Global Changes in the Rat Heart Proteome Induced by Prolonged Morphine Treatment and Withdrawal

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Drastichova, Zdenka ^a   Skrabalova, Jitka ^a   Jedelsky, Petr ^a   Neckar, Jan ^b   Kolar, Frantisek ^b   Novotny, Jiri ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; CHAPERONIN 60; EARLY PREGNANCY FACTOR; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE P38; MORPHINE; PROTEOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MEMBRANE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CYTOSOL; DRUG WITHDRAWAL; HEART; HEART MITOCHONDRION; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; TREATMENT DURATION; UPREGULATION;

ANIMALS; CHAPERONIN 10; CHAPERONIN 60; CRYSTALLINS; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MALE; MORPHINE; MORPHINE DEPENDENCE; MYOCARDIUM; PROTEOME; RATS; RATS, WISTAR; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84867301015     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047167     Document Type: Article

References (96)

1. Flemming K, (2010) The use of morphine to treat cancer-related pain: a synthesis of quantitative and qualitative research. J Pain Symptom Manage 39: 139-154.
2. Vallejo R, Barkin RL, Wang VC, (2011) Pharmacology of opioids in the treatment of chronic pain syndromes. Pain Physician 14: E343-360.
3. Gregori SD, Gregori MD, Ranzani GN, Allegri M, Minella C, et al. (2012) Morphine metabolism, transport and brain disposition. Metab Brain Dis 27: 1-5.
4. Kieffer BL, Evans CJ, (2009) Opioid receptors: from binding sites to visible molecules in vivo. Neuropharmacology 56Suppl 1: 205-212.
5. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, et al. (1994) Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350: 412-438.
6. Mansour A, Fox CA, Akil H, Watson SJ, (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18: 22-29.
7. Narita M, Funada M, Suzuki T, (2001) Regulations of opioid dependence by opioid receptor types. Pharmacol Ther 89: 1-15.
8. Manchikanti L, Atluri S, Trescot AM, Giordano J, (2008) Monitoring opioid adherence in chronic pain patients: tools, techniques, and utility. Pain Physician 11: S155-180.
9. Wang J, Yuan W, Li MD, (2011) Genes and pathways co-associated with the exposure to multiple drugs of abuse, including alcohol, amphetamine/methamphetamine, cocaine, marijuana, morphine, and/or nicotine: a review of proteomics analyses. Mol Neurobiol 44: 269-286.
10. Gintzler AR, Chakrabarti S, (2006) Post-opioid receptor adaptations to chronic morphine; altered functionality and associations of signaling molecules. Life Sci 79: 717-722.
11. Christie MJ, (2008) Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. Br J Pharmacol 154: 384-396.
12. Nestler EJ, (2004) Molecular mechanisms of drug addiction. Neuropharmacology 47Suppl 1: 24-32.
13. Fan LW, Tien LT, Tanaka S, Ma T, Chudapongse N, et al. (2003) Changes in the brain kappa-opioid receptor levels of rats in withdrawal from physical dependence upon butorphanol. Neuroscience 121: 1063-1074.
14. Murray F, Harrison NJ, Grimwood S, Bristow LJ, Hutson PH, (2007) Nucleus accumbens NMDA receptor subunit expression and function is enhanced in morphine-dependent rats. Eur J Pharmacol 562: 191-197.
15. Chen Y, Jiang Y, Yue W, Zhou Y, Lu L, et al. (2008) Chronic, but not acute morphine treatment, up-regulates alpha-Ca2+/calmodulin dependent protein kinase II gene expression in rat brain. Neurochem Res 33: 2092-2098.
16. Mickiewicz AL, Napier TC, (2011) Repeated exposure to morphine alters surface expression of AMPA receptors in the rat medial prefrontal cortex. Eur J Neurosci 33: 259-265.
17. Hamlin AS, McNally GP, Osborne PB, (2007) Induction of c-Fos and zif268 in the nociceptive amygdala parallel abstinence hyperalgesia in rats briefly exposed to morphine. Neuropharmacology 53: 330-343.
18. Kaplan GB, Leite-Morris KA, Fan W, Young AJ, Guy MD, (2011) Opiate sensitization induces FosB/DeltaFosB expression in prefrontal cortical, striatal and amygdala brain regions. PLoS One 6: e23574.
