Elevated Expression of HSP72 in the Prefrontal Cortex and Hippocampus of Rats Subjected to Chronic Mild Stress and Treated with Imipramine
Abstract
:1. Introduction
2. Results
2.1. Evaluation of Sucrose Consumption in Stress-Reactive vs. Stress-Nonreactive Animals and in Imipramine-Responding vs. Imipramine-Nonresponding Animals: Generating Experimental Groups for Biochemical Studies
2.2. Effects of Three Weeks of CMS on the mRNA Expression of HSP70 and HSP90 Family Members
2.3. Effects of Eight Weeks of CMS on the mRNA Expression of HSP70 Family Members
2.4. Effects of Eight Weeks of CMS on the mRNA Expression of HSP90 Family Members
2.5. Effects of Eight Weeks of CMS on the Cytosolic Protein Expression of HSPs
2.6. HSP72 and HSP90B Colocalize with Neuronal Cells
3. Discussion
3.1. Applicability of Experimental Groups Generated in the CMS Model
3.2. Evaluation of the Effects of CMS and IMI Therapy on the Cerebral Expression of HSP
3.2.1. HSPA Family
3.2.2. HSPC Family
3.2.3. HSP as a Potential Target for Antidepressive Treatment
3.3. Localization and Dynamics of CMS-Induced Changes in HSP Expression
4. Materials and Methods
4.1. Animals
4.2. Sucrose Consumption Test
4.3. Chronic Mild Stress Protocol
4.3.1. Stress-Reactive and -Nonreactive Animals
4.3.2. Imipramine-Responding and -Nonresponding Animals
4.4. Drug Administration
4.5. Tissue Preparation
4.6. Real-Time Analysis of HSP mRNA Levels
4.7. Immunoblot Analysis of HSP72 and HSP90B Protein Levels
4.8. Immunofluorescence Analysis
4.9. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ritossa, F. Discovery of the Heat Shock Response. Cell Stress Chaperones 1996, 1, 97–98. [Google Scholar] [CrossRef] [PubMed]
- Hartl, F.U.; Bracher, A.; Hayer-Hartl, M. Molecular Chaperones in Protein Folding and Proteostasis. Nature 2011, 475, 324–332. [Google Scholar] [CrossRef] [PubMed]
- Kampinga, H.H.; Hageman, J.; Vos, M.J.; Kubota, H.; Tanguay, R.M.; Bruford, E.A.; Cheetham, M.E.; Chen, B.; Hightower, L.E. Guidelines for the Nomenclature of the Human Heat Shock Proteins. Cell Stress Chaperones 2009, 14, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Stetler, R.A.; Gan, Y.; Zhang, W.; Liou, A.K.; Gao, Y.; Cao, G.; Chen, J. Heat Shock Proteins: Cellular and Molecular Mechanisms in the Central Nervous System. Prog. Neurobiol. 2010, 92, 184–211. [Google Scholar] [CrossRef] [PubMed]
- Lu, A.; Ran, R.; Parmentier-Batteur, S.; Nee, A.; Sharp, F.R. Geldanamycin Induces Heat Shock Proteins in Brain and Protects against Focal Cerebral Ischemia. J. Neurochem. 2002, 81, 355–364. [Google Scholar] [CrossRef] [PubMed]
- Hoter, A.; El-Sabban, M.E.; Naim, H.Y. The HSP90 Family: Structure, Regulation, Function, and Implications in Health and Disease. Int. J. Mol. Sci. 2018, 19, 2560. [Google Scholar] [CrossRef]
- Wandinger, S.K.; Richter, K.; Buchner, J. The Hsp90 Chaperone Machinery. J. Biol. Chem. 2008, 283, 18473–18477. [Google Scholar] [CrossRef]
- Chaudhuri, T.K.; Paul, S. Protein-Misfolding Diseases and Chaperone-Based Therapeutic Approaches. FEBS J. 2006, 273, 1331–1349. [Google Scholar] [CrossRef]
