Triiodothyronine modulates initiation of spermatogenesis in rats depending on treatment timing and blood level of the hormone

Molecular and Cellular Endocrinology

Volumn 341, Issue 1-2, 2011, Pages 25-34

  Marchlewska, Katarzyna ^a   Kula, Krzysztof ^a   Walczak Jedrzejowska, Renata ^a   Oszukowska, Elzbieta ^a   Orkisz, Stanisław ^a   Slowikowska Hilczer, Jolanta ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

Gonocyte; Maturation; Sertoli cell; Spermatogonia; Testes; Thyroid hormone

Indexed keywords

LIOTHYRONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DEGENERATION; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VACUOLE; CYTOPLASM; GERM CELL; LIOTHYRONINE BLOOD LEVEL; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS GROWTH; TESTIS WEIGHT; TISSUE GROWTH; WEIGHT REDUCTION;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; MALE; ORGAN SIZE; RATS; RATS, WISTAR; SEMINIFEROUS TUBULES; SERTOLI CELLS; SPERMATOGENESIS; SPERMATOZOA; TESTIS; TESTOSTERONE; TRIIODOTHYRONINE;

EID: 79960608011     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.04.022     Document Type: Article

References (66)

1. Abdallah B., Sachs L., Hourdry J., Wegnez M., Denis H., Demeneix B., Mazabraud A. Thyroid hormone regulation of germ cell-specific EF-1 alpha expression during metamorphosis of Xenopus laevis. Int. J. Dev. Biol. 1996, 40:507-514.
2. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 1946, 238:247.
3. Almiron I., Chemes H. Spermatogenic onset. II. FSH modulates mitotic activity of germ and Sertoli cells in immature rats. Int. J. Androl. 1988, 11:235-246.
4. Arambepola N.K., Bunick D., Cooke P.S. Thyroid hormone effects on androgen receptor messenger RNA expression in rat Sertoli and peritubular cells. J. Endocrinol. 1998, 156:43-50.
5. Ariyaratne H.B., Mendis-Handagama S.M., Mason J.I. Effects of tri-iodothyronine on testicular interstitial cells and androgen secretory capacity of the prepubertal Rat. Biol. Reprod. 2000, 63:493-502.
6. Atanassova N., McKinnell C., Fisher J., Sharpe R.M. Neonatal treatment of rats with diethylstilboestrol (DES) induces stromal-epithelial abnormalities of the vas deferens and cauda epididymis in adulthood following delayed basal cell development. Reproduction 2005, 129:589-601.
7. Bascom K., Osterud H. Quantitative studies of the testicle. II. Pattern of total tubul length in the testicles of certain common mammals. Anat. Rec. 1925, 31:159-169.
8. Bassett J.H., Williams G.R. The molecular actions of thyroid hormone in bone. Trends Endocrinol. Metab. 2003, 14:356-364.
9. Bernal J., Nunez J. Thyroid hormones and brain development. Eur. J. Endocrinol. 1995, 133:390-398.
10. Berndtson W.E., Thompson T.L. Changing relationships between testis size, Sertoli cell number and spermatogenesis in Sprague-Dawley rats. J. Androl. 1990, 11:429-435.
11. Botella de Maglia J., Compte Torrero L., Rivas Sanchez A., Perez Pastor J.L. Triiodothyronine intoxication. A clinical and phamacokinetic study. An. Med. Interna 2003, 20:627-629.
12. Buzzard J.J., Morrison J.R., O'Bryan M.K., Song Q., Wreford N.G. Developmental expression of thyroid hormone receptors in the rat testis. Biol. Reprod. 2000, 62:664-669.
13. Buzzard J.J., Wreford N.G., Morrison J.R. Thyroid hormone, retinoic acid, and testosterone suppress proliferation and induce markers of differentiation in cultured rat Sertoli cells. Endocrinology 2003, 144:3722-3731.
14. Canale D., Agostini M., Giorgilli G., Caglieresi C., Scartabelli G., Nardini V., Jannini E.A., Martino E., Pinchera A., Macchia E. Thyroid hormone receptors in neonatal, prepubertal, and adult rat testis. J. Androl. 2001, 22:284-288.
15. Clermont Y. Quantitative analysis of spermatogenesis of the rat: a revised model for the renewal of spermatogonia. Am. J. Anat. 1962, 111:111-129.
16. Clermont Y., Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am. J. Anat. 1957, 100:241-267.
17. Clermont Y., Perey B. The stages of the cycle of the seminiferous epithelium of the rat: practical definitions in PA-Schiff-hematoxylin and hematoxylin-eosin stained sections. Rev. Cancer Biol. 1957, 16:451-462.
18. Cooke P.S., Meisami E. Early hypothyroidism in rats causes increased adult testis and reproductive organ size but does not change testosterone levels. Endocrinology 1991, 129:237-243.
19. Cooke P.S., Porcelli J., Hess R.A. Induction of increased testis growth and sperm production in adult rats by neonatal administration of the goitrogen propylthiouracil (PTU): the critical period. Biol. Reprod. 1992, 46:146-154.