19. Boronat MA, Garcia-Fuster MJ, Garcia-Sevilla JA, (2001) Chronic morphine induces up-regulation of the pro-apoptotic Fas receptor and down-regulation of the anti-apoptotic Bcl-2 oncoprotein in rat brain. Br J Pharmacol 134: 1263-1270.
20. Emeterio EP, Tramullas M, Hurle MA, (2006) Modulation of apoptosis in the mouse brain after morphine treatments and morphine withdrawal. J Neurosci Res 83: 1352-1361.
21. Marie-Claire C, Courtin C, Roques BP, Noble F, (2004) Cytoskeletal genes regulation by chronic morphine treatment in rat striatum. Neuropsychopharmacology 29: 2208-2215.
22. Ammon-Treiber S, Hollt V, (2005) Morphine-induced changes of gene expression in the brain. Addict Biol 10: 81-89.
23. Prokai L, Zharikova AD, Stevens SM Jr, (2005) Effect of chronic morphine exposure on the synaptic plasma-membrane subproteome of rats: a quantitative protein profiling study based on isotope-coded affinity tags and liquid chromatography/mass spectrometry. J Mass Spectrom 40: 169-175.
24. Bierczynska-Krzysik A, Bonar E, Drabik A, Noga M, Suder P, et al. (2006) Rat brain proteome in morphine dependence. Neurochem Int 49: 401-406.
25. Bierczynska-Krzysik A, Pradeep John JP, Silberring J, Kotlinska J, Dylag T, et al. (2006) Proteomic analysis of rat cerebral cortex, hippocampus and striatum after exposure to morphine. Int J Mol Med 18: 775-784.
26. Li KW, Jimenez CR, van der Schors RC, Hornshaw MP, Schoffelmeer AN, et al. (2006) Intermittent administration of morphine alters protein expression in rat nucleus accumbens. Proteomics 6: 2003-2008.
27. Moron JA, Abul-Husn NS, Rozenfeld R, Dolios G, Wang R, et al. (2007) Morphine administration alters the profile of hippocampal postsynaptic density-associated proteins: a proteomics study focusing on endocytic proteins. Mol Cell Proteomics 6: 29-42.
28. Yang L, Sun ZS, Zhu YP, (2007) Proteomic analysis of rat prefrontal cortex in three phases of morphine-induced conditioned place preference. J Proteome Res 6: 2239-2247.
29. Bodzon-Kulakowska A, Suder P, Mak P, Bierczynska-Krzysik A, Lubec G, et al. (2009) Proteomic analysis of striatal neuronal cell cultures after morphine administration. J Sep Sci 32: 1200-1210.
30. Abul-Husn NS, Annangudi SP, Ma'ayan A, Ramos-Ortolaza DL, Stockton SD Jr, et al. (2011) Chronic morphine alters the presynaptic protein profile: identification of novel molecular targets using proteomics and network analysis. PLoS One 6: e25535.
31. Bu Q, Yang Y, Yan G, Hu Z, Hu C, et al. (2012) Proteomic analysis of the nucleus accumbens in rhesus monkeys of morphine dependence and withdrawal intervention. J Proteomics 75: 1330-1342.
32. Neasta J, Uttenweiler-Joseph S, Chaoui K, Monsarrat B, Meunier JC, et al. (2006) Effect of long-term exposure of SH-SY5Y cells to morphine: a whole cell proteomic analysis. Proteome Sci 4: 23.
33. Xu H, Wang X, Zimmerman D, Boja ES, Wang J, et al. (2005) Chronic morphine up-regulates G alpha12 and cytoskeletal proteins in Chinese hamster ovary cells expressing the cloned mu opioid receptor. J Pharmacol Exp Ther 315: 248-255.
34. Suder P, Bodzon-Kulakowska A, Mak P, Bierczynska-Krzysik A, Daszykowski M, et al. (2009) The proteomic analysis of primary cortical astrocyte cell culture after morphine administration. J Proteome Res 8: 4633-4640.
35. Shanazari AA, Aslani Z, Ramshini E, Alaei H, (2011) Acute and chronic effects of morphine on cardiovascular system and the baroreflexes sensitivity during severe increase in blood pressure in rats. ARYA Atheroscler 7: 111-117.