- Bei, E.S.; Salpeas, V.; Alevizos, B.; Anagnostara, C.; Pappa, D.; Moutsatsou, P. Pattern of Heat Shock Factor and Heat Shock Protein Expression in Lymphocytes of Bipolar Patients: Increased HSP70-Glucocorticoid Receptor Heterocomplex. J. Psychiatr. Res. 2013, 47, 1725–1736. [Google Scholar] [CrossRef]
- Mosser, D.D.; Caron, A.W.; Bourget, L.; Denis-Larose, C.; Massie, B. Role of the Human Heat Shock Protein Hsp70 in Protection against Stress-Induced Apoptosis. Mol. Cell. Biol. 1997, 17, 5317–5327. [Google Scholar] [CrossRef]
- Tsuchiya, D.; Hong, S.; Matsumori, Y.; Kayama, T.; Swanson, R.A.; Dillman, W.H.; Liu, J.; Panter, S.S.; Weinstein, P.R. Overexpression of Rat Heat Shock Protein 70 Reduces Neuronal Injury after Transient Focal Ischemia, Transient Global Ischemia, or Kainic Acid-Induced Seizures. Neurosurgery 2003, 53, 1179. [Google Scholar] [CrossRef] [PubMed]
- Matsumori, Y.; Northington, F.J.; Hong, S.M.; Kayama, T.; Sheldon, R.A.; Vexler, Z.S.; Ferriero, D.M.; Weinstein, P.R.; Liu, J. Reduction of Caspase-8 and -9 Cleavage Is Associated With Increased c-FLIP and Increased Binding of Apaf-1 and Hsp70 After Neonatal Hypoxic/Ischemic Injury in Mice Overexpressing Hsp70. Stroke 2006, 37, 507–512. [Google Scholar] [CrossRef] [PubMed]
- Klucken, J.; Shin, Y.; Masliah, E.; Hyman, B.T.; McLean, P.J. Hsp70 Reduces α-Synuclein Aggregation and Toxicity. J. Biol. Chem. 2004, 279, 25497–25502. [Google Scholar] [CrossRef] [PubMed]
- Birbo, B.; Madu, E.E.; Madu, C.O.; Jain, A.; Lu, Y. Role of HSP90 in Cancer. Int. J. Mol. Sci. 2021, 22, 10317. [Google Scholar] [CrossRef] [PubMed]
- Coccurello, R.; Bielawski, A.; Zelek-Molik, A.; Vetulani, J.; Kowalska, M.; D’Amato, F.R.; Nalepa, I. Brief Maternal Separation Affects Brain Alpha1-Adrenoceptors and Apoptotic Signaling in Adult Mice. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2014, 48, 161–169. [Google Scholar] [CrossRef] [PubMed]
- Heshmati, M.; Russo, S.J. Anhedonia and the Brain Reward Circuitry in Depression. Curr. Behav. Neurosci. Rep. 2015, 2, 146–153. [Google Scholar] [CrossRef] [PubMed]
- Bessa, J.M.; Morais, M.; Marques, F.; Pinto, L.; Palha, J.A.; Almeida, O.F.X.; Sousa, N. Stress-Induced Anhedonia Is Associated with Hypertrophy of Medium Spiny Neurons of the Nucleus Accumbens. Transl. Psychiatry 2013, 3, e266. [Google Scholar] [CrossRef]
- Willner, P. Validity, Reliability and Utility of the Chronic Mild Stress Model of Depression: A 10-Year Review and Evaluation. Psychopharmacology 1997, 134, 319–329. [Google Scholar] [CrossRef]
- Papp, M.; Nalepa, I.; Antkiewicz-Michaluk, L.; Sanchez, C. Behavioural and Biochemical Studies of Citalopram and WAY 100635 in Rat Chronic Mild Stress Model. Pharmacol. Biochem. Behav. 2002, 72, 465–474. [Google Scholar] [CrossRef]
- Papp, M.; Gruca, P.; Lason, M.; Tota-Glowczyk, K.; Niemczyk, M.; Litwa, E.; Willner, P. Rapid Antidepressant Effects of Deep Brain Stimulation of the Pre-Frontal Cortex in an Animal Model of Treatment-Resistant Depression. J. Psychopharmacol. 2018, 32, 1133–1140. [Google Scholar] [CrossRef]
