jeny R (1993) Anti-Müllerian hormone in early human development. Early Hum Dev 33:91–99CrossRefPubMed
go back to reference Kahn HJ, Bailey D, Marks A (2002) Monoclonal antibody D2-40, a new marker of lymphatic endothelium, reacts with Kaposi`s sarcoma and a subset of angiosarcomas. Mod Pathol 15:434–440CrossRefPubMed Kahn HJ, Bailey D, Marks A (2002) Monoclonal antibody D2-40, a new marker of lymphatic endothelium, reacts with Kaposi`s sarcoma and a subset of angiosarcomas. Mod Pathol 15:434–440CrossRefPubMed
go back to reference Kommoss F, Oliva E, Bittinger F, Kirkpatrick CJ, Amin MB, Bhan AK, Young RH, Scully RE (2000) Inhibin-α, CD99, HEA125, PLAP, and Chromogranin immunoreactivity in testicular neoplasms and the androgen insensitivity syndrome. Hum Pathol 31:1055–1061CrossRefPubMed Kommoss F, Oliva E, Bittinger F, Kirkpatrick CJ, Amin MB, Bhan AK, Young RH, Scully RE (2000) Inhibin-α, CD99, HEA125, PLAP, and Chromogranin immunoreactivity in testicular neoplasms and the androgen insensitivity syndrome. Hum Pathol 31:1055–1061CrossRefPubMed
go back to reference Kratzer SS, Ulbright TM, Talerman A, Srigley JR, Roth LM, Wahle GR, Moussa M, Stephens JK, Millos A, Young RH (1997) Large cell calcifying Sertoli cell tumour of the testis. Contrasting features of six malignant and six benign tumours and a review of the literature. Am J Surg Pathol 21:1271–1280CrossRefPubMed Kratzer SS, Ulbright TM, Talerman A, Srigley JR, Roth LM, Wahle GR, Moussa M, Stephens JK, Millos A, Young RH (1997) Large cell calcifying Sertoli cell tumour of the testis. Contrasting features of six malignant and six benign tumours and a review of the literature. Am J Surg Pathol 21:1271–1280CrossRefPubMed
go back to reference Kuroda N, Senzaki T, Yamasaki Y, Miyazaki E, Hayashi Y, Toi M, Hiroi M, Enzan H (2004) Sertoli cell tumour of the testis (not otherwise specified) with the expression of neuroendocrine markers and without the expression of inhibin-alpha. Pathol Int 54:719–724CrossRefPubMed Kuroda N, Senzaki T, Yamasaki Y, Miyazaki E, Hayashi Y, Toi M, Hiroi M, Enzan H (2004) Sertoli cell tumour of the testis (not otherwise specified) with the expression of neuroendocrine markers and without the expression of inhibin-alpha. Pathol Int 54:719–724CrossRefPubMed
go back to reference Lawrence WD, Young RH, Scully RE (1986) Sex cord-stromal tumours. In: Talerman A, Roth LM (eds) Pathology of the testis and its adnexa. Churchill Livingstone, New York, pp 67–92 Lawrence WD, Young RH, Scully RE (1986) Sex cord-stromal tumours. In: Talerman A, Roth LM (eds) Pathology of the testis and its adnexa. Churchill Livingstone, New York, pp 67–92
go back to reference Lee MM, Donahoe PK (1993) Mullerian inhibiting substance: a gonadal hormone with multiple functions. Endocr Rev 14:152–164CrossRefPubMed Lee MM, Donahoe PK (1993) Mullerian inhibiting substance: a gonadal hormone with multiple functions. Endocr Rev 14:152–164CrossRefPubMed
go back to reference Majdic G, McNeilly AS, Sharpe RM, Evans LR, Groome NP, Saunders PT (1997) Testicular expression of inhibin and activin subunits and follistatin in the rat and human fetus and neonate and during postnatal development in the rat. Endocrinology 138:2136–2147CrossRefPubMed Majdic G, McNeilly AS, Sharpe RM, Evans LR, Groome NP, Saunders PT (1997) Testicular expression of inhibin and activin subunits and follistatin in the rat and human fetus and neonate and during postnatal development in the rat. Endocrinology 138:2136–2147CrossRefPubMed
go back to reference Maric S, Bulic-Jakus F, Jezek D, Juric-Lekic G, Kos M, Vlahovic M (2004) Expression of the proliferating cell nuclear antigen and protein products of tumour suppressor genes in the human foetal testis. Andrologia 36:24–30CrossRefPubMed Maric S, Bulic-Jakus F, Jezek D, Juric-Lekic G, Kos M, Vlahovic M (2004) Expression of the proliferating cell nuclear antigen and protein products of tumour suppressor genes in the human foetal testis. Andrologia 36:24–30CrossRefPubMed
