Early Exposure to THC Alters M-Cell Development in Zebrafish Embryos
Abstract
:1. Introduction
2. Experimental Section
2.1. Animal Care and Exposure to THC
2.2. Immunohistochemistry
2.3. Escape Response in 2 dpf Embryos
2.4. qPCR of nAChR Subunits
2.5. Locomotor Activity in 5 dpf Larva
2.6. Statistics
3. Results
3.1. THC Exposure Reduces Axonal Diameter of M-Cell
3.2. Escape Response Properties Were Altered Due to THC Exposure
3.3. White and Red Muscle Fibers Appear Thinner and Slightly Disorganized in THC Treated Embryos
3.4. THC Does Not Alter nAChR Subunit Expression
3.5. THC Exposure Alters the Locomotion at 5dpf
4. Discussion
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Pertwee, R.G. Ligands that target cannabinoid receptors in the brain: From THC to anandamide and beyond. Addict. Biol. 2008, 13, 147–159. [Google Scholar] [CrossRef] [PubMed]
- Herkenham, M.; Lynn, A.B.; Little, M.D.; Johnson, M.R.; Melvin, L.S.; de Costa, B.R.; Rice, K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. USA 1990, 87, 1932–1936. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Watson, S.; Chambers, D.; Hobbs, C.; Doherty, P.; Graham, A. The endocannabinoid receptor, CB1, is required for normal axonal growth and fasciculation. Mol. Cell. Neurosci. 2008, 38, 89–97. [Google Scholar] [CrossRef] [PubMed]
- Kano, M.; Ohno-Shosaku, T.; Hashimotodani, Y.; Uchigashima, M.; Watanabe, M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 2009, 89, 309–380. [Google Scholar] [CrossRef] [PubMed]
- Smita, K.; Sushil Kumar, V.; Premendran, J.S. Anandamide: An update. Fundam. Clin. Pharmacol. 2007, 21, 1–8. [Google Scholar] [CrossRef]
- Pandey, R.; Mousawy, K.; Nagarkatti, M.; Nagarkatti, P. Endocannabinoids and immune regulation. Pharmacol. Res. 2009, 60, 85–92. [Google Scholar] [CrossRef] [Green Version]
- Benarroch, E. Endocannabinoids in basal ganglia circuits: Implications for Parkinson disease. Neurology 2007, 69, 306–309. [Google Scholar] [CrossRef]
- Stempel, A.V.; Stumpf, A.; Zhang, H.Y.; Ozdogan, T.; Pannasch, U.; Theis, A.K.; Otte, D.M.; Wojtalla, A.; Racz, I.; Ponomarenko, A.; et al. Cannabinoid Type 2 Receptors Mediate a Cell Type-Specific Plasticity in the Hippocampus. Neuron 2016, 90, 795–809. [Google Scholar] [CrossRef] [Green Version]
- Liu, Q.R.; Canseco-Alba, A.; Zhang, H.Y.; Tagliaferro, P.; Chung, M.; Dennis, E.; Sanabria, B.; Schanz, N.; Escosteguy-Neto, J.C.; Ishiguro, H.; et al. Cannabinoid type 2 receptors in dopamine neurons inhibits psychomotor behaviors, alters anxiety, depression and alcohol preference. Sci. Rep. 2017, 7, 17410. [Google Scholar] [CrossRef]
- Psychoyos, D.; Vinod, K.Y.; Cao, J.; Xie, S.; Hyson, R.L.; Wlodarczyk, B.; He, W.; Cooper, T.B.; Hungund, B.L.; Finnell, R.H. Cannabinoid receptor 1 signaling in embryo neurodevelopment. Birth Defects Res. B Dev. Reprod. Toxicol. 2012, 95, 137–150. [Google Scholar] [CrossRef] [Green Version]
- Buckley, N.E.; Hansson, S.; Harta, G.; Mezey, E. Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience 1998, 82, 1131–1149. [Google Scholar] [CrossRef]
