D-Aspartate Induces Proliferative Pathways in Spermatogonial GC-1 Cells

Journal of Cellular Physiology

Volumn 231, Issue 2, 2016, Pages 490-495

  Santillo, Alessandra ^a   Falvo, Sara ^a   Chieffi, Paolo ^a   Di Fiore, Maria Maddalena ^a   Senese, Rosalba ^a   Chieffi Baccari, Gabriella ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; ASPARTIC ACID; AURORA B KINASE; BETA ACTIN; CYCLINE; ESTROGEN RECEPTOR BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE B; AURKB PROTEIN, MOUSE; DEXTRO ASPARTIC ACID;

ANIMAL CELL; ARTICLE; CELL IMMORTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GERM CELL; MALE; MESSENGER RNA SYNTHESIS; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPERMATOGENESIS; SPERMATOGONIUM; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AROMATASE; AURORA KINASE B; CELL LINE; CELL PROLIFERATION; D-ASPARTIC ACID; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MODELS, BIOLOGICAL; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIA;

EID: 84944909686     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25095     Document Type: Article

References (58)

1. Aschim EL, Saether T, Wiger R, Grotmol T, Haugen TB. 2004. Differential distribution of splice variants of estrogen receptor beta in human testicular cells suggests specific functions in spermatogenesis. J Steroid Biochem Mol Biol 92:97-106.
2. Boscia F, Passaro C, Gigantino V, Perdonà S, Franco R, Portella G, Chieffi S, Chieffi P. 2015. High levels of GPR30 protein in human testicular carcinoma in situ and seminomas correlate with low levels of estrogen receptor-Beta and indicate a switch in estrogen responsiveness. J Cell Physiol 230:1290-1297.
3. Braydich-Stolle L, Kostereva N, Dym M, Hofmann MC. 2007. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 304:34-45.
4. Burrone L, Raucci F, Di Fiore MM. 2012a. Steroidogenic gene expression following D-aspartate treatment in frog testis. Gen Comp Endocrinol 175:109-117.
5. Burrone L, Santillo A, Pinelli C, Baccari GC, Di Fiore MM. 2012b. Induced synthesis of P450 aromatase and 17β-estradiol by D-aspartate in frog brain. J Exp Biol 215 3559-3565.
6. Carmena M, Earnshaw WC. 2003. The cellular geography of aurora kinases. Nat Rev Mol Cell Biol 4:842-854.
7. Carreau S, Bois C, Zanatta L, Silva FR, Bouraima-Lelong H, Delalande C. 2011a. Estrogen signaling in testicular cells. Life Sci 89:584-587.
8. Carreau S, Bouraima-Lelong H, Delalande C. 2011b. Estrogens: New players in spermatogenesis. Reprod Bio l11:174-193.
9. Carreau S, Bouraima-Lelong H, Delalande C. 2012. Role of estrogens in spermatogenesis. Front Biosci (Elite Ed) 4:1-11.
10. Castoria G, Migliaccio A, Bilancio A, Di Domenico M, de Falco A, Lombardi M, Fiorentino R, Varricchio L, Barone MV, Auricchio F. 2001. PI3-kinase in concert with Src promotes the S-phase entry of oestradiol-stimulated MCF-7 cells. EMBO J 20:6050-6059.
11. Chandler LJ, Sutton G, Dorairaj NR, Norwood D. 2001. N-methyl D-aspartate receptor-mediated bidirectional control of extracellular signal-regulated kinase activity in cortical neuronal cultures. J Biol Chem 276:2627-2636.
12. Chieffi P, Chieffi S. 2013. Molecular biomarkers as potential targets for therapeutic strategies in human testicular germ cell tumors: An overview. J Cell Physiol 228:1641-1646.
13. Chieffi P, Colucci-D'Amato GL, Guarino F, Salvatore G, Angelini F. 2002. 17-b estradiol induces spermatogonial proliferation through mitogen-activated protein kinase (extracellular signal-regulatedkinase 1) activity in the lizard (Podarciss. sicula). Mol Reprod Dev 61:218-225.
14. Ciraolo E, Morello F, Hobbs RM, Wolf F, Marone R, Iezzi M, Lu X, Mengozzi G, Altruda F, Sorba G, Guan K, Pandolfi PP, Wymann MP, Hirsch E. 2010. Essential role of the p110beta subunit of phosphoinositide 3-OH kinase in male fertility. Mol Biol Cell 21:704-711.
15. Cobb MH. 1999. MAP kinase pathways. ProgBiophysMolBio l71:479-500.
16. Coffer PJ, Jin J, Woodgett JR. 1998. Protein kinase B (c-Akt): A multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J 335:1-13.