go back to reference Marks A, Sutherland DR, Bailey D, Iglesias J, Law J, Lei M, Yeger H, Banerjee D, Baumal R (1999) Characterization and distribution of an oncofetal antigen (M2A antigen) expressed on testicular germ cell tumours. Br J Cancer 80:569–578CrossRefPubMed Marks A, Sutherland DR, Bailey D, Iglesias J, Law J, Lei M, Yeger H, Banerjee D, Baumal R (1999) Characterization and distribution of an oncofetal antigen (M2A antigen) expressed on testicular germ cell tumours. Br J Cancer 80:569–578CrossRefPubMed
go back to reference Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A (1992) Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360:313–319PubMedCrossRef Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A (1992) Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360:313–319PubMedCrossRef
go back to reference Matzuk MM, Finegold MJ, Mishina Y, Bradley A, Behringer RR (1995) Synergistic effects of inhibins and muellerian-inhibiting substance on testicular tumourigenesis. Mol Endocrinol 9:1337–1345CrossRefPubMed Matzuk MM, Finegold MJ, Mishina Y, Bradley A, Behringer RR (1995) Synergistic effects of inhibins and muellerian-inhibiting substance on testicular tumourigenesis. Mol Endocrinol 9:1337–1345CrossRefPubMed
go back to reference Maymon BB, Yogev L, Yavetz H, Lifschitz-Mercer B, Schreiber L, Kleiman SE, Botchan A, Hauser R, Paz G (2003) Spermatogonial proliferation patterns in men with azoospermia of different etiologies. Fertil Steril 80:1175–1180CrossRefPubMed Maymon BB, Yogev L, Yavetz H, Lifschitz-Mercer B, Schreiber L, Kleiman SE, Botchan A, Hauser R, Paz G (2003) Spermatogonial proliferation patterns in men with azoospermia of different etiologies. Fertil Steril 80:1175–1180CrossRefPubMed
go back to reference McCluggage WG, Shanks JH, Whiteside C, Maxwell P, Banerjee SS, Biggart JD (1998) Immunohistochemical study of testicular sex cord-stromal tumours, including staining with anti-inhibin antibody. Am J Surg Pathol 22:615–619CrossRefPubMed McCluggage WG, Shanks JH, Whiteside C, Maxwell P, Banerjee SS, Biggart JD (1998) Immunohistochemical study of testicular sex cord-stromal tumours, including staining with anti-inhibin antibody. Am J Surg Pathol 22:615–619CrossRefPubMed
go back to reference McKinnell C, Saunders PTK, Fraser HM, Kelnar CJH, Kivlin C, Morris KD, Sharpe RM (2001) Comparison of androgen receptor and oestrogen receptor β immunoexpression in the testes of the common marmoset (Callithrix jacchus) from birth to adulthood: low androgen receptor immunoexpression in Sertoli cells during the neonatal increase in testosterone concentrations. Reproduction 122:419–429CrossRefPubMed McKinnell C, Saunders PTK, Fraser HM, Kelnar CJH, Kivlin C, Morris KD, Sharpe RM (2001) Comparison of androgen receptor and oestrogen receptor β immunoexpression in the testes of the common marmoset (Callithrix jacchus) from birth to adulthood: low androgen receptor immunoexpression in Sertoli cells during the neonatal increase in testosterone concentrations. Reproduction 122:419–429CrossRefPubMed
go back to reference Murray TJ, Fowler PA, Abramovich DR, Haites N, Lea RG (2000) Human fetal testis: second trimester proliferative and steroidogenic capacities. J Clin Endocrinol Metab 85:4812–4817CrossRefPubMed Murray TJ, Fowler PA, Abramovich DR, Haites N, Lea RG (2000) Human fetal testis: second trimester proliferative and steroidogenic capacities. J Clin Endocrinol Metab 85:4812–4817CrossRefPubMed
go back to reference Nielsen K, Jacobsen GK (1988) Malignant Sertoli cell tumour of the testis. An immunohistochemical study and a review of the literature. APMIS 96:755–760PubMed Nielsen K, Jacobsen GK (1988) Malignant Sertoli cell tumour of the testis. An immunohistochemical study and a review of the literature. APMIS 96:755–760PubMed
