Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Gene Expression Profiling in the Striatum of Per2 KO Mice Exhibiting More Vulnerable Responses against Methamphetamine

  • Kim, Mikyung (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Jeon, Se Jin (School of Medicine and Center for Neuroscience Research, Konkuk University) ;
  • Custodio, Raly James (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Lee, Hyun Jun (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Sayson, Leandro Val (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Ortiz, Darlene Mae D. (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Cheong, Jae Hoon (School of Pharmacy, Jeonbuk National University) ;
  • Kim, Hee Jin (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University)
  • Received : 2020.07.09
  • Accepted : 2020.08.23
  • Published : 2021.03.01
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Abstract

Drug addiction influences most communities directly or indirectly. Increasing studies have reported the relationship between circadian-related genes and drug addiction. Per2 disrupted mice exhibited more vulnerable behavioral responses against some drugs including methamphetamine (METH). However, its roles and mechanisms are still not clear. Transcriptional profiling analysis in Per2 knockout (KO) mice may provide a valuable tool to identify potential genetic involvement and pathways in enhanced behavioral responses against drugs. To explore the potential genetic involvement, we examined common differentially expressed genes (DEGs) in the striatum of drug naïve Per2 KO/wild-type (WT) mice, and before/after METH treatment in Per2 KO mice, but not in WT mice. We selected 9 common DEGs (Ncald, Cpa6, Pklr, Ttc29, Cbr2, Egr2, Prg4, Lcn2, and Camsap2) based on literature research. Among the common DEGs, Ncald, Cpa6, Pklr, and Ttc29 showed higher expression levels in drug naïve Per2 KO mice than in WT mice, while they were downregulated in Per2 KO mice after METH treatment. In contrast, Cbr2, Egr2, Prg4, Lcn2, and Camsap2 exhibited lower expression levels in drug naïve Per2 KO mice than in WT mice, while they were upregulated after METH treatment in Per2 KO mice. qRT-PCR analyses validated the expression patterns of 9 target genes before/after METH treatment in Per2 KO and WT mice. Although further research is required to deeply understand the relationship and roles of the 9 target genes in drug addiction, the findings from the present study indicate that the target genes might play important roles in drug addiction.

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References

  1. Abarca, C., Albrecht, U. and Spanagel, R. J. (2002) Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc. Natl. Acad. Sci. U.S.A. 99, 9026-9030. https://doi.org/10.1073/pnas.142039099
  2. Albrecht, U., Zheng, B., Larkin, D., Sun, Z. S. and Lee, C. C. (2001) mPer1 and mPer2 are essential for normal resetting of the circadian clock. J. Biol. Rhythms 16, 100-104. https://doi.org/10.1177/074873001129001791
  3. Ammon, S., Mayer, P., Riechert, U., Tischmeyer, H. and Hollt, V. J. (2003) Microarray analysis of genes expressed in the frontal cortex of rats chronically treated with morphine and after naloxone precipitated withdrawal. Mol. Brain Res. 112, 113-125. https://doi.org/10.1016/S0169-328X(03)00057-3
  4. Bae, K., Jin, X., Maywood, E. S., Hastings, M. H., Reppert, S. M. and Weaver, D. R. (2001) Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron 30, 525-536. https://doi.org/10.1016/S0896-6273(01)00302-6
  5. Belluardo, N., Olsson, P., Mudo, G., Sommer, W., Amato, G. and Fuxe, K. (2005) Transcription factor gene expression profiling after acute intermittent nicotine treatment in the rat cerebral cortex. Neuroscience 133, 787-796. https://doi.org/10.1016/j.neuroscience.2005.01.061
  6. Binder, E. B., Kinkead, B., Owens, M. J. and Nemeroff, C. B. (2001) Neurotensin and dopamine interactions. Pharmacol. Rev. 53, 453-486.
