Advertisement

Thimet oligopeptidase and prolyl endopeptidase of spotted scat Scatophagus argus: characterization, tissue distribution, expression at different ovarian stages and down-regulation by estradiol

  • Si-ping Deng
  • Dong-neng Jiang
  • Jian-ye Liu
  • Zhi-qi Liang
  • Hua-pu Chen
  • Tian-li Wu
  • Chun-hua Zhu
  • Guang-li Li
Original Article Biology

Abstract

Thimet oligopeptidase (Top) is a thiol-sensitive metallopeptidase with increased concentrations in brain and reproductive tissues. Prolyl endopeptidase (Pep) is another endopeptidase with high enzymatic activity in the brain. The two neuropeptidases are involved in the degradation of gonadotropin-releasing hormone. To clarify their roles in reproductive regulation, the spotted scat top (sstop) and pep (sspep) genes were cloned and analyzed. Tissue distribution by RT-PCR showed that sstop and sspep were more highly expressed in reproduction-related tissues than in other tissues. The sstop and sspep mRNA was detected in female hypothalamuses at phase II (oocytes at the perinuclear stage), phase III (oocytes forming the vitelline vesicle) and phase IV (oocytes at lipidic and proteic vitellogenesis stages). Both sstop and sspep were highly expressed in phase III, moderately in phase IV, and the lowest in phase II. The sstop and sspep genes were down-regulated in hypothalamuses after treatment with estradiol both in vitro and in vivo. It is suggested that Sstop and Sspep play significant roles in the regulation of reproduction and these results suggested an ssTop- and ssPep-mediated positive feedback mechanism of ovarian function.

Keywords

Scatophagus argus Thimet oligopeptidase Prolyl endopeptidase Hypothalamuses 17β-Estradiol 

Abbreviations

Top

Thimet oligopeptidase

Pep

Prolyl endopeptidase

E2

17β-Estradiol

sstop

Spotted scat top

sspep

Spotted scat pep

Notes

Acknowledgements

This study was supported by the Natural Science Foundation of Guangdong Province (2016A030313743, 2017A030313101); Marine Fishery Science and Technology Extension Projects of Guangdong (A201608B01, 2017A0012); Introduction of Talent Research Project of Guangdong Ocean University (0712103); The National Natural Science Foundation of China (41706174, 31702326); Zhanjiang Science and Technology Bureau (2016A03017) and the College Students’ Innovation and Entrepreneurship Project (201610566007, CXXL2018132).

Compliance with ethical standards

Human and animal rights

All animal experiments throughout the study were conducted in accordance with the Regulations for the Administration of Affairs Concerning Experimental Animals for the Science and Technology Bureau of China.

