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The Role of HINT1 in Methamphetamine-Induced Conditioned Place Preference

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Abstract

Drug addiction is a chronically relapsing disorder in humans; yet, the underlying mechanism remained unclear. Recent studies suggested that the histidine triad nucleotide binding protein 1 (HINT1) may play significant roles in diverse neuropsychiatric diseases including drug addiction. In our present study, we used different batches of mice to establish the different stages of methamphetamine (METH)-induced conditioned place preference (CPP) to explore the dynamic changes throughout the process of addiction in different brain regions, including prefrontal cortex (PFC), nucleus accumbens (NAc), corpus striatum (CPu), and hippocampus (Hip). We found that in NAc of the METH group mice, the HINT1 expression level initially increased after acquisition phases, and then dropped to the normal level after extinction phase, and again increased after reinstatement phase. However, there was no statistical difference in the HINT1 expression level in other three encephalic regions (PFC, CPu, and Hip). Therefore, the HINT1 protein, particularly in the NAc, plays a vital role in the METH-induced CPP. However, the precise mechanisms will require further investigation.

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References

  • Allen RM, Everett CV, Nelson AM, Gulley JM, Zahniser NR (2007) Low and high locomotor responsiveness to cocaine predicts intravenous cocaine conditioned place preference in male Sprague-Dawley rats. Pharmacol Biochem Behav 86:37–44

    Article  CAS  PubMed  Google Scholar 

  • Barbier E, Zapata A, Oh E, Liu Q, Zhu F, Undie A, Shippenberg T, Wang JB (2007) Supersensitivity to amphetamine in protein kinase-C interacting protein/HINT1 knockout mice. Neuropsychopharmacology 32:1774–1782

    Article  CAS  PubMed  Google Scholar 

  • Baron M (2001) Genetics of schizophrenia and the new millennium: progress and pitfalls. Am J Hum Genet 68:299–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunningham CL, Gremel CM, Groblewski PA (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1:1662–1670

    Article  CAS  PubMed  Google Scholar 

  • Dang YH, Liu ZW, Chen F, Guo K, Wang JB (2014) Histidine triad nucleotide-binding protein 1 and human diseases. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 36:454–460

    CAS  PubMed  Google Scholar 

  • Fang J, Wang X, He B (2014) Association between common genetic variants in the opioid pathway and smoking behaviors in Chinese men. Behav Brain Funct 10:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Garzon J, Rodriguez-Munoz M, Sanchez-Blazquez P (2012) Direct association of mu-opioid and NMDA glutamate receptors supports their cross-regulation: molecular implications for opioid tolerance. Curr Drug Abuse Rev 5:199–226

    Article  CAS  PubMed  Google Scholar 

  • Homer BD, Solomon TM, Moeller RW, Mascia A, DeRaleau L, Halkitis PN (2008) Methamphetamine abuse and impairment of social functioning: a review of the underlying neurophysiological causes and behavioral implications. Psychol Bull 134:301–310

    Article  PubMed  Google Scholar 

  • Hyman SE (2005) Addiction: a disease of learning and memory. Am J Psychiatry 162:1414–1422

    Article  PubMed  Google Scholar 

  • Jackson KJ, Chen Q, Chen J, Aggen SH, Kendler KS, Chen X (2011) Association of the histidine-triad nucleotide-binding protein-1 (HINT1) gene variants with nicotine dependence. Pharmacogenomics J 11:251–257

    Article  CAS  PubMed  Google Scholar 

  • Jackson KJ, Wang JB, Barbier E, Damaj MI, Chen X (2013) The histidine triad nucleotide binding 1 protein is involved in nicotine reward and physical nicotine withdrawal in mice. Neurosci Lett 550:129–133

    Article  CAS  PubMed  Google Scholar 

  • Karam CS, Ballon JS, Bivens NM, Freyberg Z, Girgis RR, Lizardi-Ortiz JE, Markx S, Lieberman JA, Javitch JA (2010) Signaling pathways in schizophrenia: emerging targets and therapeutic strategies. Trends Pharmacol Sci 31:381–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauer JA (2004) Learning mechanisms in addiction: synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse. Annu Rev Physiol 66:447–475

    Article  CAS  PubMed  Google Scholar 

  • Kelley AE, Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306–3311

    CAS  PubMed  Google Scholar 

  • Kelley AE, Andrzejewski ME, Baldwin AE, Hernandez PJ, Pratt WE (2003) Glutamate-mediated plasticity in corticostriatal networks: role in adaptive motor learning. Ann N Y Acad Sci 1003:159–168

    Article  CAS  PubMed  Google Scholar 

  • Klein DA, Gulley JM (2009) Reduced sensitivity to the locomotor-stimulant effects of cocaine is associated with increased sensitivity to its discriminative stimulus properties. Behav Pharmacol 20:67–77

    Article  CAS  PubMed  Google Scholar 

  • Klein MG, Yao Y, Slosberg ED, Lima CD, Doki Y, Weinstein IB (1998) Characterization of PKCI and comparative studies with FHIT, related members of the HIT protein family. Exp Cell Res 244:26–32

    Article  CAS  PubMed  Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  • Li H, Zhang Y, Su T, Santella RM, Weinstein IB (2006) Hint1 is a haplo-insufficient tumor suppressor in mice. Oncogene 25:713–721

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Puche AC, Wang JB (2008) Distribution and expression of protein kinase C interactive protein (PKCI/HINT1) in mouse central nervous system (CNS). Neurochem Res 33:1263–1276

    Article  CAS  PubMed  Google Scholar 

  • Mandt BH, Schenk S, Zahniser NR, Allen RM (2008) Individual differences in cocaine-induced locomotor activity in male Sprague-Dawley rats and their acquisition of and motivation to self-administer cocaine. Psychopharmacology 201:195–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nestler EJ (2005) Is there a common molecular pathway for addiction? Nat Neurosci 8:1445–1449

    Article  CAS  PubMed  Google Scholar 

  • NIDA(1969). Methamphetamine. Vol., ed.^eds. NIDA(1969)

  • Paxinos G, Franklin KB (2004) The mouse brain in stereotaxic coordinates. Gulf Professional Publishing, Vol.

