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International Journal of Endocrinology
Volume 2013, Article ID 941237, 8 pages
http://dx.doi.org/10.1155/2013/941237
Review Article

Role of the Endocannabinoid System in the Central Regulation of Nonmammalian Vertebrate Reproduction

Department of Life Science and Systems Biology, University of Turin, Via Accademia Albertina 13, 10123 Torino, Italy

Received 28 June 2013; Accepted 12 August 2013

Academic Editor: Rosaria Meccariello

Copyright © 2013 Erika Cottone et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. Di Marzo and L. De Petrocellis, “Why do cannabinoid receptors have more than one endogenous ligand?” Philosophical Transactions of the Royal Society B, vol. 367, no. 1607, pp. 3216–3228, 2012. View at Google Scholar
  2. M. R. Elphick and M. Egertová, “Cannabinoid receptor genetic and evolution,” in The Cannabinoid Receptors, P. H. Reggio, Ed., pp. 123–149, Humana Press, New Yark, NY, USA, 2009. View at Google Scholar
  3. M. R. Elphick, “The evolution and comparative neurobiology of endocannabinoid signalling,” Philosophical Transactions of the Royal Society B, vol. 367, no. 1607, pp. 3201–3215, 2012. View at Google Scholar
  4. V. Di Marzo, “The endocannabinoid system: its general strategy of action, tools for its pharmacological manipulation and potential therapeutic exploitation,” Pharmacological Research, vol. 60, no. 2, pp. 77–84, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Park, J. M. McPartland, and M. Glass, “Cannabis, cannabinoids and reproduction,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 70, no. 2, pp. 189–197, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Wang, S. K. Dey, and M. Maccarrone, “Jekyll and Hyde: two faces of cannabinoid signaling in male and female fertility,” Endocrine Reviews, vol. 27, no. 5, pp. 427–448, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Chianese, T. Chioccarelli, G. Cacciola et al., “The contribution of lower vertebrate animal models in human reproduction research,” General and Comparative Endocrinology, vol. 171, no. 1, pp. 17–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. W. A. Devane, F. A. Dysarz III, M. R. Johnson, L. S. Melvin, and A. C. Howlett, “Determination and characterization of a cannabinoid receptor in rat brain,” Molecular Pharmacology, vol. 34, no. 5, pp. 605–613, 1988. View at Google Scholar · View at Scopus
  9. L. A. Matsuda, S. J. Lolait, M. J. Brownstein, A. C. Young, and T. I. Bonner, “Structure of a cannabinoid receptor and functional expression of the cloned cDNA,” Nature, vol. 346, no. 6284, pp. 561–564, 1990. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Yamaguchi, A. D. Macrae, and S. Brenner, “Molecular cloning of two cannabinoid type 1-like receptor genes from the puffer fish Fugu rubripes,” Genomics, vol. 35, no. 3, pp. 603–605, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. M. R. Elphick, “Evolution of cannabinoid receptors in vertebrates: identification of a CB2 gene in the puffer fish Fugu rubripes,” Biological Bulletin, vol. 202, no. 2, pp. 104–107, 2002. View at Google Scholar · View at Scopus
  12. O. Jatllon, J. Aury, F. Brunet et al., “Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype,” Nature, vol. 431, no. 7011, pp. 946–957, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. C. S. Lam, S. Rastegar, and U. Strähle, “Distribution of cannabinoid receptor 1 in the CNS of zebrafish,” Neuroscience, vol. 138, no. 1, pp. 83–95, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Rodriguez-Martin, M. J. Herrero-Turrion, E. M. Velasco, R. Gonzalez-Sarmiento, and R. E. Rodriguez, “Characterization of two duplicate zebrafish Cb2-like cannabinoid receptors,” Gene, vol. 389, no. 1, pp. 36–44, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Valenti, E. Cottone, R. Martinez et al., “The endocannabinoid system in the brain of Carassius auratus and its possible role in the control of food intake,” Journal of Neurochemistry, vol. 95, no. 3, pp. 662–672, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Cottone, E. Campantico, A. Guastalla, S. Aramu, A. M. Polzonetti-Magni, and M. Franzoni, “Are the cannabinoids involved in bony fish reproduction?” Annals of the New York Academy of Sciences, vol. 1040, pp. 273–276, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Cottone, V. Pomatto, F. Cerri et al., “Cannabinoid receptors are widely expressed in goldfish: molecular cloning of a CB2-like receptor and evaluation of CB1 and CB2 mRNA expression profiles in different organs,” Fish Physiology and Biochemistry. In press.
