Müllerian-Inhibiting Substance Inhibits Rat Leydig Cell Regeneration after Ethylene Dimethanesulphonate Ablation

Biology of Reproduction

Volumn 70, Issue 3, 2004, Pages 600-607

  Salva, Antonio ^a   Hardy, Matthew P ^a   Wu, Xiu Feng ^c   Sottas, Chantal M ^a   MacLaughlin, David T ^b   Donahoe, Patricia K ^b   Lee, Mary M ^c  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Leydig cells; Male reproductive tract; Mechanisms of hormone action; Testis; Testosterone

Indexed keywords

ANDROSTANOLONE; BROXURIDINE; ESTRADIOL; ETHYLENE GLYCOL DIMESYLATE; LUTEINIZING HORMONE; MUELLERIAN INHIBITING FACTOR; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOCRINE FUNCTION; ESTRADIOL BLOOD LEVEL; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; INJECTION; LEYDIG CELL; LUTEINIZING HORMONE BLOOD LEVEL; MALE; MESENCHYME; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; STEM CELL; STEREOMETRY; STEROIDOGENESIS; TESTIS; TESTOSTERONE BLOOD LEVEL;

ANIMALS; CELL COUNT; CELL DIVISION; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; GLYCOPROTEINS; IN SITU NICK-END LABELING; LEYDIG CELLS; LUTEINIZING HORMONE; MALE; MESYLATES; ORGAN SIZE; RATS; RATS, SPRAGUE-DAWLEY; STEROID 17-ALPHA-HYDROXYLASE; TESTICULAR HORMONES; TESTIS; TESTOSTERONE; TESTOSTERONE 5-ALPHA-REDUCTASE;

ANIMALIA;

EID: 1242298814     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.103.021550     Document Type: Article

References (46)

