Brain apoptosis signaling pathways are regulated by methylphenidate treatment in young and adult rats

Brain Research

Volumn 1583, Issue 1, 2014, Pages 269-276

  Réus, Gislaine Z ^a   Scaini, Giselli ^a   Jeremias, Gabriela C ^a   Furlanetto, Camila B ^a   Morais, Meline O S ^a   Mello Santos, Lis Maira ^a   Quevedo, João ^a,b   Streck, Emilio L ^a  

^a UNIVERSIDADE DO EXTREMO SUL CATARINENSE   (Brazil)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Bax; Bcl 2; Caspase 3; Cytochrome c; Methylphenidate

Indexed keywords

CASPASE 3; CYTOCHROME C; METHYLPHENIDATE; PROTEIN BAX; PROTEIN BCL 2; BAX PROTEIN, RAT; CASP3 PROTEIN, RAT; CENTRAL STIMULANT AGENT; NEUROPROTECTIVE AGENT;

ADULT; APOPTOSIS; ARTICLE; CEREBELLUM; CORPUS STRIATUM; DOSE RESPONSE; DRUG EFFECT; HIPPOCAMPUS; LONG TERM CARE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; YOUNG ADULT; ANIMAL; BRAIN; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; PHYSIOLOGY; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BRAIN; CASPASE 3; CENTRAL NERVOUS SYSTEM STIMULANTS; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; IMMUNOBLOTTING; METHYLPHENIDATE; NEUROPROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 84922553486     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.08.010     Document Type: Article

References (58)