  7. Brager, A. J., Stowie, A. C., Prosser, R. A. and Glass, J. D. (2013) The mPer2 clock gene modulates cocaine actions in the mouse circadian system. Behav. Brain Res. 243, 255-260. https://doi.org/10.1016/j.bbr.2013.01.014
  8. Caprioli, D., Venniro, M., Zhang, M., Bossert, J. M., Warren, B. L., Hope, B. T. and Shaham, Y. (2017) Role of dorsomedial striatum neuronal ensembles in incubation of methamphetamine craving after voluntary abstinence. J. Neurosci. 37, 1014-1027. https://doi.org/10.1523/JNEUROSCI.3091-16.2017
  9. Chang, L., Alicata, D., Ernst, T. and Volkow, N. (2007) Structural and metabolic brain changes in the striatum assoiciated with methamphetamine abuse. Addiction 102, 16-32. https://doi.org/10.1111/j.1360-0443.2006.01782.x
  10. dela Pena, I., de la Pena, J. B., Kim, B. N., Han, D. H., Noh, M. and Cheong, J. H. (2015) Gene expression profiling in the striatum of amphetamine-treated spontaneously hypertensive rats which showed amphetamine conditioned place preference and self-administration. Arch. Pharm. Res. 38, 865-875. https://doi.org/10.1007/s12272-014-0470-x
  11. Everitt, B. J. and Robbins, T. W. (2016) Drug addiction: updating actions to habits to compulsions ten years on. Annu. Rev. Psychol. 67, 23-50. https://doi.org/10.1146/annurev-psych-122414-033457
  12. Ferreira, A. C., Da Mesquita, S., Sousa, J. C., Correia-Neves, M., Sousa, N., Palha, J. A. and Marques, F. (2015) From the periphery to the brain: Lipocalin-2, a friend or foe? Prog. Neurobiol. 131, 120-136. https://doi.org/10.1016/j.pneurobio.2015.06.005
  13. Ferreira, A. C., Pinto, V., Mesquita, S. D., Novais, A., Sousa, J. C., Correia-Neves, M., Sousa, N., Palha, J. A. and Marques, F. (2013) Lipocalin-2 is involved in emotional behaviors and cognitive function. Front. Cell. Neurosci. 7, 122. https://doi.org/10.3389/fncel.2013.00122
  14. Gabet, Y., Baniwal, S. K., Leclerc, N., Shi, Y., Kohn-Gabet, A. E., Cogan, J., Dixon, A., Bachar, M., Guo, L., Turman, J. E., Jr. and Frenkel, B. (2010) Krox20/EGR2 deficiency accelerates cell growth and differentiation in the monocytic lineage and decreases bone mass. Am. J. Hematol. 116, 3964-3971.
  15. Gravotta, L., Gavrila, A. M., Hood, S. and Amir, S. J. (2011) Global depletion of dopamine using intracerebroventricular 6-hydroxydopamine injection disrupts normal circadian wheel-running patterns and PERIOD2 expression in the rat forebrain. J. Mol. Neurosci. 45, 162-171. https://doi.org/10.1007/s12031-011-9520-8
  16. Hampp, G., Ripperger, J. A., Houben, T., Schmutz, I., Blex, C., Perreau-Lenz, S., Brunk, I., Spanagel, R., Ahnert-Hilger, G., Meijer, J. H. and Albrecht, U. (2008) Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr. Biol. 18, 678-683. https://doi.org/10.1016/j.cub.2008.04.012
  17. Hasler, B., Smith, L., Cousins, J. and Bootzin, R. J. (2012) Circadian rhythms, sleep, and substance abuse. Sleep Med. Rev. 16, 67-81. https://doi.org/10.1016/j.smrv.2011.03.004
  18. Hood, S., Cassidy, P., Cossette, M. P., Weigl, Y., Verwey, M., Robinson, B., Stewart, J. and Amir, S. (2010) Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J. Neurosci. 30, 14046-14058. https://doi.org/10.1523/JNEUROSCI.2128-10.2010