  18. F. A. Palermo, B. Ruggeri, G. Mosconi, M. Virgili, and A. M. Polzonetti-Magni, “Partial cloning of CB1 cDNA and CB1 mRNA changes in stress responses in the Solea solea,” Molecular and Cellular Endocrinology, vol. 286, no. 1-2, supplement 1, pp. S52–S59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Cottone, S. Forno, E. Campantico et al., “Expression and distribution of CB1 cannabinoid receptors in the central nervous system of the African cichlid fish Pelvicachromis pulcher,” Journal of Comparative Neurology, vol. 485, no. 4, pp. 293–303, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Ruggeri, L. Soverchia, G. Mosconi, M. F. Franzoni, E. Cottone, and A. M. Polzonetti-Magni, “Changes of gonadal CB1 cannabinoid receptor mRNA in the gilthead seabream, Sparus aurata, during sex reversal,” General and Comparative Endocrinology, vol. 150, no. 2, pp. 263–269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Harvey-Girard, A. C. Giassi, W. Ellis, and L. Maler, “Expression of the cannabinoid CB1 receptor in the gymnotiform fish brain and its implications for the organization of the teleost pallium,” Journal of Comparative Neurology, vol. 521, no. 4, pp. 949–975, 2013. View at Google Scholar
  22. G. J. Roch, S. Wu, and N. M. Sherwood, “Hormones and receptors in fish: do duplicates matter?” General and Comparative Endocrinology, vol. 161, no. 1, pp. 3–12, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Soderstrom, M. Leid, F. L. Moore, and T. F. Murray, “Behavioral, pharmacological, and molecular characterization of an amphibian cannabinoid receptor,” Journal of Neurochemistry, vol. 75, no. 1, pp. 413–423, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Cottone, C. Salio, M. Conrath, and M. F. Franzoni, “Xenopus laevis CB1 cannabinoid receptor: molecular cloning and mRNA distribution in the central nervous system,” Journal of Comparative Neurology, vol. 464, no. 4, pp. 487–496, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Meccariello, R. Chianese, G. Cobellis, R. Pierantoni, and S. Fasano, “Cloning of type 1 cannabinoid receptor in Rana esculenta reveals differences between genomic sequence and cDNA,” FEBS Journal, vol. 274, no. 11, pp. 2909–2920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. L. S. Demski, “Feeding and aggressive behavior evoked by hypothalamic stimulation in a cichlid fish,” Comparative Biochemistry and Physiology, vol. 44, pp. 685–692, 1973. View at Google Scholar · View at Scopus
  27. M. G. Roberts and G. E. Savage, “Effects of hypothalamic lesions on the food intake of the goldfish (Carassius auratus),” Brain, Behavior and Evolution, vol. 15, no. 2, pp. 150–164, 1978. View at Google Scholar · View at Scopus
  28. L. S. Demski and R. G. Northcutt, “The terminal nerve: a new chemosensory system in vertebrates?” Science, vol. 220, no. 4595, pp. 435–437, 1983. View at Google Scholar · View at Scopus
  29. E. Cottone, D. Donna, A. Guastalla, E. Campantico, A. Polzonetti-Magni, and M. F. Franzoni, “The cannabinoid signaling system: comparative biology of an old neuromodulatory system,” in Evolutionary Molecular Strategies and Plasticity, M. Canonaco and R. M. Facciolo, Eds., pp. 73–93, Research Signpost, Kerala, India, 2007. View at Google Scholar
  30. V. Pomatto, E. Cottone, and P. Bovolin, “Influence of the endocannabinoid system on teleost neurogenesis: new insights from goldfish,” Submitted.
