The mechanism of intracerebral L-type voltage dependent calcium channels in drug addiction

logo

Journals Books
Advanced Search
Sign in Register

中文

Chinese Science Bulletin
Download PDF
Chinese Science Bulletin, Volume 61, Issue 11: 1173-1180(2016) https://doi.org/10.1360/N972015-01037

The mechanism of intracerebral L-type voltage dependent calcium channels in drug addiction

ShuBo JIN1,2,?, Fang SHEN1,?, Ying DUAN1,2, Ming LI3, Nan SUI1,*
More info
  • ReceivedNov 25, 2015
  • AcceptedMar 14, 2016
Previous Table of Contents Next
Share
Rating

Abstract

Changes of intracellular calcium are the fundament of cell physiological function and the key factor in intracellular signal transduction and gene expression. Recently more studies have been focusing on the relationship between voltage dependent calcium channels (VDCCs) and drug addiction. A great deal of evidence suggests that L-type VDCCs (LTCCs), which are activated by membrane depolarization, play an important role in drug addiction by affecting the release of neurotransmitters, excitability of neurons, gene transcription and synaptic plasticity. LTCCs are divided into four subtypes: Cav1.1, Cav1.2, Cav1.3 and Cav1.4, according to the conduction of single channel and sensitivity to calcium antagonists and agonists. Among them Cav1.2 and Cav1.3 are mainly expressed in the central nervous system. It is reported that the increasing of intracellular calcium induced by LTCCs is crucial in physical dependence and withdrawal symptoms of addictive drugs such as morphine. In addition, the enhancement of cAMP-response element binding protein (CREB) and ryanodine receptor 2 (RyR2) induced by LTCCs on endoplasmic reticulum (ER) stimulate the release of calcium in cytoplasm, leading to a long-term increase in intracellular calcium. This relation might underlie the dependence and tolerance of nicotine. Moreover, it is reported that LTCCs also take part in nonsomatic signs of drug withdrawal. For example, intraperitoneal injection of LTCCs antagonists can reduce nonsomatic withdrawal symptoms in chronic nicotine-dependent rats, like anxiety, memory impartment and depression-like effects. Furthermore, recent researches also find that Cav1.2 and Cav1.3 play an important role in the acquisition and expression of cocaine-induced behavioral sensitization through different molecular mechanisms in specific brain regions. For instance, Cav1.3 in the ventral tegmental area (VTA) affects the development of cocaine sensitization by activating extracellular regulated protein kinases 2 (ERK2); While in the expression of cocaine sensitization, on the one hand, Cav1.2 opening in the nucleus accumbens (NAc) regulated by dopamine 1 (D1) receptor, activates its downstream Ca2+/calmodulin-dependent protein kinase II (CaMK II) and ERK2, leading to the phosphorylation at GluA1Ser831 of a-amino-3-hydroxy-5- methyl-4-isoxazole-propionic acid receptor (AMPAR) and the membrane insertion of AMPA receptor GluA1 subunit. This process needs the activation of Cav1.3 in the VTA. On the other hand, activation of Cav1.3 in the dorsal striatum (DS), which is regulated by D2 receptor, suppresses its downstream activation, including CREB, DARPP-32, Akt and GSK-3b, leading to the reduction of phosphorylation at GLuA1Ser845 and the expression level of membrane GluA1. Besides, LTCCs are also involved in the acquisition, expression and reinstatement of addiction memory. Recent studies indicate that LTCCs play different roles in different phases of addiction memory. For example, LTCCs in the VTA are involved in the acquisition of morphine conditioned place preference (CPP) by activating N-methyl-D-aspartate receptor (NMDAR); Whereas LTCCs in the NAc regulate development and expression of morphine CPP via interacting with the RyR2 which can induce the calcium release from the ER. Moreover, it has been demonstrated that the scaffold protein A-kinase anchor proteins79/150 (AKAP79/150) can anchor LTCCs to synaptic membranes, which might be a potential mechanism underlying the reinstatement of addiction memory induced by drugs. Therefore, in this review, we will focus on summarizing the role and the potential cellular and molecular mechanisms of LTCCs in drug addiction, with the expectation of expanding the perspectives onto further exploration of the neurobiological mechanisms of addiction memory.


