Effects of delta-9-tetrahydrocannabinol, the primary psychoactive cannabinoid in marijuana, on human sperm function in vitro

Fertility and Sterility

Volumn 85, Issue 3, 2006, Pages 653-660

  Whan, Lynne B ^a   West, Mhairi C L ^a   McClure, Neil ^a,b   Lewis, Sheena E M ^a,c  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b ROYAL MATERNITY HOSPITAL   (United Kingdom)

^c Institute of Clinical Sciences B   (United Kingdom)

Author keywords

Acrosome reaction; Cannabis; Motility; Sperm; Tetrahydrocannabinol

Indexed keywords

CANNABINOID; CANNABIS; DRONABINOL; FLUORESCEIN ISOTHIOCYANATE; PEANUT AGGLUTININ; PSYCHOTROPIC AGENT;

ACROSOME REACTION; ADULT; ARTICLE; COMPUTER ANALYSIS; CONCENTRATION RESPONSE; CONCEPTION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DOSE RESPONSE; GENITAL SYSTEM FUNCTION; HUMAN; LABORATORY TEST; MAJOR CLINICAL STUDY; MALE; MALE FERTILITY; PRIORITY JOURNAL; SEMEN ANALYSIS; SPERM; SPERMATOZOON MOTILITY; STAINING;

ACROSOME REACTION; ADULT; CALCIMYCIN; CANNABIS; HUMANS; IONOPHORES; MALE; SPERM MOTILITY; SPERMATOZOA; TETRAHYDROCANNABINOL;

EID: 32944465828     PISSN: 00150282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2005.08.027     Document Type: Article

References (73)