  31. T. Harkany, E. Keimpema, K. Barabás, and J. Mulder, “Endocannabinoid functions controlling neuronal specification during brain development,” Molecular and Cellular Endocrinology, vol. 286, no. 1-2, supplement 1, pp. S84–S90, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. D. M. Hollis, E. J. Coddington, and F. L. Moore, “Neuroanatomical distribution of cannabinoid receptor gene expression in the brain of the rough-skinned newt, Taricha granulosa,” Brain, Behavior and Evolution, vol. 67, no. 3, pp. 135–149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Migliarini, G. Marucci, F. Ghelfi, and O. Carnevali, “Endocannabinoid system in Xenopus laevis development: CB1 receptor dynamics,” FEBS Letters, vol. 580, no. 8, pp. 1941–1945, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Cesa, K. Mackie, M. Beltramo, and M. Franzoni, “Cannabinoid receptor CB1-like and glutamic acid decarboxylase-like immunoreactivities in the brain of Xenopus laevis,” Cell and Tissue Research, vol. 306, no. 3, pp. 391–398, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Salio, E. Cottone, M. Conrath, and M. F. Franzoni, “CB1 cannabinoid receptors in amphibian spinal cord: relationships with some nociception markers,” Journal of Chemical Neuroanatomy, vol. 24, no. 3, pp. 153–162, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Cesa, A. Guastalla, E. Cottone, K. Mackie, M. Beltramo, and M. F. Franzoni, “Relationships between CB1 cannabinoid receptors and pituitary endocrine cells in Xenopus laevis: an immunohistochemical study,” General and Comparative Endocrinology, vol. 125, no. 1, pp. 17–24, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Donna, E. Cottone, S. Aramu, E. Campantico, A. Guastalla, and M. F. Franzoni, “Endocannabinoids and amphibian reproduction: an immunohistochemical study in the green frog,” Accademia delle Scienze di Torino, vol. 140, pp. 37–45, 2006. View at Google Scholar
  38. R. Meccariello, M. F. Franzoni, R. Chianese et al., “Interplay between the endocannabinoid system and GnRH-I in the forebrain of the anuran amphibian Rana esculenta,” Endocrinology, vol. 149, no. 5, pp. 2149–2158, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Meccariello, R. Chianese, G. Cacciola, G. Cobellis, R. Pierantoni, and S. Fasano, “Type-1 cannabinoid receptor expression in the frog, Rana esculenta, tissues: a possible involvement in the regulation of testicular activity,” Molecular Reproduction and Development, vol. 73, no. 5, pp. 551–558, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. L. L. Murphy, R. M. Muñoz, B. A. Adrian, and M. A. Villanúa, “Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion,” Neurobiology of Disease, vol. 5, no. 6, part B, pp. 432–446, 1998. View at Google Scholar
  41. U. Pagotto, G. Marsicano, D. Cota, B. Lutz, and R. Pasquali, “The emerging role of the endocannabinoid system in endocrine regulation and energy balance,” Endocrine Reviews, vol. 27, no. 1, pp. 73–100, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. G. Cacciola, R. Chianese, T. Chioccarelli et al., “Cannabinoids and reproduction: a lasting and intriguing history,” Pharmaceuticals, vol. 3, no. 10, pp. 3275–3323, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Wenger, C. Ledent, V. Csernus, and I. Gerendai, “The central cannabinoid receptor inactivation suppresses endocrine reproductive functions,” Biochemical and Biophysical Research Communications, vol. 284, no. 2, pp. 363–368, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Wenger, J. J. Fernández-Ruizz.ast, and J. A. Ramos, “Immunocytochemical demonstration of CB1 cannabinoid receptors in the anterior lobe of the pituitary gland,” Journal of Neuroendocrinology, vol. 11, no. 11, pp. 873–878, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Bagavandoss and S. Grimshaw, “Temporal and spatial distribution of the cannabinoid receptors (CB 1, CB2) and fatty acid amide hydroxylase in the rat ovary,” Anatomical Record, vol. 293, no. 8, pp. 1425–1432, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. R. El-Talatini, A. H. Taylor, J. C. Elson, L. Brown, A. C. Davidson, and J. C. Konje, “Localisation and function of the endocannabinoid system in the human ovary,” PLoS ONE, vol. 4, no. 2, Article ID e4579, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Peralta, E. Agirregoitia, R. Mendoza et al., “Expression and localization of cannabinoid receptors in human immature oocytes and unfertilized metaphase-II oocytes,” Reproductive BioMedicine Online, vol. 23, no. 3, pp. 372–379, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Grimaldi, P. Orlando, S. Di Siena et al., “The endocannabinoid system and pivotal role of the CB2 receptor in mouse spermatogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 27, pp. 11131–11136, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Schuel, L. J. Burkman, J. Lippes et al., “Evidence that anandamide-signaling regulates human sperm functions required for fertilization,” Molecular Reproduction and Development, vol. 