Funded by

国家自然科学基金重大研究计划培育项目(91332115)

国家自然科学基金(31170988)

国家重点基础研究发展计划(2015CB553501)


References

[1] Catterall W A, Leal K, Nanou E. Calcium channels and short-term synaptic plasticity. J Biol Chem, 2013, 288: 10742-10749 CrossRef Google Scholar

[2] Wheeler D G, Groth R D, Ma H, et al. Cav1 and Cav2 channels engage distinct modes of Ca2+ signaling to control CREB-dependent gene expression. Cell, 2012, 149: 1112-1124 CrossRef Google Scholar

[3] Simms B A, Zamponi G W. Neuronal voltage-gated calcium channels: Structure, function, and dysfunction. Neuron, 2014, 82: 24-45 CrossRef Google Scholar

[4] Pittman A N. L-type calcium channels modulate firing patterns of ventral tegmental area neurons. Doctor Dissertation. Newfoundland: Memorial University of Newfoundland. 2012, Google Scholar

[5] Simms B A, Zamponi G W. Trafficking and stability of voltage-gated calcium channels. Cell Mol Life Sci, 2012, 69: 843-856 CrossRef Google Scholar

[6] Zamponi G W, Striessnig J, Koschak A, et al. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol Rev, 2015, 67: 821-870 CrossRef Google Scholar

[7] Striessnig J, Pinggera A, Kaur G, et al. L-type Ca2+ channels in heart and brain. Wiley Interdiscip Rew Membr Transp Signal, 2014, 3: 15-38 CrossRef Google Scholar

[8] Vandael D H, Marcantoni A, Mahapatra S, et al. Cav1. 3 and BK channels for timing and regulating cell firing. Mol Neurobiol, 2010, 42: 185-198 CrossRef Google Scholar

[9] Tr?ger J, Moutty M C, Skroblin P, et al. A-kinase anchoring proteins as potential drug targets. Brit J Pharmacol, 2012, 166: 420-433 CrossRef Google Scholar

[10] Berger S M, Bartsch D. The role of L-type voltage-gated calcium channels Cav1. 2 and Cav1. 3 in normal and pathological brain function. Cell Tissue Res, 2014, 357: 463-476 CrossRef Google Scholar

[11] Schierberl K C. The emerging role of the L-type calcium channels in cocaine-induced AMPA receptor plasticity. Doctor Dissertation. New York: Weill Medical College of Cornell University. 2014, Google Scholar

[12] Bernardi R E, Uhrig S, Spanagel R, et al. Transcriptional regulation of L-type calcium channel subtypes Cav1. 2 and Cav1. 3 by nicotine and their potential role in nicotine sensitization. Nicotine Tob Res, 2014, 16: 774-785 CrossRef Google Scholar

[13] Schierberl K, Giordano T, Satpute S, et al. Cav1. 3 L-type Ca2+ channels mediate long-term adaptation in dopamine D2L-mediated GluA1 trafficking in the dorsal striatum following cocaine exposure. Channels, 2012, 6: 11-17 CrossRef Google Scholar

[14] Schierberl K, Hao J, Tropea T F, et al. Cav1. 2 L-type Ca2+ channels mediate cocaine-induced GluA1 trafficking in the nucleus accumbens, a long-term adaptation dependent on ventral tegmental area Cav1. 3 channels. J Neurosci, 2011, 31: 13562-13575 CrossRef Google Scholar

[15] Reissner K J, Uys J D, Schwacke J H, et al. AKAP signaling in reinstated cocaine seeking revealed by iTRAQ proteomic analysis. J Neurosci, 2011, 31: 5648-5658 CrossRef Google Scholar

[16] Cami J, Farré M. Drug addiction. New Engl J Med, 2003, 349: 975-986 CrossRef Google Scholar

[17] Welch S, Olson K G. Opiate tolerance-induced modulation of free intracellular calcium in synaptosomes. Life Sci, 1991, 48: 1853-1861 CrossRef Google Scholar

[18] Antkiewicz-Michaluk L, Michaluk J, Romańska I, et al. Reduction of morphine dependence and potentiation of analgesia by chronic co-administration of nifedipine. Psychopharmacology, 1993, 111: 457-464 CrossRef Google Scholar

[19] Kuzmin A, Zvartau E, Gessa G L, et al. Calcium antagonists isradipine and nimodipine suppress cocaine and morphine intravenous self-administration in drug-naive mice. Pharmacol Biochem Behav, 1992, 41: 497-500 CrossRef Google Scholar

[20] Damaj M I. The involvement of spinal Ca2+/calmodulin-protein kinase Ⅱ in nicotine-induced antinociception in mice. Eur J Pharmacol, 2000, 404: 103-110 CrossRef Google Scholar

