Abstract
Mitochondria are key organelles providing energy supply and many other vital functions to cells. Shortly after the discovery of plant-derived cannabinoid compounds, some studies indicated their impact onto mitochondrial functions. The later identification of cannabinoid receptors as classical seven-transmembrane G protein-coupled receptors suggested that these mitochondrial effects might be due to unspecific membrane-altering properties of cannabinoids. However, the recent discovery that brain mitochondria contain significant amounts of functional type-1 cannabinoid receptors (CB1) shed new light on cannabinoid physiology and pharmacology. In this chapter, we will summarize historical and recent evidence of the cannabinoid impact on mitochondrial functions in peripheral and central organs of the body.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Acin-Perez R et al (2009) Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 9:265–276. doi:10.1016/j.cmet.2009.01.012
Adams R (1942) Marihuana: Harvey Lecture, February 19, 1942. Bull NY Acad Med 18:705–730
Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247–286
Aquila S et al (2010) Human sperm anatomy: ultrastructural localization of the cannabinoid1 receptor and a potential role of anandamide in sperm survival and acrosome reaction. Anat Rec (Hoboken) 293:298–309. doi:10.1002/ar.21042
Athanasiou A et al (2007) Cannabinoid receptor agonists are mitochondrial inhibitors: a unified hypothesis of how cannabinoids modulate mitochondrial function and induce cell death. Biochem Biophys Res Commun 364:131–137. doi:10.1016/j.bbrc.2007.09.107
Badawy ZS et al (2009) Cannabinoids inhibit the respiration of human sperm. Fertil Steril 91:2471–2476. doi:10.1016/j.fertnstert.2008.03.075
Bartova A, Birmingham MK (1976) Effect of delta9-tetrahydrocannabinol on mitochondrial NADH-oxidase activity. J Biol Chem 251:5002–5006
Behnke HD (1977) The origin of plastids and mitochondria. The endosymbiotic hypothesis. MMW Munchener medizinische Wochenschrift 119:317–318
Bellocchio L et al (2010) Bimodal control of stimulated food intake by the endocannabinoid system. Nat Neurosci 13:281–283. doi:10.1038/nn.2494
Belous A et al (2004) Mitochondrial P2Y-Like receptors link cytosolic adenosine nucleotides to mitochondrial calcium uptake. J Cell Biochem 92:1062–1073. doi:10.1002/jcb.20144
Benard G et al (2012) Mitochondrial CB(1) receptors regulate neuronal energy metabolism. Nat Neurosci 15:558–564. doi:10.1038/nn.3053
Benedict AL et al (2012) Neuroprotective effects of sulforaphane after contusive spinal cord injury. J Neurotrauma 29:2576–2586. doi:10.1089/neu.2012.2474
Bermudez-Silva FJ, Cardinal P, Cota D (2012) The role of the endocannabinoid system in the neuroendocrine regulation of energy balance. J Psychopharmacol 26:114–124. doi:10.1177/0269881111408458
Bianchi C, Genova ML, Parenti Castelli G, Lenaz G (2004) The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J Biol Chem 279:36562–36569. doi:10.1074/jbc.M405135200
Billups B, Forsythe ID (2002) Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22:5840–5847
Bino T, Chari-Bitron A, Shahar A (1972) Biochemical effects and morphological changes in rat liver mitochondria exposed to 1-tetrahydrocannabinol. Biochim Biophys Acta 288:195–202
Boesmans W, Ameloot K, van den Abbeel V, Tack J, Vanden Berghe P (2009) Cannabinoid receptor 1 signalling dampens activity and mitochondrial transport in networks of enteric neurones. Neurogastroenterol Motil 21:958–e977. doi:10.1111/j.1365-2982.2009.01300.x
Bosier B et al (2013) Astroglial CB1 cannabinoid receptors regulate leptin signaling in mouse brain astrocytes. Mol Metab 2(4):393–404. doi:10.1016/j.molmet.2013.08.001
