Sertoli cells are capable of proliferation into adulthood in the transition region between the seminiferous tubules and the rete testis in Wistar rats

References

• Russell LD, Ettlin RA, Sinha-Hikim AP, Clegg ED. Histological and histopathological evaluation of the testis. 1st ed. Russel LD, Ettlin RA, Sinha-Hikim AP, technical editors. Clearwater: Cache River Press; 1990.
   Google Scholar
• Sharpe RM. The physiology of reproduction. 2nd ed. New York: Raven Press: 1994. Regulation of spermatogenesis; p.1363-1434
   Google Scholar
• França LR, Russell LD. Male reproduction: a multidisciplinary overview. 1st ed. Madrid: Churchill Livingstone; 1998. The testis of domestic animals; p.197-219.
   Google Scholar
• Oatley JM, Brinster RL. The germline stem cell niche unit in Mammalian testes. Physiol Rev 2012; 92(2):577-95; PMID:22535892
   PubMed Web of Science ®Google Scholar
• Yoshida S. Elucidating the identity and behavior of spermatogenic stem cells in the mouse testis. Reproduction 2012; 144(3):293-302; PMID:22733803; http://dx.doi.org/10.1530/REP-11-0320
   PubMed Web of Science ®Google Scholar
• Chen SR, Liu YX. Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by Sertoli. Reproduction 2015; 149(4):R159-67; PMID:25504872; http://dx.doi.org/10.1530/REP-14-0481
   PubMed Web of Science ®Google Scholar
• Zakhidov ST, Marshak TL. Experimental evidence of proliferation and reproduction of highly differentiated Sertoli cells. Izv Akad Nauk Ser Biol 2015; 42(4):350-60; PMID:26415275
   PubMedGoogle Scholar
• França LR, Hess RA, Dufour JM, Hofmann MC, Griswold MD. The Sertoli cell: one hundred fifty years of beauty and plasticity. Andrology 2016; 4(2):189–212; PMID:26846984; http://dx.doi.org/10.1111/andr.12165
   PubMed Web of Science ®Google Scholar
• Hess RA, Cooke PS, Bunick D, Kirby JD. Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased Sertoli and germ cell numbers. Endocrinology 1993; 132(6):2607-13; PMID:8504761
   PubMed Web of Science ®Google Scholar
• França LR, Ye S, Ying L, Sandberg M, Russell LD. Morphometry of rat germ cells during spermatogenesis. Anat Rec 1995; 241(2):181-204; PMID:7710135
   PubMedGoogle Scholar
• Hess RA, França LR. Molecular Mechanisms in Spermatogenesis. 1st ed. New York: Landes Bioscience; 2007. Spermatogenesis and Cycle of the Seminiferous Epithelium; p.1-15.
   Google Scholar
• Steinberger A, Steinberger E. Replication pattern of Sertoli cells in maturing rat testis in vivo and organ culture. Biol Reprod 1971; 4(1):84-7; PMID:5110903
   PubMed Web of Science ®Google Scholar
• Orth JM. Proliferation of sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 1982; 203(4):485-92; PMID:7137603
   PubMedGoogle Scholar
• Auharek AS, França LR. Postnatal testis development, Sertoli cell proliferation and number of different spermatogonial types in C57BL/6J mice made transiently hypo- and hyperthyroidic during the neonatal period. J Anat 2010; 216(5):577-88; PMID:20525087; http://dx.doi.org/10.1111/j.1469-7580.2010.01219.x
   PubMed Web of Science ®Google Scholar
• Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003; 125(6):769-84; PMID:12773099
   PubMed Web of Science ®Google Scholar
• Hayrabedyan S, Todorova K, Pashova S, Mollova M, Fernández N. Sertoli cell quiescence - new insights. Am J Reprod Immunol 2012; 68(6):451-5; PMID:22531009; http://dx.doi.org/10.1111/j.1600-0897.2012.01137.x
   PubMed Web of Science ®Google Scholar
• Ekwall H, Jansson A, Sjöberg P, Plöen L. Differentiation of the rat testis between 20 and 120 days of age. Arch Androl 1984; 13(1):27-36; PMID:6534278
   PubMed Web of Science ®Google Scholar
• Berndtson WE, Thompson TL. 1990 Changing relationships between testis size, Sertoli cell number and spermatogenesis in Sprague-Dawley rats. J Androl 1990; 11(5):429-35; PMID:2254176
   PubMedGoogle Scholar
• Castro ACS, Cardoso FM, França LR. Effects of puberty and sexual development on daily sperm production and epididymal sperm reserves on Piau boars. Anim Reprod Sci 25:83-90