go back to reference Nistal M, Paniagua R, Diez-Pardo JA (1980) Histological classification of undescended testes. Human Pathol 11:666–673CrossRef Nistal M, Paniagua R, Diez-Pardo JA (1980) Histological classification of undescended testes. Human Pathol 11:666–673CrossRef
go back to reference Nistal M, Paniagua R, Abaurrea MA, Santamaria L (1982) Hyperplasia and the immature appearance of Sertoli cells in primary testicular disorders. Hum Pathol 13:3–12PubMedCrossRef Nistal M, Paniagua R, Abaurrea MA, Santamaria L (1982) Hyperplasia and the immature appearance of Sertoli cells in primary testicular disorders. Hum Pathol 13:3–12PubMedCrossRef
go back to reference Paranko J, Kallajoki M, Pelliniemi LJ, Lehto VP, Virtannen I (1986) Transient coexpression of cytokeratin and vimentin in differentiated rat Sertoli cells. Dev Biol 117:34–44 Paranko J, Kallajoki M, Pelliniemi LJ, Lehto VP, Virtannen I (1986) Transient coexpression of cytokeratin and vimentin in differentiated rat Sertoli cells. Dev Biol 117:34–44
go back to reference Pelletier RM (1995) The distribution of connexin 43 is associated with the germ cell differentiation and with the modulation of the Sertoli cell junctional barrier in continual (guinea pig) and seasonal breeders (mink) testes. J Androl 16:400–409PubMed Pelletier RM (1995) The distribution of connexin 43 is associated with the germ cell differentiation and with the modulation of the Sertoli cell junctional barrier in continual (guinea pig) and seasonal breeders (mink) testes. J Androl 16:400–409PubMed
go back to reference Pelletier RM, Byers SW (1992) The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc Res Tech 20:3–33CrossRefPubMed Pelletier RM, Byers SW (1992) The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc Res Tech 20:3–33CrossRefPubMed
go back to reference Pelliniemi LJ, Fröjdman K, Paranko J (1993) Embryological and prenatal development and function of Sertoli cells. In: Griswold MD, Russell LD (eds) The Sertoli cell. Cache River Press, Clearwater, pp 88–113 Pelliniemi LJ, Fröjdman K, Paranko J (1993) Embryological and prenatal development and function of Sertoli cells. In: Griswold MD, Russell LD (eds) The Sertoli cell. Cache River Press, Clearwater, pp 88–113
go back to reference Proppe KH, Scully RE (1980) Large-cell calcifying Sertoli cell tumour of the testis. Am J Clin Pathol 74:607–619PubMed Proppe KH, Scully RE (1980) Large-cell calcifying Sertoli cell tumour of the testis. Am J Clin Pathol 74:607–619PubMed
go back to reference Racine C, Rey R, Forest MG, Louis F, Ferre A, Huhtaniemi I, Josso N, di Clemente N (1998) Receptors for anti-mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci USA 95:594–599CrossRefPubMed Racine C, Rey R, Forest MG, Louis F, Ferre A, Huhtaniemi I, Josso N, di Clemente N (1998) Receptors for anti-mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci USA 95:594–599CrossRefPubMed
go back to reference Rajpert-De Meyts E, Jorgensen N, Graem N, Müller J, Cate RL, Skakkebaek NE (1999) Expression of anti-Müllerian hormone during normal and pathological gonadal development: Association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab 84:3836–3844CrossRefPubMed Rajpert-De Meyts E, Jorgensen N, Graem N, Müller J, Cate RL, Skakkebaek NE (1999) Expression of anti-Müllerian hormone during normal and pathological gonadal development: Association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab 84:3836–3844CrossRefPubMed
go back to reference Regadera J, Martinez-Garcia F, Gonzalez-Peramato P, Serrano A, Nistal M, Suarez-Quian C (2001) Androgen receptor expression in Sertoli cells as a function of seminiferous tubule maturation in the human cryptorchid testis. J Clin Endocrinol Metab 86:413–421CrossRefPubMed Regadera J, Martinez-Garcia F, Gonzalez-Peramato P, Serrano A, Nistal M, Suarez-Quian C (2001) Androgen receptor expression in Sertoli cells as a function of seminiferous tubule maturation in the human cryptorchid testis. J Clin Endocrinol Metab 86:413–421CrossRefPubMed
