Expression of type-1 cannabinoid receptor during rat postnatal testicular development: Possible involvement in adult leydig cell differentiation

Biology of Reproduction

Volumn 79, Issue 4, 2008, Pages 758-765

  Cacciola, Giovanna ^a   Chioccarelli, Teresa ^a   Mackie, Ken ^b   Meccariello, Rosaria ^c   Ledent, Catherine ^d   Fasano, Silvia ^a   Pierantoni, Riccardo ^a   Cobellis, Gilda ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

CNR1; Endocannabinoid system; Leydig cells; Prepubertal development; Testis

Indexed keywords

CANNABINOID 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; LEYDIG CELL; MALE; MITOSIS; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOGENESIS; SPERMATOZOON; TESTIS DEVELOPMENT; WESTERN BLOTTING;

MAMMALIA; MUS; RATTUS;

EID: 53349108792     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.108.070128     Document Type: Article

References (46)

1. Hollister LE. Health aspects of cannabis. Pharmacol Rev 1986; 38:1-20.
2. Mackie K, Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J 2006; 8:E298-E306.
3. Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R. The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr Rev 2006; 27:73-100.
4. Mechoulam R, Gaoni Y. A total synthesis of delta-1-tetrahydrocannabinol, the active constituent of hashish. J Am Chem Soc 1965; 87:3273-3275.
5. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990; 346:561-564.
6. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993; 365:61-65.
7. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG. International Union of Pharmacology, XXVII: classification of cannabinoid receptors. Pharmacol Rev 2002; 54:161-202.
8. Pertwee RG. Cannabis and cannabinoids: pharmacology and rationale for clinical use. Forsch Komplementarmed 1999; 6(suppl 3):12-15.
9. Mechoulam R, Hanus L. A historical overview of chemical research on cannabinoids. Chem Phys Lipids 2000; 108:1-13.
10. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992; 258:1946-1949.
11. Stella N, Schweitzer P, Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 1997; 388:773-778.
12. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 1994; 372:686-691.
13. Maccarrone M, Cecconi S, Rossi G, Battista N, Pauselli R, Finazzi-Agro A. Anandamide activity and degradation are regulated by early postnatal aging and follicle-stimulating hormone in mouse Sertoli cells. Endocrinology 2003; 144:20-28.
14. Wenger T, Ledent C, Csernus V, Gerendai I. The central cannabinoid receptor inactivation suppresses endocrine reproductive functions. Biochem Biophys Res Commun 2001; 284:363-368.
15. Gye MC, Kang HH, Kang HJ. Expression of cannabinoid receptor 1 in mouse testes. Arch Androl 2005; 51:247-255.
16. Rossato M, Ion PF, Ferigo M, Clari G, Foresta C. Human sperm express cannabinoid receptor Cb1, the activation of which inhibits motility, acrosome reaction, and mitochondrial function. J Clin Endocrinol Metab 2005; 90:984-991.
17. Cobellis G, Cacciola G, Scarpa D, Meccariello R, Chianese R, Franzoni MF, Mackie K, Pierantoni R, Fasano S. Endocannabinoid system in frog and rodent testis: type-1 cannabinoid receptor and fatty acid amide hydrolase activity in male germ cells. Biol Reprod 2006; 75:82-89.
18. Maccarrone M, Barboni B, Paradisi A, Bernabo N, Gasperi V, Pistilli MG, Fezza F, Lucidi P, Mattioli M. Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction. J Cell Sci 2005; 118:4393-4404.
19. Meccariello R, Chianese R, Cacciola G, Cobellis G, Pierantoni R, Fasano S. Type-1 cannabinoid receptor expression in the frog, Rana esculenta, tissues: a possible involvement in the regulation of testicular activity. Mol Reprod Dev 2006; 73:551-558.
20. Kolodny RC, Masters WH, Kolodner RM, Toro G. Depression of plasma testosterone levels after chronic intensive marihuana use. N Engl J Med 1974; 290:872-874.
21. Harclerode J, Nyquist SE, Nazar B, Lowe D. Effects of cannabis on sex hormones and testicular enzymes of the rodent. Adv Biosci 1978; 22-23:395-405.