- Navarro, M.; Rubio, P.; de Fonseca, F.R. Behavioural consequences of maternal exposure to natural cannabinoids in rats. Psychopharmacology 1995, 122, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Morris, C.V.; DiNieri, J.A.; Szutorisz, H.; Hurd, Y.L. Molecular mechanisms of maternal cannabis and cigarette use on human neurodevelopment. Eur. J. Neurosci. 2011, 34, 1574–1583. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harkany, T.; Guzman, M.; Galve-Roperh, I.; Berghuis, P.; Devi, L.A.; Mackie, K. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol. Sci. 2007, 28, 83–92. [Google Scholar] [CrossRef]
- Williams, E.J.; Walsh, F.S.; Doherty, P. The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J. Cell Biol. 2003, 160, 481–486. [Google Scholar] [CrossRef] [Green Version]
- Bernard, C.; Milh, M.; Morozov, Y.M.; Ben-Ari, Y.; Freund, T.F.; Gozlan, H. Altering cannabinoid signaling during development disrupts neuronal activity. Proc. Natl. Acad. Sci. USA 2005, 102, 9388–9393. [Google Scholar] [CrossRef] [Green Version]
- Oltrabella, F.; Melgoza, A.; Nguyen, B.; Guo, S. Role of the endocannabinoid system in vertebrates: Emphasis on the zebrafish model. Dev. Growth Differ. 2017, 59, 194–210. [Google Scholar] [CrossRef]
- Kimmel, C.B.; Ballard, W.W.; Kimmel, S.R.; Ullmann, B.; Schilling, T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203, 253–310. [Google Scholar] [CrossRef]
- Kimmel, C.B.; Sessions, S.K.; Kimmel, R.J. Morphogenesis and synaptogenesis of the zebrafish Mauthner neuron. J. Comp. Neurol. 1981, 198, 101–120. [Google Scholar] [CrossRef]
- Ahmed, K.T.; Amin, M.R.; Shah, P.; Ali, D.W. Motor neuron development in zebrafish is altered by brief (5-hr) exposures to THC ((9)-tetrahydrocannabinol) or CBD (cannabidiol) during gastrulation. Sci. Rep. 2018, 8, 10518. [Google Scholar] [CrossRef] [Green Version]
- Hatta, K. Role of the floor plate in axonal patterning in the zebrafish CNS. Neuron 1992, 9, 629–642. [Google Scholar] [CrossRef]
- Miller, J.B.; Crow, M.T.; Stockdale, F.E. Slow and fast myosin heavy chain content defines three types of myotubes in early muscle cell cultures. J. Cell Biol. 1985, 101, 1643–1650. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kok, F.O.; Oster, E.; Mentzer, L.; Hsieh, J.C.; Henry, C.A.; Sirotkin, H.I. The role of the SPT6 chromatin remodeling factor in zebrafish embryogenesis. Dev. Biol. 2007, 307, 214–226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shan, S.D.; Boutin, S.; Ferdous, J.; Ali, D.W. Ethanol exposure during gastrulation alters neuronal morphology and behavior in zebrafish. Neurotoxicol. Teratol. 2015, 48C, 18–27. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, K.T.; Ali, D.W. Nicotinic acetylcholine receptors (nAChRs) at zebrafish red and white muscle show different properties during development. Dev. Neurobiol. 2016, 76, 916–936. [Google Scholar] [CrossRef] [PubMed]
- Baraban, S.C.; Taylor, M.R.; Castro, P.A.; Baier, H. Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 2005, 131, 759–768. [Google Scholar] [CrossRef] [PubMed]
- Leighton, P.L.A.; Kanyo, R.; Neil, G.J.; Pollock, N.M.; Allison, W.T. Prion gene paralogs are dispensable for early zebrafish development and have nonadditive roles in seizure susceptibility. J. Biol. Chem. 2018, 293, 12576–12592. [Google Scholar] [CrossRef] [Green Version]