Brdiczka DG, Zorov DB, Sheu SS (2006) Mitochondrial contact sites: their role in energy metabolism and apoptosis. Biochim Biophys Acta 1762:148–163. doi:10.1016/j.bbadis.2005.09.007
Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230
Cai Q, Davis ML, Sheng ZH (2011) Regulation of axonal mitochondrial transport and its impact on synaptic transmission. Neurosci Res 70:9–15. doi:10.1016/j.neures.2011.02.005
Campbell VA (2001) Tetrahydrocannabinol-induced apoptosis of cultured cortical neurones is associated with cytochrome c release and caspase-3 activation. Neuropharmacology 40:702–709
Catanzaro G, Rapino C, Oddi S, Maccarrone M (2009) Anandamide increases swelling and reduces calcium sensitivity of mitochondria. Biochem Biophys Res Commun 388:439–442. doi:10.1016/j.bbrc.2009.08.037
Chance B, Williams GR (1955) A method for the localization of sites for oxidative phosphorylation. Nature 176:250–254
Chari-Bitron A, Bino T (1971) Effect of 1-tetrahydrocannabinol on ATPase activity of rat liver mitochondria. Biochem Pharmacol 20:473–475
Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461–472
Colburn RW, Ng LK, Lemberger L, Kopin IJ (1974) Subcellular distribution of delta9-tetrahydrocannabinol in rat brain. Biochem Pharmacol 23:873–877
Cunha JM et al (1980) Chronic administration of cannabidiol to healthy volunteers and epileptic patients. Pharmacology 21:175–185
Czabotar PE, Lessene G, Strasser A, Adams JM (2014) Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 15:49–63. doi:10.1038/nrm3722
Denton RM (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta 1787:1309–1316. doi:10.1016/j.bbabio.2009.01.005
Devane WA et al (1992) A novel probe for the cannabinoid receptor. J Med Chem 35:2065–2069
Di Benedetto G, Scalzotto E, Mongillo M, Pozzan T (2013) Mitochondrial Ca(2)(+) uptake induces cyclic AMP generation in the matrix and modulates organelle ATP levels. Cell Metab 17:965–975. doi:10.1016/j.cmet.2013.05.003
Di Marzo V, De Petrocellis L (2012) Why do cannabinoid receptors have more than one endogenous ligand? Philos Trans R Soc Lond B Biol Sci 367:3216–3228. doi:10.1098/rstb.2011.0382
Dubreucq S et al (2012) Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37:1885–1900. doi:10.1038/npp.2012.36
Erecinska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128:263–276
Ferguson CJ et al (2001) Cellular localization of divalent metal transporter DMT-1 in rat kidney. Am J Physiol Renal Physiol 280:F803–F814
Fiedorowicz JG, Swartz KL (2004) The role of monoamine oxidase inhibitors in current psychiatric practice. J Psychiatr Pract 10:239–248
Fisar Z (2010) Inhibition of monoamine oxidase activity by cannabinoids. Naunyn Schmiedebergs Arch Pharmacol 381:563–572. doi:10.1007/s00210-010-0517-6
Fisar Z, Singh N, Hroudova J (2014) Cannabinoid-induced changes in respiration of brain mitochondria. Toxicol Lett 231:62–71. doi:10.1016/j.toxlet.2014.09.002
Fonseca BM, Correia-da-Silva G, Teixeira NA (2013) The endocannabinoid anandamide induces apoptosis of rat decidual cells through a mechanism involving ceramide synthesis and p38 MAPK activation. Apoptosis 18:1526–1535. doi:10.1007/s10495-013-0892-9
Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319–324
Gallily R et al (2003) Gamma-irradiation enhances apoptosis induced by cannabidiol, a non-psychotropic cannabinoid, in cultured HL-60 myeloblastic leukemia cells. Leuk lymphoma 44:1767–1773. doi:10.1080/1042819031000103917
Gaoni Y, Mechoulam R (1964) Isolation, structure, and partial synthesis of an active constituent of hashish. J Am Chem Soc 86:1646–1647. doi:10.1021/ja01062a046
