The spatiotemporal expression changes of 16 epididymis-specific genes induced by testosterone, heat, and combination treatment in cynomolgus monkey
Xiangqi Li
College of Life Science, Sichuan University, Chengdu 610064, China
Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
These authors contributed equally to this work
Search for more papers by this authorQiang Liu
Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
These authors contributed equally to this work
Search for more papers by this authorShigui Liu
College of Life Science, Sichuan University, Chengdu 610064, China
Search for more papers by this authorXuesen Zhang
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China
Search for more papers by this authorYixun Liu
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China
Search for more papers by this authorCorresponding Author
Yonglian Zhang
Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
Shanghai Institute of Planned Parenthood Research, Shanghai 200032, China
*Corresponding author: Tel/Fax, 86-21-54921163; E-mail, [email protected]Search for more papers by this authorXiangqi Li
College of Life Science, Sichuan University, Chengdu 610064, China
Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
These authors contributed equally to this work
Search for more papers by this authorQiang Liu
Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
These authors contributed equally to this work
Search for more papers by this authorShigui Liu
College of Life Science, Sichuan University, Chengdu 610064, China
Search for more papers by this authorXuesen Zhang
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China
Search for more papers by this authorYixun Liu
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China
Search for more papers by this authorCorresponding Author
Yonglian Zhang
Shanghai Key Laboratory for Molecular Andrology, State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
Shanghai Institute of Planned Parenthood Research, Shanghai 200032, China
*Corresponding author: Tel/Fax, 86-21-54921163; E-mail, [email protected]Search for more papers by this authorThis study was supported by the grants from the National Natural Science Foundation of China (30230190 and 30570684), the National Basic Science Research and Development Project (2006CB504002 and 2006CB944002) and the Chinese Academy of Sciences Knowledge Innovation Program (No. KSCX1-YW-R-54)
Abstract
The experimental infertility model of treatments involving testicular warming, testosterone implant, and a combination of the two was developed to confirm a synergistic action induced by the combination treatment on germ cell apoptosis in cynomolgus monkey testis. Using this model, the spatio-temporal expression changes of 16 reported or novel genes in epididymis were investigated to examine the treatment's effect on epididymal genes. It was demonstrated that these region-specific genes, some of which were not regionally fixed, changed greatly with these treatments. The expression levels of these epididymal genes fluctuated, and the expression of most of the genes returned to nearly normal level at the end of treatments. Moreover, the expression changes resulting from the combination treatment were not more significant than those resulting from the single treatment. This suggests that the combination treatment has an antagonistic action on the expression of epididymal genes and that its effect is not as adverse on epididymis as that of the two single treatments.
References
- 1 Wu FC. Hormonal approaches to male contraception: approaching reality. Mol Cell Endocrinol 2006, 250: 2–7.
- 2 Lue YH, Hikim AP, Swerdloff RS, Im P, Taing KS, Bui T, Leung A et al. Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinology 1999, 140: 1709–1717.
- 3 Hikim AP, Wang C, Leung A, Swerdloff RS. Involvement of apoptosis in the induction of germ cell degeneration in adult rats after gonadotropin-releasing hormone antagonist treatment. Endocrinology 1995, 136: 2770–2775.
- 4 Sinha Hikim AP, Rajavashisth TB, Sinha Hikim I, Lue Y, Bonavera JJ, Leung A, Wang C et al. Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biol Reprod 1997, 57: 1193–1201.
- 5 Lue Y, Hikim AP, Wang C, Im M, Leung A, Swerdloff RS. Testicular heat exposure enhances the suppression of spermatogenesis by testosterone in rats: the “two-hit” approach to male contraceptive development. Endocrinology 2000, 141: 1414–1424.
- 6 Zhang XS, Yuan JX, Liu T, Lue YH, Jin X, Tao SX, Hu ZY et al. Expression of orphan receptors TR2, TR3, TR4, and p53 in heat-treated testis of cynomolgus monkeys (Macaca fascicularis). J Androl 2006, 27: 405–413.
- 7 Lue Y, Wang C, Liu YX, Hikim AP, Zhang XS, Ng CM, Hu ZY et al. Transient testicular warming enhances the suppressive effect of testosterone on spermatogenesis in adult cynomolgus monkeys (Macaca fascicularis). J Clin Endocrinol Metab 2006, 91: 539–545.