1. Benton L, Shan LX, Hardy MP. Differentiation of adult Leydig cells. J Steroid Biochem Mol Biol 1995; 53:61-68.
2. Ewing LL, Keeney DS. Leydig cells: structure and function. In: Desjardins C, Ewing LL (eds.), Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993:137-165.
3. Tapanainen J, Kuopio T, Pelliniemi LJ, Huhtaniemi I. Rat testicular endogenous steroids and the number of Leydig cells between the fetal period and sexual maturity. Biol Reprod 1984; 31:1027-1035.
4. Kerr JB, Donachie K, Rommerts FF. Selective destruction and regeneration of rat Leydig cells in vivo. A new method for the study of seminiferous tubular-interstitial tissue interaction. Cell Tissue Res 1985; 242:145-156.
5. Morris ID. Leydig cell resistance to the cytotoxic effect of ethylene dimethanesulphonate in the adult rat testis. J Endocrinol 1985; 105:311-316.
6. Bartlett JM, Kerr JB, Sharpe RM. The effect of selective destruction and regeneration of rat Leydig cells on the intratesticular distribution of testosterone and morphology of the seminiferous epithelium. J Androl 1986; 7:240-253.
7. Molenaar R, de Rooij DG, Rommerts FF, van der Molen HJ. Repopulation of Leydig cells in mature rats after selective destruction of the existent Leydig cells with ethylene dimethane sulfonate is dependent on luteinizing hormone and not follicle-stimulating hormone. Endocrinology 1986; 118:2546-2554.
8. Kerr JB, Bartlett JM, Donachie K, Sharpe RM. Origin of regenerating Leydig cells in the testis of the adult rat. An ultrastructural, morphometric and hormonal assay study. Cell Tissue Res 1987; 249:367-377.
9. Tena-Sempere M, Rannikko A, Kero J, Zhang FP, Huhtaniemi IT. Molecular mechanisms of reappearance of luteinizing hormone receptor expression and function in rat testis after selective Leydig cell destruction by ethylene dimethane sulfonate. Endocrinology 1997; 138:3340-3348.
10. Ariyaratne HB, Mills N, Mason JI, Mendis-Handagama SM. Effects of thyroid hormone on Leydig cell regeneration in the adult rat following ethane dimethane sulphonate treatment. Biol Reprod 2000; 63:1115-1123.
11. Yan W, Kero J, Huhtaniemi I, Toppari J. Stem cell factor functions as a survival factor for mature Leydig cells and a growth factor for precursor Leydig cells after ethylene dimethane sulfonate treatment: implication of a role of the stem cell factor/c-Kit system in Leydig cell development. Dev Biol 2000; 227:169-182.
12. Teixeira J, Maheswaran S, Donahoe P. Mullerian Inhibiting Substance: an instructive developmental hormone with diagnostic and possible therapeutic applications. Endocr Rev 2001; 22:657-674.
13. Lee MM, Seah CC, Masiakos PT, Sottas CM, Preffer FI, Donahoe PK, MacLaughlin DT, Hardy MP. Mullerian Inhibiting Substance type II receptor expression and function in purified rat Leydig cells. Endocrinology 1999; 140:2819-2827.
14. Racine C, Rey R, Forest M, Louis F, Ferre A, Huhtaniemi I, Josso N, Di Clemente N. Receptors for anti-Mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci U S A 1998; 95:594-599.
15. Lee MM. MIS Actions in the Developing Testis. In: Goldberg E (ed.), The Testis: From Stem Cell to Sperm Function. New York: Springer-Verlag; 2000:30-42.
16. Behringer RR, Finegold MJ, Cate RL. Mullerian-inhibiting substance function during mammalian sexual development. Cell 1994; 79:415-425.
17. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, Cate RL, Behringer RL. Genetic analysis of the Mullerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev 1996; 10:2577-2587.
18. Lyet L, Louis F, Forest MG, Josso N, Behringer RR, Vigier B. Ontogeny of reproductive abnormalities induced by deregulation of anti-Mullerian hormone expression in transgenic mice. Biol Reprod 1995; 52:444-454.
19. Behringer RR, Cate RL, Froelick GJ, Palmiter RD, Brinster RL. Abnormal sexual development in transgenic mice chronically expressing Mullerian Inhibiting Substance. Nature 1990; 345:167-170.
20. Sriraman V, Niu E, Matias J, Donahoe PK, MacLaughlin DT, Hardy MP, Lee MM. Mullerian Inhibiting Substance inhibits testosterone synthesis in adult rats. J Androl 2001; 22:750-758.
21. Trbovich AM, Sluss PM, Laurich VM, O'Neill FH, MacLaughlin DT, Donahoe PK, Teixeira J. Mullerian Inhibiting Substance lowers testosterone in luteinizing hormone-stimulated rodents. Proc Natl Acad Sci U S A 2001; 98:3393-3397.
22. MacLaughlin DT, Epstein J, Donahoe PK. Bioassay, purification, cloning, and expression of Mullerian Inhibiting Substance. Meth Enzymol 1991; 198:358-369.
