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Endocrinology Vol. 138, No. 5 2081-2088
Copyright © 1997 by The Endocrine Society

Articles

The Fas System Is a Key Regulator of Germ Cell Apoptosis in the Testis1

Jeongwu Lee, John H. Richburg, Sarah C. Younkin and Kim Boekelheide2

Department of Pathology and Laboratory Medicine, Brown University, Providence, Rhode Island 02912

Address all correspondence and requests for reprints to: Kim Boekelheide, M.D., Ph.D., Department of Pathology and Laboratory Medicine, Brown University, Box G-B518, Providence, Rhode Island 02912. E-mail: Kim-Boekelheide{at}Brown.edu

Apoptosis occurs in the testis as an important physiological mechanism to limit the number of germ cells in the seminiferous epithelium. Sertoli cells, which tightly regulate germ cell proliferation and differentiation, are implicated in the control of germ cell apoptosis. Fas (APO-1, CD95), a transmembrane receptor protein, transmits an apoptotic signal within cells when bound by Fas ligand (FasL). The Fas system has been implicated in immune regulation, including cytotoxic T cell-mediated cytotoxicity, activation-induced suicide of T cells, and control of immune-privileged sites. Here we propose the Fas system as a key regulator of spermatogenesis. In this model, FasL expressed by Sertoli cells initiates the apoptotic death of germ cells expressing Fas. Using immunohistochemistry, we localized Fas to germ cells and FasL to Sertoli cells. The expression of these genes was dramatically up-regulated after exposure to mono-(2-ethylhexyl) phthalate and 2,5-hexanedione, two widely studied Sertoli cell toxicants known to induce germ cell apoptosis. Mouse germ cells in vitro were susceptible to anti-Fas antibody-induced death, and the survival of rat germ cells was increased after disruption of FasL by antisense oligonucleotide treatment. Unlike its expression in other tissues, testicular expression of Fas in the lpr mouse, a spontaneous mutant of the Fas gene, is similar to that in the normal mouse, arguing for the importance of the Fas system in maintaining testicular homeostasis. These data implicate the Sertoli cell in the paracrine control of germ cell output during spermatogenesis by a Fas-mediated pathway.




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[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
C.-L. Hu, R. G. Cowan, R. M. Harman, D. A. Porter, and S. M. Quirk
Apoptosis of Bovine Granulosa Cells After Serum Withdrawal Is Mediated by Fas Antigen (CD95) and Fas Ligand
Biol Reprod, February 1, 2001; 64(2): 518 - 526.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
K. A. Young, G. F. Ball, and R. J. Nelson
Photoperiod-Induced Testicular Apoptosis in European Starlings (Sturnus vulgaris)
Biol Reprod, February 1, 2001; 64(2): 706 - 713.
[Abstract] [Full Text]

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 Exp. Biol. Med.Home page
K. Boekelheide, S. L. Fleming, K. J. Johnson, S. R. Patel, and H. A. Schoenfeld
Role of Sertoli Cells in Injury-Associated Testicular Germ Cell Apoptosis
Experimental Biology and Medicine, November 1, 2000; 225(2): 105 - 115.
[Abstract] [Full Text]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
M. E. De Paepe, L. P. Rubin, C. Jude, A. M. Lesieur-Brooks, D. R. Mills, and F. I. Luks
Fas ligand expression coincides with alveolar cell apoptosis in late-gestation fetal lung development
Am J Physiol Lung Cell Mol Physiol, November 1, 2000; 279(5): L967 - L976.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J. J. Lysiak, S. D. Turner, and T. T. Turner
Molecular Pathway of Germ Cell Apoptosis Following Ischemia/Reperfusion of the Rat Testis
Biol Reprod, November 1, 2000; 63(5): 1465 - 1472.
[Abstract] [Full Text]

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 Hum ReprodHome page
H. Yazawa, I. Sasagawa, and T. Nakada
Apoptosis of testicular germ cells induced by exogenous glucocorticoid in rats
Hum. Reprod., September 1, 2000; 15(9): 1917 - 1920.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
S. Francavilla, P. D’Abrizio, N. Rucci, G. Silvano, G. Properzi, E. Straface, G. Cordeschi, S. Necozione, L. Gnessi, M. Arizzi, et al.
Fas and Fas Ligand Expression in Fetal and Adult Human Testis with Normal or Deranged Spermatogenesis
J. Clin. Endocrinol. Metab., August 1, 2000; 85(8): 2692 - 2700.
[Abstract] [Full Text]

