ADAM17 As Inducer of Male Germ Cell Apoptosis

ADAM17 As Inducer of Male Germ Cell Apoptosis

Contenido principal del artículo

Ricardo Moreno

Resumen

Apoptosis during mammalian spermatogenesis is important to control sperm output and to eliminate damaged unwanted cells. A deregulation in apoptosis rate has deleterious consequences and leads to low sperm production. Apoptosis in spermatogenesis has been widely studied, but the mechanism by which it is induced under physiological or pathological conditions has not been clarified. We have recently identified the metalloprotease ADAM17 (TACE) as a putative physiological inducer of germ cell apoptosis. ADAM17 is widely distributed enzyme in many tissues, its main function is to shed (release) its substrates, which leads to the activation of different signaling pathways according to the cellular context. However, in spermatogenesis, ADAM17 is involved in the control or induction of germ cell apoptosis, this seems to be unique and may reflect the complexity of spermatogenesis. In this review I will focus on the published evidence that show how this enzyme involved in the control of germ cell apoptosis during physiological condition and in different insults such as heat stress, DNA damaging agent or endocrine disruptors.

Citas

Allemand, I.; Anglo, A.; Jeantet, A. Y.; Cerutti, I. & May, E. Testicular wild-type p53 expression in transgenic mice induces spermiogenesis alterations ranging from differentiation defects to apoptosis. Oncogene, 18(47):6521-30, 1999.

Bedell, M. A. & Mahakali Zama, A. Genetic analysis of Kit ligand functions during mouse spermatogenesis. J. Androl., 25(2):188-99, 2004.

Beumer, T. L.; Roepers-Gajadien, H. L.; Gademan, I. S.; van Buul, P. P.; Gil-Gomez, G.; Rutgers, D. H. & de Rooij, D. G. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ., 5(8):669-77, 1998.

Black, R. A.; Rauch, C. T.; Kozlosky, C. J.; Peschon, J. J.; Slack, J. L.; Wolfson, M. F.; Castner, B. J.; Stocking, K. L.; Reddy, P.; Srinivasan, S.; Nelson, N.; Boiani, N.; Schooley, K. A.; Gerhart, M.; Davis, R.; Fitzner, J. N.; Johnson, R. S.; Paxton, R. J.; March, C. J. & Cerretti, D. P. A metalloproteinase disintegrin that releases tumour-necrosis factoralpha from cells. Nature, 385(6618):729-33, 1997.

Blobel, C. P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol., 6(1):32- 43, 2005.

Calafat, A. M.; Kuklenyik, Z.; Reidy, J. A.; Caudill, S. P.; Ekong, J. & Needham, L. L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ. Health Perspect., 113(4):391-5, 2005.

Codelia, V. A.; Cisterna, M.; Alvarez, A. R. & Moreno, R. D. p73 participates in male germ cells apoptosis induced by etoposide. Mol. Hum. Reprod., 16(10):734-42, 2010.

Codelia, V. A.; Cisternas, P. & Moreno, R. D. Relevance of caspase activity during apoptosis in pubertal rat spermatogenesis. Mol. Reprod. Dev., 75(5):881- 9, 2008.

Comitato, R.; Esposito, T.; Cerbo, G.; Angelini, F.; Varriale, B. & Cardone, A. Impairment of spermatogenesis and enhancement of testicular germ cell apoptosis induced by exogenous all-transretinoic acid in adult lizard Podarcis sicula. J. Exp. Zool. A Comp. Exp. Biol., 305(3):288-98, 2006.

Coureuil, M.; Fouchet, P.; Prat, M.; Letallec, B.; Barroca, V.; Dos Santos, C.; Racine, C. & Allemand, I. Caspaseindependent death of meiotic and postmeiotic cells overexpressing p53: calpain involvement. Cell Death Differ., 13(11):1927-37, 2006.

Cruz, A. C.; Frank, B. T.; Edwards, S. T.; Dazin, P. F.; Peschon, J. J. & Fang, K. C. Tumor necrosis factoralpha-converting enzyme controls surface expression of c-Kit and survival of embryonic stem cell-derived mast cells. J. Biol. Chem., 279(7):5612-20, 2004.

Chitra, K. C.; Latchoumycandane, C. & Mathur, P. P. Effect of nonylphenol on the antioxidant system in epididymal sperm of rats. Arch. Toxicol., 76(9):545- 51, 2002.