go back to reference Rey R, Al-Attar L, Louis F, Jaubert F, Barbet P, Nihoul-Felkete C, Chaussain JL, Josso N (1996) Testicular dysgenesis does not affect expression of anti-Müllerian hormone by Sertoli cells in pre-meiotic seminiferous tubules. Am J Pathol 148:1689–1698PubMed Rey R, Al-Attar L, Louis F, Jaubert F, Barbet P, Nihoul-Felkete C, Chaussain JL, Josso N (1996) Testicular dysgenesis does not affect expression of anti-Müllerian hormone by Sertoli cells in pre-meiotic seminiferous tubules. Am J Pathol 148:1689–1698PubMed
go back to reference Rey R, Sabourin JC, Venara M, Long WQ, Jaubert F, Zeller WP, Duvillard P, Chemes H, Bidart JM (2000) Anti-Müllerian hormone is a specific marker of Sertoli- and granulosa cell origin in gonadal tumours. Hum Pathol 31:1202–1208CrossRefPubMed Rey R, Sabourin JC, Venara M, Long WQ, Jaubert F, Zeller WP, Duvillard P, Chemes H, Bidart JM (2000) Anti-Müllerian hormone is a specific marker of Sertoli- and granulosa cell origin in gonadal tumours. Hum Pathol 31:1202–1208CrossRefPubMed
go back to reference Rogatsch H, Jezek D, Hittmair A, Mikuz G, Feichtinger H (1996) Expression of vimentin, cytokeratin, and desmin in Sertoli cells of human fetal, cryptorchid, and tumour-adjacent testicular tissue. Virchows Arch 427:497–502CrossRefPubMed Rogatsch H, Jezek D, Hittmair A, Mikuz G, Feichtinger H (1996) Expression of vimentin, cytokeratin, and desmin in Sertoli cells of human fetal, cryptorchid, and tumour-adjacent testicular tissue. Virchows Arch 427:497–502CrossRefPubMed
go back to reference Sasano H, Nakashima N, Matsuzaki O, Kato H, Aizawa S, Sasano N, Nagura H (1992) Testicular sex cord-stromal lesions. Immunohistochemical analysis of cytokeratin, vimentin and steroidogenic enzymes. Virchows Archiv A Pathol Anat 421:163–169CrossRef Sasano H, Nakashima N, Matsuzaki O, Kato H, Aizawa S, Sasano N, Nagura H (1992) Testicular sex cord-stromal lesions. Immunohistochemical analysis of cytokeratin, vimentin and steroidogenic enzymes. Virchows Archiv A Pathol Anat 421:163–169CrossRef
go back to reference Sharpe RM, McKinnell C, Kivlin C, Fisher JS (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125:769–784CrossRefPubMed Sharpe RM, McKinnell C, Kivlin C, Fisher JS (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125:769–784CrossRefPubMed
go back to reference Skakkebaek NE (1969) Two types of tubules containing only Sertoli cells in adults with Klinefelter’s syndrome. Nature 223:643–645PubMedCrossRef Skakkebaek NE (1969) Two types of tubules containing only Sertoli cells in adults with Klinefelter’s syndrome. Nature 223:643–645PubMedCrossRef
go back to reference Skakkebaek NE, Rajpert-De Meyts E, Main KM (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972–978CrossRefPubMed Skakkebaek NE, Rajpert-De Meyts E, Main KM (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972–978CrossRefPubMed
go back to reference Skakkebaek NE, Hoei-Hansen CE, Holm M, Jørgensen N, Rajpert-De Meyts E (2003) Association between testicular dysgenesis syndrome (TDS) and testicular neoplasia: evidence from 20 adult patients with signs of maldevelopment of the testis. APMIS 111:1–11CrossRefPubMed Skakkebaek NE, Hoei-Hansen CE, Holm M, Jørgensen N, Rajpert-De Meyts E (2003) Association between testicular dysgenesis syndrome (TDS) and testicular neoplasia: evidence from 20 adult patients with signs of maldevelopment of the testis. APMIS 111:1–11CrossRefPubMed
go back to reference Sohval AR (1956) Testicular dysgenesis in relation to neoplasm of the testicle. J Urol 75:285–291PubMed Sohval AR (1956) Testicular dysgenesis in relation to neoplasm of the testicle. J Urol 75:285–291PubMed