23. Donahoe PK, Ito Y, Hendren WHI. A graded organ culture assay for the detection of Mullerian Inhibiting Substance. J Surg Res 1977; 23:141-148.
24. Hudson PL, Dougas I, Donahoe PK, Cate RL, Epstein J, Pepinsky RB, MacLaughlin DT. An immunoassay to detect human Mullerian Inhibiting Substance in males and females during normal development. J Clin Endocrinol Metab 1990; 70:16-22.
25. di Clemente N, Ghaffari S, Pepinsky RB, Pieau C, Josso N, Cate RL, Vigier B. A quantitative and interspecific test for biological activity of anti-Mullerian hormone: the fetal ovary aromatase assay. Development 1992; 114:721-727.
26. Sprando RL, Santulli R, Awoniyi CA, Ewing LL, Zirkin BR. Does ethane 1,2-dimethanesulphonate (EDS) have a direct cytotoxic effect on the seminiferous epithelium of the rat testis? J Androl 1990; 11:344-352.
27. Hardy MP, Zirkin BR, Ewing LL. Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 1989; 124:762-770.
28. Mendis-Handagama SM. Estimation error of Leydig cell numbers in atrophied rat testes due to the assumption of spherical nuclei. J Microsc 1992; 168(Pt 1):25-32.
29. Mendis-Handagama SM, Keeney DS, Hardy MP, Ewing LL. Application of the dissector method to enumerate cells in the testis. Ann N Y Acad Sci 1989; 564:86-98.
30. Sorensen FB. Unbiased stereologic techniques for practical use in diagnostic histopathology. Pathologica 1995; 87:263-278.
31. Wreford NG. Theory and practice of stereological techniques applied to the estimation of cell number and nuclear volume in the testis. Microsc Res Tech 1995; 32:423-436.
32. Cochran R, Ewing L, Niswender G. Serum levels of follicle stimulating hormone, luteinizing hormone, prolactin, testosterone, 5α -dihydrotestosterone, 5α-androstane-3α, 17β-diol, 5α-androstane-3β-, 17β-diol, and 17β-estradiol from male beagles with spontaneous or induced benign prostatic hyperplasia. Invest Urol 1981; 19:142-147.
33. Knorr D, Vanha-Perittula T, Lipsett M. Structure and function of rat testis through pubescence. Endocrinology 1970; 86:1298-1304.
34. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119:493-501.
35. Viger RS, Robaire B. Steady state steroid 5 alpha-reductase messenger ribonucleic acid levels and immunocytochemical localization of the type 1 protein in the rat testis during postnatal development. Endocrinology 1995; 136:5409-5415.
36. Morris ID, McCluckie JA. Temporal changes in serum androgen after temporary impairment of Leydig cell function by ethane-1,2-dimethane sulphonate. J Steroid Biochem 1979; 10:467-469.
37. Baarends WM, Hoogerbrugge JW, Post M, Visser JA, De Rooij DG, Parvinen M, Themmen AP, Grootegoed JA. Anti-Mullerian hormone and anti-Mullerian hormone type II receptor messenger ribonucleic acid expression during postnatal testis development and in the adult testis of the rat. Endocrinology 1995; 136:5614-5622.
38. Nandi S, Banerjee PP, Zirkin BR. Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1,2-dimethanesulfonate administration: relationship to Fas? Biol Reprod 1999; 61:70-75.
39. Price J, Donahoe P, Ito Y, Hendren III W. Programmed cell death in the Mullerian duct induced by Mullerian Inhibiting Substance. Am J Anat 1977; 149:353-376.
40. Ingraham HA, Hirokawa Y, Roberts LM, Mellon SH, McGee E, Nachtigal MW, Visser JA. Autocrine and paracrine Mullerian Inhibiting Substance hormone signaling in reproduction. Recent Prog Horm Res 2000; 55:53-67;67-58 (discussion).
41. Allard S, Adin P, Gouedard L, di Clemente N, Josso N, Orgebin-Crist MC, Picard JY, Xavier F. Molecular mechanisms of hormone-mediated Mullerian duct regression: involvement of beta-catenin. Development 2000; 127:3349-3360.
42. Catlin EA, Tonnu VC, Ebb RG, Pacheco BA, Manganaro TF, Ezzell RM, Donahoe PK, Teixeira J. Mullerian Inhibiting Substance inhibits branching morphogenesis and induces apoptosis in fetal rat lung. Endocrinology 1997; 138:790-796.
43. Shan LX, Hardy MP. Developmental changes in levels of luteinizing hormone receptor and androgen receptor in rat Leydig cells. Endocrinology 1992; 131:1107-1114.
44. Myers RB, Abney TO. Interstitial cell proliferation in the testis of the ethylene dimethane sulfonate-treated rat. Steroids 1991; 56:91-96.
45. Moger WH. Serum 5alpha-androstane-3alpha, 17beta-diol, androsterone, and testosterone concentrations in the male rat. Influence of age and gonadotropin stimulation. Endocrinology 1977; 100:1027-1032.
46. Corpechot C, Baulieu EE, Robel P. Testosterone, dihydrotestosterone and androstanediols in plasma, testes and prostates of rats during development. Acta Endocrinol (Copenh) 1981; 96:127-135.