63, no. 3, pp. 376–387, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Maccarrone, B. Barboni, A. Paradisi et al., “Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction,” Journal of Cell Science, vol. 118, part 19, pp. 4393–4404, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Rossato, F. I. Popa, M. Ferigo, G. Clari, and C. Foresta, “Human sperm express cannabinoid receptor Cb1, the activation of which inhibits motility, acrosome reaction, and mitochondrial function,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 2, pp. 984–991, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Ricci, G. Cacciola, L. Altucci et al., “Endocannabinoid control of sperm motility: the role of epididymus,” General and Comparative Endocrinology, vol. 153, no. 1–3, pp. 320–322, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Cobellis, G. Cacciola, D. Scarpa et al., “Endocannabinoid system in frog and rodent testis: type-1 cannabinoid receptor and fatty acid amide hydrolase activity in male germ cells,” Biology of Reproduction, vol. 75, no. 1, pp. 82–89, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Battista, R. Meccariello, G. Cobellis et al., “The role of endocannabinoids in gonadal function and fertility along the evolutionary axis,” Molecular and Cellular Endocrinology, vol. 355, no. 1, pp. 1–14, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Cottone, A. Guastalla, K. Mackie, and M. F. Franzoni, “Endocannabinoids affect the reproductive functions in teleosts and amphibians,” Molecular and Cellular Endocrinology, vol. 286, no. 1-2, supplement 1, pp. S41–S45, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. B. Migliarini and O. Carnevali, “A novel role for the endocannabinoid system during zebrafish development,” Molecular and Cellular Endocrinology, vol. 299, no. 2, pp. 172–177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Pierantoni, G. Cobellis, R. Meccariello et al., “Chapter 14 CB1 activity in male reproduction: mammalian and nonmammalian animal models,” Vitamins and Hormones, vol. 81, pp. 367–387, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. C. M. Gammon, G. M. Freeman Jr., W. Xie, S. L. Petersen, and W. C. Wetsel, “Regulation of gonadotropin-releasing hormone secretion by cannabinoids,” Endocrinology, vol. 146, no. 10, pp. 4491–4499, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Cardinaletti, M. F. Franzoni, F. A. Palermo et al., “Enrironmental and neuroendocrine control of fish reproduction,” in Recent Advances in Fish Reproduction Biology, A. Garcia-Ayala, J. M. Penalver, and E. Chavez-Pozo, Eds., pp. 65–87, Research Signpost, Kerala, India, 2010. View at Google Scholar
  60. R. Chianese, G. Cobellis, R. Pierantoni, S. Fasano, and R. Meccariello, “Non-mammalian vertebrate models and the endocannabinoid system: relationships with gonadotropin-releasing hormone,” Molecular and Cellular Endocrinology, vol. 286, no. 1-2, supplement 1, pp. S46–S51, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Chianese, V. Ciaramella, S. Fasano, R. Pierantoni, and R. Meccariello, “Anandamide modulates the expression of GnRH-II and GnRHRs in frog, Rana esculenta, diencephalon,” General and Comparative Endocrinology, vol. 173, no. 3, pp. 389–395, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Chianese, V. Ciaramella, D. Scarpa, S. Fasano, R. Pierantoni, and R. Meccariello, “Anandamide regulates the expression of GnRH1, GnRH2, and GnRH-Rs in frog testis,” American Journal of Physiology, vol. 303, no. 4, pp. E475–E487, 2012. View at Google Scholar
  63. B. Levavi-Sivan, M. Ofir, and Z. Yaron, “Possible sites of dopaminergic inhibition of gonadotropin release from the pituitary of a teleost fish, tilapia,” Molecular and Cellular Endocrinology, vol. 109, no. 1, pp. 87–95, 1995. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Le Page, N. Diotel, C. Vaillant et al., “Aromatase, brain sexualization and plasticity: the fish paradigm,” European Journal of Neuroscience, vol. 32, no. 12, pp. 2105–2115, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Pomatto, F. Palermo, G. Mosconi et al., “Xenoestrogens elicit a modulation of endocannabinoid system and estrogen receptors in 4NP treated goldfish, Carassius auratus,” General and Comparative Endocrinology, vol. 174, no. 1, pp. 30–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. N. Diotel, J. L. Do Rego, I. Anglade et al., “The brain of teleost fish, a source, and a target of sexual steroids,” Frontiers in Neuroscience, vol. 5, article 137, 2011. View at Google Scholar
  67. P. M. Forlano, D. L. Deitcher, D. A. Myers, and A. H. Bass, “Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source,” The Journal of Neuroscience, vol. 21, no. 22, pp. 8943–8955, 2001. View at Google Scholar · View at Scopus
  68. A. Menuet, E. Pellegrini, F. Brion et al., “Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene,” Journal of Comparative Neurology, vol. 485, no. 4, pp. 304–320, 2005. View at Publisher · View at Google Scholar · View at Scopus