1. S. Fishel, K. Dowell, S. Thornton Reproductive possibilities for infertile couples present and future G.R. Bentley C.G.N. Mascie-Taylor Infertility in the modern world 2000 Cambridge University Press Cambridge (UK) 17 45
2. B. Park, J.M. McPartland, M. Glass Cannabis, cannabinoids and reproduction Prostaglandins Leukot Essent Fatty Acids 70 2004 189 197
3. P. Sharpe, G. Smith Cannabis Time for scientific evaluation of this ancient remedy Anesth Analg 90 2000 237 240
4. N. Hall W Solowij Adverse effects of cannabis Lancet 352 1998 1611 1616
5. K. Bolling, S. Clemens, A. Phelps, P. Smith 2001 British Crime Survey in England and Wales Technical Report 2002 BMRB London
6. H. Ashton Pharmacology and effects of cannabis a brief review Br J Psychiatry 178 2001 101 106
7. Royal Society and the Academy of Medical Sciences Use of cannabis and its derivatives for medical and recreational purposes Interdisc Sci Rev 23 1998 325 328
8. P. Consroe, R. Musty, J. Rein, W. Tillery, R.G. Pertwee The perceived effects of smoked cannabis on patients with multiple sclerosis Eur Neurol 38 1997 44 48
9. J. Zajicek, P. Fox, H. Sanders, D. Wright, J. Vickery, A. Nunn Cannabinoids for treatment of spasticity and other symptoms related to multiple sclerosis (CAMS study) multicentre randomised placebo-controlled trial Lancet 362 2003 1517 1526
10. R.A. Hirst, D.G. Lambert, W.G. Notcutt Pharmacology and potential therapeutic uses of cannabis Br J Anaesth 81 1998 77 84
11. C.C. Felder, M. Glass Cannabinoid receptors and their endogenous agonists Annu Rev Pharmacol Toxicol 38 1998 179 200
12. R.G. Pertwee Cannabis and cannabinoids pharmacology and rationale for clinical use Pharm Sci 3 1997 539 545
13. R.G. Pertwee Pharmacology of cannabinoid CB1 and CB2 receptors Pharmacol Ther 74 1997 129 180
14. H. Schuel, L.J. Burkman, J. Lippes, K. Crickard, E. Forester, D. Piomelli N-Acylethanolamines in human reproductive fluids Chem Phys Lipids 121 2002 211 227
15. M. Salzet, C. Breton, T. Bisogno, V. Di Marzo Comparative biology of the endocannabinoid system. Possible role in the immune response Eur J Biochem 267 2000 4917 4927
16. R.G. Pertwee, R.A. Ross, S.J. Craib, A. Thomas Cannabidiol antagonizes cannabinoid receptor agonists and noradrenaline in the mouse vas deferens Eur J Pharmacol 456 2002 99 106
17. C. Gerard, C. Mollereau, G. Vassart, M. Parmentier Nucleotide sequence of a human cannabinoid receptor cDNA Nucleic Acids Res 18 1990 7142
18. T. Sugiura, S. Kondo, A. Sukagawa, T. Tonegawa, S. Nakane, A. Yamashita 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 218 1996 113 117
19. R.G. Pertwee, G. Joe-Adigwe, G.M. Hawksworth Further evidence for the presence of cannabinoid CB1 receptors in mouse vas deferens Eur J Pharmacol 296 1996 169 172
20. H. Schuel, E. Goldstein, R. Mechoulam, A.M. Zimmerman, S. Zimmerman 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 91 1994 7678 7682
21. H. Schuel, L.J. Burkman, J. Lippes, K. Crickard, M.C. Mahony, A. Giuffrida Evidence that anandamide-signaling regulates human sperm functions required for fertilization Mol Reprod Dev 63 2002 376 387
22. M.C. Chang, D. Berkery, R. Schuel, S.G. Laychock, A.M. Zimmerman, S. Zimmerman Evidence for a cannabinoid receptor in sea urchin sperm and its role in blockade of the acrosome reaction Mol Reprod Dev 36 1993 507 516
23. H. Schuel, M.C. Chang, D. Berkery, R. Schuel, A.M. Zimmerman, S. Zimmerman Cannabinoids inhibit fertilization in sea urchins by reducing the fertilizing capacity of sperm Pharmacol Biochem Behav 40 1991 609 615
24. C. Gerard, C. Mollereau, G. Vassart, M. Parmentier Molecular cloning of a human cannabinoid receptor which is also expressed in testis Biochem J 279 1991 129 134
25. S.K. Das, B.C. Paria, I. Chakraborty, S.K. Dey Cannabinoid ligand-receptor signaling in the mouse uterus Proc Natl Acad Sci U S A 92 1995 4332 4336
26. B.C. Paria, S.K. Das, S.K. Dey The preimplantation mouse embryo is a target for cannabinoid ligand-receptor signaling Proc Natl Acad Sci U S A 92 1995 9460 9464