Giorgi C et al (2012) Mitochondrial calcium homeostasis as potential target for mitochondrial medicine. Mitochondrion 12:77–85. doi:10.1016/j.mito.2011.07.004
Gorman AM, Ceccatelli S, Orrenius S (2000) Role of mitochondria in neuronal apoptosis. Dev Neurosci 22:348–358. doi:10.1159/000017460
Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD (2004) Calcium and mitochondria. FEBS Lett 567:96–102. doi:10.1016/j.febslet.2004.03.071
Hackenbrock CR (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol 30:269–297
Hajnoczky G et al (2006) Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium 40:553–560. doi:10.1016/j.ceca.2006.08.016
Han J et al (2012) Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 148:1039–1050. doi:10.1016/j.cell.2012.01.037
Haring M, Marsicano G, Lutz B, Monory K (2007) Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience 146:1212–1219. doi:10.1016/j.neuroscience.2007.02.021
Harris JJ, Jolivet R, Attwell D (2012) Synaptic energy use and supply. Neuron 75:762–777. doi:10.1016/j.neuron.2012.08.019
Hebert-Chatelain E et al (2014a) Cannabinoid control of brain bioenergetics: exploring the subcellular localization of the CB1 receptor. Mol Metab 3:495–504. doi:10.1016/j.molmet.2014.03.007
Hebert-Chatelain E et al (2014b) Studying mitochondrial CB1 receptors: yes we can. Mol Metab 3:339. doi:10.1016/j.molmet.2014.03.008
Hebert-Chatelain E et al (2016) A cannabinoid link between mitochondria and memory. Nature. doi:10.1038/nature20127
Heimann AS et al (2007) Hemopressin is an inverse agonist of CB1 cannabinoid receptors. Proc Natl Acad Sci USA 104:20588–20593. doi:10.1073/pnas.0706980105
Herkenham M et al (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87:1932–1936
Herkenham M et al (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563–583
Herrmann JM, Riemer J (2010) The intermembrane space of mitochondria. Antioxid Redox Signal 13:1341–1358. doi:10.1089/ars.2009.3063
Hill MN, Gorzalka BB (2005) Pharmacological enhancement of cannabinoid CB1 receptor activity elicits an antidepressant-like response in the rat forced swim test. Eur Neuropsychopharmacol 15:593–599. doi:10.1016/j.euroneuro.2005.03.003
Horvath TL, Andrews ZB, Diano S (2009) Fuel utilization by hypothalamic neurons: roles for ROS. Trends Endocrinol Metab 20:78–87. doi:10.1016/j.tem.2008.10.003
Howlett AC (2002) The cannabinoid receptors. Prostaglandins Other Lipid Mediat 68–69:619–631
Hroudova J, Fisar Z (2013) Control mechanisms in mitochondrial oxidative phosphorylation. Neural Regen Res 8:363–375. doi:10.3969/j.issn.1673-5374.2013.04.009
Irannejad R, von Zastrow M (2014) GPCR signaling along the endocytic pathway. Curr Opin Cell Biol 27:109–116. doi:10.1016/j.ceb.2013.10.003
Jia W et al (2006) Delta9-tetrahydrocannabinol-induced apoptosis in Jurkat leukemia T cells is regulated by translocation of Bad to mitochondria. Mol Cancer Res 4:549–562. doi:10.1158/1541-7786.MCR-05-0193
Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380. doi:10.1152/physrev.00019.2008
Katona I et al (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544–4558
Kety SS (1957) Determinants of tissue oxygen tension. Fed Proc 16:666–671
Kishida KT, Klann E (2007) Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxid Redox Signal 9:233–244. doi:10.1089/ars.2007.9.ft-8
Knapp LT, Klann E (2002) Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. J Neurosci 22:674–683
Koch M et al (2015) Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature 519:45–50. doi:10.1038/nature14260
Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97–129. doi:10.1016/S0893-133X(00)00195-0
Kuan CY, Roth KA, Flavell RA, Rakic P (2000) Mechanisms of programmed cell death in the developing brain. Trends Neurosci 23:291–297
