Regucalcin is broadly expressed in male reproductive tissues and is a new androgen-target gene in mammalian testis

Reproduction

Volumn 142, Issue 3, 2011, Pages 447-456

  Laurentino, S S ^a   Correia, S ^a   Cavaco, J E ^a   Oliveira, P F ^a   Rato, L ^a   Sousa, M ^b   Barros, A ^b,c   Socorro, S ^a  

^a UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c University of Porto   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; DIHYDROTACHYSTEROL; REGUCALCIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; EPIDIDYMIS; GERM CELL; GROUPS BY AGE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROSTATE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SEMINAL VESICLE; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE FLUID; SPERMATOGENESIS; TESTIS; UPREGULATION;

ANDROGENS; ANIMALS; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENITALIA, MALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MAMMALS; RATS; SERTOLI CELLS; SPERMATOGENESIS; TESTIS; TESTOSTERONE; TISSUE DISTRIBUTION;

MAMMALIA; RATTUS;

EID: 80051992405     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-11-0085     Document Type: Article

References (63)

1. Almeida S.A., Teofilo J.M., Anselmo Franci J.A., Brentegani LG & Lamano-Carvalho T.L. 2000 Antireproductive effect of the calcium channel blocker amlodipine in male rats. Experimental and Toxicologic Pathology 52 353-356. (Pubitemid 30663499)
2. Andersen C.L., Jensen JL & Orntoft T.F. 2004 Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research 64 5245-5250. (doi:10.1158/0008-5472.CAN-04-0496)
3. Benoff S., Cooper G.W., Hurley I., Mandel F.S., Rosenfeld D.L., Scholl G.M., Gilbert BR & Hershlag A. 1994 The effect of calcium ion channel blockers on sperm fertilization potential. Fertility and Sterility 62 606-617. (Pubitemid 24273213)
4. Carolan J.C., Fitzroy C.I., Ashton P.D., Douglas AE & Wilkinson T.L. 2009 The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9 2457-2467. (doi:10.1002/pmic. 200800692)
5. Erkkila K., Henriksen K., Hirvonen V., Rannikko S., Salo J., Parvinen M & Dunkel L. 1997 Testosterone regulates apoptosis in adult human seminiferous tubules in vitro. Journal of Clinical Endocrinology and Metabolism 82 2314-2321. (doi:10.1210/jc.82.7.2314)
6. Fisher D. 2002 New light shed on fluid formation in the seminiferous tubules of the rat. Journal of Physiology 542 445-452. (doi:10.1113/jphysiol. 2002.018648)
7. 2+ chelator and a calmodulin blocker interfere with the structure of inter-Sertoli junctions. Tissue & Cell 17 13-25. (doi:10.1016/0040-8166(85)90012-6)
8. Fujita T., Uchida K & Maruyama N. 1992 Purification of senescence marker protein-30 (SMP30) and its androgen-independent decrease with age in the rat liver. Biochimica et Biophysica Acta 1116 122-128. (doi:10.1016/0304- 4165(92)90108-7)
9. Fujita T., Shirasawa T., Uchida K & Maruyama N. 1996 Gene regulation of senescence marker protein-30 (SMP30): Coordinated up-regulation with tissue maturation and gradual down-regulation with aging. Mechanisms of Ageing and Development 87 219-229. (doi:10.1016/0047-6374(96)01711-3)
10. Geoffroy-Siraudin C., Perrard M.H., Chaspoul F., Lanteaume A., Gallice P., Durand P & Guichaoua M.R. 2010 Validation of a rat seminiferous tubule culture model as a suitable system for studying toxicant impact on meiosis effect of hexavalent chromium. Toxicological Sciences 116 286-296. (doi:10.1093/toxsci/kfq099)
11. Giampietri C., Petrungaro S., Coluccia P., D'Alessio A., Starace D., Riccioli A., Padula F., Palombi F., Ziparo E., Filippini A. et al. 2005 Germ cell apoptosis control during spermatogenesis. Contraception 72 298-302. (doi:10.1016/j.contraception.2005.04.011)
12. Gilleron J., Carette D., Carpentier F., Segretain D & Pointis G. 2009 Three-dimensional analysis of connexin 43 gap junction in the ex vivo rat seminiferous tubules: Short-term effects of hormonal effectors. Microscopy Research and Technique 72 845-855. (doi:10.1002/jemt.20731)