20. Cooke P.S., Zhao Y.D., Bunick D. Triiodothyronine inhibits proliferation and stimulates differentiation of cultured neonatal Sertoli cells: possible mechanism for increased adult testis weight and sperm production induced by neonatal goitrogen treatment. Biol. Reprod. 1994, 51:1000-1005.
21. Davis P.J., Davis F.B. Nongenomic actions of thyroid hormone on the heart. Thyroid 2002, 12:459-466.
22. de Rooij D.G. Stem cells in the testis. Int. J. Exp. Pathol. 1998, 79:67-80.
23. de Rooij D.G. Proliferation and differentiation of spermatogonial stem cells. Reproduction 2001, 121:347-354.
24. de Rooij D.G., Grootegoed J.A. Spermatogonial stem cells. Curr. Opin. Cell Biol. 1998, 10:694-701.
25. de Rooij D.G., Lok D. Regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster: II. Differentiating spermatogonia. Anat. Rec. 1987, 217:131-136.
26. de Rooij D.G., Lok D., Weenk D. Feedback regulation of the proliferation of the undifferentiated spermatogonia in the Chinese hamster by the differentiating spermatogonia. Cell Tissue Kinet. 1985, 18:71-81.
27. de Rooij D.G., Russell L.D. All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 2000, 21:776-798.
28. Faraone-Mennella M.R., Ferone A., Marino L., Cardone A., Comitato R., Venditti P., Di Meo S., Farina B. Poly(ADP-ribosyl)ation of proteins and germ cell development in hyperthyroid rat testes. Mol. Cell. Biochem. 2009, 323:119-129.
29. Hardy M.P., Sharma R.S., Arambepola N.K., Sottas C.M., Russell L.D., Bunick D., Hess R.A., Cooke P.S. Increased proliferation of Leydig cells induced by neonatal hypothyroidism in the rat. J. Androl. 1996, 17:231-238.
30. Haywood M., Spaliviero J., Jimemez M., King N.J., Handelsman D.J., Allan C.M. Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone. Endocrinology 2003, 144:509-517.
31. Holsberger D.R., Cooke P.S. Understanding the role of thyroid hormone in Sertoli cell development: a mechanistic hypothesis. Cell Tissue Res. 2005, 322:133-140.
32. Holsberger D.R., Kiesewetter S.E., Cooke P.S. Regulation of neonatal Sertoli cell development by thyroid hormone receptor alpha1. Biol. Reprod. 2005, 73:396-403.
33. Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat. Rec. 1971, 169:533-557.
34. Huckins C. The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat. Rec. 1978, 190:905-926.
35. Huckins C., Clermont Y. Evolution of gonocytes in the rat testis during late embryonic and early post-natal life. Arch. Anat. Histol. Embryol. 1968, 51:341-354.
36. Huckins C., Oakberg E.F. Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules. II. The irradiated testes. Anat. Rec. 1978, 192:529-542.
37. Jannini E.A., Olivieri M., Francavilla S., Gulino A., Ziparo E., D'Armiento M. Ontogenesis of the nuclear 3,5,3′-triiodothyronine receptor in the rat testis. Endocrinology 1990, 126:2521-2526.
38. Jannini E.A., Ulisse S., Piersanti D., Carosa E., Muzi P., Lazar J., D'Armiento M. Early thyroid hormone treatment in rats increases testis size and germ cell number. Endocrinology 1993, 132:2726-2728.
39. Kirby J.D., Jetton A.E., Cooke P.S., Hess R.A., Bunick D., Ackland J.F., Turek F.W., Schwartz N.B. Developmental hormonal profiles accompanying the neonatal hypothyroidism-induced increase in adult testicular size and sperm production in the rat. Endocrinology 1992, 131:559-565.
40. Kula K. The completion of spermatogenic cells in the course of spermatogenesis in immature rats. Folia Morphol. (Warsz) 1977, 36:167-173.
41. Kula K., Walczak-Jedrzejowska R., Slowikowska-Hilczer J., Oszukowska E. Estradiol enhances the stimulatory effect of FSH on testicular maturation and contributes to precocious initiation of spermatogenesis. Mol. Cell. Endocrinol. 2001, 178:89-97.
42. Orth J.M. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat. Rec. 1982, 203:485-492.
43. Palmero S., Prati M., Barreca A., Minuto F., Giordano G., Fugassa E. Thyroid hormone stimulates the production of insulin-like growth factor I (IGF-I) by immature rat Sertoli cells. Mol. Cell. Endocrinol. 1990, 68:61-65.
44. Panno M.L., Salerno M., Lanzino M., De Luca G., Maggiolini M., Straface S.V., Prati M., Palmero S., Bolla E., Fugassa E., Ando S. Follow-up study on the effects of thyroid hormone administration on androgen metabolism of peripubertal rat Sertoli cells. Eur. J. Endocrinol. 1995, 132:236-241.