Kuyznierewicz I, Thomson M (2002) GTP-binding proteins G(salpha), G(ialpha), and Ran identified in mitochondria of human placenta. Cell Biol Int 26:99–108. doi:10.1006/cbir.2001.0823
Ledent C et al (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283:401–404
Lee CY et al (2008) A comparative study on cannabidiol-induced apoptosis in murine thymocytes and EL-4 thymoma cells. Int immunopharmacol 8:732–740. doi:10.1016/j.intimp.2008.01.018
Lee KY, Chung K, Chung JM (2010) Involvement of reactive oxygen species in long-term potentiation in the spinal cord dorsal horn. J Neurophysiol 103:382–391. doi:10.1152/jn.90906.2008
Li Z, Sheng M (2012) Caspases in synaptic plasticity. Mol Brain 5:15. doi:10.1186/1756-6606-5-15
Li Z et al (2010) Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141:859–871. doi:10.1016/j.cell.2010.03.053
Ligresti A et al (2006) Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast carcinoma. J Pharmacol Exp Ther 318:1375–1387. doi:10.1124/jpet.106.105247
Ma T et al (2011) Amyloid beta-induced impairments in hippocampal synaptic plasticity are rescued by decreasing mitochondrial superoxide. J Neurosci 31:5589–5595. doi:10.1523/JNEUROSCI.6566-10.2011
Ma L et al (2015) Mitochondrial CB1 receptor is involved in ACEA-induced protective effects on neurons and mitochondrial functions. Sci Rep 5:12440. doi:10.1038/srep12440
Mahoney JM, Harris RA (1972) Effect of 9-tetrahydrocannabinol on mitochondrial processes. Biochem Pharmacol 21:1217–1226
Mailleux P, Parmentier M, Vanderhaeghen JJ (1992) Distribution of cannabinoid receptor messenger RNA in the human brain: an in situ hybridization histochemistry with oligonucleotides. Neurosci Lett 143:200–204
Marchi S et al (2012) Mitochondria-ros crosstalk in the control of cell death and aging. J Signal Transduct 2012:329635. doi:10.1155/2012/329635
Marsicano G, Kuner R (2008) Anatomical distribution of receptors, ligands and enzymes in the brain and in the spinal cord: circuitries and neurochemistry. Cannabinoids Brain. doi:10.1007/978-0-387-74349-3_10
Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213–4225
Marsicano G et al (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84–88. doi:10.1126/science.1088208
Massi P et al (2006) The non-psychoactive cannabidiol triggers caspase activation and oxidative stress in human glioma cells. Cell Mol Life Sci 63:2057–2066. doi:10.1007/s00018-006-6156-x
Mato S, Victoria Sanchez-Gomez M, Matute C (2010) Cannabidiol induces intracellular calcium elevation and cytotoxicity in oligodendrocytes. Glia 58:1739–1747. doi:10.1002/glia.21044
Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564. doi:10.1038/346561a0
Mattson MP, Gleichmann M, Cheng A (2008) Mitochondria in neuroplasticity and neurological disorders. Neuron 60:748–766. doi:10.1016/j.neuron.2008.10.010
Mendizabal-Zubiaga J et al (2016) Cannabinoid CB1 receptors are localized in striated muscle mitochondria and regulate mitochondrial respiration. Front Physiol 7:476. doi:10.3389/fphys.2016.00476
Metna-Laurent M et al (2012) Bimodal control of fear-coping strategies by CB(1) cannabinoid receptors. J Neurosci 32:7109–7118. doi:10.1523/JNEUROSCI.1054-12.2012
Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148
Moldrich G, Wenger T (2000) Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides 21:1735–1742
Monory K et al (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455–466. doi:10.1016/j.neuron.2006.07.006
Moreira PI, Santos MS, Moreno A, Oliveira C (2001) Amyloid beta-peptide promotes permeability transition pore in brain mitochondria. Biosci Rep 21:789–800