13. Gorczynska E & Handelsman D.J. 1995 Androgens rapidly increase the cytosolic calcium concentration in Sertoli cells. Endocrinology 136 2052-2059. (doi:10.1210/en.136.5.2052)
14. Gorczynska-Fjalling E. 2004 The role of calcium in signal transduction processes in Sertoli cells. Reproductive Biology 4 219-241.
15. Grima J., Wong C.C., Zhu L.J., Zong SD & Cheng C.Y. 1998 Testin secreted by Sertoli cells is associated with the cell surface, and its expression correlates with the disruption of Sertoli-germ cell junctions but not the inter-Sertoli tight junction. Journal of Biological Chemistry 273 21040-21053. (doi:10.1074/jbc.273.33.21040)
16. Hellemans J., Mortier G., De Paepe A., Speleman F & Vandesompele J. 2007 qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8 R19. (doi:10.1186/gb-2007-8-2-r19)
17. Inagaki S & Yamaguchi M. 2001 Regulatory role of endogenous regucalcin in the enhancement of nuclear deoxyribonuleic acid synthesis with proliferation of cloned rat hepatoma cells (H4-II-E). Journal of Cellular Biochemistry 82 704-711. (doi:10.1002/jcb.1193)
18. Ishigami A., Fujita T., Handa S., Shirasawa T., Koseki H., Kitamura T., Enomoto N., Sato N., Shimosawa T & Maruyama N. 2002 Senescence marker protein-30 knockout mouse liver is highly susceptible to tumor necrosis factor-alpha- and Fas-mediated apoptosis. American Journal of Pathology 161 1273-1281. (doi:10.1016/S0002-9440(10)64404-5)
19. Isogai M., Oishi K & Yamaguchi M. 1994a Serum release of hepatic calcium-binding protein regucalcin by liver injury with galactosamine administration in rats. Molecular and Cellular Biochemistry 136 85-90. (doi:10.1007/BF00931609)
20. Isogai M., Shimokawa N & Yamaguchi M. 1994b Hepatic calcium-binding protein regucalcin in released into the serum of rats administered orally carbon tetrachloride. Molecular and Cellular Biochemistry 131 173-179. (doi:10.1007/BF00925954)
21. Izumi T & Yamaguchi M. 2004a Overexpression of regucalcin suppresses cell death and apoptosis in cloned rat hepatoma H4-II-E cells induced by lipopolysaccharide, PD 98059, dibucaine, or Bay K 8644. Journal of Cellular Biochemistry 93 598-608. (doi:10.1002/jcb.20214)
22. Izumi T & Yamaguchi M. 2004b Overexpression of regucalcin suppresses cell death in cloned rat hepatoma H4-II-E cells induced by tumor necrosis factor-alpha or thapsigargin. Journal of Cellular Biochemistry 92 296-306. (doi:10.1002/jcb.20056)
23. Johnson C., Jia Y., Wang C., Lue Y.H., Swerdloff R.S., Zhang X.S., Hu Z.Y., Li Y.C., Liu YX & Hikim A.P. 2008 Role of caspase 2 in apoptotic signaling in primate and murine germ cells. Biology of Reproduction 79 806-814. (doi:10.1095/biolreprod.108.068833)
24. Juneja R., Gupta I., Wali A., Sanyal S.N., Chakravarti RN & Majumdar S. 1990 Effect of verapamil on different spermatozoal functions in guinea pigs - a preliminary study. Contraception 41 179-187. (doi:10.1016/0010-7824(90)90146- M)
25. Kaisman-Elbaz T., Sekler I., Fishman D., Karol N., Forberg M., Kahn N., Hershfinkel M & Silverman W.F. 2009 Cell death induced by zinc and cadmium is mediated by clusterin in cultured mouse seminiferous tubules. Journal of Cellular Physiology 220 222-229. (doi:10.1002/jcp.21754)
26. Kurota H & Yamaguchi M. 1996 Steroid hormonal regulation of calcium-binding protein regucalcin mRNA expression in the kidney cortex of rats. Molecular and Cellular Biochemistry 155 105-111. (doi:10.1007/BF00229307)
27. Lee J.H., Kim H., Kim DH & Gye M.C. 2006 Effects of calcium channel blockers on the spermatogenesis and gene expression in peripubertal mouse testis. Archives of Andrology 52 311-318. (doi:10.1080/01485010600664024)
28. Lee J.H., Ahn H.J., Lee S.J., Gye MC & Min C.K. 2011 Effects of L- and T-type Ca(2+) channel blockers on spermatogenesis and steroidogenesis in the prepubertal mouse testis. Journal of Assisted Reproduction and Genetics 28 23-30. (doi:10.1007/s10815-010-9480-x)