References

  1. Agirregoitia N, Irazusta A, Ruiz F, Irazusta J, Gil J (2003) Ontogeny of soluble and particulate prolyl endopeptidase activity in several areas of the rat brain and in the pituitary gland. Dev Neurosci 25(5):316–323CrossRefPubMedGoogle Scholar
  2. Agirregoitia N, Bizet P, Agirregoitia E, Boutelet I, Peralta L, Vaudry H, Jégou S (2010) Prolyl endopeptidase mRNA expression in the central nervous system during rat development. J Chem Neuroanat 40(1):53–62CrossRefPubMedGoogle Scholar
  3. Bellemère G, Vaudry H, Mounien L, Boutelet I, Jégou S (2004) Localization of the mRNA encoding prolyl endopeptidase in the rat brain and pituitary. J Comp Neurol 471(2):128–143CrossRefPubMedGoogle Scholar
  4. Bourguignon JP, Alvarez Gonzalez ML, Gerard A, Franchimont P (1994) Gonadotropin releasing hormone inhibitory autofeedback by subproducts antagonist at n-methyl-d-aspartate receptors: a model of autocrine regulation of peptide secretion. Endocrinology 134(3):1589–1592CrossRefPubMedGoogle Scholar
  5. Brandt I, Scharpé S, Lambeir AM (2007) Suggested functions for prolyl oligopeptidase: a puzzling paradox. Clin Chim Acta 377(1–2):50–61CrossRefPubMedGoogle Scholar
  6. Bruce LA, Cyr NE, Qiao JW, Defries CC, Tetel MJ, Wolfson AJ (2012) Neuropeptidase activity is down-regulated by estradiol in steroid-sensitive regions of the hypothalamus in female mice. Neuropeptides 46(4):167–172CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cai ZP, Yi W, Hu JW, Zhang JB, Lin YG (2010) Reproductive biology of Scatophagus argus and artificial induction of spawning. J Trop Oceanogr 29(5):180–185Google Scholar
  8. Chu TG, Orlowski M (1985) Soluble metalloendopeptidase from rat brain: action on enkephalin-containing peptides and other bioactive peptides. Endocrinology 116(4):1418–1425CrossRefPubMedGoogle Scholar
  9. Cleverly K, Wu TJ (2010) Is the metalloendopeptidase EC 3.4.24.15 (ep24.15), the enzyme that cleaves luteinizing hormone-releasing hormone (lhrh), an activating enzyme? Reproduction 139(2):319–330CrossRefPubMedGoogle Scholar
  10. Cui XF (2017) Molecular cloning of gonadotropin-releasing hormones and their regulatory functions in reproduction in Scatophagus argus. PhD dissertation, Guangdong Ocean University, ZhanjiangGoogle Scholar
  11. Cui XF, Zhao Y, Chen HP, Deng SP, Jiang DN, Wu TL, Zhu CH, Li GL (2017) Cloning, expression and functional characterization on vitellogenesis of estrogen receptors in Scatophagus argus. Gen Comp Endocr 246:37–45CrossRefPubMedGoogle Scholar
  12. Cyr NE, Kua LH, Bruce LA, Chadwick JG, Tetel MJ, Wolfson AJ (2010) Nuclear thimet oligopeptidase is coexpressed with oestrogen receptor alpha in hypothalamic cells and regulated by oestradiol in female mice. J Neuroendocrinol 22(8):936–943PubMedPubMedCentralGoogle Scholar
  13. Dauch P, Masuo Y, Vincent JP, Checler F (1993) A survey of the cerebral regionalization and ontogeny of eight exo- and endopeptidases in murines. Peptides 14(3):593–599CrossRefPubMedGoogle Scholar
  14. Dotolo R, Kim JD, Pariante P, Minucci S, Diano S (2016) Prolyl endopeptidase (prep) is associated with male reproductive functions and gamete physiology in mice. J Cell Physiol 231(3):551–557CrossRefPubMedGoogle Scholar
  15. Easton A (2006) Hormonal, neural, and genomic mechanisms for female reproductive behaviors, motivation, and arousal. In: Knobil and Neill’s physiology of reproduction. Elsevier, Boston, pp 1825–1920Google Scholar