- Escribá, P.V.; Ozaita, A.; García-Sevilla, J.A. Increased mRNA Expression of α2A-Adrenoceptors, Serotonin Receptors and μ-Opioid Receptors in the Brains of Suicide Victims. Neuropsychopharmacology 2004, 29, 1512–1521. [Google Scholar] [CrossRef] [PubMed]
- Zelek-Molik, A.; Taracha, E.; Nawrat, D.; Bielawski, A.; Lehner, M.; Płaźnik, A.; Nalepa, I. Effects of Morphine and Methadone Treatment on mRNA Expression of Gα(i) Subunits in Rat Brains. Pharmacol. Rep. 2010, 62, 1197–1203. [Google Scholar] [CrossRef] [PubMed]
- Dowell, J.; Elser, B.A.; Schroeder, R.E.; Stevens, H.E. Cellular Stress Mechanisms of Prenatal Maternal Stress: Heat Shock Factors and Oxidative Stress. Neurosci. Lett. 2019, 709, 134368. [Google Scholar] [CrossRef] [PubMed]
- Tripathy, K.; Sodhi, M.; Kataria, R.S.; Chopra, M.; Mukesh, M. In Silico Analysis of HSP70 Gene Family in Bovine Genome. Biochem. Genet. 2021, 59, 134–158. [Google Scholar] [CrossRef] [PubMed]
- Pratt, W.B.; Galigniana, M.D.; Harrell, J.M.; DeFranco, D.B. Role of Hsp90 and the Hsp90-Binding Immunophilins in Signalling Protein Movement. Cell. Signal. 2004, 16, 857–872. [Google Scholar] [CrossRef] [PubMed]
- Daugaard, M.; Rohde, M.; Jaattela, M. The Heat Shock Protein 70 Family: Highly Homologous Proteins with Overlapping and Distinct Functions. FEBS Lett. 2007, 581, 3702–3710. [Google Scholar] [CrossRef] [PubMed]
- Freeman, B.C.; Morimoto, R.I. The Human Cytosolic Molecular Chaperones Hsp90, Hsp70 (Hsc70) and Hdj-1 Have Distinct Roles in Recognition of a Non-Native Protein and Protein Refolding. EMBO J. 1996, 15, 2969–2979. [Google Scholar] [CrossRef]
- Nollen, E.A.A.; Brunsting, J.F.; Roelofsen, H.; Weber, L.A.; Kampinga, H.H. In Vivo Chaperone Activity of Heat Shock Protein 70 and Thermotolerance. Mol. Cell. Biol. 1999, 19, 2069–2079. [Google Scholar] [CrossRef]
- Zhang, M.-H.; Zhou, X.-M.; Cui, J.-Z.; Wang, K.-J.; Feng, Y.; Zhang, H.-A. Neuroprotective Effects of Dexmedetomidine on Traumatic Brain Injury: Involvement of Neuronal Apoptosis and HSP70 Expression. Mol. Med. Rep. 2018, 17, 8079. [Google Scholar] [CrossRef]
- Sinn, D.I.; Chu, K.; Lee, S.T.; Song, E.C.; Jung, K.H.; Kim, E.H.; Park, D.K.; Kang, K.M.; Kim, M.; Roh, J.K. Pharmacological Induction of Heat Shock Protein Exerts Neuroprotective Effects in Experimental Intracerebral Hemorrhage. Brain Res. 2007, 1135, 167–176. [Google Scholar] [CrossRef]
- Sato, K.; Matsuki, N. A 72 kDa Heat Shock Protein Is Protective against the Selective Vulnerability of CA1 Neurons and Is Essential for the Tolerance Exhibited by CA3 Neurons in the Hippocampus. Neuroscience 2002, 109, 745–756. [Google Scholar] [CrossRef] [PubMed]
- Escobedo, I.; Peraile, I.; Orio, L.; Colado, M.I.; O’Shea, E. Evidence for a Role of Hsp70 in the Neuroprotection Induced by Heat Shock Pre-Treatment against 3,4-Methylenedioxymethamphetamine Toxicity in Rat Brain. J. Neurochem. 2007, 101, 1272–1283. [Google Scholar] [CrossRef] [PubMed]