go back to reference Soroceanu L, Manning TJ, Sontheimer H (2001) Reduced expression of connexin43 and functional gap junction coupling in human gliomas. Glia 33:107–117CrossRefPubMed Soroceanu L, Manning TJ, Sontheimer H (2001) Reduced expression of connexin43 and functional gap junction coupling in human gliomas. Glia 33:107–117CrossRefPubMed
go back to reference Steger K, Rey R, Kliesch S, Louis F, Schleicher G, Bergmann M (1996) Immunohistochemical detection of immature Sertoli cell markers in testicular tissue of infertile men: a preliminary study. Int J Androl 19:122–128PubMedCrossRef Steger K, Rey R, Kliesch S, Louis F, Schleicher G, Bergmann M (1996) Immunohistochemical detection of immature Sertoli cell markers in testicular tissue of infertile men: a preliminary study. Int J Androl 19:122–128PubMedCrossRef
go back to reference Steger K, Aleithe I, Behre H, Bergmann M (1998) The proliferation of spermatogonia in normal and pathological human seminiferous epithelium: an immunohistochemical study using monoclonal antibodies against Ki-67 protein and proliferating cell nuclear antigen. Mol Hum Reprod 4:227–233CrossRefPubMed Steger K, Aleithe I, Behre H, Bergmann M (1998) The proliferation of spermatogonia in normal and pathological human seminiferous epithelium: an immunohistochemical study using monoclonal antibodies against Ki-67 protein and proliferating cell nuclear antigen. Mol Hum Reprod 4:227–233CrossRefPubMed
go back to reference Steger K, Rey R, Louis F, Kliesch S, Behre HM, Nieschlag E, Hoepffner W, Bailey D, Marks A, Bergmann M (1999a) Reversion of differentiated phenotype and maturation block in Sertoli cells in pathological human testis. Hum Reprod 14:136–143CrossRef Steger K, Rey R, Louis F, Kliesch S, Behre HM, Nieschlag E, Hoepffner W, Bailey D, Marks A, Bergmann M (1999a) Reversion of differentiated phenotype and maturation block in Sertoli cells in pathological human testis. Hum Reprod 14:136–143CrossRef
go back to reference Steger K, Tetens F, Bergmann M (1999b) Expression of connexin43 in human testis. Histochem Cell Biol 112:215–220CrossRef Steger K, Tetens F, Bergmann M (1999b) Expression of connexin43 in human testis. Histochem Cell Biol 112:215–220CrossRef
go back to reference Stosiek P, Kasper M, Karsten U (1990) Expression of cytokeratin 8 and 18 in human Sertoli cells of immature and atrophic seminiferous tubules. Differentiation 43:66–70PubMedCrossRef Stosiek P, Kasper M, Karsten U (1990) Expression of cytokeratin 8 and 18 in human Sertoli cells of immature and atrophic seminiferous tubules. Differentiation 43:66–70PubMedCrossRef
go back to reference Suarez-Quian CA, Martinez-Garcia F, Nistal M, Regadera J (1999) Androgen receptor distribution in adult human testis. J Clin Endocrinol Metab 84:350–358CrossRefPubMed Suarez-Quian CA, Martinez-Garcia F, Nistal M, Regadera J (1999) Androgen receptor distribution in adult human testis. J Clin Endocrinol Metab 84:350–358CrossRefPubMed
go back to reference Toppari J, Kaipia A, Kaleva M, Laato M, de Kretser DM, Krummen LA, Mather JP, Salmi TT (1998) Inhibin gene expression in a large cell calcifying Sertoli cell tumour and serum inhibin and activin levels. APMIS 106:101–113PubMedCrossRef Toppari J, Kaipia A, Kaleva M, Laato M, de Kretser DM, Krummen LA, Mather JP, Salmi TT (1998) Inhibin gene expression in a large cell calcifying Sertoli cell tumour and serum inhibin and activin levels. APMIS 106:101–113PubMedCrossRef
go back to reference Tran D, Picard JY, Campargue J, Josso N (1987) Immunocytochemical detection of anti-Mullerian hormone in Sertoli cells of various mammalian species including human. J Histochem Cytochem 35:733–743PubMed Tran D, Picard JY, Campargue J, Josso N (1987) Immunocytochemical detection of anti-Mullerian hormone in Sertoli cells of various mammalian species including human. J Histochem Cytochem 35:733–743PubMed