  19. Ivings, L., Pennington, S. R., Jenkins, R., Weiss, J. L. and Burgoyne, R. D. (2002) Identification of Ca2+-dependent binding partners for the neuronal calcium sensor protein neurocalcin δ: interaction with actin, clathrin and tubulin. Biochem. J. 363, 599-608. https://doi.org/10.1042/bj3630599
  20. Jha, M. K., Lee, S., Park, D. H., Kook, H., Park, K. G., Lee, I. K. and Suk, K. (2015) Diverse functional roles of lipocalin-2 in the central nervous system. Neurosci. Biobehav. Rev. 49, 135-156. https://doi.org/10.1016/j.neubiorev.2014.12.006
  21. Kasckow, J. and Nemeroff, C. B. (1991) The neurobiology of neurotensin: focus on neurotensin-dopamine interactions. Regul. Pept. 36, 153-164. https://doi.org/10.1016/0167-0115(91)90053-J
  22. Kim, B. W., Jeong, K. H., Kim, J. H., Jin, M., Kim, J. H., Lee, M. G., Choi, D. K., Won,S. Y., McLean, C., Jeon, M. T., Lee, H. W., Kim, S. R. and Suk, K. (2016) Pathogenic upregulation of glial lipocalin-2 in the parkinsonian dopaminergic system. J. Neurosci. 36, 5608-5622. https://doi.org/10.1523/JNEUROSCI.4261-15.2016
  23. Kim, M., Custodio, R. J., Botanas, C. J., de la Pena, J. B., Sayson, L. V., Abiero, A., Ryoo, Z. Y., Cheong, J. H. and Kim, H. J. (2019) The circadian gene, Per2, influences methamphetamine sensitization and reward through the dopaminergic system in the striatum of mice. Addict. Biol. 24, 946-957. https://doi.org/10.1111/adb.12663
  24. Kim, M., De La Pena, J. B., Cheong, J. H. and Kim, H. J. J. (2018) Neurobiological functions of the period circadian clock 2 gene, Per2. Biomol. Ther. (Seoul) 26, 358-367. https://doi.org/10.4062/biomolther.2017.131
  25. Kovanen, L., Saarikoski, S. T., Haukka, J., Pirkola, S., Aromaa, A., Lonnqvist, J. and Partonen, T. (2010) Circadian clock gene polymorphisms in alcohol use disorders and alcohol consumption. Alcohol Alcohol. 45, 303-311. https://doi.org/10.1093/alcalc/agq035
  26. Kuntz, K. L., Patel, K. M., Grigson, P. S., Freeman, W. M. and Vrana, K. E. (2008) Heroin self-administration: II. CNS gene expression following withdrawal and cue-induced drug-seeking behavior. Pharmacol. Biochem. Behav. 90, 349-356. https://doi.org/10.1016/j.pbb.2008.03.019
  27. Lee, Y. H. (2018) Investigating the possible causal association of coffee consumption with osteoarthritis risk using a Mendelian randomization analysis. Clin. Rheumatol. 37, 3133-3139. https://doi.org/10.1007/s10067-018-4252-6
  28. Lyons, P. J., Callaway, M. B. and Fricker, L. D. (2008) Characterization of carboxypeptidase A6, an extracellular matrix peptidase. J. Biol. Chem. 283, 7054-7063. https://doi.org/10.1074/jbc.M707680200
  29. Ma, W. W., Ding, B. J., Yuan, L. H., Zhao, L., Yu, H. L. and Xiao, R. (2017) Neurocalcin-delta: a potential memory-related factor in hippocampus of obese rats induced by high-fat diet. Afr. Health Sci. 17, 1211-1221. https://doi.org/10.4314/ahs.v17i4.32