1. Andersen, S.L., Arvanitogiannis, A., Pliakas, A.M., LeBlanc, C., Carlezon Jr., W.A., 2002. Altered responsiveness to cocaine in rats exposed to methylphenidate during development. Nat. Neurosci. 5, 13-14.
2. Baird, A.L., Coogan, A.N., Kaufling, J., Barrot, M., Thome, J., 2013. Daily methylphenidate and atomoxetine treatment impacts on clock gene protein expression in the mouse brain. Brain Res. 1513, 61-71.
3. Berman, S.B., Hastings, T.G., 1999. Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson's disease. J. Neurochem. 73, 1127-1137.
4. Berridge, C.W., Devilbiss, D.M., Andrzejewski, M.E., Arnsten, A.F. T., Kelley, A.E., Schmeichel, B., Hamilton, C.M., Spencer, R.C., 2006. Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function. Biol. Psychiatry. 60, 1111-1120.
5. Biederman, J., Wilens, T., Mick, E., Spencer, T., Faraone, S.V., 1999. Pharmacotherapy of attention-deficit/hyperactivity disorder reduces risk for substance use disorder. Pediatrics 104, e20.
6. Cabezas, R., El-Bacha, R.S., Gonzalez, J., Barreto, G.E., 2012. Mitochondrial functions in astrocytes: neuroprotective implications from oxidative damage by rotenone. Neurosci. Res. 74, 80-90.
7. Carboni, E., Silvagni, A., Valentini, V., Di Chiara, G., 2003. Effect of amphetamine, cocaine and depolarization by high potassium on extracellular dopamine in the nucleus accumbens shell of SHR rat. An in vivo microdyalisis study. Neurosci. Biobehav. Rev. 27, 653-659.
8. Carlezon Jr., W.A., Mague, S.D., Andersen, S.L., 2003. Enduring behavioral effects of early exposure to methylphenidate in rats. Biol. Psychiatry 54, 1330-1337.
9. Challman, T.D., Lipsky, J.J., 2000. Methylphenidate: Its pharmacology and uses. Mayo Clin. Proc. 75, 711-721.
10. Cory, S., Huang, D.C., Adams, J.M., 2003. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22, 8590-8607.
11. Cui, S., Sun, Y., Liu, C., 2012. Effect of bushenyisui formula on brain tissue apoptosis and Bcl-2 in beta-amyloid protein- induced Alzheimer's disease rat models. J. Tradit. Chin. Med. 32, 646-650.
12. dela Peña, I., Kim, H.J., Sohn, A., Ryu, J.H., Shin, C.Y., Noh, M., Cheong, J.H., 2014. Prefrontal cortical and striatal transcriptional responses to the reinforcing effect of repeated methylphenidatetreatment in the spontaneously hypertensive rat, animal model of attention-deficit/hyperactivity disorder (ADHD). Behav. Brain Funct. 10, 17.
13. Drye, L.T., Scherer, R.W., Lanctôt, K.L., Rosenberg, P.B., Herrmann, N., Bachman, D., Mintzer, J.E., 2013. Designing a trial to evaluate potential treatments for apathy in dementia: The apathy in dementia methylphenidate trial (ADMET). Am. J. Geriatr. Psychiatry 21, 549-559.
14. Dygalo, N.N., Kalinina, T.S., Bulygina, V.V., Shishkina, G.T., 2012. Increased expression of the anti-apoptotic protein Bcl-xL in the brain is associated with resilience to stress-induced depression-like behavior. Cell. Mol. Neurobiol. 32, 767-776.
15. Eyo, U.B., Dailey, M.E., 2013. Microglia: key elements in neural development, plasticity, and pathology. J. Neuroimmune Pharmacol. 8, 494-509.
16. Fagundes, A.O., Rezin, G.T., Zanette, F., Grandi, E., Assis, L.C., Dal- Pizzol, F., Quevedo, J., Streck, E.L., 2007. Chronic administration of methylphenidate activates mitochondrial respiratory chain in brain of young rats. Int. J. Dev. Neurosci. 25, 47-51.
17. Gerasimov, M.R., Franceschi, M., Volkow, N.D., Rice, O., Schiffer, W.K., Dewey, S.L., 2000. Synergistic interactions between nicotine and cocaine or methylphenidate depend on the dose of dopamine transporter inhibitor. Synapse 38, 432-437.
18. Gomes, K.M., Inácio, C.G., Valvassori, S.S., Reus, G.Z., Boeck, C.R., Dal-Pizzol, F., Quevedo, J., 2009. Superoxide production after acute and chronic treatment with methylphenidate in young and adult rats. Neurosci. Lett. 465, 95-98.
19. Gomes, K.M., Comim, C.M., Valvassori, S.S., Reus, G.Z., Inácio, C.I., Martins, M.R., Souza, R.P., Quevedo, J., 2010. Diurnal differences in memory and learning in young and adult rats treated with methylphenidate. J. Neural Transm. 117, 457-462.
