Effects of synthetic (JWH-018) cannabinoids treatment on spermatogenesis and sperm function

References

• Aktaş, C., 2011. Effects of experimental diabetes on testis proliferations and apoptosis in rats. Journal of Experimental and Clinical Medicine, 28, 94–98.
   Google Scholar
• Bari, M., 2011. The manifold actions of endocannabinoids on female and male reproductive events. Frontiers in Bioscience, 16(1), 498–516.
   Google Scholar
• Battista, N., et al., 2008. Regulation of male fertility by the endocannabinoid system. Molecular and Cellular Endocrinology, 286(1–2), S17–S23.
   PubMed Web of Science ®Google Scholar
• Boekelheide, K., 2005. Mechanisms of toxic damage to spermatogenesis. Journal of the National Cancer Institute Monographs, 34, 6–8.
   PubMedGoogle Scholar
• Brents, L.K. and Prather, P.L., 2014. The K2/Spice phenomenon: emergence, identification, legislation and metabolic characterization of synthetic cannabinoids in herbal incense products. Drug Metabolism Reviews, 46(1), 72–85.
   PubMed Web of Science ®Google Scholar
• Brighton, P.J., et al., 2011. Characterization of the endocannabinoid system, CB(1) receptor signalling and desensitization in human myometrium. British Journal of Pharmacology, 164(5), 1479–1494.
   PubMed Web of Science ®Google Scholar
• Clermont, Y., 1972. Kinetics of spermatogenesis in mammals. Physiological Reviews, 52(1), 198–204.
   PubMed Web of Science ®Google Scholar
• Cone, E.J., et al., 1986. Acute effects of smoking marijuana on hormones, subjective effects and performance in male human subjects. Pharmacology Biochemistry and Behavior, 24(6), 1749–1754.
   PubMed Web of Science ®Google Scholar
• Creasy, D., et al., 2012. Proliferative and nonproliferative lesions of the rat and mouse male reproductive system. Toxicologic Pathology, 40(6_Suppl.), 40S–121S.
   PubMed Web of Science ®Google Scholar
• D'Andrea, M.R., et al., 2008. PCNA indexing as a preclinical immunohistochemical biomarker for testicular toxicity. Biotechnic & Histochemistry, 83(5), 211–220.
   PubMed Web of Science ®Google Scholar
• De Luca, M.A., et al., 2015. Stimulation of in vivo dopamine transmission and intravenous self-administration in rats and mice by JWH-018, a Spice cannabinoid. Neuropharmacology, 99, 705–714.
   PubMed Web of Science ®Google Scholar
• De Luca, M.A., et al., 2016. Native CB1 receptor affinity, intrinsic activity and accumbens shell dopamine stimulant properties of third generation SPICE/K2 cannabinoids: BB-22, 5F-PB-22, 5F-AKB-48 and STS-135. Neuropharmacology, 105, 630–638.
   PubMed Web of Science ®Google Scholar
• De Petrocellis, L. and Di Marzo, V., 2010. Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: focus on G-protein-coupled receptors and transient receptor potential channels. Journal of Neuroimmune Pharmacology, 5(1), 103–121.
   PubMed Web of Science ®Google Scholar
• [DEA] Drug Enforcement Administration, 2010. Schedules of controlled substances: temporary placement of five synthetic cannabinoids into schedule I. Federal Register, 75, 71635–71638.
   Google Scholar
• du Plessis, S.S., Agarwal, A., and Syriac, A., 2015. Marijuana, phytocannabinoids, the endocannabinoid system, and male fertility. Journal of Assisted Reproduction and Genetics, 32(11), 1575–1588.
   PubMed Web of Science ®Google Scholar
• Eddy, E.M., et al., 1996. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology, 137(11), 4796–4805.
   PubMed Web of Science ®Google Scholar
• El-Talatini, M.R., et al., 2009. Localisation and function of the endocannabinoid system in the human ovary. PLoS One, 4(2), e4579.
   PubMed Web of Science ®Google Scholar
• European Monitoring Centre for Drugs and Drug Addiction, 2009. Understanding the ‘Spice’ phenomenon. In: L.P.O.o.t.E. Union, ed. Luxembourg: Office for Official Publications of the European Communities, 99.
   Google Scholar
• Every-Palmer, S., 2011. Synthetic cannabinoid JWH-018 and psychosis: an explorative study. Drug and Alcohol Dependence, 117(2–3), 152–157.