29. Lv S., Wei L., Wang J.H., Wang JY & Liu F. 2007 Identification of novel molecular candidates for acute liver failure in plasma of BALB/c murine model. Journal of Proteome Research 6 2746-2752. (doi:10.1021/pr0701759)
30. Lv S., Wang J.H., Liu F., Gao Y., Fei R., Du SC & Wei L. 2008 Senescence marker protein 30 in acute liver failure: Validation of a mass spectrometry proteomics assay. BMC Gastroenterology 8 17. (doi:10.1186/1471- 230X-8-17)
31. Maia C.J., Santos C.R., Schmitt F & Socorro S. 2008 Regucalcin is expressed in rat mammary gland and prostate and down-regulated by 17betaestradiol. Molecular and Cellular Biochemistry 311 81-86. (doi:10.1007/s11010-007-9697-x)
32. Maia C., Santos C., Schmitt F & Socorro S. 2009 Regucalcin is underexpressed in human breast and prostate cancers: Effect of sex steroid hormones. Journal of Cellular Biochemistry 107 667-676. (doi:10.1002/jcb.22158)
33. Manna P.R., Pakarinen P., El-Hefnawy T & Huhtaniemi I.T. 1999 Functional assessment of the calcium messenger system in cultured mouse Leydig tumor cells: Regulation of human chorionic gonadotropin-induced expression of the steroidogenic acute regulatory protein. Endocrinology 140 1739-1751. (doi:10.1210/en.140.4.1739)
34. Matsuyama S., Kitamura T., Enomoto N., Fujita T., Ishigami A., Handa S., Maruyama N., Zheng D., Ikejima K., Takei Y. et al. 2004 Senescence marker protein-30 regulates Akt activity and contributes to cell survival in Hep G2 cells. Biochemical and Biophysical Research Communications 321 386-390. (doi:10.1016/j.bbrc.2004.06.161)
35. Meachem S.J., Schlatt S., Ruwanpura SM & Stanton P.G. 2007 The effect of testosterone, dihydrotestosterone and oestradiol on the re-initiation of spermatogenesis in the adult photoinhibited Djungarian hamster. Journal of Endocrinology 192 553-561. (doi:10.1677/JOE-06-0136)
36. 2+channel blockade. Endocrinology 149 2517-2526. (doi:10.1210/en. 2007-1288)
37. 2+ signaling factors: involvement of protein kinase C. Molecular and Cellular Biochemistry 198 101-107. (doi:10.1023/A:1006996506238)
38. Nandi S., Banerjee PP & Zirkin B.R. 1999 Germ cell apoptosis in the testes of Sprague-Dawley rats following testosterone withdrawal by ethane 1,2- dimethanesulfonate administration: Relationship to Fas? Biology of Reproduction 61 70-75. (doi:10.1095/biolreprod61.1.70)
39. Oliveira P.F., Sousa M., Barros A., Moura T & Rebelo da Costa A. 2009a Membrane transporters and cytoplasmatic pH regulation on bovine Sertoli cells. Journal of Membrane Biology 227 49-55. (doi:10.1007/s00232-008-9139-z)
40. Oliveira P.F., Sousa M., Barros A., Moura T & Rebelo da Costa A. 2009b Intracellular pH regulation in human Sertoli cells: Role of membrane transporters. Reproduction 137 353-359. (doi:10.1530/REP-08-0363)
41. Oliver V.L., Anderson C., Ventura S & Haynes J.M. 2010 Androgens regulate adenylate cyclase activity and intracellular calcium in stromal cells derived from human prostate. Prostate 70 1222-1232. (doi:10.1002/pros.21157)
42. Omura M & Yamaguchi M. 1999 Effect of anti-regucalcin antibody on neutral phosphatase activity in rat liver cytosol: Involvement of endogenous regucalcin. Molecular and Cellular Biochemistry 197 25-29. (doi:10.1023/A: 1006979606225)
43. O'Shaughnessy P.J., Verhoeven G., De Gendt K., Monteiro A & Abel M.H. 2010 Direct action through the Sertoli cells is essential for androgen stimulation of spermatogenesis. Endocrinology 151 2343-2348. (doi:10.1210/en.2009-1333)
44. Otomo Y & Yamaguchi M. 2006 Regulatory effect of exogenous regucalcin on cell function in osteoblastic MC3T3-E1 cells: Involvement of intracellular signaling factor. International Journal of Molecular Medicine 18 321-327.