- Pasquali, M.A.; Harlow, B.L.; Soares, C.N.; Otto, M.W.; Cohen, L.S.; Minuzzi, L.; Gelain, D.P.; Moreira, J.C.F.; Frey, B.N. A Longitudinal Study of Neurotrophic, Oxidative, and Inflammatory Markers in First-Onset Depression in Midlife Women. Eur. Arch. Psychiatry Clin. Neurosci. 2018, 268, 771–781. [Google Scholar] [CrossRef] [PubMed]
- Elaković, I.; Brkljačić, J.; Matić, G. Long-Term Imipramine Treatment Affects Rat Brain and Pituitary Corticosteroid Receptors and Heat Shock Proteins Levels in a Gender-Specific Manner. J. Neural Transm. 2007, 114, 1069–1080. [Google Scholar] [CrossRef] [PubMed]
- Papp, M.; Gruca, P.; Boyer, P.-A.; Mocaër, E. Effect of Agomelatine in the Chronic Mild Stress Model of Depression in the Rat. Neuropsychopharmacology 2003, 28, 694–703. [Google Scholar] [CrossRef] [PubMed]
- Filipović, D.; Gavrilović, L.; Dronjak, S.; Radojčić, M.B. Brain Glucocorticoid Receptor and Heat Shock Protein 70 Levels in Rats Exposed to Acute, Chronic or Combined Stress. Neuropsychobiology 2005, 51, 107–114. [Google Scholar] [CrossRef] [PubMed]
- Samson, J.; Sheeladevi, R.; Ravindran, R.; Senthilvelan, M. Stress Response in Rat Brain after Different Durations of Noise Exposure. Neurosci. Res. 2007, 57, 143–147. [Google Scholar] [CrossRef] [PubMed]
- Hamed, R.; Elmalt, H.; Salama, A.; Younes, S.; Ahmed, A. Biomarkers of Oxidative Stress in Major Depressive Disorder. Open Access Maced. J. Med. Sci. 2020, 8, 501–506. [Google Scholar] [CrossRef]
- Yoshino, Y.; Dwivedi, Y. Elevated Expression of Unfolded Protein Response Genes in the Prefrontal Cortex of Depressed Subjects: Effect of Suicide. J. Affect. Disord. 2020, 262, 229–236. [Google Scholar] [CrossRef]
- Bachis, A.; Cruz, M.I.; Nosheny, R.L.; Mocchetti, I. Chronic Unpredictable Stress Promotes Neuronal Apoptosis in the Cerebral Cortex. Neurosci. Lett. 2008, 442, 104–108. [Google Scholar] [CrossRef]
- Yao, S.; Peng, M.; Zhu, X.; Cheng, M.; Qi, X. Heat Shock Protein72 Protects Hippocampal Neurons from Apoptosis Induced by Chronic Psychological Stress. Int. J. Neurosci. 2007, 117, 1551–1564. [Google Scholar] [CrossRef] [PubMed]
- Politi, P.; Brondino, N.; Emanuele, E. Increased Proapoptotic Serum Activity in Patients with Chronic Mood Disorders. Arch. Med. Res. 2008, 39, 242–245. [Google Scholar] [CrossRef] [PubMed]
- Eilat, E.; Mendlovic, S.; Doron, A.; Zakuth, V.; Spirer, Z. Increased Apoptosis in Patients with Major Depression: A Preliminary Study. J. Immunol. 1999, 163, 533–534. [Google Scholar] [CrossRef] [PubMed]
- Szuster-Ciesielska, A.; Slotwinska, M.; Stachura, A.; Marmurowska-Michalowska, H.; Dubas-Slemp, H.; Bojarska-Junak, A.; Kandefer-Szerszen, M. Accelerated Apoptosis of Blood Leukocytes and Oxidative Stress in Blood of Patients with Major Depression. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2008, 32, 686–694. [Google Scholar] [CrossRef] [PubMed]
- Peng, C.H.; Chiou, S.H.; Chen, S.J.; Chou, Y.C.; Ku, H.H.; Cheng, C.K.; Yen, C.J.; Tsai, T.H.; Chang, Y.L.; Kao, C.L. Neuroprotection by Imipramine against Lipopolysaccharide-Induced Apoptosis in Hippocampus-Derived Neural Stem Cells Mediated by Activation of BDNF and the MAPK Pathway. Eur. Neuropsychopharmacol. J. Eur. Coll. Neuropsychopharmacol. 2008, 18, 128–140. [Google Scholar] [CrossRef] [PubMed]