  30. McCoy, M. T., Jayanthi, S., Wulu, J. A., Beauvais, G., Ladenheim, B., Martin, T. A., Krasnova, I. N., Hodges, A. B. and Cadet, J. L. (2011) Chronic methamphetamine exposure suppresses the striatal expression of members of multiple families of immediate early genes (IEGs) in the rat: normalization by an acute methamphetamine injection. Psychopharmacology (Berl.) 215, 353-365. https://doi.org/10.1007/s00213-010-2146-7
  31. Miller, J. A., Woltjer, R. L., Goodenbour, J. M., Horvath, S. and Geschwind, D. H. (2013) Genes and pathways underlying regional and cell type changes in Alzheimer's disease. Genome Med. 5, 48. https://doi.org/10.1186/gm452
  32. Mucha, M., Skrzypiec, A. E., Schiavon, E., Attwood, B. K., Kucerova, E. and Pawlak, R. (2011) Lipocalin-2 controls neuronal excitability and anxiety by regulating dendritic spine formation and maturation. Proc. Natl. Acad. Sci. U.S.A. 108, 18436-18441. https://doi.org/10.1073/pnas.1107936108
  33. Nestler, E. J. and Malenka, R. C. (2004) The addicted brain. Sci. Am. 290, 78-85. https://doi.org/10.1038/scientificamerican0304-78
  34. Perreau-Lenz, S., Sanchis-Segura, C., Leonardi-Essmann, F., Schneider, M. and Spanagel, R. (2010) Development of morphine-induced tolerance and withdrawal: involvement of the clock gene mPer2. Eur. Neuropsychopharmacol. 20, 509-517. https://doi.org/10.1016/j.euroneuro.2010.03.006
  35. Qadri, M. M., Jay, G. D., Ostrom, R. S., Zhang, L. X. and Elsaid, K. A. (2018) cAMP attenuates TGF-β's profibrotic responses in osteoarthritic synoviocytes: involvement of hyaluronan and PRG4. Am. J. Physiol. Cell Physiol. 315, C432-C443. https://doi.org/10.1152/ajpcell.00041.2018
  36. Riessland, M., Kaczmarek, A., Schneider, S., Swoboda, K. J., Lohr, H., Bradler, C., Grysko, V., Dimitriadi, M., Hosseinibarkooie, S., TorresBenito, L., Peters, M., Upadhyay, A., Biglari, N., Krober, S., Holker, I., Garbes, L., Gilissen, C., Hoischen, A., Nurnberg, G., Nurnberg, P., Walter, M., Rigo, F., Bennett, C. F., Kye, M. J., Hart, A. C., Hammerschmidt, M., Kloppenburg, P. and Wirth, B. (2017) Neurocalcin delta suppression protects against spinal muscular atrophy in humans and across species by restoring impaired endocytosis. Am. J. Hum. Genet. 100, 297-315. https://doi.org/10.1016/j.ajhg.2017.01.005
  37. Servonnet, A., Minogianis, E. A., Bouchard, C., Bedard, A. M., Levesque, D., Rompre, P. P. Samaha, A. N. (2017) Neurotensin in the nucleus accumbens reverses dopamine supersensitivity evoked by antipsychotic treatment. Neuropharmacology 123, 10-21. https://doi.org/10.1016/j.neuropharm.2017.05.015
  38. Shimohama, S., Chachin, M., Taniguchi, T., Hidaka, H. and Kimura, J. (1996) Changes of neurocalcin, a calcium-binding protein, in the brain of patients with Alzheimer's disease. Brain Res. 716, 233-236. https://doi.org/10.1016/0006-8993(96)00070-4
  39. Solinas, M., Belujon, P., Fernagut, P. O., Jaber, M. and Thiriet, N. J. (2019) Dopamine and addiction: what have we learned from 40 years of research. J. Neural Transm. (Vienna) 126, 481-516. https://doi.org/10.1007/s00702-018-1957-2
  40. Spanagel, R., Pendyala, G., Abarca, C., Zghoul, T., Sanchis-Segura, C., Magnone, M. C.,Lascorz, J., Depner, M., Holzberg, D., Soyka, M., Schreiber, S., Matsuda, F., Lathrop, M., Schumann, G. and Albrecht, U. (2005) The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat. Med. 11, 35-42. https://doi.org/10.1038/nm1163