    Google Scholar 

  • Robertson SD, Matthies HJ, Galli A (2009) A closer look at amphetamine-induced reverse transport and trafficking of the dopamine and norepinephrine transporters. Mol Neurobiol 39:73–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson TE, Berridge KC (2003) Addiction. Annu Rev Psychol 54:25–53

    Article  PubMed  Google Scholar 

  • Robison AJ, Nestler EJ (2011) Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12:623–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Munoz M, de la Torre-Madrid E, Sanchez-Blazquez P, Wang JB, Garzon J (2008) NMDAR-nNOS generated zinc recruits PKCgamma to the HINT1-RGS17 complex bound to the C terminus of mu-opioid receptors. Cell Signal 20:1855–1864

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Munoz M, Sanchez-Blazquez P, Vicente-Sanchez A, Bailon C, Martin-Aznar B, Garzon J (2011) The histidine triad nucleotide-binding protein 1 supports mu-opioid receptor-glutamate NMDA receptor cross-regulation. Cell Mol Life Sci 68:2933–2949

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Munoz, M, Sanchez-Blazquez, P, Merlos, M, Garzon-Nino, J (2016) Endocannabinoid control of glutamate NMDA receptors: the therapeutic potential and consequences of dysfunction. Oncotarget

    Google Scholar 

  • Romanova EV, Lee JE, Kelleher NL, Sweedler JV, Gulley JM (2010) Mass spectrometry screening reveals peptides modulated differentially in the medial prefrontal cortex of rats with disparate initial sensitivity to cocaine. AAPS J 12:443–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabeti J, Gerhardt GA, Zahniser NR (2003) Individual differences in cocaine-induced locomotor sensitization in low and high cocaine locomotor-responding rats are associated with differential inhibition of dopamine clearance in nucleus accumbens. J Pharmacol Exp Ther 305:180–190

    Article  CAS  PubMed  Google Scholar 

  • Straub RE, MacLean CJ, O'Neill FA, Walsh D, Kendler KS (1997) Support for a possible schizophrenia vulnerability locus in region 5q22-31 in Irish families. Mol Psychiatry 2:148–155

    Article  CAS  PubMed  Google Scholar 

  • Su T, Suzui M, Wang L, Lin CS, Xing WQ, Weinstein IB (2003) Deletion of histidine triad nucleotide-binding protein 1/PKC-interacting protein in mice enhances cell growth and carcinogenesis. Proc Natl Acad Sci U S A 100:7824–7829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su HL, Zhu J, Chen YJ, Zhao N, Han W, Dang YH, Xu M, Chen T (2013) Roles of levo-tetrahydropalmatine in modulating methamphetamine reward behavior. Physiol Behav 118:195–200

    Article  CAS  PubMed  Google Scholar 

  • Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462

    Article  CAS  PubMed  Google Scholar 

  • Vicente-Sanchez A, Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J (2013) HINT1 protein cooperates with cannabinoid 1 receptor to negatively regulate glutamate NMDA receptor activity. Mol Brain 6:42

    Article  PubMed  PubMed Central  Google Scholar 

  • Volkow ND, Morales M (2015) The brain on drugs: from reward to addiction. Cell 162:712–725

    Article  CAS  PubMed  Google Scholar 

  • Volz TJ, Hanson GR, Fleckenstein AE (2007) The role of the plasmalemmal dopamine and vesicular monoamine transporters in methamphetamine-induced dopaminergic deficits. J Neurochem 101:883–888

    Article  CAS  PubMed  Google Scholar 

  • Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679–720

    Article  CAS  PubMed  Google Scholar 

  • Zhao N, Chen Y, Zhu J, Wang L, Cao G, Dang Y, Yan C, Wang J, Chen T (2014) Levo-tetrahydropalmatine attenuates the development and expression of methamphetamine-induced locomotor sensitization and the accompanying activation of ERK in the nucleus accumbens and caudate putamen in mice. Neuroscience 258:101–110

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Science Foundation of China (NSFC81171262, 81771435, 81371473 to Yong-hui Dang), and the Natural Science Basic Research Plan in Shaanxi Province of China (No. 2016JM8078 to Yong-hui Dang).

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Correspondence to Yong-hui Dang or Teng Chen.

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The experimental protocol was approved by the Institutional Animal Care Committee of Xi’an Jiaotong University.

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The authors declare that they have no conflicts of interest.

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Li, Jp., Liu, P., Lei, G. et al. The Role of HINT1 in Methamphetamine-Induced Conditioned Place Preference. Neurotox Res 33, 353–361 (2018). https://doi.org/10.1007/s12640-017-9797-7

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