- Larsen, M.H.; Hay-Schmidt, A.; Ronn, L.C.; Mikkelsen, J.D. Temporal Expression of Brain-Derived Neurotrophic Factor (BDNF) mRNA in the Rat Hippocampus after Treatment with Selective and Mixed Monoaminergic Antidepressants. Eur. J. Pharmacol. 2008, 578, 114–122. [Google Scholar] [CrossRef] [PubMed]
- Kosten, T.A.; Galloway, M.P.; Duman, R.S.; Russell, D.S.; D’Sa, C. Repeated Unpredictable Stress and Antidepressants Differentially Regulate Expression of the Bcl-2 Family of Apoptotic Genes in Rat Cortical, Hippocampal, and Limbic Brain Structures. Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 2007, 33, 1545–1558. [Google Scholar] [CrossRef] [PubMed]
- Huang, Y.-Y.; Peng, C.-H.; Yang, Y.-P.; Wu, C.-C.; Hsu, W.-M.; Wang, H.-J.; Chan, K.-H.; Chou, Y.-P.; Chen, S.-J.; Chang, Y.-L. Desipramine Activated Bcl-2 Expression and Inhibited Lipopolysaccharide-Induced Apoptosis in Hippocampus-Derived Adult Neural Stem Cells. J. Pharmacol. Sci. 2007, 104, 61–72. [Google Scholar] [CrossRef]
- Chiou, S.H.; Ku, H.H.; Tsai, T.H.; Lin, H.L.; Chen, L.H.; Chien, C.S.; Ho, L.L.; Lee, C.H.; Chang, Y.L. Moclobemide Upregulated Bcl-2 Expression and Induced Neural Stem Cell Differentiation into Serotoninergic Neuron via Extracellular-Regulated Kinase Pathway. Br. J. Pharmacol. 2006, 148, 587–598. [Google Scholar] [CrossRef]
- Johnson, J.D.; Campisi, J.; Sharkey, C.M.; Kennedy, S.L.; Nickerson, M.; Fleshner, M. Adrenergic Receptors Mediate Stress-Induced Elevations in Extracellular Hsp72. J. Appl. Physiol. 2005, 99, 1789–1795. [Google Scholar] [CrossRef]
- Chin, J.H.; Okazaki, M.; Hu, Z.-W.; Miller, J.W.; Hoffman, B.B. Activation of Heat Shock Protein (Hsp)70 and Proto-Oncogene Expression by A1 Adrenergic Agonists in Rat Aorta with Age. J. Clin. Investig. 1996, 97, 2316–2323. [Google Scholar] [CrossRef] [PubMed]
- Meng, X.; Brown, J.M.; Ao, L.; Banerjee, A.; Harken, A.H. Norepinephrine Induces Cardiac Heat Shock Protein 70 and Delayed Cardioprotection in the Rat through A1 Adrenoceptors. Cardiovasc. Res. 1996, 32, 374–383. [Google Scholar] [CrossRef] [PubMed]
- Lacoste, A.; De Cian, M.-C.; Cueff, A.; Poulet, S.A. Noradrenaline and A-Adrenergic Signaling Induce the Hsp70 Gene Promoter in Mollusc Immune Cells. J. Cell Sci. 2001, 114, 3557–3564. [Google Scholar] [CrossRef] [PubMed]
- Heneka, M.T.; Gavrilyuk, V.; Landreth, G.E.; O’Banion, M.K.; Weinberg, G.; Feinstein, D.L. Noradrenergic Depletion Increases Inflammatory Responses in Brain: Effects on IκB and HSP70 Expression. J. Neurochem. 2003, 85, 387–398. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.J.; Liu, X.; Liu, D.X.; Jiang, H.; Mao, X.Q.; Wang, C.; Pan, F. Effects of Different Adrenergic Blockades on the Stress Resistance of Wistar Rats. Neurosci. Lett. 2012, 511, 95–100. [Google Scholar] [CrossRef]
- Koga, H.; Martinez-Vicente, M.; Arias, E.; Kaushik, S.; Sulzer, D.; Cuervo, A.M. Constitutive Upregulation of Chaperone-Mediated Autophagy in Huntington’s Disease. J. Neurosci. 2011, 31, 18492–18505. [Google Scholar] [CrossRef]