Morozov YM et al (2013) Antibodies to cannabinoid type 1 receptor co-react with stomatin-like protein 2 in mouse brain mitochondria. Eur J Neurosci 38:2341–2348. doi:10.1111/ejn.12237
Morozov YM, Horvath TL, Rakic P (2014) A tale of two methods: identifying neuronal CB1 receptors. Mol Metab 3:338. doi:10.1016/j.molmet.2014.03.006
Mukherjee J, Yang ZY (1999) Monoamine oxidase A inhibition by fluoxetine: an in vitro and in vivo study. Synapse 31:285–289. doi:10.1002/(SICI)1098-2396(19990315)31:4<285::AID-SYN6>3.0.CO;2-5
Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365(6441):61–65. doi:10.1038/365061a0
Navarrete M, Araque A (2008) Endocannabinoids mediate neuron-astrocyte communication. Neuron 57:883–893. doi:10.1016/j.neuron.2008.01.029
Navarrete M, Araque A (2010) Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68:113–126. doi:10.1016/j.neuron.2010.08.043
Navarro A, Boveris A (2007) The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292:C670–C686. doi:10.1152/ajpcell.00213.2006
Nicholls DG (2005) Mitochondria and calcium signaling. Cell Calcium 38:311–317. doi:10.1016/j.ceca.2005.06.011
Nonomura K et al (2013) Local apoptosis modulates early mammalian brain development through the elimination of morphogen-producing cells. Dev Cell 27:621–634. doi:10.1016/j.devcel.2013.11.015
Nunez E et al (2004) Cannabinoid CB2 receptors are expressed by perivascular microglial cells in the human brain: an immunohistochemical study. Synapse 53:208–213. doi:10.1002/syn.20050
Olsen KM, Sheng M (2012) NMDA receptors and BAX are essential for Abeta impairment of LTP. Sci Rep 2:225. doi:10.1038/srep00225
Olsen RH, Johnson LA, Zuloaga DG, Limoli CL, Raber J (2013) Enhanced hippocampus-dependent memory and reduced anxiety in mice over-expressing human catalase in mitochondria. J Neurochem 125:303–313. doi:10.1111/jnc.12187
Onaivi ES et al (2006) Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann NY Acad Sci 1074:514–536. doi:10.1196/annals.1369.052
Onaivi ES, Ishiguro H, Gu S, Liu QR (2012) CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity. J Psychopharmacol 26:92–103. doi:10.1177/0269881111400652
Ong WY, Mackie K (1999) A light and electron microscopic study of the CB1 cannabinoid receptor in the primate spinal cord. J Neurocytol 28:39–45
Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R (2006) The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr Rev 27:73–100. doi:10.1210/er.2005-0009
Palmisano G, Sardanelli AM, Signorile A, Papa S, Larsen MR (2007) The phosphorylation pattern of bovine heart complex I subunits. Proteomics 7:1575–1583. doi:10.1002/pmic.200600801
Papa S et al (1996) The nuclear-encoded 18 kDa (IP) AQDQ subunit of bovine heart complex I is phosphorylated by the mitochondrial cAMP-dependent protein kinase. FEBS Lett 379:299–301. doi:10.1016/0014-5793(95)01532-9
Pellerito O et al (2014) WIN induces apoptotic cell death in human colon cancer cells through a block of autophagic flux dependent on PPARgamma down-regulation. Apoptosis 19:1029–1042. doi:10.1007/s10495-014-0985-0
Pertwee RG, Ross RA, Craib SJ, Thomas A (2002) (-)-Cannabidiol antagonizes cannabinoid receptor agonists and noradrenaline in the mouse vas deferens. Eur J Pharmacol 456:99–106
Pettit DA, Harrison MP, Olson JM, Spencer RF, Cabral GA (1998) Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J Neurosci Res 51:391–402
Pickel VM, Chan J, Kash TL, Rodriguez JJ, MacKie K (2004) Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127:101–112. doi:10.1016/j.neuroscience.2004.05.015
Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873–884. doi:10.1038/nrn1247
Puighermanal E et al (2009) Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nature Neurosci 12:1152–1158. doi:10.1038/nn.2369
