Skip to main content
SpringerLink
Log in

Expression of VIP and its Receptors in the Testis of the Spotted Ray Torpedo marmorata (Risso 1880)

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

The aim of this work was to study, by immunoprecipitation, in situ hybridization and immunohistochemistry, and the expression of the vasoactive intestinal peptide (VIP) and of its receptors (VPAC1R and VPAC2R) in the testis of a nonmammalian vertebrate, the cartilaginous fish Torpedo marmorata. We demonstrated that, differently from mammals, VIP and VPAC2R were widely distributed in the testicular cells while the VPAC1R had a limited distribution. In details, we showed that VIP and VPAC2R were present in mitotic and differentiating germ cells as well as in the cells involved in the steroidogenesis, i.e., Leydig, Sertoli cells, and prespermatogonia and spermatogonia. The possibility that VIP is involved in the spermatogenesis and particularly in the steroidogenesis of T. marmorata is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agnese M, Valiante S, Angelini F, Laforgia V, Andreuccetti P, Prisco M (2010) Pituitary adenylate cyclase-activating polypeptide and its receptor PAC1 in the testis of Triturus carnifex and Podarcis sicula. Gen Comp Endocrinol 168:256–261

    Article  PubMed  CAS  Google Scholar 

  • Brubel R, Kiss P, Vincze A, Varga A, Varnagy A, Bodis J, Mark L, Jambor E, Maasz G, Hashimoto H, Helyes Z, Toth G, Tamas A, Koppan M, Reglodi D (2012) Effects of pituitary adenylate cyclase activating polypeptide on human sperm motility. J Mol Neurosci. doi:10.1007/s12031-012-9806-5

  • Bryant MG, Polak MM, Modlin I, Bloom SR, Albuquerque RH, Pearse AG (1976) Possible dual role for vasoactive intestinal peptide as gastrointestinal hormone and neurotransmitter substance. Lancet 1:991–993

    Article  PubMed  CAS  Google Scholar 

  • Cardoso JC, Vieira FA, Gomes AS, Power DM (2007) PACAP, VIP and their receptors in the metazoa: insights about the origin and evolution of the ligand-receptor pair. Peptides 28:1902–1919

    Article  PubMed  CAS  Google Scholar 

  • Chan KW, Yu KL, Rivier J, Chow BK (1998) Identification and characterization of a receptor from goldfish specific for a teleost growth hormone-releasing hormone-like peptide. Neuroendocrinology 68:44–56

    Article  PubMed  CAS  Google Scholar 

  • Csaba ZS, Csernus V, Gerendai I (1997) Local effect of PACAP and VIP on testicular function in immature and adult rats. Peptides 18:1561–1567

    Article  PubMed  CAS  Google Scholar 

  • Duckles SP, Said SI (1982) Vasoactive intestinal peptide as a neurotransmitter in the cerebral circulation. Eur J Pharmacol 78:371–374

    Article  PubMed  CAS  Google Scholar 

  • El-Gehani F, Tena-Sempere M, Huhtaniemi I (1998a) Vasoactive intestinal peptide is an important endocrine regulatory factor of fetal rat testicular steroidogenesis. Endocrinology 139:1474–1480

    Article  PubMed  CAS  Google Scholar 

  • El-Gehani F, Tena-Sempere M, Huhtaniemi I (1998b) Vasoactive intestinal peptide stimulates testosterone production by cultured fetal rat testicular cells. Mol Cell Endocrinol 140:175–178

    Article  PubMed  CAS  Google Scholar 

  • Fahrenkrug J (1993) Transmitter role of vasoactive intestinal peptide. Pharmacol Toxicol 72:354–363

    Article  PubMed  CAS  Google Scholar 

  • Fahrenkrug J (2010) VIP and PACAP. Results Probl Cell Differ 50:221–234

    PubMed  CAS  Google Scholar 

  • Fahrenkrug J, Hannibal J (2004) Neurotransmitters co-existing with VIP or PACAP. Peptides 25:393–401

    Article  PubMed  CAS  Google Scholar 

  • Fradinger EA, Tello JA, Rivier JE, Sherwood NM (2005) Characterization of four receptor cDNAs: PAC1, VPAC1, a novel PAC1 and a partial GHRH in zebrafish. Mol Cell Endocrinol 231:49–63

    Article  PubMed  CAS  Google Scholar 

  • Gozes I, Perl O, Zamostiano R, Rubinraut S, Fridkin M, Shochat L, Lewin LM (1998) Multiple actions of a hybrid PACAP antagonist: neuronal cell killing and inhibition of sperm motility. Ann N Y Acad Sci 865:266–273

    Article  PubMed  CAS  Google Scholar 

  • Heindel JJ, Powell CJ, Paschall CS, Arimura A, Culler MD (1992) A novel hypothalamic peptide, pituitary adenylate cyclase activating peptide, modulates Sertoli cell function in vitro. Biol Reprod 47:800–806

    Article  PubMed  CAS  Google Scholar 

  • Hueso C, Carmena MJ, Prieto JC (1989) Identification of specific binding sites for vasoactive intestinal peptide in rat testis Leydig cells and study of developmental changes. Biochem Int 19:951–958

    PubMed  CAS  Google Scholar 

  • Itoh N, Obata K, Yanaihara N, Okamoto H (1983) Human preprovasoactive intestinal polypeptide contains a novel PHI-27-like peptide, PHM-27. Nature 304:547–549