17. D'Aniello A, Di Cosmo A, Di Cristo C, Annunziato L, Petrucelli L, Fisher G. 1996. Involvement of D-aspartic acid in the synthesis of testosterone in rat testes. Life Sci 59:97-104.
18. D'Aniello A, Di Fiore MM, Fisher GH, Milone A, Seleni A, D'Aniello S, Perna AF, Ingrosso D. 2000. Occurrence of D-aspartic acid and N-methyl-D-aspartic acid in rat neuroendocrine tissues and their role in the modulation of luteinizing hormone and growth hormone release. FASEB J 14:699-714.
19. D'Aniello G, Ronsini S, Guida F, Spinelli P, D'Aniello A. 2005. Occurrence of D-aspartic acid in human seminal plasma and spermatozoa: Possible role in reproduction. Fertil Steril 84:1444-1449.
20. D'Aniello A. 2007. D-Aspartic acid: An endogenous amino acid with an important neuroendocrine role. Brain Res Rev 53:215-234.
21. Di Fiore MM, Lamanna C, Assisi L, Botte V. 2008. Opposing effects of D-aspartic acid and nitric oxide on tuning of testosterone production in mallard testis during the reproductive cycle. Reprod Biol Endocrinol 6:28.
22. Di Fiore MM, Santillo A, Chieffi Baccari. 2014. Current knowledge of D-aspartate in glandular tissues. Amino Acids 46::1805-1818.
23. Esposito F, Libertini S, Franco R, Abagnale A, Marra L, Portella G, Chieffi P. 2009. Aurora B expression in post-puberal testicular germ cell tumours. J Cell Physiol 221:435-439.
24. Esposito F, Boscia F, Franco R, Tornincasa M, Fusco A, Kitazawa S, Looijenga LH, Chieffi P. 2011. Down-regulation of oestrogen receptor-β associates with transcriptional co-regulator PATZ1 delocalization in human testicular seminomas. J Pathol 224:110-120.
25. (2+)-dependent routes to Ras: Mechanisms for neuronal survival, differentiation, and plasticity?. Neuron 16:233-236.
26. Gill SS, Mueller RW, McGuire PF, Pulido OM. 2000. Potential target sites in peripheral tissues for excitatory neurotransmission and excitotoxicity. Toxicol Pathol 28:277-284.
27. Hasegawa K, Namekawa SH, Saga Y. 2013. MEK/ERK signaling directly and indirectly contributes to the cyclical self-renewal of spermatogonialstem cells. Stem Cells 31:2517-2527.
28. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Ström A, Treuter E, Warner M, Gustafsson JA. 2007. Estrogen receptors: How do they signal and what are their targets. Physiol Rev 87:905-931.
29. Hofmann MC, Narisawa S, Hess RA, Millan JL. 1992. Immortalization of germcells and somatic testicular cells using the SV40 large T antigen. Exp Cell Res 201:417-435.
30. Honda S, Harada N, Ito S, Takagi Y, Maeda S. 1998. Disruption of sexualbehavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19gene. Biochem Biophys Res Commun 252:445-449.
31. Jefferson WN, Couse JF, Banks EP, Korach KS, Newbold RR. 2000. Expression of estrogen receptor beta is developmentally regulated in reproductive tissues of male and female mice. Biol Reprod 62:310-317.
32. Lamanna C, Assisi L, Botte V, Di Fiore MM. 2006. Endogenous testicular D-aspartic acid regulates gonadal aromatase activity in boar. J Endocrinol Invest 29:141-146.
33. Lamanna C, Assisi L, Vittoria A, Botte V, Di Fiore MM. 2007a. D-Aspartic acid and nitric oxide as regulators of androgen production in boar testis. Theriogenology 67:249-254.
34. Lamanna C, Assisi L, Botte V, Di Fiore MM. 2007b. Involvement of D-Asp in P450 aromatase activity and estrogen receptors in boar testis. Amino Acids 32:45-51.
35. Merola E, Mattioli E, Minimo C, Zuo W, Rabitti C, Cicala M, Caviglia R, Pollice L, Gabbrielli A, Giordano A, Claudio PP. 2006. Immunohistochemical evaluation of pRb2/p130, VEGF, EZH2, p53, p16, p21waf-1, p27, and PCNA in Barrett's esophagus. J Cell Physiol 207:512-519.
36. Migliaccio A, Castoria G, Di Domenico M, De Falco A, Bilancio A, Lombardi M, Bottero D, Varricchio L, Nanayakkara M, Rotondi A, Auricchio F. 2004. Sex steroid hormones act as growth factors. J Steroid BiochemMol Biol 83:31-35.
37. Monteforte R, Santillo A, Di Giovanni M, D'Aniello A, Di Maro A, Chieffi Baccari. 2009. D-Aspartate affects secretory activity in rat Harderian gland: Molecular mechanism and functional significance. Amino Acids 37:653-664.