- Furay, A.R.; Murphy, E.K.; Mattson, M.P.; Guo, Z.; Herman, J.P. Region-Specific Regulation of Glucocorticoid Receptor/HSP90 Expression and Interaction in Brain. J. Neurochem. 2006, 98, 1176–1184. [Google Scholar] [CrossRef]
- Galigniana, N.M.; Ballmer, L.T.; Toneatto, J.; Erlejman, A.G.; Lagadari, M.; Galigniana, M.D. Regulation of the Glucocorticoid Response to Stress-Related Disorders by the Hsp90-Binding Immunophilin FKBP51. J. Neurochem. 2012, 122, 4–18. [Google Scholar] [CrossRef]
- Kirschke, E.; Goswami, D.; Southworth, D.; Griffin, P.R.; Agard, D.A. Glucocorticoid Receptor Function Regulated by Coordinated Action of the Hsp90 and Hsp70 Chaperone Cycles. Cell 2014, 157, 1685–1697. [Google Scholar] [CrossRef]
- Baker, J.D.; Ozsan, I.; Rodriguez Ospina, S.; Gulick, D.; Blair, L.J. Hsp90 Heterocomplexes Regulate Steroid Hormone Receptors: From Stress Response to Psychiatric Disease. Int. J. Mol. Sci. 2018, 20, 79. [Google Scholar] [CrossRef]
- Guo, Y.; Guettouche, T.; Fenna, M.; Boellmann, F.; Pratt, W.B.; Toft, D.O.; Smith, D.F.; Voellmy, R. Evidence for a Mechanism of Repression of Heat Shock Factor 1 Transcriptional Activity by a Multichaperone Complex. J. Biol. Chem. 2001, 276, 45791–45799. [Google Scholar] [CrossRef] [PubMed]
- Vamvakopoulos, N.O. Tissue-Specific Expression of Heat Shock Proteins 70 and 90: Potential Implication for Differential Sensitivity of Tissues to Glucocorticoids. Mol. Cell. Endocrinol. 1993, 98, 49–54. [Google Scholar] [CrossRef] [PubMed]
- Pandey, P.; Saleh, A.; Nakazawa, A.; Kumar, S.; Srinivasula, S.M.; Kumar, V.; Weichselbaum, R.; Nalin, C.; Alnemri, E.S.; Kufe, D.; et al. Negative Regulation of Cytochrome C-Mediated Oligomerization of Apaf-1 and Activation of Procaspase-9 by Heat Shock Protein 90. EMBO J. 2000, 19, 4310–4322. [Google Scholar] [CrossRef] [PubMed]
- Gerges, N.Z.; Tran, I.C.; Backos, D.S.; Harrell, J.M.; Chinkers, M.; Pratt, W.B.; Esteban, J.A. Independent Functions of Hsp90 in Neurotransmitter Release and in the Continuous Synaptic Cycling of AMPA Receptors. J. Neurosci. Off. J. Soc. Neurosci. 2004, 24, 4758–4766. [Google Scholar] [CrossRef] [PubMed]
- Jochems, J.; Teegarden, S.L.; Chen, Y.; Boulden, J.; Challis, C.; Ben-Dor, G.A.; Kim, S.F.; Berton, O. Enhancement of Stress Resilience Through Histone Deacetylase 6–Mediated Regulation of Glucocorticoid Receptor Chaperone Dynamics. Biol. Psychiatry 2015, 77, 345–355. [Google Scholar] [CrossRef] [PubMed]
- Linsen, F.; Broeder, C.; Sep, M.S.C.; Verhoeven, J.E.; Bet, P.M.; Penninx, B.W.J.H.; Meijer, O.C.; Vinkers, C.H. Glucocorticoid Receptor (GR) Antagonism as Disease-Modifying Treatment for MDD with Childhood Trauma: Protocol of the RESET-Medication Randomized Controlled Trial. BMC Psychiatry 2023, 23, 331. [Google Scholar] [CrossRef] [PubMed]
- Brivio, P.; Sbrini, G.; Tarantini, L.; Parravicini, C.; Gruca, P.; Lason, M.; Litwa, E.; Favero, C.; Riva, M.A.; Eberini, I.; et al. Stress Modifies the Expression of Glucocorticoid-Responsive Genes by Acting at Epigenetic Levels in the Rat Prefrontal Cortex: Modulatory Activity of Lurasidone. Int. J. Mol. Sci. 2021, 22, 6197. [Google Scholar] [CrossRef]