   Web of Science ®Google Scholar
• Meisami E, Sendera TJ, Clay LB. Paradoxical hypertrophy and plasticity of the testis in rats recovering from early thyroid deficiency: a growth study including effects of age and duration of hypothyroidism. J Endocrinol 1992; 135(3):495-505; PMID:1487702
   PubMed Web of Science ®Google Scholar
• Russell LD. Pathobiology of the aging rat. 1st ed. Washington: ILSI Press; 1992. Normal development of the testis; p.395-405
   Google Scholar
• França LR, Silva-Jr VA, Chiarini-Garcia H, Garcia SK, Debeljuk L. Cell proliferation and hormonal changes during postnal development of the testis in the pig. Biol Reprod 2000; 63(6):1629-36; PMID:11090429
   PubMed Web of Science ®Google Scholar
• Tarulli GA, Stanton PG, Meachem SJ. Is the adult Sertoli cell terminally differentiated? Biol Reprod 2012; 1:87(1): 13, 1-11; PMID:22492971; http://dx.doi.org/10.1095/biolreprod.111.095091
   PubMed Web of Science ®Google Scholar
• Tarulli GA, Stanton PG, Meyts ER, Loveland KL, McLachlan RI, Meachem SJ. A survey of Sertoli cell differentiation in men after gonadotropin suppression and in testicular cancer. Spermatogenesis 2013; 1:3(1):e24014; PMID:23687617
   PubMedGoogle Scholar
• Johnson L, Thompson DL. Age-related and seasonal variation in the Sertoli cell population, daily sperm production and serum concentrations of follicle-stimulating hormone, luteinizing hormone and testosterone in stallions. Biol Reprod 1983; 29(3):777-89; PMID:6414546
   PubMed Web of Science ®Google Scholar
• Johnson L, Varner DD, Tatum ME, Scrutchfield WL. Season but not age affects Sertoli cell number in adult stallions. Biol Reprod 1991; 45(3):404-10; PMID:1782288
   PubMed Web of Science ®Google Scholar
• Schulz RW, França LR, Lareyre JJ, LeGac F, Chiarini-Garcia H, Nobrega RH, Miura T. Spermatogenesis in fish. Gen Comp Endocrinol 2010; 1:165(3):390-411; PMID:19348807; http://dx.doi.org/10.1016/j.ygcen.2009.02.013
   PubMed Web of Science ®Google Scholar
• Perey B, Clermont Y, Lehlond CP. The wave of the seminiferous epithelium in the rat. Am J Anat 1961; 108:47-78
   Google Scholar
• Roosen-Runge EC. The rete testis in the albino rat: its structure, development and morphological significance. Acta Anat (Basel) 1961; 45:1-30; PMID:14493722
   PubMedGoogle Scholar
• Dym M. Spermatogonial stem cells of the testis. Proc Natl Acad Sci USA 1994; 22:91(24): 11287-9; PMID:7972051
   PubMed Web of Science ®Google Scholar
• Nykänen M. Fine structure of the transitional zone of the rat seminiferous tubule. Cell Tissue Res 1979; 25:198(3):441-54; PMID:466681
   PubMed Web of Science ®Google Scholar
• Osman DI. On the histochemistry of the seminiferous tubules and their terminal segments in the ram testis. Anat Histol Embryol 1984; 13(4):319-26; PMID:6240947
   PubMed Web of Science ®Google Scholar
• Hermo L, Dworkin J. Transitional cells at the junction of seminiferous tubules with the rete testis of the rat: their fine structure, endocytic activity, and basement membrane. Am J Anat 1988; 181(2):111-31; PMID:3285659
   PubMedGoogle Scholar
• Takahashi K, Naito M, Terayama H, Qu N, Cheng L, Tainosho S, Itoh M. Immunomorphological aspects of the tubuli recti and the surrounding interstitium in normal mice. Int J Androl 2007; 30(1):21-7; PMID:17328721
   PubMedGoogle Scholar
• Russell LD. The Sertoli cell. 1st ed. Clearwater: Cache River Press; 1993. Form, dimensions, and citology of mammalian Sertoli cells; p.1-37
   Google Scholar
• Aiyama Y, Tsunekawa N, Kishi K, Kawasumi M, Suzuki H, Kanai-Azuma M, Kurohmaru M, Kanay Y. A niche for GFRα1-positive spermatogonia in the terminal segments of the seminiferous tubules in hamster testes. Stem Cells 2015; 33(9):2811-24; PMID:26013732; http://dx.doi.org/10.1002/stem.2065
   PubMed Web of Science ®Google Scholar
• Tan KA, De Gendt K, Atanassova N, Walker M, Sharpe RM, Saunders PT, Denolet E, Verhoeven G. The role of androgen in Sertoli cell proliferation and functional maturation: studies in mice with total or Sertoli cell-selective ablation of androgen receptor. Endocrinology 2005; 146(6):2674-83; PMID:15761038