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 J. Immunol.Home page
A. Riccioli, D. Starace, A. D'Alessio, G. Starace, F. Padula, P. De Cesaris, A. Filippini, and E. Ziparo
TNF-{alpha} and IFN-{gamma} Regulate Expression and Function of the Fas System in the Seminiferous Epithelium
J. Immunol., July 15, 2000; 165(2): 743 - 749.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
E. T. Donnelly, M. O'Connell, N. McClure, and S. E.M. Lewis
Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa
Hum. Reprod., July 1, 2000; 15(7): 1552 - 1561.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
L. Lustig, B. Denduchis, R. Ponzio, M. Lauzon, and R.-M. Pelletier
Passive Immunization with Anti-Laminin Immunoglobulin G Modifies the Integrity of the Seminiferous Epithelium and Induces Arrest of Spermatogenesis in the Guinea Pig
Biol Reprod, June 1, 2000; 62(6): 1505 - 1514.
[Abstract] [Full Text]

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 EndocrinologyHome page
J. H. Richburg, A. Nanez, L. R. Williams, M. E. Embree, and K. Boekelheide
Sensitivity of Testicular Germ Cells to Toxicant-Induced Apoptosis in gld Mice That Express a Nonfunctional Form of Fas Ligand
Endocrinology, February 1, 2000; 141(2): 787 - 793.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
W Yan, J Suominen, and J Toppari
Stem cell factor protects germ cells from apoptosis in vitro
J. Cell Sci., January 1, 2000; 113(1): 161 - 168.
[Abstract] [PDF]

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 Nephrol Dial TransplantHome page
A. Ortiz, C. Lorz, and J. Egido
The Fas ligand/Fas system in renal injury
Nephrol. Dial. Transplant., August 1, 1999; 14(8): 1831 - 1834.
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 EndocrinologyHome page
M. F. Taylor, M. de Boer-Brouwer, I. Woolveridge, K. J. Teerds, and I. D. Morris
Leydig Cell Apoptosis after the Administration of Ethane Dimethanesulfonate to the Adult Male Rat Is a Fas-Mediated Process
Endocrinology, August 1, 1999; 140(8): 3797 - 3804.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
M. Ikeda, H. Kodama, J. Fukuda, Y. Shimizu, M. Murata, J. Kumagai, and T. Tanaka
Role of Radical Oxygen Species in Rat Testicular Germ Cell Apoptosis Induced by Heat Stress
Biol Reprod, August 1, 1999; 61(2): 393 - 399.
[Abstract] [Full Text]

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 EndocrinologyHome page
K. A. Young, B. R. Zirkin, and R. J. Nelson
Short Photoperiods Evoke Testicular Apoptosis in White-Footed Mice (Peromyscus leucopus)
Endocrinology, July 1, 1999; 140(7): 3133 - 3139.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
S. Nandi, P. P. Banerjee, and B. R. Zirkin
Germ Cell Apoptosis in the Testes of Sprague Dawley Rats Following Testosterone Withdrawal by Ethane 1,2-Dimethanesulfonate Administration: Relationship to Fas?
Biol Reprod, July 1, 1999; 61(1): 70 - 75.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
V. Syed, E. Gomez, and N. B. Hecht
mRNAs Encoding a von Ebner's-like Protein and the Huntington Disease Protein Are Induced in Rat Male Germ Cells by Sertoli Cells
J. Biol. Chem., April 16, 1999; 274(16): 10737 - 10742.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. F. McClure, C. J. Heppelmann, and C. V. Paya
Constitutive Fas Ligand Gene Transcription in Sertoli Cells Is Regulated By Sp1
J. Biol. Chem., March 19, 1999; 274(12): 7756 - 7762.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. Lee, J. H. Richburg, E. B. Shipp, M. L. Meistrich, and K. Boekelheide
The Fas System, a Regulator of Testicular Germ Cell Apoptosis, Is Differentially Up-Regulated in Sertoli Cell Versus Germ Cell Injury of the Testis
Endocrinology, February 1, 1999; 140(2): 852 - 858.
[Abstract] [Full Text]

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 Am. J. Physiol. Endocrinol. Metab.Home page
V. Pentikainen, K. Erkkila, and L. Dunkel
Fas regulates germ cell apoptosis in the human testis in vitro
Am J Physiol Endocrinol Metab, February 1, 1999; 276(2): E310 - E316.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
I. Woolveridge, M. de Boer-Brouwer, M. F. Taylor, K. J. Teerds, F. C.W. Wu, and I. D. Morris
Apoptosis in the Rat Spermatogenic Epithelium Following Androgen Withdrawal: Changes in Apoptosis-Related Genes
Biol Reprod, February 1, 1999; 60(2): 461 - 470.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
C. P. Leo, S. Y. Hsu, E. A. McGee, M. Salanova, and A. J. W. Hsueh
DEFT, a Novel Death Effector Domain-Containing Molecule Predominantly Expressed in Testicular Germ Cells
Endocrinology, December 1, 1998; 139(12): 4839 - 4848.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
A. D'Alessio, A. Riccioli, P. Lauretti, F. Padula, B. Muciaccia, P. De Cesaris, A. Filippini, S. Nagata, and E. Ziparo
Testicular FasL is expressed by sperm cells
PNAS, March 13, 2001; 98(6): 3316 - 3321.
[Abstract] [Full Text] [PDF]


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