20. Gomes, K.M., Souza, T.P., Inácio, C.I., Valvassori, S.S., Reus, G.Z., Martins, M.R., Comim, C.M., Quevedo, J., 2011. Evaluation of light/dark cycle in anxiety- And depressive-like behaviors after regular treatment with methylphenidate hydrochloride in rats of different ages. Rev. Bras. Psiquiatr. 33, 55-58.
21. Guerdjikova, A.I., McElroy, S.L., 2013. Adjunctive methylphenidate in the treatment of bulimia nervosa co-occurring with bipolar disorder and substance dependence. Innov. Clin. Neurosci. 10, 30-33.
22. Hu, S.Q., Cui, W., Xu, D.P., Mak, S.H., Tang, J., Choi, C.L., Pang, Y.P., Han, Y.F., 2013. Substantial neuroprotection against K+ deprivation-induced apoptosis in primary cerebellar granule neurons by novel dimer bis(propyl)-cognitin via the activation of VEGFR-2 signaling pathway. CNS Neurosci. Ther. 19, 764-772.
23. Husson, I., Mesples, B., Medja, F., Leroux, P., Kosofsky, B., Gressens, P., 2004. Methylphenidate and MK-801, an n-methyl- D-aspartate receptor antagonist: shared biological properties. Neuroscience 125, 163-170.
24. Hyman, B.T., Yuan, J., 2012. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat. Rev. Neurosci. 13, 395-406.
25. Jiao, S., Li, Z., 2011. Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 70, 758-772.
26. Kaushal, N., Matsumoto, R.R., 2011. Role of sigma receptors in methamphetamine-induced neurotoxicity. Curr. Neuropharmacol. 9, 54-57.
27. Kuczenski, R., Segal, D.S., 1997. Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J. Neurochem. 68, 2032-2037.
28. Lakhani, S.A., Masud, A., Kuida, K., Porter Jr., G.A., Booth, C.J., Mehal, W.Z., Inayat, I., Flavell, R.A., 2006. Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311, 847-851.
29. Leonard, B., Maes, M., 2012. Mechanistic explanations how cell- mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci. Biobehav. Rev. 36, 764-785.
30. Li, Q., Lu, G., Antonio, G.E., Mak, Y.T., Rudd, J.A., Fan, M., Yew, D.T., 2007. The usefulness of the spontaneously hypertensive rat to model attention-deficit/disorder (ADHD) may be explained by the differential expression of dopamine-related genes in the brain. Neurochem. Int. 50, 848-857.
31. Li, Z., Jo, J., Jia, J.M., Lo, S.C., Whitcomb, D.J., Jiao, S., Cho, K., Sheng, M., 2010. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141, 859-871.
32. Lindsten, T., Zong, W.X., Thompson, C.B., 2005. Defining the role of the Bcl-2 family of proteins in the nervous system. Neuroscientist 11, 10-15.
33. Ma, J., Wan, J., Meng, J., Banerjee, S., Ramakrishnan, S., Roy, S., 2014. Methamphetamine induces autophagy as a pro-survival response against apoptotic endothelial cell death through the Kappa opioid receptor. Cell Death Dis. 5, e1099.
34. Madras, B.K., Miller, G.M., Fischman, A.J., 2005. The dopamine transporterandattention-deficit/hyperactivity disorder. Biol. Psychiatry 57, 1397-1409.
35. Marazziti, D., Baroni, S., Picchetti, M., Landi, P., Silvestri, S., Vatteroni, E., Catena Dell'Osso, M., 2012. Psychiatric disorders and mitochondrial dysfunctions. Eur. Rev. Med. Pharmacol. Sci. 16, 270-275.
36. Martinou, J.C., Dubois-Dauphin, M., Staple, J.K., Rodriguez, I., Frankowski, H., Missotten, M., Albertini, P., Talabot, D., Catsicas, S., Pietra, C., 1994. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13, 1017-1030.
37. Martins, M.R., Reinke, A., Petronilho, F.C., Gomes, K.M., Dal- Pizzol, F., Quevedo, J., 2006. Methylphenidate treatment induces oxidative stress in young rat brain. Brain Res. 1078, 189-197.
38. Page, G., Peeters, M., Najimi, M., Maloteaux, J.M., Hermans, E., 2001. Modulation of the neuronal dopamine transporter activity by the metabotropic glutamate receptor mGluR5 in rat striatal synaptosomes through phosphorylation mediated processes. J. Neurochem. 76, 1282-1290.
39. Paxinos, G., Watson, C., 1986. The Rat Brain: Stereotaxic Coordinates, second ed. Academic Press, Australia.