[21] Biala G, Budzynska B. Reinstatement of nicotine-conditioned place preference by drug priming: Effects of calcium channel antagonists. Eur J Pharmacol, 2006, 537: 85-93 CrossRef Google Scholar

[22] Bia?a G, Polak P, Michalak A, et al. Influence of calcium channel antagonists on nonsomatic signs of nicotine and D-amphetamine withdrawal in mice. Pharmacol Rep, 2014, 66: 212-222 CrossRef Google Scholar

[23] Kulak J M, McIntosh J M, Yoshikami D, et al. Nicotine-evoked transmitter release from synaptosomes: Functional association of specific presynaptic acetylcholine receptors and voltage-gated calcium channels. J Neurochem, 2001, 77: 1581-1589 CrossRef Google Scholar

[24] Shibasaki M, Kurokawa K, Ohkuma S. Upregulation of L-type Cav1 channels in the development of psychological dependence. Synapse, 2010, 64: 440-444 CrossRef Google Scholar

[25] Ziviani E, Lippi G, Bano D, et al. Ryanodine receptor-2 upregulation and nicotine-mediated plasticity. Embo J, 2011, 30: 194-204 CrossRef Google Scholar

[26] Kurokawa K, Mizuno K, Ohkuma S. Dopamine D1 receptor signaling system regulates ryanodine receptor expression in ethanol physical dependence. Alcohol Clin Exp Res, 2013, 37: 771-783 CrossRef Google Scholar

[27] Robinson T E, Berridge K C. The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Rev, 1993, 18: 247-291 CrossRef Google Scholar

[28] Reisi Z, Bani-Ardalan M, Zarepour L, et al. Involvement of D1/D2 dopamine receptors within the nucleus accumbens and ventral tegmental area in the development of sensitization to antinociceptive effect of morphine. Pharmacol Biochem Behav, 2014, 118: 16-21 CrossRef Google Scholar

[29] Brebner K, Wong T P, Liu L D, et al. Nucleus accumbens long-term depression and the expression of behavioral sensitization. Science, 2005, 310: 1340-1343 CrossRef Google Scholar

[30] Zhang Q, Li J X, Zheng J W, et al. L-type Ca2+ channel blockers inhibit the development but not the expression of sensitization to morphine in mice. Eur J Pharmacol, 2003, 467: 145-150 CrossRef Google Scholar

[31] Licata S C, Schmidt H D, Pierce R C. Suppressing calcium/calmodulin-dependent protein kinase Ⅱ activity in the ventral tegmental area enhances the acute behavioural response to cocaine but attenuates the initiation of cocaine-induced behavioural sensitization in rats. Eur J Neurosci, 2004, 19: 405-414 CrossRef Google Scholar

[32] Pierce R C, Quick E A, Reeder D C, et al. Calcium-mediated second messengers modulate the expression of behavioral sensitization to cocaine. J Pharmacol Exp Ther, 1998, 286: 1171-1176 Google Scholar

[33] Bowers M S, Chen B T, Bonci A. AMPA receptor synaptic plasticity induced by psychostimulants: The past, present, and therapeutic future. Neuron, 2010, 67: 11-24 CrossRef Google Scholar

[34] Wolf M E, Ferrario C R. AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci Biobehav Rev, 2010, 35: 185-211 CrossRef Google Scholar

[35] Roche K W, O’Brien R J, Mammen A L, et al. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron, 1996, 16: 1179-1188 CrossRef Google Scholar

[36] Rajadhyaksha A, Husson I, Satpute S S, et al. L-type Ca2+ channels mediate adaptation of extracellular signal-regulated kinase 1/2 phosphorylation in the ventral tegmental area after chronic amphetamine treatment. J Neurosci, 2004, 24: 7464-7476 CrossRef Google Scholar

[37] Giordano T P, Tropea T F, Satpute S S, et al. Molecular switch from L-type Cav1. 3 to Cav1. 2 Ca2+ channel signaling underlies long-term psychostimulant-induced behavioral and molecular plasticity. J Neurosci, 2010, 30: 17051-17062 CrossRef Google Scholar

[38] Han H, Dong Z, Jia Y, et al. Opioid addiction and withdrawal differentially drive long-term depression of inhibitory synaptic transmission in the hippocampus. Sci Rep, 2015, 5: 9666 CrossRef Google Scholar

[39] Huber K M, Mauk M D, Kelly P T. Distinct LTP induction mechanisms: Contribution of NMDA receptors and voltage-dependent calcium channels. J Neurophysiol, 1995, 73: 270-279 Google Scholar