- Waterman, R.E. Development of the lateral musculature in the teleost, Brachydanio rerio: A fine structural study. Am. J. Anat. 1969, 125, 457–493. [Google Scholar] [CrossRef] [Green Version]
- Lefebvre, J.L.; Jing, L.; Becaficco, S.; Franzini-Armstrong, C.; Granato, M. Differential requirement for MuSK and dystroglycan in generating patterns of neuromuscular innervation. Proc. Natl. Acad. Sci. USA 2007, 104, 2483–2488. [Google Scholar] [CrossRef] [Green Version]
- Park, J.Y.; Mott, M.; Williams, T.; Ikeda, H.; Wen, H.; Linhoff, M.; Ono, F. A single mutation in the acetylcholine receptor delta-subunit causes distinct effects in two types of neuromuscular synapses. J. Neurosci. Off. J. Soc. Neurosci. 2014, 34, 10211–10218. [Google Scholar] [CrossRef] [Green Version]
- Palazuelos, J.; Ortega, Z.; Diaz-Alonso, J.; Guzman, M.; Galve-Roperh, I. CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J. Biol. Chem. 2012, 287, 1198–1209. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xapelli, S.; Agasse, F.; Sarda-Arroyo, L.; Bernardino, L.; Santos, T.; Ribeiro, F.F.; Valero, J.; Braganca, J.; Schitine, C.; de Melo Reis, R.A.; et al. Activation of type 1 cannabinoid receptor (CB1R) promotes neurogenesis in murine subventricular zone cell cultures. PLoS ONE 2013, 8, e63529. [Google Scholar] [CrossRef] [PubMed]
- Diaz-Alonso, J.; Aguado, T.; Wu, C.S.; Palazuelos, J.; Hofmann, C.; Garcez, P.; Guillemot, F.; Lu, H.C.; Lutz, B.; Guzman, M.; et al. The CB(1) cannabinoid receptor drives corticospinal motor neuron differentiation through the Ctip2/Satb2 transcriptional regulation axis. J. Neurosci. Off. J. Soc. Neurosci. 2012, 32, 16651–16665. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galve-Roperh, I.; Chiurchiu, V.; Diaz-Alonso, J.; Bari, M.; Guzman, M.; Maccarrone, M. Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Prog. Lipid Res. 2013, 52, 633–650. [Google Scholar] [CrossRef]
- McCabe, J.E.; Arndt, S. Demographic and substance abuse trends among pregnant and non-pregnant women: Eleven years of treatment admission data. Matern. Child Health J. 2012, 16, 1696–1702. [Google Scholar] [CrossRef]
- Brown, Q.L.; Sarvet, A.L.; Shmulewitz, D.; Martins, S.S.; Wall, M.M.; Hasin, D.S. Trends in Marijuana Use Among Pregnant and Nonpregnant Reproductive-Aged Women, 2002–2014. JAMA 2017, 317, 207–209. [Google Scholar] [CrossRef] [Green Version]
- Mehmedic, Z.; Chandra, S.; Slade, D.; Denham, H.; Foster, S.; Patel, A.S.; Ross, S.A.; Khan, I.A.; ElSohly, M.A. Potency trends of Delta9-THC and other cannabinoids in confiscated cannabis preparations from 1993 to 2008. J. Forensic Sci. 2010, 55, 1209–1217. [Google Scholar] [CrossRef]
- Begbie, J.; Doherty, P.; Graham, A. Cannabinoid receptor, CB1, expression follows neuronal differentiation in the early chick embryo. J. Anat. 2004, 205, 213–218. [Google Scholar] [CrossRef]
- Berghuis, P.; Dobszay, M.B.; Wang, X.; Spano, S.; Ledda, F.; Sousa, K.M.; Schulte, G.; Ernfors, P.; Mackie, K.; Paratcha, G.; et al. Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc. Natl. Acad. Sci. USA 2005, 102, 19115–19120. [Google Scholar] [CrossRef] [Green Version]