   PubMed Web of Science ®Google Scholar
• [FDA] US Food and Drug Administration Guidance for Industry, 2005. Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. Available from: http://www.fda.gov/downloads/Drugs/Guidances/UCM078932.pdf
   Google Scholar
• Fride, E. and Shohami, E., 2002. The endocannabinoid system: function in survival of the embryo, the newborn and the neuron. NeuroReport, 28, 1833–1841.
   Google Scholar
• Galiegue, S., et al., 1995. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. European Journal of Biochemistry, 232(1), 54–61.
   PubMedGoogle Scholar
• Goldschmidt, L., et al., 2012. School achievement in 14-year-old youths prenatally exposed to marijuana. Neurotoxicology and Teratology, 34(1), 161–167.
   PubMed Web of Science ®Google Scholar
• Griswold, M.D., 2016. Spermatogenesis: the commitment to meiosis. Physiological Reviews, 96(1), 1–17.
   PubMed Web of Science ®Google Scholar
• Habayeb, O.M., et al., 2008. Expression of the endocannabinoid system in human first trimester placenta and its role in trophoblast proliferation. Endocrinology, 149(10), 5052–5060.
   PubMed Web of Science ®Google Scholar
• Hancock, J.L., 1952. Morphology of bull spermatozoa. Journal of Experimental Biology, 29, 445–453.
   Web of Science ®Google Scholar
• Hermanns-Clausen, M., et al., 2013. Acute toxicity due to the confirmed consumption of synthetic cannabinoids: clinical and laboratory findings. Addiction, 108(3), 534–544.
   PubMed Web of Science ®Google Scholar
• Horne, A.W., et al., 2008. CB1 expression is attenuated in Fallopian tube and decidua of women with ectopic pregnancy. PLoS One, 3(12), e3969.
   PubMed Web of Science ®Google Scholar
• Hou, M., et al., 2014. Bortezomib treatment causes long-term testicular dysfunction in young male mice. Molecular Cancer, 13(1), 155.
   PubMedGoogle Scholar
• Kanter, M., Aktas, C., and Erboga, M., 2013. Heat stress decreases testicular germ cell proliferation and increases apoptosis in short term: an immunohistochemical and ultrastructural study. Toxicology and Industrial Health, 29(2), 99–113.
   PubMed Web of Science ®Google Scholar
• Kolodny, R.C., et al., 1974. Depression of plasma testosterone levels after chronic intensive marihuana use. New England Journal of Medicine, 290(16), 872–874.
   PubMed Web of Science ®Google Scholar
• Lewis, S.E., et al., 2012. Long-term use of HU210 adversely affects spermatogenesis in rats by modulating the endocannabinoid system. International Journal of Andrology, 35(5), 731–740.
   PubMedGoogle Scholar
• Macrì, S., et al., 2013. The Directive 2010/63/EU on animal experimentation may skew the conclusions of pharmacological and behavioural studies. Scientific Reports, 3(1), 2380.
   PubMedGoogle Scholar
• Martinotti, G., et al., 2015. Novel psychoactive substances: use and knowledge among adolescents and young adults in urban and rural areas. Human Psychopharmacology: Clinical and Experimental, 30(4), 295–301.
   PubMed Web of Science ®Google Scholar
• Martinotti, G., et al., 2017. Synthetic cannabinoids: psychopharmacology, clinical aspects, psychotic onset. CNS Neurological Disorders Drug Targets, 16(5), 567–575.
   PubMed Web of Science ®Google Scholar
• McQuade, D., et al., 2013. First European case of convulsions related to analytically confirmed use of the synthetic cannabinoid receptor agonist AM-2201. European Journal of Clinical Pharmacology, 69(3), 373–376.
   PubMed Web of Science ®Google Scholar
• Migliarini, B. and Carnevali, O., 2009. A novel role for the endocannabinoid system during zebrafish development. Molecular and Cellular Endocrinology, 299(2), 172–177.
   PubMed Web of Science ®Google Scholar
• Oakberg, E.F., 1956. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. American Journal of Anatomy, 99(3), 507–516.
   PubMedGoogle Scholar
• Ossato, A., et al., 2015. JWH-018 impairs sensorimotor functions in mice. Neuroscience, 300, 174–188.
   PubMed Web of Science ®Google Scholar
• Paria, B.C., et al., 1998. Effects of cannabinoids on preimplantation mouse embryo development and implantation are mediated by brain-type cannabinoid receptors. Biology of Reproduction, 58(6), 1490–1495.