D'Alessio, A.; Riccioli, A.; Lauretti, P.; Padula, F.; Muciaccia, B.; De Cesaris, P.; Filippini, A.; Nagata, S. & Ziparo, E. Testicular FasL is expressed by sperm cells. Proc. Natl. Acad. Sci. U. S. A., 98(6):3316- 21, 2001.

Degterev, A. & Yuan, J. Expansion and evolution of cell death programmes. Nat. Rev. Mol. Cell Biol., 9(5):378-90, 2008.

Elliott, M. R.; Zheng, S.; Park, D.; Woodson, R. I.; Reardon, M. A.; Juncadella, I. J.; Kinchen, J. M.; Zhang, J.; Lysiak, J. J. & Ravichandran, K. S. Unexpected requirement for ELMO1 in clearance of apoptotic germ cells in vivo. Nature, 467(7313):333-7, 2010.

Feng, H. L.; Sandlow, J. I.; Sparks, A. E.; Sandra, A. & Zheng, L. J. Decreased expression of the c-kit receptor is associated with increased apoptosis in subfertile human testes. Fertil. Steril., 71(1):85- 9, 1999.

Francavilla, S.; D'Abrizio, P.; Cordeschi, G.; Pelliccione, F.; Necozione, S.; Ulisse, S.; Properzi, G. & Francavilla, F. Fas expression correlates with human germ cell degeneration in meiotic and postmeiotic arrest of spermatogenesis. Mol. Hum. Reprod., 8(3):213-20, 2002.

Francavilla, S.; D'Abrizio, P.; Rucci, N.; Silvano, G.; Properzi, G.; Straface, E.; Cordeschi, G.; Necozione, S.; Gnessi, L.; Arizzi, M. & Ulisse, S. Fas and Fas ligand expression in fetal and adult human testis with normal or deranged spermatogenesis. J. Clin. Endocrinol. Metab., 85(8):2692-700, 2000.

Giammona, C. J.; Sawhney, P.; Chandrasekaran, Y. & Richburg, J. H. Death receptor response in rodent testis after mono-(2-ethylhexyl) phthalate exposure. Toxicol. Appl. Pharmacol., 185(2):119- 27, 2002.

Gould, J. C.; Leonard, L. S.; Maness, S. C.; Wagner, B. L.; Conner, K.; Zacharewski, T.; Safe, S.; McDonnell, D. P. & Gaido, K. W. Bisphenol A interacts with the estrogen receptor alpha in a distinct manner from estradiol. Mol. Cell. Endocrinol., 142(1-2):203-14, 1998.

Henkler, F.; Behrle, E.; Dennehy, K. M.; Wicovsky, A.; Peters, N.; Warnke, C.; Pfizenmaier, K. & Wajant, H. The extracellular domains of Fas L and Fas are sufficient for the formation of supramolecular FasL-Fas clusters of high stability. J. Cell Biol., 168(7):1087-98, 2005.

Hu, Y.; Li, D.; Lu, Y. & Han, X. Monobutyl phthalate induces the expression change of G-ProteinCoupled Receptor 30 in rat testicular Sertoli cells. Folia Histochem. Cytobiol., 51(1):18-24, 2013.

Inoue, K.; Wada, M.; Higuchi, T.; Oshio, S.; Umeda, T.; Yoshimura, Y. & Nakazawa, H. Application of liquid chromatography-mass spectrometry to the quantification of bisphenol A in human semen. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 773(2):97-102, 2002.

Jahnukainen, K.; Chrysis, D.; Hou, M.; Parvinen, M.; Eksborg, S. & Söder, O. Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis. Biol. Reprod., 70(2):290-6, 2004.

Knudson, C. M.; Tung, K. S.; Tourtellotte, W. G.; Brown, G. A. & Korsmeyer, S. J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science, 270(5233):96-9, 1995.

Kua, C. Y. & Kuida, K. Cell death in mammalian development. In: Yin, X. M. & Dong, Z. (Eds.). Essential of Apoptosis: A guide for basic and Clinical Research. Totowa, Humana Press, 2003.

Kuribayashi, K.; Mayes, P. A. & El-Deiry, W. S. What are caspases 3 and 7 doing upstream of the mitochondria? Cancer Biol. Ther., 5(7):763-5,2006.