Rangaraju V, Calloway N, Ryan TA (2014) Activity-driven local ATP synthesis is required for synaptic function. Cell 156:825–835. doi:10.1016/j.cell.2013.12.042
Rimmerman N et al (2013) Direct modulation of the outer mitochondrial membrane channel, voltage-dependent anion channel 1 (VDAC1) by cannabidiol: a novel mechanism for cannabinoid-induced cell death. Cell Death Dis 4:e949. doi:10.1038/cddis.2013.471
Rodriguez JJ, Mackie K, Pickel VM (2001) Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat Caudate putamen nucleus. J Neurosci 21:823–833
Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758
Rossato M, Ion Popa F, Ferigo M, Clari G, Foresta C (2005) Human sperm express cannabinoid receptor Cb1, the activation of which inhibits motility, acrosome reaction, and mitochondrial function. J Clin Endocrinol Metab 90:984–991. doi:10.1210/jc.2004-1287
Rozenfeld R, Devi LA (2008) Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J 22:2311–2322. doi:10.1096/fj.07-102731
Ryan D, Drysdale AJ, Lafourcade C, Pertwee RG, Platt B (2009) Cannabidiol targets mitochondria to regulate intracellular Ca2+ levels. J Neurosci 29:2053–2063. doi:10.1523/JNEUROSCI.4212-08.2009
Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255–274
Sarafian TA, Kouyoumjian S, Khoshaghideh F, Tashkin DP, Roth MD (2003) Delta 9-tetrahydrocannabinol disrupts mitochondrial function and cell energetics. Am J Physiol Lung Cell Mol Physiol 284:L298–L306. doi:10.1152/ajplung.00157.2002
Sardanelli AM et al (2006) Occurrence of A-kinase anchor protein and associated cAMP-dependent protein kinase in the inner compartment of mammalian mitochondria. FEBS Lett 580:5690–5696. doi:10.1016/j.febslet.2006.09.020
Schurr A, Livne A (1975) Proceedings: differential inhibition of mitochondrial monoamine oxidase from brain by hashish components. Isr J Med Sci 11:1188
Schurr A, Livne A (1976) Differential inhibition of mitochondrial monoamine oxidase from brain by hashish components. Biochem Pharmacol 25:1201–1203
Schurr A, Porath O, Krup M, Livne A (1978) The effects of hashish components and their mode of action on monoamine oxidase from the brain. Biochem Pharmacol 27:2513–2517
Scorrano L et al (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2:55–67
Shih JC, Chen K, Ridd MJ (1999) Monoamine oxidase: from genes to behavior. Annu Rev Neurosci 22:197–217. doi:10.1146/annurev.neuro.22.1.197
Shoshan-Barmatz V et al (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Asp Med 31:227–285. doi:10.1016/j.mam.2010.03.002
Shrivastava A, Kuzontkoski PM, Groopman JE, Prasad A (2011) Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy. Mol Cancer Ther 10:1161–1172. doi:10.1158/1535-7163.MCT-10-1100
Siegmund SV et al (2007) The endocannabinoid 2-arachidonoyl glycerol induces death of hepatic stellate cells via mitochondrial reactive oxygen species. FASEB J 21:2798–2806. doi:10.1096/fj.06-7717com
Sierra S et al (2014) Detection of cannabinoid receptors CB1 and CB2 within basal ganglia output neurons in macaques: changes following experimental parkinsonism. Brain Struct Funct. doi:10.1007/s00429-014-0823-8
Sokoloff L (1960) Quantitative measurements of cerebral blood flow in man. Methods Med Res 8:253–261
Soria-Gomez E et al (2014) The endocannabinoid system controls food intake via olfactory processes. Nat Neurosci 17:407–415. doi:10.1038/nn.3647
Suen DF, Norris KL, Youle RJ (2008) Mitochondrial dynamics and apoptosis. Genes Dev 22:1577–1590. doi:10.1101/gad.1658508
Szabo B, Schlicker E (2005) Effects of cannabinoids on neurotransmission. Handb Exp Pharmacol 168:327–365