22. Dalterio S, Badr F, Bartke A, Mayfield D. Cannabinoids in male mice: effects on fertility and spermatogenesis. Science 1982; 216:315-316.
23. Dixit VP, Sharma VN, Lohiya NK. The effect of chronically administered cannabis extract on the testicular function of mice. Eur J Pharmacol 1974; 26:111-114.
24. Wang H, Dey SK, Maccarrone M. Jekyll and Hyde: two faces of cannabinoid signaling in male and female fertility. Endocr Rev 2006; 27:427-448.
25. Schuel H, Burkman LJ, Lippes J, Crickard K, Forester E, Piomelli D, Giuffrida A. N-Acylethanolamines in human reproductive fluids. Chem Phys Lipids 2002; 121:211-227.
26. Sugiura T, Kondo S, Sukagawa A, Tonegawa T, Nakane S, Yamashita A, Waku K. Enzymatic synthesis of anandamide, an endogenous cannabinoid receptor ligand, through N-acylphosphatidylethanolamine pathway in testis: involvement of Ca(2+)-dependent transacylase and phosphodiesterase activities. Biochem Biophys Res Commun 1996; 218:113-117.
27. Schuel H, Goldstein E, Mechoulam R, Zimmerman AM, Zimmerman S. Anandamide (arachidonylethanolamide), a brain cannabinoid receptor agonist, reduces sperm fertilizing capacity in sea urchins by inhibiting the acrosome reaction. Proc Natl Acad Sci U S A 1994; 91:7678-7682.
28. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Bohme GA, Imperato A, Pedrazzini T, Roques BP, Vassart G, Fratta W, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999; 283:401-404.
29. Le Mellay V, Grosse B, Lieberherr M. Phospholipase C beta and membrane action of calcitriol and estradiol. J Biol Chem 1997; 272:11902-11907.
30. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193:265-275.
31. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 1998; 83:393-411.
32. Twitchell W, Brown S, Mackie K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 1997; 78:43-50.
33. Hsieh C, Brown S, Derleth C, Mackie K. Internalization and recycling of the CB1 cannabinoid receptor. J Neurochem 1999; 73:493-501.
34. Hajos N, Katona I, Naiem SS, Mackie K, Ledent C, Mody I, Freund TF. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 2000; 12:3239-3249.
35. Salio C, Cottone E, Conrath M, Franzoni MF. CB1 cannabinoid receptors in amphibian spinal cord: relationships with some nociception markers. J Chem Neuroanat 2002; 24:153-162.
36. Renlund N, Jo Y, Svechnikova I, Holst M, Stocco DM, Soder O, Svechnikov K. Induction of steroidogenesis in immature rat Leydig cells by interleukin-1alpha is dependent on extracellular signal-regulated kinases. J Mol Endocrinol 2006; 36:327-336.
37. Hardy MP, Zirkin BR, Ewing LL. Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 1989; 124:762-770.
38. Hembree WCI, Nahas GG, Zeidenberg P, Huang HF. Changes in human spermatozoa associated with high dose marihuana smoking. Adv Biosci 1978; 22-23:429-439.
39. Issidorides MR. Observations in chronic hashish users: nuclear aberrations in blood and sperm and abnormal acrosomes in spermatozoa. Adv Biosci 1978; 22-23:377-388.
40. Zimmerman AM, Bruce WR, Zimmerman S. Effects of cannabinoids on sperm morphology. Pharmacology 1979; 18:143-148.
41. Knobil E, Neill JD eds. Encyclopedia of Reproduction. San Diego: Academic Press; 1998:381-386.
42. Habert R, Lejeune H, Saez JM. Origin, differentiation and regulation of fetal and adult Leydig cells. Mol Cell Endocrinol 2001; 179:47-74.
43. Haider SG. Cell biology of Leydig cells in the testis. Int Rev Cytol 2004; 233:181-241.
44. Siril Ariyaratne HB, Chamindrani Mendis-Handagama S, Buchanan Hales D, Ian Mason J. Studies on the onset of Leydig precursor cell differentiation in the prepubertal rat testis. Biol Reprod 2000; 63:165-171.
45. Rossi P, Dolci S, Sette C, Geremia R. Molecular mechanisms utilized by alternative c-kit gene products in the control of spermatogonial proliferation and sperm-mediated egg activation. Andrologia 2003; 35:71-78.
46. Russell LD, Ren HP, Sinha HI, Schulze W, Sinha Hikim AP. A comparative study in twelve mammalian species of volume densities, volumes, and numerical densities of selected testis components, emphasizing those related to the Sertoli cell. Am J Anat 1990; 188:21-30.