Lagos-Cabré, R. & Moreno, R. D. Contribution of environmental pollutants to male infertily: a working model of germ cell apoptosis induced by plasticizers. Biol. Res., 45(1):5-14, 2012.

Lee, J.; Richburg, J. H.; Shipp, E. B.; Meistrich, M. L. & Boekelheide, K. The Fas system, a regulator of testicular germ cell apoptosis, is differentially upregulated in Sertoli cell versus germ cell injury of the testis. Endocrinology, 140(2):852-8, 1999.

Lee, J.; Richburg, J. H.; Younkin, S. C. & Boekelheide, K. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology, 138(5):2081-8, 1997.

Lee, J. D.; Lee, T. H.; Cheng, W. H. & Jeng, S. Y. Involved intrinsic apoptotic pathway of testicular tissues in varicocele-induced rats. World J. Urol., 27(4):527-32, 2009.

Lizama, C.; Lagos, C. F.; Lagos-Cabré, R.; Cantuarias, L.; Rivera, F.; Huenchuñir, P.; Pérez-Acle, T.; Carrión, F. & Moreno, R. D. Calpain inhibitors prevent p38 MAPK activation and germ cell apoptosis after heat stress in pubertal rat testes. J. Cell Physiol., 221(2):296-305, 2009.

Lizama, C.; Ludwig, A. & Moreno, R. D. Etoposide induces apoptosis and upregulation of TACE/ ADAM17 and ADAM10 in an in vitro male germ cell line model. Biochim. Biophys. Acta, 1813(1):120-8, 2011a.

Lizama, C.; Rojas-Benítez, D.; Antonelli, M.; Ludwig, A.; Bustamante-Marín, X.; Brouwer-Visser, J. & Moreno, R. D. TACE/ADAM17 is involved in germ cell apoptosis during rat spermatogenesis. Reproduction, 140(2):305-17, 2010c.

Lizama, C.; Rojas-Benitez, D.; Antonelli, M.; Ludwig, A. & Moreno, R. D. Involvement of TACE/ADAM17 and ADAM10 in etoposide-induced apoptosis of germ cells in rat spermatogenesis. J. Cell. Physiol., 227(2):829-38, 2011b.

Main, K. M.; Mortensen, G. K.; Kaleva, M. M.; Boisen, K. A.; Damgaard, I. N.; Chellakooty, M.; Schmidt, I. M.; Suomi, A. M.; Virtanen, H. E.; Petersen, D. V.; Andersson, A. M.; Toppari, J. & Skakkebaek, N. E. Human breast milk contamination with phthalates and alterations of endogenous reproductive hormones in infants three months of age. Environ. Health Perspect., 114(2):270-6, 2006.

Matsui, J.; Wakabayashi, T.; Asada, M.; Yoshimatsu, K. & Okada, M. Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells. J. Biol. Chem., 279(18):18600-7, 2004.

Meeker, J. D. & Ferguson, K. K. Relationship between urinary phthalate and bisphenol A concentrations and serum thyroid measures in U.S. adults and adolescents from the National Health and Nutrition Examination Survey (NHANES) 2007-2008.

Environ. Health Perspect., 119(10):1396-402, 2011.

Moreno, R. D.; Lizama, C.; Urzúa, N.; Vergara, S. P. & Reyes, J. G. Caspase activation throughout the first wave of spermatogenesis in the rat. Cell Tissue Res., 325(3):533-40, 2006.

Moreno, R. D.; Urriola-Muñoz, P. & Lagos-Cabré, R. The emerging role of matrix metalloproteases of the ADAM family in male germ cell apoptosis. Spermatogenesis, 1(3):195-208, 2011.

Oakberg, E. F. A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am. J. Anat., 99(3):391-413, 1956.

Ortiz, R. J.; Lizama, C.; Codelia, V. A. & Moreno, R. D. A molecular evaluation of germ cell death induced by etoposide in pubertal rat testes. Mol. Hum. Reprod., 15(6):363-71, 2009.

Ott, M.; Gogvadze, V.; Orrenius, S. & Zhivotovsky, B. Mitochondria, oxidative stress and cell death. Apoptosis, 12(5):913-22, 2007.

Park, S. H.; Kim, K. Y.; An, B. S.; Choi, J. H.; Jeung, E. B.; Leung, P. C. & Choi, K. C. Cell growth of ovarian cancer cells is stimulated by xenoestrogens through an estrogen-dependent pathway, but their stimulation of cell growth appears not to be involved in the activation of the mitogen-activated protein kinases ERK-1 and p38. J. Reprod. Dev., 55(1):23- 9, 2009.