27. R.C. Kolodny, W.H. Masters, R.M. Kolodner, G. Toro Depression of plasma testosterone levels after chronic intensive marihuana use N Engl J Med 290 1974 872 874
28. W.C. Hembree, G.G. Nahas, P. Zeidenberg, H.F.S. Huang Changes in human spermatozoa associated with high dose marijuana smoking G.G. Nahas M. Paron Marihuana biological effects 1980 Pergamon Press Oxford (UK) 429 439
29. R.C. Kolodny, P. Lessin, G. Toro, W.H. Masters, J. Cohen Depression of plasma testosterone with acute administration M.C. Braude S. Szara The pharmacology of marijuana 1974 Raven Press New York 217 225
30. J.H. Mendelson, J. Kuehnle, J. Ellingboe, T.F. Babor Plasma testosterone levels before, during and after chronic marihuana smoking N Engl J Med 291 1974 1051 1055
31. E.J. Cone, R.E. Johnston, J.D. Moore, J.D. Roache Acute effects of smoking marijuana on hormones, subjective effects and performance in male human subjects Pharmacol Biochem Behav 24 1976 1749 1754
32. C.Y. Hong, D.M. Chaput de Saintonge, P. Turner Delta 9- tetrahydrocannabinol inhibits human sperm motility J Pharm Pharmacol 33 1981 746 747
33. C.Y. Hong, D.M. Chaput de Saintonge, P. Turner, J.W. Fairbairn Comparison of the inhibitory action of delta-9-tetrahydrocannabinol and petroleum spirit extract of herbal cannabis on human sperm motility Hum Toxicol 1 1982 151 154
34. L.E. Perez, C.G. Smith, R.H. Asch Delta 9-tetrahydrocannabinol inhibits fructose utilization and motility in human, rhesus monkey, and rabbit sperm in vitro Fertil Steril 35 1981 703 705
35. S. Husain THC effects on fructose utilization and sperm motility Fertil Steril 37 1982 448
36. A. Shahar, T. Bino In vitro effects of delta9 tetrahydrocannabinol (THC) on bull sperm Biochem Pharmacol 23 1974 1341 1342
37. W.C. Hembree, P. Zeidenberg, G.G. Nahas Marihuana's effects on human gonadal function G.G. Nahas Marijuana chemistry, biochemistry and cellular effects 1976 Springer Verlag New York 521 532
38. World Health Organization WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction 1999 Cambridge University Press Cambridge (UK)
39. M. Plachot, J. Mandelbaum, A.M. Junca Acrosome reaction of human sperm used for in vitro fertilization Fertil Steril 42 1984 418 423
40. H. Breitbart, Z. Naor Protein kinases in mammalian sperm capacitation and the acrosome reaction Rev Reprod 4 1999 151 159
41. D. Mortimer Sperm fertilizing ability testing D. Mortimer Practical laboratory andrology 1994 Oxford University Press Oxford 199 240
42. E.T. Donnelly, S.E. Lewis, J.A. McNally, W. Thompson In vitro fertilization and pregnancy rates the influence of sperm motility and morphology on IVF outcome Fertil Steril 70 1998 305 314
43. J.D. Biggers, W.K. Whitten, D.G. Whittingham The culture of mouse embryos in vitro J.D. Daniel Methods in mammalian embryology 1971 WH Freeman San Francisco 86 116
44. M. O'Connell, N. McClure, L.A. Powell, E.K. Steele, S.E. Lewis Differences in mitochondrial and nuclear DNA status of high-density and low-density sperm fractions after density centrifugation preparation Fertil Steril 79 Suppl 1 2003 754 762
45. D. Mortimer, E.F. Curtis, R.G. Miller Specific labelling by peanut agglutinin of the outer acrosomal membrane of the human spermatozoon J Reprod Fertil 81 1987 127
46. M.A. Huestis, A.H. Sampson, B.J. Holicky, J.E. Henningfield, E.J. Cone Characterisation of the absorption phase of marjuana smoking Clin Pharmacol Ther 52 1992 31 41
47. H. Schuel, R. Schuel, A.M. Zimmerman, S. Zimmerman Cannabinoids reduce fertility of sea urchin sperm Biochem Cell Biol 65 1987 130 136
48. M.C. Chang, D. Berkery, S.G. Laychock, H. Schuel Reduction of the fertilizing capacity of sea urchin sperm by cannabinoids derived from marihuana. III. Activation of phospholipase A2 in sperm homogenate by delta 9-tetrahydrocannabinol Biochem Pharmacol 42 1991 899 904
49. R.G. Pertwee Cannabinoid receptors and pain Prog Neurobiol 63 2001 569 611
50. L.A. Matsuda Molecular aspects of cannabinoid receptors Crit Rev Neurobiol 11 1997 143 166
51. R.G. Pertwee Evidence for the presence of CB1 cannabinoid receptors on peripheral neurones and for the existence of neuronal nonCB1 cannabinoid receptors Life Sci 65 1999 597 605