Szoke E, Czeh G, Szolcsanyi J, Seress L (2002) Neonatal anandamide treatment results in prolonged mitochondrial damage in the vanilloid receptor type 1-immunoreactive B-type neurons of the rat trigeminal ganglion. Neuroscience 115:805–814
Taylor RW, Turnbull DM (2005) Mitochondrial DNA mutations in human disease. Nat Rev Genet 6:389–402. doi:10.1038/nrg1606
Technikova-Dobrova Z et al (2001) Cyclic adenosine monophosphate-dependent phosphorylation of mammalian mitochondrial proteins: enzyme and substrate characterization and functional role. Biochemistry 40:13941–13947. doi:10.1021/bi011066p
Tedesco L et al (2008) Cannabinoid type 1 receptor blockade promotes mitochondrial biogenesis through endothelial nitric oxide synthase expression in white adipocytes. Diabetes 57:2028–2036. doi:10.2337/db07-1623
Tedesco L et al (2010) Cannabinoid receptor stimulation impairs mitochondrial biogenesis in mouse white adipose tissue, muscle, and liver: the role of eNOS, p38 MAPK, and AMPK pathways. Diabetes 59:2826–2836. doi:10.2337/db09-1881
Trimmer PA et al (2000) Abnormal mitochondrial morphology in sporadic Parkinson’s and Alzheimer’s disease cybrid cell lines. Exp Neurol 162:37–50. doi:10.1006/exnr.2000.7333
Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393–411
Tuppen HA, Blakely EL, Turnbull DM, Taylor RW (2010) Mitochondrial DNA mutations and human disease. Biochim Biophys Acta 1797:113–128. doi:10.1016/j.bbabio.2009.09.005
Vallee M et al (2014) Pregnenolone can protect the brain from cannabis intoxication. Science 343:94–98. doi:10.1126/science.1243985
Whyte DA et al (2010) Cannabinoids inhibit cellular respiration of human oral cancer cells. Pharmacology 85:328–335. doi:10.1159/000312686
Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–592. doi:10.1038/35069076
Wilson-Poe AR, Morgan MM, Aicher SA, Hegarty DM (2012) Distribution of CB1 cannabinoid receptors and their relationship with mu-opioid receptors in the rat periaqueductal gray. Neuroscience 213:191–200. doi:10.1016/j.neuroscience.2012.03.038
Zaccagnino P, Corcelli A, Baronio M, Lorusso M (2011) Anandamide inhibits oxidative phosphorylation in isolated liver mitochondria. FEBS Lett 585:429–434. doi:10.1016/j.febslet.2010.12.032
Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 96:5780–5785
Acknowledgments
The work in Marsicano’s lab is supported by INSERM, EU–Fp7 (REPROBESITY, HEALTH–F2–2008–223713 and PAINCAGE, HEALTH-603191), European Research Council (Endofood, ERC–2010–StG–260515, and CannaPreg, ERC-2014-PoC-640923), Fondation pour la Recherche Medicale (DRM20101220445, DPP20151033974), Human Frontiers Science Program, Region Aquitaine, and Agence Nationale de la Recherche (ANR Blanc NeuroNutriSens ANR-13-BSV4-0006 and BRAIN ANR-10-LABX-0043). We thank all the members of Marsicano’s lab for the useful discussions. The work of Etienne Hebert-Chatelain is supported by the Natural Sciences and Engineering Research Council of Canada (Discovery grant: RGPIN-2015-05880), Alzheimer Society of Canada (New Investigator Award: 17-09), the Canadian Breast Cancer Foundation (Research grant 16880-2015-17342), Beatrice Hunter Cancer Research Institute (Seed Fund), New Brunswick Health Research Foundation, New Brunswick Innovation Foundation, and Université de Moncton.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Hebert-Chatelain, E., Marsicano, G., Desprez, T. (2017). Cannabinoids and Mitochondria. In: Melis, M. (eds) Endocannabinoids and Lipid Mediators in Brain Functions. Springer, Cham. https://doi.org/10.1007/978-3-319-57371-7_8
Download citation
DOI: https://doi.org/10.1007/978-3-319-57371-7_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-57369-4
Online ISBN: 978-3-319-57371-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)