36. Pang PS, Komajda M, Gheorghiade M, (2010) The current and future management of acute heart failure syndromes. Eur Heart J 31: 784-793.
37. Murphy GS, Szokol JW, Marymont JH, Avram MJ, Vender JS, (2006) Opioids and cardioprotection: the impact of morphine and fentanyl on recovery of ventricular function after cardiopulmonary bypass. J Cardiothorac Vasc Anesth 20: 493-502.
38. Li R, Wong GT, Wong TM, Zhang Y, Xia Z, et al. (2009) Intrathecal morphine preconditioning induces cardioprotection via activation of delta, kappa, and mu opioid receptors in rats. Anesth Analg 108: 23-29.
39. Peart JN, Hoe LE, Gross GJ, Headrick JP, (2011) Sustained ligand-activated preconditioning via delta-opioid receptors. J Pharmacol Exp Ther 336: 274-281.
40. Skrabalova J, Neckar J, Hejnova L, Bartonova I, Kolar F, et al. (2012) Antiarrhythmic effect of prolonged morphine exposure is accompanied by altered myocardial adenylyl cyclase signaling in rats. Pharmacol Rep 64: 351-359.
41. Drastichova Z, Skrabalova J, Neckar J, Kolar F, Novotny J, (2011) Prolonged morphine administration alters protein expression in the rat myocardium. J Biomed Sci 18: 89.
42. Yan W, Chen SS, (2005) Mass spectrometry-based quantitative proteomic profiling. Brief Funct Genomic Proteomic 4: 27-38.
43. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169.
44. Wu WW, Wang G, Baek SJ, Shen RF, (2006) Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J Proteome Res 5: 651-658.
45. Shadforth IP, Dunkley TP, Lilley KS, Bessant C, (2005) i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics 6: 145.
46. Ernoult E, Gamelin E, Guette C, (2008) Improved proteome coverage by using iTRAQ labelling and peptide OFFGEL fractionation. Proteome Sci 6: 27.
47. Polisetty RV, Gautam P, Sharma R, Harsha HC, Nair SC, et al. (2012) LC-MS/MS analysis of differentially expressed glioblastoma membrane proteome reveals altered calcium signaling and other protein groups of regulatory functions. Mol Cell Proteomics 11: M111 013565.
48. Molloy MP, (2000) Two-dimensional electrophoresis of membrane proteins using immobilized pH gradients. Anal Biochem 280: 1-10.
49. Rabilloud T, (2009) Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 30Suppl 1: S174-180.
50. Chung JH, Choi HJ, Kim SY, Hong KS, Min SK, et al. (2011) Proteomic and biochemical analyses reveal the activation of unfolded protein response, ERK-1/2 and ribosomal protein S6 signaling in experimental autoimmune myocarditis rat model. BMC Genomics 12: 520.
51. Huang QY, Fang CW, Huang HQ, (2011) Alteration of heart tissue protein profiles in acute cadmium-treated scallops Patinopecten yessoensis. Arch Environ Contam Toxicol 60: 90-98.
52. Seabra MC, Wasmeier C, (2004) Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 16: 451-457.
53. Shisheva A, Chinni SR, DeMarco C, (1999) General role of GDP dissociation inhibitor 2 in membrane release of Rab proteins: modulations of its functional interactions by in vitro and in vivo structural modifications. Biochemistry 38: 11711-11721.
54. Quest AF, Leyton L, Parraga M, (2004) Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease. Biochem Cell Biol 82: 129-144.
55. Rebecchi MJ, Pentyala SN, (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev. 80: 1291-1335.
56. Sidhu RS, Clough RR, Bhullar RP, (2005) Regulation of phospholipase C-delta1 through direct interactions with the small GTPase Ral and calmodulin. J Biol Chem 280: 21933-21941.
57. Baek KJ, Kang S, Damron D, Im M, (2001) Phospholipase Cdelta1 is a guanine nucleotide exchanging factor for transglutaminase II (Galpha h) and promotes alpha 1B-adrenoreceptor-mediated GTP binding and intracellular calcium release. J Biol Chem 276: 5591-5597.