- Berghuis, P.; Rajnicek, A.M.; Morozov, Y.M.; Ross, R.A.; Mulder, J.; Urban, G.M.; Monory, K.; Marsicano, G.; Matteoli, M.; Canty, A.; et al. Hardwiring the brain: Endocannabinoids shape neuronal connectivity. Science 2007, 316, 1212–1216. [Google Scholar] [CrossRef] [Green Version]
- Huestis, M.A. Human cannabinoid pharmacokinetics. Chem. Biodivers. 2007, 4, 1770–1804. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, F.; Qin, W.; Zhang, J.P.; Hu, C.Q. Antibiotic toxicity and absorption in zebrafish using liquid chromatography-tandem mass spectrometry. PLoS ONE 2015, 10, e0124805. [Google Scholar] [CrossRef] [PubMed]
- Brox, S.; Ritter, A.P.; Kuster, E.; Reemtsma, T. A quantitative HPLC-MS/MS method for studying internal concentrations and toxicokinetics of 34 polar analytes in zebrafish (Danio rerio) embryos. Anal. Bioanal. Chem. 2014, 406, 4831–4840. [Google Scholar] [CrossRef] [PubMed]
- Brusco, A.; Tagliaferro, P.A.; Saez, T.; Onaivi, E.S. Ultrastructural localization of neuronal brain CB2 cannabinoid receptors. Ann. N. Y. Acad. Sci. 2008, 1139, 450–457. [Google Scholar] [CrossRef]
- Onaivi, E.S.; Ishiguro, H.; Gu, S.; Liu, Q.R. CNS effects of CB2 cannabinoid receptors: Beyond neuro-immuno-cannabinoid activity. J. Psychopharmacol. 2012, 26, 92–103. [Google Scholar] [CrossRef] [Green Version]
- Lam, C.S.; Rastegar, S.; Strahle, U. Distribution of cannabinoid receptor 1 in the CNS of zebrafish. Neuroscience 2006, 138, 83–95. [Google Scholar] [CrossRef]
- Rodriguez-Martin, I.; de Velasco, E.M.F.; Rodriguez, R.E. Characterization of cannabinoid-binding sites in zebrafish brain. Neurosci. Lett. 2007, 413, 249–254. [Google Scholar] [CrossRef]
- Rodriguez-Martin, I.; Herrero-Turrion, M.J.; de Velasco, E.M.F.; Gonzalez-Sarmiento, R.; Rodriguez, R.E. Characterization of two duplicate zebrafish Cb2-like cannabinoid receptors. Gene 2007, 389, 36–44. [Google Scholar] [CrossRef]
- Avallone, B.; Agnisola, C.; Cerciello, R.; Panzuto, R.; Simoniello, P.; Creti, P.; Motta, C.M. Structural and functional changes in the zebrafish (Danio rerio) skeletal muscle after cadmium exposure. Cell Biol. Toxicol. 2015, 31, 273–283. [Google Scholar] [CrossRef]
- Devoto, S.H.; Melancon, E.; Eisen, J.S.; Westerfield, M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 1996, 122, 3371–3380. [Google Scholar]
- Stickney, H.L.; Barresi, M.J.; Devoto, S.H. Somite development in zebrafish. Dev. Dyn. 2000, 219, 287–303. [Google Scholar] [CrossRef]
- Westerfield, M.; McMurray, J.V.; Eisen, J.S. Identified motoneurons and their innervation of axial muscles in the zebrafish. J. Neurosci. Off. J. Soc. Neurosci. 1986, 6, 2267–2277. [Google Scholar] [CrossRef] [Green Version]
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Amin, M.R.; Ahmed, K.T.; Ali, D.W. Early Exposure to THC Alters M-Cell Development in Zebrafish Embryos. Biomedicines 2020, 8, 5. https://doi.org/10.3390/biomedicines8010005
Amin MR, Ahmed KT, Ali DW. Early Exposure to THC Alters M-Cell Development in Zebrafish Embryos. Biomedicines. 2020; 8(1):5. https://doi.org/10.3390/biomedicines8010005
Chicago/Turabian StyleAmin, Md Ruhul, Kazi T. Ahmed, and Declan W. Ali. 2020. "Early Exposure to THC Alters M-Cell Development in Zebrafish Embryos" Biomedicines 8, no. 1: 5. https://doi.org/10.3390/biomedicines8010005