45. Parmacek M.S., Magid N.M., Lesch M., Decker R.S., Samarel A.M. Cardiac protein synthesis and degradation during thyroxine-induced left ventricular hypertrophy. Am. J. Physiol. 1986, 251:C727-C736.
46. Pineau C., Velez de la Calle J.F., Pinon-Lataillade G., Jegou B. Assessment of testicular function after acute and chronic irradiation: further evidence for an influence of late spermatids on Sertoli cell function in the adult rat. Endocrinology 1989, 124:2720-2728.
47. Rodriguez I., Ody C., Araki K., Garcia I., Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J. 1997, 16:2262-2270.
48. Russell, L., Etilin, R., Shina-Hikim, A. and Clegg, E. 1990 Histological and histopathological evaluation of the testis, Cache River Press Clearwater.
49. Russell L., Frank B. Characterization of rat spermatocytes after plastic embedding. Arch. Androl. 1978, 1:5-18.
50. Russell L.D., Alger L.E., Nequin L.G. Hormonal control of pubertal spermatogenesis. Endocrinology 1987, 120:1615-1632.
51. Russell L.D., Bartke A., Goh J.C. Postnatal development of the Sertoli cell barrier, tubular lumen, and cytoskeleton of Sertoli and myoid cells in the rat, and their relationship to tubular fluid secretion and flow. Am. J. Anat. 1989, 184:179-189.
52. Russell L.D., Clermont Y. Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anat. Rec. 1977, 187:347-366.
53. Russell L.D., Peterson R.N. Determination of the elongate spermatid-Sertoli cell ratio in various mammals. J. Reprod. Fertil. 1984, 70:635-641.
54. Simorangkir D.R., Wreford N.G., De Kretser D.M. Impaired germ cell development in the testes of immature rats with neonatal hypothyroidism. J. Androl. 1997, 18:186-193.
55. St-Pierre N., Dufresne J., Rooney A.A., Cyr D.G. Neonatal hypothyroidism alters the localization of gap junctional protein connexin 43 in the testis and messenger RNA levels in the epididymis of the rat. Biol. Reprod. 2003, 68:1232-1240.
56. Steinberger A., Steinberger E. Replication pattern of Sertoli cells in maturing rat testis in vivo and in organ culture. Biol. Reprod. 1971, 4:84-87.
57. Ulisse S., Jannini E.A., Pepe M., De Matteis S., D'Armiento M. Thyroid hormone stimulates glucose transport and GLUT1 mRNA in rat Sertoli cells. Mol. Cell. Endocrinol. 1992, 87:131-137.
58. Ulisse S., Rucci N., Piersanti D., Carosa E., Graziano F.M., Pavan A., Ceddia P., Arizzi M., Muzi P., Cironi L., Gnessi L., D'Armiento M., Jannini E.A. Regulation by thyroid hormone of the expression of basement membrane components in rat prepubertal Sertoli cells. Endocrinology 1998, 139:741-747.
59. van Haaster L.H., De Jong F.H., Docter R., De Rooij D.G. The effect of hypothyroidism on Sertoli cell proliferation and differentiation and hormone levels during testicular development in the rat. Endocrinology 1992, 131:1574-1576.
60. van Haaster L.H., de Jong F.H., Docter R., de Rooij D.G. High neonatal triiodothyronine levels reduce the period of Sertoli cell proliferation and accelerate tubular lumen formation in the rat testis, and increase serum inhibin levels. Endocrinology 1993, 133:755-760.
61. van Haaster L.H., de Rooij D.G. Spermatogenesis is accelerated in the immature Djungarian and Chinese hamster and rat. Biol. Reprod. 1993, 49:1229-1235.
62. van Keulen C.J., de Rooij D.G. Spermatogenetic clones developing from repopulating stem cells surviving a high dose of an alkylating agent. Cell Tissue Kinet. 1975, 8:543-551.
63. Vitale R., Fawcett D.W., Dym M. The normal development of the blood-testis barrier and the effects of clomiphene and estrogen treatment. Anat. Rec. 1973, 176:331-344.
64. Wahlgren A., Svechnikov K., Strand M.L., Jahnukainen K., Parvinen M., Gustafsson J.A., Soder O. Estrogen receptor beta selective ligand 5alpha-Androstane-3beta, 17beta-diol stimulates spermatogonial deoxyribonucleic acid synthesis in rat seminiferous epithelium in vitro. Endocrinology 2008, 149:2917-2922.
65. Walczak-Jedrzejowska R., Slowikowska-Hilczer J., Marchlewsk K., Oszukowska E., Kula K. During seminiferous tubule maturation testosterone and synergistic action of FSH with estradiol support germ cell survival while estradiol alone has pro-apoptotic effect. Folia Histochem. Cytobiol. 2007, 45(Suppl. 1):S59-64.
66. Walczak-Jedrzejowska R., Slowikowska-Hilczer J., Marchlewska K., Kula K. Maturation, proliferation and apoptosis of seminal tubule cells at puberty after administration of estradiol, follicle stimulating hormone or both. Asian J. Androl. 2008, 10:585-592.