40. Reus, G.Z., Scaini, G., Furlanetto, C.B., Morais, M.O., Jeremias, I.C., Mello-Santos, L.M., Freitas, K.V., Quevedo, J., Streck, E.L., 2013. Methylphenidate treatment leads to abnormalities on krebs cycle enzymes in the brain of young and adult rats. Neurotoxic. Res. 24, 251-257.
41. Rosenthal, R.E., Hamud, F., Fiskum, G., Varghese, P.J., Sharpe, S., 1987. Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine. J. Cereb. Blood Flow Metab. 7, 752-758.
42. Rowland, S.A., Lesesne, C.A., Abramowitz, A.J., 2002. The epidemiology of attention deficit/hyperactivity disorder (ADHD): A public health view. Ment. Retard. Dev. Disabil. Res. Rev. 8, 162-170.
43. Sadasivan, S., Pond, B.B., Pani, A.K., Qu, C., Jiao, Y., Smeyne, R.J., 2012. Methylphenidate exposure induces dopamine neuron loss and activation of microglia in the basal ganglia of mice. PLoS One 7, e33693.
44. Saelens, X., Festjens, N., Vande Walle, L., van Gurp, M., van Loo, G., Vandenabeele, P., 2004. Toxic proteins released from mitochondria in cell death. Oncogene 23, 2861-2874.
45. Scaini, G., Fagundes, A.O., Rezin, G.T., Gomes, K.M., Zugno, A.I., Quevedo, J., Streck, E.L., 2008. Methylphenidate increases creatine kinase activity in the brain of young and adult rats. Life Sci. 83, 795-800.
46. Schmitz, F., Scherer, E.B., Machado, F.R., da Cunha, A.A., Tagliari, B., Netto, C.A., Wyse, A.T., 2012. Methylphenidate induces lipid and protein damage in prefrontal cortex, but not in cerebellum, striatum and hippocampus of juvenile rats. Metab. Brain Dis. 27, 605-612.
47. Souza, R.P., Soares, E.C., Rosa, D.V.F., Souza, B.R., Reus, G.Z., Barichello, T., Gomes, K.M., Gomez, M.V., Quevedo, J., Romano- Silva, M.A., 2008. Methylphenidate alters NCS-1 expression in rat brain. Neurochem. Int. 53, 12-16.
48. Suzuki, T., Shindo, K., Miyatake, M., Kurokawa, K., Higashiyama, K., Suzuki, M., Narita, M., 2007. Lack of development of behavioral sensitization to methylphenidate in mice: correlation with reversible astrocytic activation. Eur. J. Pharmacol. 574, 39-48.
49. Swanson, J., Volkow, N., 2006. Pharmacokinetic and pharmacodynamic properties of methylphenidate in humans. In: Solanto, M.V., Arnsten, A.F.T., Castellanos, F.X. (Eds.), Stimulant Drugs and ADHD: Basic and Clinical Neuroscience. Oxford University Press, New York, pp. 259-282.
50. Takuma, K., Baba, A., Matsuda, T., 2004. Astrocyte apoptosis: implication for neuroprotection. Prog. Neurobiol. 72, 111-127.
51. Tekpli, X., Holme, J.A., Sergent, A., Lagadic-Gossmann, D., 2013. Role for membrane remodeling in cell death: implication for health and disease. Toxicology 304, 141-157.
52. Torres-Reverón, A., Dow-Edwards, D.L., 2005. Repeated administration of methylphenidate in young, adolescent, and mature rats affects the response to cocaine later in adulthood. Psychopharmacology 181, 38-47.
53. Urban, K.R., Li, Y., Gao, W., 2013. Treatment with a clinically- relevant dose of methylphenidate alters NMDA receptor composition and synaptic plasticity in the juvenile rat prefrontal cortex. Neurobiol. Learn. Mem. 101, 65-74.
54. Virmani, A., Gaetani, F., Imam, S., Binienda, Z., Ali, S., 2002. The protective role of L-carnitine against neurotoxicity evoked by drug of abuse, methamphetamine, could be related to mitochondrial dysfunction. Ann. N. Y. Acad. Sci. 965, 225-232.
55. Volkow, N.D., Fowler, J.S., Wang, G., Ding, Y., Gatley, S.J., 2002. Mechanism of action of methylphenidate: insights from PET imaging studies. J. Atten. Disord. 6, 31-43.
56. Widlak, P., Garrard, W.T., 2005. Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. J. Cell. Biochem. 94, 1078-1087.
57. Yuan, J., 2009. Neuroprotective strategies targeting apoptotic and necrotic cell death for stroke. Apoptosis 14, 469-477.
58. Zhang, C.L., Feng, Z.J., Liu, Y., Ji, X.H., Peng, J.Y., Zhang, X.H., Zhen, X.C., Li, B.M., 2012. Methylphenidate enhances NMDA- receptor response in medial prefrontal cortex via sigma-1 receptor: A novel mechanism for methylphenidate action. PLoS One 7, 51910.