  16. Fuse Y, Polk DH, Lam RW, Reviczky AL, Fisher DA (1990) Distribution and ontogeny of thyrotropin-releasing hormone degrading enzymes in rats. Am J Physiol 259(6 Pt 1):787–791Google Scholar
  17. Goossens F, De Meester I, Vanhoof G, Scharpé S (1996) Distribution of prolyl oligopeptidase in human peripheral tissues and body fluids. Eur J Clin Chem Clin Biochem 34(1):17–22PubMedGoogle Scholar
  18. Healy DP, Orlowski M (1992) Immunocytochemical localization of endopeptidase 24.15 in rat brain. Brain Res 571(1):121–128CrossRefPubMedGoogle Scholar
  19. Irazusta J, Larrinaga G, González-Maeso J, Gil J, Meana JJ, Casis L (2002) Distribution of prolyl endopeptidase activities in rat and human brain. Neurochem Int 40(4):337–345CrossRefPubMedGoogle Scholar
  20. Kimura A, Ohnishi J, Okimura H, Hamabata T, Takahashi T (1998) Localization of prolyl endopeptidase mRNA in small growing follicles of porcine ovary. Mol Reprod Dev 50(2):121–127CrossRefPubMedGoogle Scholar
  21. Kimura A, Matsui H, Takahashi T (2002) Expression and localization of prolyl oligopeptidase in mouse testis and its possible involvement in sperm motility. Zool Sci 19(1):93–102CrossRefPubMedGoogle Scholar
  22. Lew RA, Tetaz TJ, Glucksman MJ, Roberts JL, Smith AI (1994) Evidence for a two-step mechanism of gonadotropin-releasing hormone metabolism by prolyl endopeptidase and metalloendopeptidase EC 3.4.24.15 in ovine hypothalamic extracts. J Biol Chem 269(17):12626–12632PubMedGoogle Scholar
  23. Lew RA, Cowley M, Clarke IJ, Smith AI (1997) Peptidases that degrade gonadotropin-releasing hormone: influence on LH secretion in the ewe. J Neuroendocrinol 9(9):707–712CrossRefPubMedGoogle Scholar
  24. Li M, Chen C (2000) Progress in the studies of prolyl endopeptidase. Prog Biochem Biophys 27(2):171–174Google Scholar
  25. Li GL, Zhang MZ, Deng SP, Chen HP, Zhu CH (2015) Effects of temperature and fish oil supplementation on ovarian development and foxl2 mRNA expression in spotted scat Scatophagus argus. J Fish Biol 86(1):248–260CrossRefPubMedGoogle Scholar
  26. Lone AM, Leidl M, McFedries AK, Horner JW, Creemers J, Saghatelian A (2014) Deletion of prepl causes growth impairment and hypotonia in mice. PLoS ONE 9(2):e89160CrossRefPubMedPubMedCentralGoogle Scholar
  27. Massarelli EE, Casatti CA, Kato A, Camargo AC, Bauer JA, Glucksman MJ, Roberts JL, Hirose S, Ferro ES (1999) Differential subcellular distribution of neurolysin (EC 3.4.24.16) and thimet oligopeptidase (EC 3.4.24.15) in the rat brain. Brain Res 851(1–2):261–265CrossRefPubMedGoogle Scholar
  28. Molineaux CJ, Yu B, Ayala JM (1991) Distribution of endopeptidase-24.15 in rat brain nuclei using a novel fluorogenic substrate: comparison with endopeptidase-24.11. Neuropeptides 18(1):49–54CrossRefPubMedGoogle Scholar
  29. Myöhänen TT, Venäläinen JI, Tupala E, Garcia-Horsman JA, Miettinen R, Männistö PT (2007) Distribution of immunoreactive prolyl oligopeptidase in human and rat brain. Neurochem Res 32(8):1365–1374CrossRefPubMedGoogle Scholar
  30. Myöhänen TT, Venäläinen JI, García-Horsman JA, Piltonen M, Männistö PT (2008) Distribution of prolyl oligopeptidase in the mouse whole-body sections and peripheral tissues. Histochem Cell Biol 130(5):993–1003CrossRefPubMedGoogle Scholar
  31. Neves PR, Natali MRM, Ribeiro RP, Vargas L, Maehana KR, Marengoni NG (2009) Morphological characteristics of ovarian development of two Nile tilapia (Oreochromis niloticus) strains in mixed-culture systems. Arq Bras Med Vet Zootec 61(5):1173–1182CrossRefGoogle Scholar