52. S. Munro, K.L. Thomas, M. Abu-Shaar Molecular characterization of a peripheral receptor for cannabinoids Nature 365 1993 61 65
53. L.A. Matsuda, S.J. Lolait, M.J. Brownstein, A.C. Young, T.I. Bonner Structure of a cannabinoid receptor and functional expression of the cloned cDNA Nature 346 1990 561 564
54. P.C. Schmid, B.C. Paria, R.J. Krebsbach, H.H. Schmid, S.K. Dey Changes in anandamide levels in mouse uterus are associated with uterine receptivity for embryo implantation Proc Natl Acad Sci U S A 94 1997 4188 4192
55. R.H. Asch, C.G. Smith Effects of delta 9-THC, the principal psychoactive component of marijuana, during pregnancy in the rhesus monkey J Reprod Med 31 1986 1071 1081
56. H. Schuel, D. Berkery, R. Schuel, M.C. Chang, A.M. Zimmerman, S. Zimmerman Reduction of the fertilizing capacity of sea urchin sperm by cannabinoids derived from marihuana. I. Inhibition of the acrosome reaction induced by egg jelly Mol Reprod Dev 29 1991 51 59
57. T.A. Sarafian, S. Kouyoumjian, F. Khoshaghideh, D.P. Tashkin, M.D. Roth Delta 9-tetrahydrocannabinol disrupts mitochondrial function and cell energetics Am J Physiol Lung Cell Mol Physiol 284 2003 L298 L306
58. J.M. Cummins, A.M. Jequier, R. Martin, D. Mehmet, J. Goldblatt Semen levels of mitochondrial DNA deletions in men attending an infertility clinic do not correlate with phenotype Int J Androl 21 1998 47 52
59. M. Hayakawa, K. Hattori, S. Sugiyama, T. Ozawa Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts Biochem Biophys Res Commun 189 1992 979 985
60. M. Corral-Debrinski, T. Horton, M.T. Lott, J.M. Shoffner, A.C. McKee, M.F. Beal Marked changes in mitochondrial DNA deletion levels in Alzheimer brains Genomics 23 1994 471 476
61. B. Fromenty, R. Carrozzo, S. Shanske, E.A. Schon High proportions of mtDNA duplications in patients with Kearns-Sayre syndrome occur in the heart Am J Med Genet 71 1997 443 452
62. H. Wiseman, B. Halliwell Damage to DNA by reactive oxygen and nitrogen species role in inflammatory disease and progression to cancer Biochem J 313 1996 17 29
63. Y.H. Wei, C.Y. Lu, H.C. Lee, C.Y. Pang, Y.S. Ma Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function Ann N Y Acad Sci 854 1998 155 170
64. S.E. Lewis, P.M. Boyle, K.A. McKinney, I.S. Young, W. Thompson Total antioxidant capacity of seminal plasma is different in fertile and infertile men Fertil Steril 64 1995 868 870
65. T.A. Sarafian, J.A.M. Magallanes, H. Shau, D.P. Tashkin, M.D. Roth Oxidative stress produced by marijuana smoke. An adverse effect enhanced by cannabinoids Am J Respir Cell Mol Biol 20 1999 1286 1293
66. A.J. Hampson, M. Grimaldi, J. Axelrod, D. Wink Cannabidiol and (-)delta9-tetrahydrocannabinol are neuroprotective antioxidants Proc Natl Acad Sci U S A 95 1998 8268 8273
67. S.P. Boyers, B.C. Tarlatzis, J.N. Stronk, A.H. DeCherney Fertilization and cleavage rates of heparin-exposed human oocytes in vitro, and the effect of heparin on the acrosome reaction Fertil Steril 48 1987 628 632
68. A.I. Yudin, W. Gottlieb, S. Meizel Ultrastructural studies of the early events of the human sperm acrosome reaction as initiated by human follicular fluid Gamete Res 20 1988 11 24
69. C. Zoratti, D. Kipmen-Korgun, K. Osibow, R. Malli, W.F. Graier Anandamide initiates Ca(2+) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells Br J Pharmacol 140 2003 1351 1362
70. G.G. Nahas, D.J. Harvey, K.M. Sutin Psychoactive cannabinoids and membrane signaling Hum Psychopharmacol 15 2000 535 549
71. R.J. Aitken, A. Ross, T. Hargreave, D. Richardson, F. Best Analysis of human sperm function following exposure to the ionophore A23187. Comparison of normospermic and oligozoospermic men J Androl 5 1984 321 329
72. R.J. Aitken, D.W. Buckingham, H.G. Fang Analysis of the responses of human spermatozoa to A23187 employing a novel technique for assessing the acrosome reaction J Androl 14 1993 132 141
73. R.J. Aitken The extragenomic action of progesterone on human spermatozoa Hum Reprod 12 Suppl 1997 38 42