- 8 Zhang XS, Lue YH, Guo SH, Yuan JX, Hu ZY, Han CS, Hikim AP et al. Expression of HSP105 and HSP60 during germ cell apoptosis in the heat-treated testes of adult cynomolgus monkeys (Macaca fascicularis). Front Biosci 2005, 10: 3110–3121.
- 9 Sullivan R. Male fertility markers, myth or reality. Anim Reprod Sci 2004, 82-83: 341–347.
- 10 Brooks DE. Epididymal functions and their hormonal regulation. Aust J Biol Sci 1983, 36: 205–221.
- 11 Kirchhoff C. Gene expression in the epididymis. Int Rev Cytol 1999, 188: 133–202.
- 12 Reyes A, Chavarria ME. Interference with epididymal physiology as possible site of male contraception. Arch Androl 1981, 7: 159–168.
- 13 Perry AC, Jones R, Niang LS, Jackson RM, Hall L. Genetic evidence for an androgen-regulated epididymal secretory glutathione peroxidase whose transcript does not contain a selenocysteine codon. Biochem J 1992, 285: 863–870.
- 14 Perry AC, Jones R, Hall L. Identification of an abundant monkey epididymal transcript encoding a homologue of human CAMPATH-1 antigen precursor. Biochim Biophys Acta 1992, 1171: 122–124.
- 15 Perry AC, Jones R, Barker PJ, Hall L. A mammalian epididymal protein with remarkable sequence similarity to snake venom haemorrhagic peptides. Biochem J 1992, 286: 671–675.
- 16 Perry AC, Jones R, Hall L. The monkey ESP14.6 mRNA, a novel transcript expressed at high levels in the epididymis. Gene 1995, 153: 291–292.
- 17 Perry AC, Jones R, Moisyadi S, Coadwell J, Hall L. The novel epididymal secretory protein ESP13.2 in Macaca fascicularis. Biol Reprod 1999, 61: 965–972.
- 18 Sivashanmugam P, Richardson RT, Hall S, Hamil KG, French FS, O'Rand MG. Cloning and characterization of an androgen-dependent acidic epididymal glycoprotein/CRISPl-like protein from the monkey. J Androl 1999, 20: 384–393.
- 19 Hamil KG, Liu Q, Sivashanmugam P, Anbalagan M, Yenugu S, Soundararajan R, Grossman G et al. LCN6, a novel human epididymal lipocalin. Reprod Biol Endocrinol 2003, 1: 112.
- 20 Liu Q, Hamil KG, Sivashanmugam P, Grossman G, Soundararajan R, Rao AJ, Richardson RT et al. Primate epididymis-specific proteins: characterization of ESC42, a novel protein containing a trefoil-like motif in monkey and human. Endocrinology 2001, 142: 4529–4539.
- 21 Bedford JM, Berrios M, Dry den GL. Biology of the scrotum. IV. Testis location and temperature sensitivity. J Exp Zool 1982, 224: 379–388.
- 22 Foldesy RG, Bedford JM. Biology of the scrotum. I. Temperature and androgen as determinants of the sperm storage capacity of the rat cauda epididymidis. Biol Reprod 1982, 26: 673–682.
- 23 Rasweiler JJ 4th, Bedford JM. Biology of the scrotum. III. Effects of abdominal temperature upon the epithelial cells of the rat cauda epididymidis. Biol Reprod 1982, 26: 691–705.
- 24 Wong PY, Au CL, Bedford JM. Biology of the scrotum. II. Suppression by abdominal temperature of transepithelial ion and water transport in the cauda epididymidis. Biol Reprod 1982, 26: 683–689.
- 25 Zhou X, Wang J, Liu Q, Shen J, Zheng M, Zhang Y. Identification of the gene imds-60 in mouse epididymis. Acta Biochim Biophys Sin 2007, 39: 939–946.
- 26 Regalado F, Esponda P, Nieto A. Temperature and androgens regulate the biosynthesis of secretory proteins from rabbit cauda epididymidis. Mol Reprod Dev 1993, 36: 448–453.