    Article  PubMed  CAS  Google Scholar 

  • Kasson BG, Lim P, Hsueh AJW (1986) Vasoactive intestinal peptide stimulates androgen biosynthesis by cultured neonatal testicular cells. Mol Cell Endocrinol 48:21–29

    Article  PubMed  CAS  Google Scholar 

  • Krempels K, Usdin TB, Harta G, Mezey E (1995) PACAP acts through VIP type 2 receptors in the rat testis. Neuropeptides 29:315–320

    Article  PubMed  CAS  Google Scholar 

  • Lacombe A, Lelievre V, Roselli CE, Muller JM, Waschek JA, Vilain E (2007) Lack of vasoactive intestinal peptide reduces testosterone levels and reproductive aging in mouse testis. J Endocrinol 194:153–160

    Article  PubMed  CAS  Google Scholar 

  • Larsson LI, Edvinsson L, Fahrenkrug J et al (1976a) Immunohistochemical localization of a vasodilatory polypeptide (VIP) in cerebrovascular nerves. Brain Res 113:400–404

    Article  PubMed  CAS  Google Scholar 

  • Larsson LI, Fahrenkrug J, de Schaffalitzky M, Sundler F, Hakanson R, Rehfeld JR (1976b) Localization of vasoactive intestinal polypeptide (VIP) to central and peripheral neurons. Proc Natl Acad Sci USA 73:3197–3200

    Google Scholar 

  • Li M, Arimura A (2003) Neuropeptides of the pituitary adenylate cyclase-activating polypeptide/vasoactive intestinal polypeptide/growth hormone-releasing hormone/secretin family in testis. Endocrin 20:201–214

    Article  CAS  Google Scholar 

  • Mazzi V (ed) (1977) Manuale di tecniche istologiche e istochimiche. Piccin ed., Padova, p. 63, 278.

  • Moretti C, Mencacci C, Frajese GV, Cerilli M, Frajese G (2002) Growth hormone-realising hormone and pituitary adenylate cyclase-activating polypeptide in the reproductive system. Trends Endocrinol Metab 13:428–435

    Article  PubMed  CAS  Google Scholar 

  • Mutt V, Said SI (1974) Structure of the porcine vasoactive intestinal octacosapeptide. The amino-acid sequence. Use of kallikrein in its determination. Eur J Biochem 42:581–589

    Article  PubMed  CAS  Google Scholar 

  • Prisco M, Liguoro A, D’Onghia B, Ricchiari L, Andreuccetti P, Angelini F (2002) Fine structure of Leydig and Sertoli cells in the testis of immature and mature Spotted Ray Torpedo marmorata. Mol Reprod Dev 63:192–201

    Article  CAS  Google Scholar 

  • Prisco M, Liguoro A, Ricchiari L, Del Giudice G, Angelini F, Andreuccetti P (2008) Immunolocalization of 3beta-HSD and 17beta-HSD in the testis of the Spotted Ray Torpedo marmorata. Gen Comp Endocrinol 155:157–163

    Article  PubMed  CAS  Google Scholar 

  • Said SI, Mutt V (1970) Polypeptide with broad biological activity: isolation from small intestine. Science 169:1217–1218

    Article  PubMed  CAS  Google Scholar 

  • Sherwood NM, Krueckl SL, McRory JE (2000) The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/Glucagon superfamily. Endocrine Review 21:619–670

    Article  CAS  Google Scholar 

  • Stanley HP (1966) The structure and development of the seminiferous follicle in Scyliorhinus canicula and Torpedo marmorata (Elasmobranchii). Z Zallforsch 75:453–468

    Article  CAS  Google Scholar 

  • Van Geldre LA, Lefebvre RA (2004) Interaction of NO and VIP in gastrointestinal smooth muscle relaxation. Curr Pharm Des 10:2483–2497

    Article  PubMed  Google Scholar 

  • Vaudry D, Gonzales BJ, Basille M, Yon L, Fournier A, Vaudry H (2000) Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52:269–324

    PubMed  CAS  Google Scholar 

  • Vaudry D, Falluel-Morel A, Bourgault S et al (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283–357

    Article  PubMed  CAS  Google Scholar 

  • West AP, McKinnell C, Sharpe RM, Saunders PTK (1995) Pituitary adenylate cyclase-activating polypeptide can regulate testicular germ cell protein synthesis in vitro. J Endocrinol 144:215–223

    Article  PubMed  CAS  Google Scholar 

  • Zhu BC, Chiocchio SR, Suburo AM, Tramezzani JH (1995) Monoaminergic and peptidergic contributions of the superior and the inferior spermatic nerves to the innervation of the testis in the rat. J Androl 16:248–258

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Naples Federico II, Via Mezzocannone 8, 80134, Naples, Italy

    Marisa Agnese, Luigi Rosati, Francesco Muriano, Salvatore Valiante, Vincenza Laforgia, Piero Andreuccetti & Marina Prisco

Authors
  1. Marisa Agnese
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luigi Rosati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesco Muriano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Salvatore Valiante
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vincenza Laforgia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Piero Andreuccetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marina Prisco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Piero Andreuccetti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Agnese, M., Rosati, L., Muriano, F. et al. Expression of VIP and its Receptors in the Testis of the Spotted Ray Torpedo marmorata (Risso 1880). J Mol Neurosci 48, 638–646 (2012). https://doi.org/10.1007/s12031-012-9857-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-012-9857-7

Keywords

Search

Navigation