   PubMed Web of Science ®Google Scholar
• Paria, B.C., Wang, H., and Dey, S.K., 2002. Endocannabinoid signaling in synchronizing embryo development and uterine receptivity for implantation. Chemistry and Physics of Lipids, 121(1–2), 201–210.
   PubMed Web of Science ®Google Scholar
• Pertwee, R.G., 2008. The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9-tetrahydrocannabivarin. British Journal of Pharmacology, 153(2), 199–215.
   PubMed Web of Science ®Google Scholar
• Pertwee, R.G., et al., 2010. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB and CB. Pharmacological Reviews, 62(4), 588–631.
   PubMed Web of Science ®Google Scholar
• Ramu, S. and Jeyendran, R. S., 2013. The hypo-osmotic swelling test for evaluation of sperm membrane integrity. In: D. Carrell and K. Aston, eds. Spermatogenesis methods in molecular biology. Totowa, NJ: Humana Press, 20–25.
   Google Scholar
• Rominger, A., et al., 2013. Effects of acute detoxification of the herbal blend ‘Spice Gold’ on dopamine D 2/3 receptor availability: a [18 F] Fallypride PET study. European Neuropsychopharmacology, 23(11), 1606–1610.
   PubMed Web of Science ®Google Scholar
• Seely, K.A., et al., 2012. Spice drugs are more than harmless herbal blends: a review of the pharmacology and toxicology of synthetic cannabinoids. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 39(2), 234–243.
   PubMed Web of Science ®Google Scholar
• Soethoudt, M., et al., 2017. Cannabinoid CB2 receptor ligand profiling reveals biased signalling and off-target activity. Nature Communications, 8(1), 13958.
   PubMedGoogle Scholar
• Sönmez, M., Türk, G., and Yüce, A., 2005. The effect of ascorbic acid supplementation on sperm quality, lipid peroxidation and testosterone levels of male Wistar rats. Theriogenology, 63(7), 2063–2072.
   PubMed Web of Science ®Google Scholar
• Sun, X. and Dey, S.K., 2012. Endocannabinoid signaling in female reproduction. ACS Chemical Neuroscience, 3(5), 349–355.
   PubMed Web of Science ®Google Scholar
• Tai, S. and Fantegrossi, W.E., 2017. Pharmacological and toxicological effects of synthetic cannabinoids and their metabolites. Current Topics in Behavioral Neurosciences, 32, 249–262.
   PubMedGoogle Scholar
• Taylor, A.H., et al., 2007. The role of the endocannabinoid system in gametogenesis, implantation and early pregnancy. Human Reproduction Update, 13(5), 501–513.
   PubMed Web of Science ®Google Scholar
• Uchiyama, N., et al., 2010. Chemical analysis of synthetic cannabinoids as designer drugs in herbal products. Forensic Science International, 198(1–3), 31–38.
   PubMed Web of Science ®Google Scholar
• van Amsterdam, J., Brunt, T., and van den Brink, W., 2015. The adverse health effects of synthetic cannabinoids with emphasis on psychosis-like effects. Journal of Psychopharmacology, 29(3), 254–263.
   PubMed Web of Science ®Google Scholar
• Vardakou, I., Pistos, C., and Spiliopoulou, C., 2010. Spice drugs as a new trend: mode of action, identification and legislation. Toxicology Letters, 197(3), 157–162.
   PubMed Web of Science ®Google Scholar
• Vidal, J.D. and Whitney, K.M., 2014. Morphologic manifestations of testicular and epididymal toxicity. Spermatogenesis, 4(2), e979099.
   PubMedGoogle Scholar
• Wenger, T., et al., 2001. The central cannabinoid receptor inactivation suppresses endocrine reproductive functions. Biochemical and Biophysical Research Communications, 284(2), 363–368.
   Google Scholar
• Wiley, J.L., et al., 2012. 1-Pentyl-3-phenylacetylindoles and JWH-018 share in vivo cannabinoid profiles in mice. Drug and Alcohol Dependence, 123(1–3), 148–153.
   PubMed Web of Science ®Google Scholar
• Xie, B.G., Li, J., and Zhu, W.J., 2014. Pathological changes of testicular tissue in normal adult mice: a retrospective analysis. Experimental and Therapeutic Medicine, 7(3), 654–656.
   PubMed Web of Science ®Google Scholar
• Yokoi, K., Uthus, E.O., and Nielsen, F.H., 2003. Nickel deficiency diminishes sperm quantity and movement in rats. Biological Trace Element Research, 93(1–3), 141–154.
   PubMed Web of Science ®Google Scholar