- Brivio, P.; Buoso, E.; Masi, M.; Gallo, M.T.; Gruca, P.; Lason, M.; Litwa, E.; Papp, M.; Fumagalli, F.; Racchi, M.; et al. The Coupling of RACK1 with the Beta Isoform of the Glucocorticoid Receptor Promotes Resilience to Chronic Stress Exposure. Neurobiol. Stress 2021, 15, 100372. [Google Scholar] [CrossRef]
- Calabrese, F.; Brivio, P.; Sbrini, G.; Gruca, P.; Lason, M.; Litwa, E.; Niemczyk, M.; Papp, M.; Riva, M.A. Effect of Lurasidone Treatment on Chronic Mild Stress-Induced Behavioural Deficits in Male Rats: The Potential Role for Glucocorticoid Receptor Signalling. J. Psychopharmacol. 2020, 34, 420–428. [Google Scholar] [CrossRef]
- Belzeaux, R.; Bergon, A.; Jeanjean, V.; Loriod, B.; Formisano-Tréziny, C.; Verrier, L.; Loundou, A.; Baumstarck-Barrau, K.; Boyer, L.; Gall, V.; et al. Responder and Nonresponder Patients Exhibit Different Peripheral Transcriptional Signatures during Major Depressive Episode. Transl. Psychiatry 2012, 2, e185. [Google Scholar] [CrossRef]
- Ding, X.Z.; Fernandez-Prada, C.M.; Bhattacharjee, A.K.; Hoover, D.L. Over-Expression of Hsp-70 Inhibits Bacterial Lipopolysaccharide-Induced Production of Cytokines in Human Monocyte-Derived Macrophages. Cytokine 2001, 16, 210–219. [Google Scholar] [CrossRef] [PubMed]
- Chio, C.-C.; Lin, H.-J.; Tian, Y.-F.; Chen, Y.-C.; Lin, M.-T.; Lin, C.-H.; Chang, C.-P.; Hsu, C.-C. Exercise Attenuates Neurological Deficits by Stimulating a Critical HSP70/NF-κB/IL-6/Synapsin I Axis in Traumatic Brain Injury Rats. J. Neuroinflamm. 2017, 14, 90. [Google Scholar] [CrossRef]
- Rossetti, A.C.; Papp, M.; Gruca, P.; Paladini, M.S.; Racagni, G.; Riva, M.A.; Molteni, R. Stress-Induced Anhedonia Is Associated with the Activation of the Inflammatory System in the Rat Brain: Restorative Effect of Pharmacological Intervention. Pharmacol. Res. 2016, 103, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Duda, W.; Curzytek, K.; Kubera, M.; Connor, T.J.; Fagan, E.M.; Basta-Kaim, A.; Trojan, E.; Papp, M.; Gruca, P.; Budziszewska, B.; et al. Interaction of the Immune-Inflammatory and the Kynurenine Pathways in Rats Resistant to Antidepressant Treatment in Model of Depression. Int. Immunopharmacol. 2019, 73, 527–538. [Google Scholar] [CrossRef] [PubMed]
- Kucharczyk, M.; Kurek, A.; Pomierny, B.; Detka, J.; Papp, M.; Tota, K.; Budziszewska, B. The Reduced Level of Growth Factors in an Animal Model of Depression Is Accompanied by Regulated Necrosis in the Frontal Cortex but Not in the Hippocampus. Psychoneuroendocrinology 2018, 94, 121–133. [Google Scholar] [CrossRef]
- Kelly, S.; Zhang, Z.J.; Zhao, H.; Xu, L.; Giffard, R.G.; Sapolsky, R.M.; Yenari, M.A.; Steinberg, G.K. Gene Transfer of HSP72 Protects Cornu Ammonis 1 Region of the Hippocampus Neurons from Global Ischemia: Influence of Bcl-2. Ann. Neurol. 2002, 52, 160–167. [Google Scholar] [CrossRef]