  32. Okida N, Tokumoto M, Tokumoto T, Nagahama Y, Ohe Y, Miyamoto K et al (2007) Cloning of cDNA encoding thimet oligopeptidase from Xenopus oocytes and regulation of the mRNA during oogenesis. Zoologicalence 17:431–436Google Scholar
  33. Orlowski M, Reznik S, Ayala J, Pierotti AR (1989) Endopeptidase 24.15 from rat testes. Isolation of the enzyme and its specificity toward synthetic and natural peptides, including enkephalin-containing peptides. Biochem J 261(3):951–958CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pierotti AR, Lasdun A, Ayala JM, Roberts JL, Molineaux CJ (1991) Endopeptidase-24.15 in rat hypothalamic/pituitary/gonadal axis. Mol Cell Endocrinol 76(1–3):95–103CrossRefPubMedGoogle Scholar
  35. Pierotti A, Dong KW, Glucksman MJ, Orlowski M, Roberts JL (1994) Molecular cloning and primary structure of rat testes metalloendopeptidase EC 3.4.24.15. Biochemistry 33(2):10323CrossRefGoogle Scholar
  36. Pineau C, McCool S, Glucksman MJ, Jégou B, Pierotti AR (1999) Distribution of thimet oligopeptidase (EC 3.4.24.15) in human and rat testes. J Cell Sci 112(Pt20):3455–3462PubMedGoogle Scholar
  37. Shen G, Shi J (1999) Cloning and nucleotide sequencing of prolyl endopeptidase gene from Aeromonas punctata subsp. punctata. Acta Biochim Biophys Sin 31(5):567–571PubMedGoogle Scholar
  38. Shrimpton CN, Smith AI, Lew RA (2002) Soluble metalloendopeptidases and neuroendocrine signaling. Endocr Rev 23(5):647–664CrossRefPubMedGoogle Scholar
  39. Smith AI, Tetaz T, Roberts JL, Glucksman M, Clarke IJ, Lew RA (1994) The role of EC 3.4.24.15 in the post-secretory regulation of peptide signals. Biochimie 76(3–4):288–294CrossRefPubMedGoogle Scholar
  40. Wu TJ, Pierotti AR, Jakubowski M, Sheward WJ, Glucksman MJ, Smith AI, King JC, Fink G, Roberts JL (1997) Endopeptidase EC 3.4.24.15 presence in the rat median eminence and hypophysial portal blood and its modulation of the luteinizing hormone surge. J Neuroendocrinol 9(11):813–822CrossRefPubMedGoogle Scholar
  41. Yamanaka C, Lebrethon MC, Vandersmissen E, Gerard A, Purnelle G, Lemaitre M, Wilk S, Bourguignon JP (1999) Early prepubertal ontogeny of pulsatile gonadotropin-releasing hormone (GnRH) secretion: I. Inhibitory auto feedback control through prolyl endopeptidase degradation of GnRH. Endocrinology 140(10):4609–4615CrossRefPubMedGoogle Scholar
  42. Zhang MZ, Li GL, Zhu CH, Deng SP (2013) Effects of fish oil on ovarian development in spotted scat (Scatophagus argus). Anim Reprod Sci 141(1–2):90–97CrossRefPubMedGoogle Scholar
  43. Zheng Y, Sheng J, Ji XF, Zheng LH, Sun M (2013) Structure analysis of zinc metalloproteases. Chin J Biochem Mol Biol 29(8):719–726Google Scholar

Copyright information

© Japanese Society of Fisheries Science 2018

Authors and Affiliations

  • Si-ping Deng
    • 1
    • 2
    • 3
  • Dong-neng Jiang
    • 1
    • 3
  • Jian-ye Liu
    • 1
    • 2
    • 3
  • Zhi-qi Liang
    • 1
  • Hua-pu Chen
    • 1
    • 2
  • Tian-li Wu
    • 1
    • 2
  • Chun-hua Zhu
    • 1
    • 2
  • Guang-li Li
    • 1
    • 2
  1. 1.Fisheries CollegeGuangdong Ocean UniversityZhanjiangChina
  2. 2.Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish SpeciesZhanjiangChina
  3. 3.Marine Ecology and Aquaculture Environment of ZhanjiangZhanjiangChina

Personalised recommendations