go back to reference Ulbright TM, Amin MB, Young RH (1999) Tumours of the testis, adnexa, spermatic cord, and scrotum. In: Atlas of tumour pathology, 3rd series, Armed forces Institute of Pathology, Washington, pp 185–233 Ulbright TM, Amin MB, Young RH (1999) Tumours of the testis, adnexa, spermatic cord, and scrotum. In: Atlas of tumour pathology, 3rd series, Armed forces Institute of Pathology, Washington, pp 185–233
go back to reference Ulbright TM, Srigley JR, Reuter VE, Wojno K, Lawrence MR, Young RH (2000) Sex cord-stromal tumours of the testis with entrapped germ cells. A lesion mimicking unclassified mixed germ cell sex cord-stromal tumours. Am J Surg Pathol 24:535–542CrossRefPubMed Ulbright TM, Srigley JR, Reuter VE, Wojno K, Lawrence MR, Young RH (2000) Sex cord-stromal tumours of the testis with entrapped germ cells. A lesion mimicking unclassified mixed germ cell sex cord-stromal tumours. Am J Surg Pathol 24:535–542CrossRefPubMed
go back to reference Venara M, Rey R, Bergada I, Mendilaharzu H, Campo S, Chemes H (2001) Sertoli cell proliferations of the infantile testis: an intratubular form of Sertoli cell tumour? Am J Surg Pathol 25:1237–1244CrossRefPubMed Venara M, Rey R, Bergada I, Mendilaharzu H, Campo S, Chemes H (2001) Sertoli cell proliferations of the infantile testis: an intratubular form of Sertoli cell tumour? Am J Surg Pathol 25:1237–1244CrossRefPubMed
go back to reference Vliegen MK, Schlatt S, Weinbauer GF, Bergmann M, Groome NP, Nieschlag E (1993) Localization of inhibin/activin subunits in the testis of adult nonhuman primates and men. Cell Tissue Res 273:261–268CrossRefPubMed Vliegen MK, Schlatt S, Weinbauer GF, Bergmann M, Groome NP, Nieschlag E (1993) Localization of inhibin/activin subunits in the testis of adult nonhuman primates and men. Cell Tissue Res 273:261–268CrossRefPubMed
go back to reference Waxman M, Damjanov I, Khapra A, Landau SJ (1984) Large cell calcifying Sertoli tumour of the testis. Light microscopic and ultrastructural study. Cancer 54:1574–1581PubMedCrossRef Waxman M, Damjanov I, Khapra A, Landau SJ (1984) Large cell calcifying Sertoli tumour of the testis. Light microscopic and ultrastructural study. Cancer 54:1574–1581PubMedCrossRef
go back to reference Williams K, McKinnell C, Saunders PTK, Walker M, Fisher JS, Turner KJ, Atanassova N, Sharpe RM (2001) Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen:oestrogen balance and assessment of the relevance to man. Hum Reprod Update 7:236–247CrossRefPubMed Williams K, McKinnell C, Saunders PTK, Walker M, Fisher JS, Turner KJ, Atanassova N, Sharpe RM (2001) Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen:oestrogen balance and assessment of the relevance to man. Hum Reprod Update 7:236–247CrossRefPubMed
go back to reference Yan W, Burns KH, Matzuk MM (2003) Genetic engineering to study testicular tumourigenesis. APMIS 111:174–183CrossRefPubMed Yan W, Burns KH, Matzuk MM (2003) Genetic engineering to study testicular tumourigenesis. APMIS 111:174–183CrossRefPubMed
go back to reference Young RH, Koelliker DD, Scully RE (1998) Sertoli cell tumours of the testis, not otherwise specified. Am J Surg Pathol 22:709–721CrossRefPubMed Young RH, Koelliker DD, Scully RE (1998) Sertoli cell tumours of the testis, not otherwise specified. Am J Surg Pathol 22:709–721CrossRefPubMed
Metadata
Title
Mitotic activity of Sertoli cells in adult human testis: an immunohistochemical study to characterize Sertoli cells in testicular cords from patients showing testicular dysgenesis syndrome
Authors
Ralph Brehm
Rodolfo Rey
Sabine Kliesch
Klaus Steger
Alexander Marks
Martin Bergmann
Publication date
01-06-2006
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 3/2006
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-005-0075-8

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