58. Yagisawa H, (2006) Nucleocytoplasmic shuttling of phospholipase C-delta1: a link to Ca2+. J Cell Biochem 97: 233-243.
59. Hodson EA, Ashley CC, Hughes AD, Lymn JS, (1998) Regulation of phospholipase C-delta by GTP-binding proteins-rhoA as an inhibitory modulator. Biochim Biophys Acta 1403: 97-101.
60. Allen V, Swigart P, Cheung R, Cockcroft S, Katan M, (1997) Regulation of inositol lipid-specific phospholipase cdelta by changes in Ca2+ ion concentrations. Biochem J 327 (Pt 2): 545-552.
61. Lien YC, Noel T, Liu H, Stromberg AJ, Chen KC, et al. (2006) Phospholipase C-delta1 is a critical target for tumor necrosis factor receptor-mediated protection against adriamycin-induced cardiac injury. Cancer Res 66: 4329-4338.
62. Quillan JM, Carlson KW, Song C, Wang D, Sadee W, (2002) Differential effects of mu-opioid receptor ligands on Ca(2+) signaling. J Pharmacol Exp Ther 302: 1002-1012.
63. Chakrabarti S, Liu NJ, Gintzler AR, (2003) Reciprocal modulation of phospholipase Cbeta isoforms: adaptation to chronic morphine. Proc Natl Acad Sci U S A 100: 13686-13691.
64. Barrere-Lemaire S, Combes N, Sportouch-Dukhan C, Richard S, Nargeot J, et al. (2005) Morphine mimics the antiapoptotic effect of preconditioning via an Ins(1,4,5)P3 signaling pathway in rat ventricular myocytes. Am J Physiol Heart Circ Physiol 288: H83-88.
65. Bhat RS, Bhaskaran M, Mongia A, Hitosugi N, Singhal PC, (2004) Morphine-induced macrophage apoptosis: oxidative stress and strategies for modulation. J Leukoc Biol 75: 1131-1138.
66. Singhal PC, Bhaskaran M, Patel J, Patel K, Kasinath BS, et al. (2002) Role of p38 mitogen-activated protein kinase phosphorylation and Fas-Fas ligand interaction in morphine-induced macrophage apoptosis. J Immunol 168: 4025-4033.
67. Lin X, Wang YJ, Li Q, Hou YY, Hong MH, et al. (2009) Chronic high-dose morphine treatment promotes SH-SY5Y cell apoptosis via c-Jun N-terminal kinase-mediated activation of mitochondria-dependent pathway. FEBS J 276: 2022-2036.
68. Mao J, Sung B, Ji RR, Lim G, (2002) Neuronal apoptosis associated with morphine tolerance: evidence for an opioid-induced neurotoxic mechanism. J Neurosci 22: 7650-7661.
69. Hu S, Sheng WS, Lokensgard JR, Peterson PK, (2002) Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 42: 829-836.
70. Ohara T, Itoh T, Takahashi M (2005) Immunosuppression by morphine-induced lymphocyte apoptosis: is it a real issue? Anesth Analg 101: 1117-1122, table of contents.
71. Kim MS, Cheong YP, So HS, Lee KM, Kim TY, et al. (2001) Protective effects of morphine in peroxynitrite-induced apoptosis of primary rat neonatal astrocytes: potential involvement of G protein and phosphatidylinositol 3-kinase (PI3 kinase). Biochem Pharmacol 61: 779-786.
72. Chen Y, Sun R, Han W, Zhang Y, Song Q, et al. (2001) Nuclear translocation of PDCD5 (TFAR19): an early signal for apoptosis? FEBS Lett 509: 191-196.
73. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, et al. (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126: 177-189.
74. Chen L, Gong Q, Stice JP, Knowlton AA, (2009) Mitochondrial OPA1, apoptosis, and heart failure. Cardiovasc Res 84: 91-99.
75. John GB, Shang Y, Li L, Renken C, Mannella CA, et al. (2005) The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol Biol Cell 16: 1543-1554.
76. Gill C, Mestril R, Samali A, (2002) Losing heart: the role of apoptosis in heart disease-a novel therapeutic target? FASEB J 16: 135-146.