   PubMed Web of Science ®Google Scholar
• Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957; 100(2):241-67; PMID:13435229
   PubMedGoogle Scholar
• Russell LD, Clermont Y. Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anat Rec 1977; 187(3):347-66; PMID:851237
   PubMedGoogle Scholar
• Matthiesson KL, McLachlan RI, O'Donnell L, Frydenberg M, Robertson DM, Stanton PG, Meachem SJ. The relative roles of follicle-stimulating hormone and luteinizing hormone in maintaining spermatogonial maturation and spermiation in normal men. J Clin Endocrinol Metab 2006; 91(10):3962-9; PMID:16895950
   PubMed Web of Science ®Google Scholar
• Sridharan S, Simon L, Meling DD, Cyr DG, Gutstein DE, Fishman GI, Guillou F, Cooke PS. Proliferation of adult Sertoli cells following conditional knockout of the Gap junctional protein GJA1 (connexin 43) in mice. Biol Reprod 2007; 76(5):804-12; PMID:17229929
   PubMed Web of Science ®Google Scholar
• Ahmed EA, Rijbroek AV, Kal HB, Sadri-Ardekani H, Mizrak SC, Pelt A, De Rooij DG. Proliferative activity in vitro and DNA repair indicate that adult mouse and human Sertoli cells are not terminally differentiated, quiescent cells. Biol Reprod 2009; 80(6):1084-91; PMID:19164176; http://dx.doi.org/10.1095/biolreprod.108.071662
   PubMed Web of Science ®Google Scholar
• Swierstra EE. Influence of breed, age, and ejaculation frequency on boars semen composition. Can J Anim Sci 1973; 53:43-53
   Web of Science ®Google Scholar
• Russell LD, Bartke A, Goh JC. 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(3):179-89; PMID:2750675
   PubMedGoogle Scholar
• Kyrönlahti A, Euler R, Bielinska M, Schoeller EL, Moley KH, Toppari J, Heikinheimo M, Wilson DB. GATA4 regulates Sertoli cell function and fertility in adult male mice. Mol Cell Endocrinol 2011; 10:333(1):85-95; PMID:21172404; http://dx.doi.org/10.1016/j.mce.2010.12.019
   PubMed Web of Science ®Google Scholar
• Yang JZ, Zhao YF, Wang YM, Jing CX, Miao NZ, Ai QY. Determination of GATA-4 in the testis of the mouse. Zhonghua Nan Ke Xue 2010; 16(10):901-4; PMID:21243753
   PubMedGoogle Scholar
• Oreal E, Mazaud S, Picard JY, Magre S, Carre-Eusebe D. Different patterns of anti-Mullerian hormone expression, as related to Dmrt1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads. Dev Dyn 2002; 225(3):221-32; PMID:12412004
   PubMed Web of Science ®Google Scholar
• Viger RS, Guittot SM, Anttonen M, Wilson DB, Heikinheimo M. Role of the GATA family of transcription factors in endocrine development, function, and disease. Mol Endocrinol 2008; 22(4):781-98; PMID:18174356; http://dx.doi.org/10.1210/me.2007-0513
   PubMed Web of Science ®Google Scholar
• Bielinska M, Seehra A, Toppari J, Heikinheimo M, Wilson DB. GATA-4 is required for sex steroidogenic cell development in the fetal mouse. Dev Dyn 2007; 236(1):203-13; PMID:17096405
   PubMed Web of Science ®Google Scholar
• Tevosian SG. Transgenic mouse models in the study of reproduction: insights into GATA protein function. Reproduction 2014; 148(1):R1-R14; PMID:24700325; http://dx.doi.org/10.1530/REP-14-0086
   PubMed Web of Science ®Google Scholar
• Raymond CS, Murphy MW, O'sullivan G, Bardwell VJ, Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 2000; 15:14(20):2587-95; PMID:11040213
   PubMed Web of Science ®Google Scholar
• Lei N, Heckert LL. Gata4 regulates testis expression of Dmrt1. Mol Cell Biol 2004; 24(1):377-88; PMID:14673170
   PubMed Web of Science ®Google Scholar
• Manuylov NL, Zhou B, Ma Q, Fox SC, Pu WT, Tevosian SG. Conditional ablation of Gata4 and Fog2 genes in mice reveals their distinct roles in mammalian sexual differentiation. Dev Biol 2011; 15:353(2):229-41; PMID:21385577; http://dx.doi.org/10.1016/j.ydbio.2011.02.032
   PubMed Web of Science ®Google Scholar
• Heinlein CA, Chang C. Androgen receptor (AR) coregulators: an overview. Endocr Rev 2002; 23(2):175-200; PMID:11943742
   PubMed Web of Science ®Google Scholar