Reyes, J. G.; Farias, J. G.; Henriquez-Olavarrieta, S.; Madrid, E.; Parraga, M.; Zepeda, A. B. & Moreno, R. D. The hypoxic testicle: physiology and pathophysiology. Oxid. Med. Cell Longev., 2012:929285, 2012.

Riedl, S. J. & Shi, Y. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol., 5(11):897-907, 2004.

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. E. M. B. O. J., 16(9):2262-70, 1997.

Rönnstrand, L. Signal transduction via the stem cell factor receptor/c-Kit. Cell. Mol. Life Sci., 61(19- 20):2535-48, 2004.

Salian, S.; Doshi, T. & Vanage, G. Neonatal exposure of male rats to Bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis. Toxicology, 265(1-2):56-67, 2009.

Salvesen, G. S. Caspases: opening the boxes and interpreting the arrows. Cell Death Differ., 9(1):3- 5, 2002.

Shi, Y. Apoptosome: the cellular engine for the activation of caspase-9. Structure, 10(3):285-8, 2002.

Sinawat, S. The environmental impact on male fertility. J. Med. Assoc. Thai., 83(8):880-5, 2000.

Squier, M. K. & Cohen, J. J. Calpain and cell death. Cell Death Differ., 3(3):275-83, 1996.

Swan, S. H.; Main, K. M.; Liu, F.; Stewart, S. L.; Kruse, R. L.; Calafat, A. M.; Mao, C. S.; Redmon, J. B.; Ternand, C. L.; Sullivan, S.; Teague, J. L. & Study for Future Families Research Team. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ. Health Perspect., 113(8):1056-61, 2005.

Tanuma, S. I. Molecular mechanisms of apoptosis. In: Sluyser, M. (Eds.). Apoptosis in Normal Development and Cancer. Bristol, Taylor and Francis, 1996. pp. 39-61.

Tomasini, R.; Tsuchihara, K.; Wilhelm, M.; Fujitani, M.; Rufini, A.; Cheung, C. C.; Khan, F.; Itie-Youten, A.; Wakeham, A.; Tsao, M. S.; Iovanna, J. L.; Squire, J.; Jurisica, I.; Kaplan, D.; Melino, G.; Jurisicova, A. & Mak, T. W. TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev., 22(19):2677-91, 2008.

Urriola-Muñoz, P.; Lagos-Cabré, R. & Moreno, R. D. A mechanism of male germ cell apoptosis induced by bisphenol-A and nonylphenol involving ADAM17 and p38 MAPK activation. PLoS One, 9(12):e113793, 2014a.

Urriola-Muñoz, P.; Lizama, C.; Lagos-Cabré, R.; Reyes, J. G. & Moreno, R. D. Differential expression and localization of ADAM10 and ADAM17 during rat spermatogenesis suggest a role in germ cell differentiation. Biol. Res., 47:31, 2014b. Vera, Y.; Rodriguez, S.; Castanares, M.; Lue, Y.; Atienza, V.; Wang, C.; Swerdloff, R. S. & Sinha Hikim, A. P. Functional role of caspases in heat-induced testicular germ cell apoptosis. Biol. Reprod., 72(3):516-22, 2005.

Watanabe, H.; Suzuki, A.; Goto, M.; Lubahn, D. B.; Handa, H. & Iguchi, T. Tissue-specific estrogenic and non-estrogenic effects of a xenoestrogen, nonylphenol. J. Mol. Endocrinol., 33(1):243-52, 2004.

Weikert, S.; Schrader, M.; Müller, M.; Krause, H. & Miller, K. Expression of the apoptosis inhibitor survivin in testicular tissue of infertile patients. Int. J. Androl., 27(3):161-5, 2004.

White Lab. Table of the ADAMs. Charlottesville, University of Virginia, School of Medicine, Department of Cell Biology, 2015. Available from: http://people.virginia.edu/~jw7g/ Table_of_the_ADAMs.html. White, J. M.; Bridges, L.; DeSimone, D.; Tomezuk, M. & Wolfsberg, T. G. Introduction to the ADAM Family. In: Hooper, N. M.; Lendeckel, U. (Eds.). The ADASM family of Proteases. Dordrecht, Springer, 2005.pp.1-29.