77. Wu HY, Lynch DR, (2006) Calpain and synaptic function. Mol Neurobiol 33: 215-236.
78. Chan SL, Mattson MP, (1999) Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 58: 167-190.
79. Goll DE, Thompson VF, Li H, Wei W, Cong J, (2003) The calpain system. Physiol Rev 83: 731-801.
80. Lin KM, Lin B, Lian IY, Mestril R, Scheffler IE, et al. (2001) Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation 103: 1787-1792.
81. Lau S, Patnaik N, Sayen MR, Mestril R, (1997) Simultaneous overexpression of two stress proteins in rat cardiomyocytes and myogenic cells confers protection against ischemia-induced injury. Circulation 96: 2287-2294.
82. Kirchhoff SR, Gupta S, Knowlton AA, (2002) Cytosolic heat shock protein 60, apoptosis, and myocardial injury. Circulation 105: 2899-2904.
83. Gray CC, Amrani M, Yacoub MH, (1999) Heat stress proteins and myocardial protection: experimental model or potential clinical tool? Int J Biochem Cell Biol 31: 559-573.
84. Martin JL, Mestril R, Hilal-Dandan R, Brunton LL, Dillmann WH, (1997) Small heat shock proteins and protection against ischemic injury in cardiac myocytes. Circulation 96: 4343-4348.
85. Ray PS, Martin JL, Swanson EA, Otani H, Dillmann WH, et al. (2001) Transgene overexpression of alphaB crystallin confers simultaneous protection against cardiomyocyte apoptosis and necrosis during myocardial ischemia and reperfusion. FASEB J 15: 393-402.
86. Dokas LA, Malone AM, Williams FE, Nauli SM, Messer WS Jr, (2011) Multiple protein kinases determine the phosphorylated state of the small heat shock protein, HSP27, in SH-SY5Y neuroblastoma cells. Neuropharmacology 61: 12-24.
87. Hoover HE, Thuerauf DJ, Martindale JJ, Glembotski CC, (2000) alpha B-crystallin gene induction and phosphorylation by MKK6-activated p38. A potential role for alpha B-crystallin as a target of the p38 branch of the cardiac stress response. J Biol Chem 275: 23825-23833.
88. Bitar KN, (2002) HSP27 phosphorylation and interaction with actin-myosin in smooth muscle contraction. Am J Physiol Gastrointest Liver Physiol 282: G894-903.
89. Almela P, Martinez-Laorden E, Atucha NM, Milanes MV, Laorden ML, (2011) Naloxone-precipitated morphine withdrawal evokes phosphorylation of heat shock protein 27 in rat heart through extracellular signal-regulated kinase. J Mol Cell Cardiol 51: 129-139.
90. Martinez-Laorden E, Hurle MA, Milanes MV, Laorden ML, Almela P (2012) Morphine withdrawal activates hypothalamic-pituitary adrenal axis and heat shock protein 27 in the left ventricle: Role of extracellular signal-regulated kinase. J Pharmacol Exp Ther.
91. Lambert H, Charette SJ, Bernier AF, Guimond A, Landry J, (1999) HSP27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus. J Biol Chem 274: 9378-9385.
92. Benndorf R, Hayess K, Ryazantsev S, Wieske M, Behlke J, et al. (1994) Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. J Biol Chem 269: 20780-20784.
93. Robinson AA, Dunn MJ, McCormack A, dos Remedios C, Rose ML, (2010) Protective effect of phosphorylated Hsp27 in coronary arteries through actin stabilization. J Mol Cell Cardiol 49: 370-379.
94. Shimura H, Miura-Shimura Y, Kosik KS, (2004) Binding of tau to heat shock protein 27 leads to decreased concentration of hyperphosphorylated tau and enhanced cell survival. J Biol Chem 279: 17957-17962.
95. Sahara N, Maeda S, Yoshiike Y, Mizoroki T, Yamashita S, et al. (2007) Molecular chaperone-mediated tau protein metabolism counteracts the formation of granular tau oligomers in human brain. J Neurosci Res 85: 3098-3108.
96. Bjorkdahl C, Sjogren MJ, Zhou X, Concha H, Avila J, et al. (2008) Small heat shock proteins Hsp27 or alphaB-crystallin and the protein components of neurofibrillary tangles: tau and neurofilaments. J Neurosci Res 86: 1343-1352.