• O'Donnell L, Pratis K, Wagenfeld A, Gottwald U, Muller J, Leder G, McLachlan RI, Stanton PG. Transcriptional profiling of the hormone-responsive stages of spermatogenesis reveals cell-,stage-, and hormone-specifics events. Endocrinology 2009; 150(11):5074-84; PMID:19797402; http://dx.doi.org/10.1210/en.2009-0755
   PubMed Web of Science ®Google Scholar
• Stanton PG, Sluka P, Foo CFH, Stephens AN, Smith AI, McLachlan RI, O'Donnell L. Proteomic changes in rat spermatogenesis in response to in vivo manipulation; impact on meiotic cells. PLoS One 2012; 7(7):e41718; PMID:22860010; http://dx.doi.org/10.1371/journal.pone.0041718
   PubMed Web of Science ®Google Scholar
• Hazra R, Corcoran L, Robson M, McTavish KJ, Upton D, Handelsman DJ, Allan CM. Temporal role of Sertoli cell androgen receptor expression in spermatogenic development. Mol Endocrinol 2013; 27(1):12-24; PMID:23160479; http://dx.doi.org/10.1210/me.2012-1219
   PubMed Web of Science ®Google Scholar
• Willems A, Batlouni SR, Esnal A, Swinnen JV, Saunders PTK, Sharpe RM, França LR, De Gendt K, Verhoeven G. Selective ablation of the androgen receptor in mouse Sertoli cells affects Sertoli cells maturation, barrier formation and cytoskeletal development. PLoS One 2010; 30:5(11):e14168; PMID:21152390; http://dx.doi.org/10.1371/journal.pone.0014168
   PubMed Web of Science ®Google Scholar
• Orth JM. The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats. Endocrinology 1984; 115(4):1248-55; PMID:6090096
   PubMed Web of Science ®Google Scholar
• Cooke PS, Zhao YD, Bunick D. Tri-iodothyronine 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(5):1000-5; PMID:7531505
   PubMed Web of Science ®Google Scholar
• Holsberger DR, Jirawatnotai S, Kiyokawa H, Cooke OS. Thyroid hormone regulates the cell cycle inhibitor p27Kip1 in postnatal murine Sertoli cells. Endocrinology 2003; 144(9):3732-8; PMID:12933641
   PubMed Web of Science ®Google Scholar
• Van Haaster LH, De Jong FH, Docter R, De Rooij DG. 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(2):755-60; PMID:8344214
   PubMed Web of Science ®Google Scholar
• Cooke PS, Holsberger DR, França LR. The Sertoli Cell Biology. San Diego: Elsevier – Academic Press; 2005. Thyroid hormone regulation of Sertoli cell development; p.217-226
   Google Scholar
• Holsberger DR, Buchold GM, Leal MC, Kiesewetter SE, O'Brien DA, Hess RA, França LR, Kiyokawa H, Cooke PS. Cell-cycle inhibitors p27Kip1 and p21Cip1 regulate murine Sertoli cell proliferation. Biol Reprod 2005; 72(6):1429-36; PMID:15728790
   PubMed Web of Science ®Google Scholar
• Arambepola NK, Bunick D, Cooke PS. Thyroid hormone effects on androgen receptor messenger RNA expression in rat Sertoli and peritubular cells. J Endocrinol 1998; 156(1):43-50; PMID:9496232
   PubMed Web of Science ®Google Scholar
• Ilio KY, Hess RA. Structure and function of the ductuli efferentes: a review. Microsc Res Tech 1994; 15:29(6):432-67; PMID:7873793
   PubMed Web of Science ®Google Scholar
• Lunstra DD, Wise TH, Ford JJ. Sertoli cells in the boar testis: changes during development and compensatory hypertrophy after hemicastration at different ages. Biol Reprod 2003; 68(1):140-50; PMID:12493706
   PubMed Web of Science ®Google Scholar
• Mital P, Kaur G, Bowlin B, Paniagua NJ, Korbutt GS, Dufour JM. Biol Reprod 2014; 23:90(1):13; PMID:24285718; http://dx.doi.org/10.1095/biolreprod.113.110197
   PubMed Web of Science ®Google Scholar
• Tarulli GA, Stanton PG, Lerchl A, Meachem SJ. Adult sertoli cells are not terminally differentiated in the Djungarian hamster: effect of FSH on proliferation and junction protein organization. Biol Reprod 2006; 74(5):798-806; PMID:16407497
   PubMed Web of Science ®Google Scholar
• Giorno R. A comparison of two immunoperoxidase staining methods based on the avidin-biotin interaction. Diagn Immunol 1984; 2(3):161-6; PMID:6388981
   PubMedGoogle Scholar
• Ramos-Vara JÁ. Technical aspects of Immunohistochemistry. Vet Pathol 2005; 42(4):405-26; PMID:16006601
   PubMed Web of Science ®Google Scholar