[40] Morgan S L, Coussens C M, Teyler T J. Depotentiation of vdccLTP requires NMDAR activation. Neurobiol Learn Mem, 2001, 76: 229-238 CrossRef Google Scholar

[41] Brimblecombe K R, Gracie C J, Platt N J, et al. Gating of dopamine transmission by calcium and axonal N-, Q-, T- and L-type voltage- gated calcium channels differs between striatal domains. J Physiol, 2015, 593: 929-946 CrossRef Google Scholar

[42] Ginty D D, Kornhauser J M, Thompson M A, et al. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science, 1993, 260: 238-241 CrossRef Google Scholar

[43] Narita M, Matsumura Y, Ozaki S, et al. Role of the calcium/calmodulin-dependent protein kinase ii (CaMKⅡ) in the morphine-induced pharmacological effects in the mouse. Neuroscience, 2004, 126: 415-421 CrossRef Google Scholar

[44] Pucilowski O, Garges P L, Rezvani A H, et al. Verapamil suppresses D-amphetamine-induced place preference conditioning. Eur J Pharmacol, 1993, 240: 89-92 CrossRef Google Scholar

[45] Calcagnetti D J, Keck B J, Quatrella L A, et al. Blockade of cocaine-induced conditioned place preference: Relevance to cocaine abuse therapeutics. Life Sci, 1995, 56: 475-483 CrossRef Google Scholar

[46] Degoulet M, Stelly C E, Ahn K C, et al. L-type Ca2+ channel blockade with antihypertensive medication disrupts VTA synaptic plasticity and drug-associated contextual memory. Mol Psychiatry, 2015, 21: 394-402 Google Scholar

[47] Martellotta M C, Kuzmin A, Muglia P, et al. Effects of the calcium antagonist isradipine on cocaine intravenous self-administration in rats. Psychopharmacology, 1994, 113: 378-380 CrossRef Google Scholar

[48] Biala G, Budzynska B. Calcium-dependent mechanisms of the reinstatement of nicotine-conditioned place preference by drug priming in rats. Pharmacol Biochem Behav, 2008, 89: 116-125 CrossRef Google Scholar

[49] Katsura M, Mohri Y, Shuto K, et al. Up-regulation of L-type voltage-dependent calcium channels after long term exposure to nicotine in cerebral cortical neurons. J Biol Chem, 2002, 277: 7979-7988 CrossRef Google Scholar

[50] Bia?a G, Kruk M. Influence of bupropion and calcium channel antagonists on the nicotine-induced memory-related response of mice in the elevated plus maze in mice. Pharmacol Rep, 2009, 61: 236-244 CrossRef Google Scholar

[51] Salmanzadeh F, Fathollahi Y, Semnanian S, et al. Dependence on morphine leads to a prominent sharing among the different mechanisms of long-term potentiation in the CA1 region of rat hippocampus. Brain Res, 2003, 963: 93-100 CrossRef Google Scholar

[52] Liu Y, Harding M, Pittman A, et al. Cav1. 2 and Cav1. 3 L-type calcium channels regulate dopaminergic firing activity in the mouse ventral tegmental area. J Neurophysiol, 2014, 112: 1119-1130 CrossRef Google Scholar

[53] Cooper D C, White F J. L-type calcium channels modulate glutamate-driven bursting activity in the nucleus accumbens in vivo. Brain Res, 2000, 880: 212-218 CrossRef Google Scholar

[54] Kurokawa K, Mizuno K, Ohkuma S. Increase of type 2 ryanodine receptors in mouse nucleus accumbens in the development and expression of morphine-induced place preference. J Pharmacol Sci, 2014, 126: 285-290 CrossRef Google Scholar

  • Click to view Download high-quality image

    隋南

    中国科学院心理研究所研究员, 博士生导师, 中国心理学会生理心理学分会理事长, 北京神经科学学会常务理事; 北京心理学会副理事长. 研究领域以小鸡、啮齿类动物及树鼩为动物行为模型, 通过内窥成像、光遗传学等技术手段, 研究药物成瘾的脑机制, 并拓展到药物成瘾患者行为决策认知机制的研究, 胚胎期成瘾药物暴露对子代神经发育及成瘾易感性的影响, 以及对抑郁症神经机制的研究和新型抗抑郁药物的筛选.

Copyright 2019 Science China Press Co., Ltd. 科学大众杂志社有限责任公司 版权所有

京ICP备18024590号-1