45. Pandey A.K., Li W., Yin X., Stocco D.M., Grammas P & Wang X. 2010 Blocking L-type calcium channels reduced the threshold of cAMP-induced steroidogenic acute regulatory gene expression in MA-10 mouse Leydig cells. Journal of Endocrinology 204 67-74. (doi:10.1677/JOE-09-0206)
46. Pentikainen V., Erkkila K., Suomalainen L., Parvinen M & Dunkel L. 2000 Estradiol acts as a germ cell survival factor in the human testis in vitro. Journal of Clinical Endocrinology and Metabolism 85 2057-2067. (doi:10.1210/jc.85.5.2057)
47. Popova N.Y., Dukhanin AS & Shimanovskii N.L. 2007 Nongenomic effect of androgens on Ca(2+) concentration in human lymphocytes. Bulletin of Experimental Biology and Medicine 143 605-607. (doi:10.1007/s10517-007-0193-9)
48. Print CG & Loveland K.L. 2000 Germ cell suicide: New insights into apoptosis during spermatogenesis. BioEssays 22 423-430. (doi:10.1002/(SICI)1521- 1878(200005)22:5⟨423::AID-BIES4⟩3.0.CO;2-0)
49. Shimokawa N & Yamaguchi M. 1992 Calcium administration stimulates the expression of calcium-binding protein regucalcin mRNA in rat liver. FEBS Letters 305 151-154. (doi:10.1016/0014-5793(92)80884-J)
50. 2+/calmodulin in rat liver. FEBS Letters 316 79-84. (doi:10.1016/0014-5793(93)81740-Q)
51. Singh J., O'Neill C & Handelsman D.J. 1995 Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology 136 5311-5321. (doi:10.1210/en.136.12.5311)
52. Sousa M., Cremades N., Silva J., Oliveira C., Ferraz L., Teixeira da Silva J., Viana P & Barros A. 2002a Predictive value of testicular histology in secretory azoospermic subgroups and clinical outcome after microinjection of fresh and frozen-thawed sperm and spermatids. Human Reproduction 17 1800-1810. (doi:10.1093/humrep/17.7.1800)
53. Sousa M., Cremades N., Alves C., Silva J & Barros A. 2002b Developmental potential of human spermatogenic cells co-cultured with Sertoli cells. Human Reproduction 17 161-172. (doi:10.1093/humrep/17.1.161)
54. Tesarik J., Martinez F., Rienzi L., Iacobelli M., Ubaldi F., Mendoza C & Greco E. 2002 In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Human Reproduction 17 1811-1819. (doi:10.1093/humrep/ 17.7.1811)
55. Tsurusaki Y & Yamaguchi M. 2004 Role of regucalcin in liver nuclear function: Binding of regucalcin to nuclear protein or DNA and modulation of tumor-related gene expression. International Journal of Molecular Medicine 14 277-281.
56. Turner T.T., Jones C.E., Howards S.S., Ewing L.L., Zegeye B & Gunsalus G.L. 1984 On the androgen microenvironment of maturing spermatozoa. Endocrinology 115 1925-1932. (doi:10.1210/endo-115-5-1925)
57. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A & Speleman F. 2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3 RESEARCH0034. (doi:10.1186/gb-2002-3-7-research0034)
58. Vera Y., Erkkila K., Wang C., Nunez C., Kyttanen S., Lue Y., Dunkel L., Swerdloff RS & Sinha Hikim A.P. 2006 Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signaling of murine and human male germ cells after hormone deprivation. Molecular Endocrinology 20 1597-1609. (doi:10.1210/me.2005-0395)
59. Yamaguchi M. 2005 Role of regucalcin in maintaining cell homeostasis and function (review). International Journal of Molecular Medicine 15 371-389.
60. Yamaguchi M & Kurota H. 1995 Expression of calcium-binding protein regucalcin mRNA in the kidney cortex of rats: The stimulation by calcium administration. Molecular and Cellular Biochemistry 146 71-77. (doi:10.1007/BF00926884)
61. Yamaguchi M & Oishi K. 1995 17 beta-Estradiol stimulates the expression of hepatic calcium-binding protein regucalcin mRNA in rats. Molecular and Cellular Biochemistry 143 137-141. (doi:10.1007/BF01816947)
62. Yamaguchi M & Yamamoto T. 1978 Purification of calcium binding substance from soluble fraction of normal rat liver. Chemical & Pharmaceutical Bulletin 26 1915-1918.
63. Yamaguchi M., Otomo Y., Uchiyama S & Nakagawa T. 2008 Hormonal regulation of regucalcin mRNA expression in osteoblastic MC3T3-E1 cells. International Journal of Molecular Medicine 21 771-775.