  41. Upadhyay, A., Hosseinibarkooie, S., Schneider, S., Kaczmarek, A., Torres-Benito, L., Mendoza-Ferreira, N., Overhoff, M., Rombo, R., Grysko, V., Kye, M. J., Kononenko, N. L. and Wirth, B. (2019) Neurocalcin delta knockout impairs adult neurogenesis whereas half reduction is not pathological. Front. Mol. Neurosci. 12, 19. https://doi.org/10.3389/fnmol.2019.00019
  42. Vercauteren, F. G., Flores, G., Ma, W., Chabot, J. G., Geenen, L., Clerens, S., Fazel, A., Bergeron, J. J., Srivastava, L. K., Arckens, L. and Quirion, R. (2007) An organelle proteomic method to study neurotransmission-related proteins, applied to a neurodevelopmental model of schizophrenia. Proteomics 7, 3569-3579. https://doi.org/10.1002/pmic.200700379
  43. Volkow, N. D., Wise, R. A. and Baler, R. J. (2017) The dopamine motive system: implications for drug and food addiction. Nat. Rev. Neurosci. 18, 741-752. https://doi.org/10.1038/nrn.2017.130
  44. Williams, J., Dragunow, M., Lawlor, P., Mason, S., Abraham, W., Leah, J., Bravo,R., Demmer, J. and Tate, W. (1995) Krox20 may play a key role in the stabilization of long-term potentiation. Mol. Brain Res. 28, 87-93. https://doi.org/10.1016/0169-328X(94)00187-J
  45. Wu, L., Zhang, S., Shkhyan, R., Lee, S., Gullo, F., Eliasberg, C. D., Petrigliano, F. A., Ba, K., Wang, J., Lin, Y. J. and Evseenko, D. (2017) Kappa opioid receptor signaling protects cartilage tissue against posttraumatic degeneration. JCI Insight 2, e88553.
  46. Xia, B., Li, Y., Li, R., Yin, D., Chen, X., Li, J. and Liang, W. (2018) Effect of sirtuin-1 on synaptic plasticity in nucleus accumbens in a rat model of heroin addiction. Med. Sci. Monit. 24, 3789-3803. https://doi.org/10.12659/MSM.910550
  47. Xu, H., Wang, Y., Song, N., Wang, J., Jiang, H. and Xie, J. (2018) New progress on the role of glia in iron metabolism and iron-induced degeneration of dopamine neurons in Parkinson's disease. Front. Mol. Neurosci. 10, 455. https://doi.org/10.3389/fnmol.2017.00455
  48. Yamamoto, V. J., Paula, V. d. J. R. d., Forlenza, O. V., Santos, B. D. and Kerr, D. S. (2015) Association study in Alzheimer's disease of single nucleotide polymorphisms implicated with coffee consumption. Arch. Clin. 42, 69-73.
  49. Yamatani, H., Kawasaki, T., Mita, S., Inagaki, N. and Hirata, T. (2010) Proteomics analysis of the temporal changes in axonal proteins during maturation. Dev. Neurobiol. 70, 523-537. https://doi.org/10.1002/dneu.20794
  50. Ye, J., Yang, Z., Li, C., Cai, M., Zhou, D., Zhang, Q., Wei, Y., Wang, T. and Liu, Y. (2014) NF-κB signaling and vesicle transport are correlated with the reactivation of the memory trace of morphine dependence. Diagn. Pathol. 9, 142. https://doi.org/10.1186/1746-1596-9-142
  51. Zhang, X., Cui, Y., Jing, J., Cui, Y., Xin, W. and Liu, X. (2011) Involvement of p38/NF-κB signaling pathway in the nucleus accumbens in the rewarding effects of morphine in rats. Behav. Brain Res. 218, 184-189. https://doi.org/10.1016/j.bbr.2010.11.049