38. Nagata Y, Homma H, Lee J-A, Imai K. 1999a. D-Aspartate stimulation of testosterone synthesis in rat Leydig cells. FEBS Lett 444:160-164.
39. Nagata Y, Homma H, Matsumoto M, Imai K, 1999b. Stimulation of steroidogenic acute regulatory (StAR) gene expression by D-aspartate in rat Leydig cells. FEBS Lett 454:317-320.
40. Nitta H, Bunick D, Hess RA, Janulis L, Newton SC, Millette CF, Osawa Y, Shizuta Y, Toda K, Bahr JM. 1993. Germ cells of the mouse testis express P450 aromatase. Endocrinology 132:1396-1401.
41. Pentikäinen V, Erkkilä K, Suomalainen L, Parvinen M, Dunkel L. 2000. Estradiol acts as a germ cell survival factor in the human testis in vitro. J Clin Endocrinol Metab 85:2057-2067.
42. Portella G, Passaro C, Chieffi P. 2011. Aurora B: A new prognostic marker and therapeutic target in cancer. Curr Med Chem 18:482-496.
43. Raucci F, Di Fiore MM. 2009. The reproductive activity in the testis of Podarcis s. sicula involves D-aspartic acid: A study on c-kit receptor protein, tyrosine kinase activity and PCNA proteinduring annual sexual cycle. Gen Comp Endocrinol 161:373-383.
44. Raucci F, Di Fiore MM. 2011. D-Asp: A new player in reproductive endocrinology of the amphibianRana esculenta. J Chromatogr B Anal Technol Biomed Life Sci 879:3268-3276.
45. Raucci F, Assisi L, D'Aniello S, Spinelli P, Botte V, Di Fiore MM. 2004. Testicular endocrine activity is upregulated by D-aspartic acid in the green frog, Rana esculenta. J Endocrinol 182:365-376.
46. Raucci F, D'Aniello S, Di Fiore MM. 2005a. Endocrine roles of D-aspartic acid in the testis of lizard Podarcis s. sicula. J Endocrinol 187:347-359.
47. Raucci F, Santillo A, D'Aniello A, Chieffi P, Chieffi Baccari G. 2005b. D-aspartate modulates transcriptional activity in Harderian gland offrog, Rana esculenta: Morphological and molecular evidence. J Cell Physiol 204:445-454.
48. Robertson KM, O'Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI, Simpson ER. 1999. Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci US A96:7986-7991.
49. Sakai K, Homma H, Lee J-A, Fukushima T, Santa T, Tashiro K, Iwatsubo T, Imai K. 1998. Localization of D-aspartic acid in elongate spermatids in rat testis. Arch Biochem Biophys 351:96-105.
50. Santillo A, Pinelli C, Burrone L, Chieffi Baccari. 2013. D-Aspartic acid implication in the modulation of frog brain sex steroid levels. Gen Comp Endocrinol 181:72-76.
51. Santillo A, Falvo S, Chieffi P, Burrone L, Chieffi Baccari, Di Fiore S. 2014. D-Aspartate affects NMDA receptor-extracellular signal-regulated kinase pathway and upregulates androgen receptor expression in the rat testis. Theriogenology 81:744-751.
52. Selva DM, Tirado OM, Toran N, Suarez-Quian CA, Reventos J, Munell F. 2004. Estrogen receptor beta expression and apoptosis of spermatocytes of mice overexpressing a rat androgen binding protein transgene. Biol Reprod 71:1461-1468.
53. Simpson ER, Mahendroo MS, Means GD, Kilgore MW, Hinshelwood MM, Graham-Lorence S, Amarneh B, Ito Y, Fisher CR, Michael MD, Mendelson CR, Bulun SE. 1994. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr Rev 15:342-355.
54. Stabile V, Russo M, Chieffi P. 2006. 17beta-estradiol induces Akt-1 through estrogen receptor-beta in the frog (Rana esculenta) male germ cells. Reproduction 132:477-484.
55. Topo E, Soricelli A, D'Aniello A, Ronsini S, D'Aniello G. 2009. The role and molecular mechanism of D-aspartic acid in the release and synthesis of LH and testosterone in humans and rats. Reprod Biol Endocrinol 7:120.
56. Vicini E, Loiarro M, Di Agostino S, Corallini S, Capolunghi F, Carsetti R, Chieffi P, Geremia R, Stefanini M, Sette C. 2006. 17-beta-estradiol elicits genomic and non-genomic responses in mouse male germ cells. J Cell Physiol 206:238-245.
57. Vogiatzi P, Giordano A. 2007. Following the tracks of AKT1 gene. Cancer Biol Ther 6:1521-1524.
58. Zhang W, Dziak RM, Aletta JM. 1995. EGF-mediated phosphorylation of extracellular signal-regulated kinases in osteoblastic cells. J Cell Physiol 162:348-358.