- 27 Esponda P, Bedford JM. The influence of body temperature and castration on the protein composition of fluid in the rat cauda epididymidis. J Reprod Fertil 1986, 78: 505–514.
- 28 Fawcett DW, Hoffer AP. Failure of exogenous androgen to prevent regression of the initial segments of the rat epididymis after efferent duct ligation or orchidectomy. Biol Reprod 1979, 20: 162–181.
- 29 Holland MK, Vreeburg JT, Orgebin-Crist MC. Testicular regulation of epididymal protein secretion. J Androl 1992, 13: 266–273.
- 30 Sipila P, Pujianto DA, Shariatmadari R, Nikkila J, Lehtoranta M, Huhtaniemi IT, Poutanen M. Differential endocrine regulation of genes enriched in initial segment and distal caput of the mouse epididymis as revealed by genome-wide expression profiling. Biol Reprod 2006, 75: 240–251.
- 31 Syntin P, Dacheux JL, Dacheux F. Postnatal development and regulation of proteins secreted in the boar epididymis. Biol Reprod 1999, 61: 1622–1635.
- 32 Alvarez JG, Storey BT. Spontaneous lipid peroxidation in rabbit and mouse epididymal spermatozoa: dependence of rate on temperature and oxygen concentration. Biol Reprod 1985, 32: 342–351.
- 33 Jara M, Esponda P, Carballada R. Abdominal temperature induces region-specific p53-independent apoptosis in the cauda epididymidis of the mouse. Biol Reprod 2002, 67: 1189–1196.
- 34 Yaeram J, Setchell BP, Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev 2006, 18: 647–653.
- 35 Pera I, Ivell R, Kirchhoff C. Body temperature (37 °C) specifically down-regulates the messenger ribonucleic acid for the major sperm surface antigen CD52 in epididymal cell culture. Endocrinology 1996, 137: 4451–4459.
- 36 Rissman EF, Crews D. Effect of castration on epididymal sperm storage in male musk shrews (Suncus murinus) and mice (Mas musculus). J Reprod Fertil 1989, 86: 219–222.
- 37 Fan X, Robaire B. Orchidectomy induces a wave of apoptotic cell death in the epididymis. Endocrinology 1998, 139: 2128–2136.
- 38
Pera I,
Derr P,
Yeung CH,
Cooper TG,
Kirchhoff C.
Regionalized expression of CD52 in rat epididymis is related to mRNA poly(A) tail length.
Mol Reprod Dev
1997, 48: 433–441.
10.1002/(SICI)1098-2795(199712)48:4<433::AID-MRD3>3.0.CO;2-R CAS PubMed Web of Science® Google Scholar
- 39 Kappler-Hanno K, Kirchhoff C. Rodent epididymal cDNAs identified by sequence homology to human and canine counterparts. Asian J Androl 2003, 5: 277–286.
- 40 Chaturapanich G, Jones RC, Clulow J. Role of androgens in survival of spermatozoa in epididymis of tammar wallaby (Macropus eugenii). J Reprod Fertil 1992, 95: 421–429.
- 41 Hamil KG, Liu Q, Sivashanmugam P, Yenugu S, Soundararajan R, Grossman G, Richardson RT et al. Cystatin 11: a new member of the cystatin type 2 family. Endocrinology 2002, 143: 2787–2796.
- 42 Anderson RA, Baird DT. Male contraception. Endocr Rev 2002, 23: 735–762.
- 43 Cornwall GA, Hann SR. Specialized gene expression in the epididymis. J Androl 1995, 16: 379–383.
- 44 Lei ZM, Zou W, Mishra S, Li X, Rao Ch V. Epididymal phenotype in luteinizing hormone receptor knockout animals and its response to testosterone replacement therapy. Biol Reprod 2003, 68: 888–895.
- 45 Dahia CL, Rao AJ. Demonstration of follicle-stimulating hormone receptor in cauda epididymis of rat. Biol Reprod 2006, 75: 98–106.
- 46 Grover A, Smith CE, Gregory M, Cyr DG, Sairam MR, Hermo L. Effects of FSH receptor deletion on epididymal tubules and sperm morphology, numbers, and motility. Mol Reprod Dev 2005, 72: 135–144.