- Beere, H.M.; Wolf, B.B.; Cain, K.; Mosser, D.D.; Mahboubi, A.; Kuwana, T.; Tailor, P.; Morimoto, R.I.; Cohen, G.M.; Green, D.R. Heat-Shock Protein 70 Inhibits Apoptosis by Preventing Recruitment of Procaspase-9 to the Apaf-1 Apoptosome. Nat. Cell Biol. 2000, 2, 469–475. [Google Scholar] [CrossRef]
- Lee, S.-H.; Kwon, H.-M.; Kim, Y.-J.; Lee, K.-M.; Kim, M.; Yoon, B.-W. Effects of Hsp70.1 Gene Knockout on the Mitochondrial Apoptotic Pathway After Focal Cerebral Ischemia. Stroke 2004, 35, 2195–2199. [Google Scholar] [CrossRef]
- Ozdamar Unal, G.; Demirdas, A.; Nazıroglu, M.; Ovey, I.S. Agomelatine Attenuates Calcium Signaling and Apoptosis via the Inhibition of TRPV1 Channel in the Hippocampal Neurons of Rats with Chronic Mild Stress Depression Model. Behav. Brain Res. 2022, 434, 114033. [Google Scholar] [CrossRef]
- Zhao, Y.; Shang, P.; Wang, M.; Xie, M.; Liu, J. Neuroprotective Effects of Fluoxetine Against Chronic Stress-Induced Neural Inflammation and Apoptosis: Involvement of the P38 Activity. Front. Physiol. 2020, 11, 351. [Google Scholar] [CrossRef]
- Solarz-Andrzejewska, A.; Majcher-Maślanka, I.; Kryst, J.; Chocyk, A. Modulation of the Endoplasmic Reticulum Stress and Unfolded Protein Response Mitigates the Behavioral Effects of Early-Life Stress. Pharmacol. Rep. 2023, 75, 293–319. [Google Scholar] [CrossRef] [PubMed]
- McEwen, B.S. Glucocorticoids, Depression, and Mood Disorders: Structural Remodeling in the Brain. Metab. Clin. Exp. 2005, 54, 20–23. [Google Scholar] [CrossRef] [PubMed]
- Gourley, S.L.; Swanson, A.M.; Koleske, A.J. Corticosteroid-Induced Neural Remodeling Predicts Behavioral Vulnerability and Resilience. J. Neurosci. 2013, 33, 3107–3112. [Google Scholar] [CrossRef] [PubMed]
- Patel, D.; Anilkumar, S.; Chattarji, S.; Buwalda, B. Repeated Social Stress Leads to Contrasting Patterns of Structural Plasticity in the Amygdala and Hippocampus. Behav. Brain Res. 2018, 347, 314–324. [Google Scholar] [CrossRef] [PubMed]
- Godsil, B.P.; Kiss, J.P.; Spedding, M.; Jay, T.M. The Hippocampal–Prefrontal Pathway: The Weak Link in Psychiatric Disorders? Eur. Neuropsychopharmacol. 2013, 23, 1165–1181. [Google Scholar] [CrossRef] [PubMed]
- Begni, V.; Marizzoni, M.; Creutzberg, K.C.; Silipo, D.M.; Papp, M.; Cattaneo, A.; Riva, M.A. Transcriptomic Analyses of Rats Exposed to Chronic Mild Stress: Modulation by Chronic Treatment with the Antipsychotic Drug Lurasidone. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2024, 129, 110885. [Google Scholar] [CrossRef] [PubMed]
- Calabrese, F.; Brivio, P.; Gruca, P.; Lason-Tyburkiewicz, M.; Papp, M.; Riva, M.A. Chronic Mild Stress-Induced Alterations of Local Protein Synthesis: A Role for Cognitive Impairment. ACS Chem. Neurosci. 2017, 8, 817–825. [Google Scholar] [CrossRef]
- Luoni, A.; Macchi, F.; Papp, M.; Molteni, R.; Riva, M.A. Lurasidone Exerts Antidepressant Properties in the Chronic Mild Stress Model through the Regulation of Synaptic and Neuroplastic Mechanisms in the Rat Prefrontal Cortex. Int. J. Neuropsychopharmacol. 2015, 18, pyu061. [Google Scholar] [CrossRef]
- Rafa-Zabłocka, K.; Zelek-Molik, A.; Tepper, B.; Chmielarz, P.; Kreiner, G.; Wilczkowski, M.; Nalepa, I. Chronic Restraint Stress Induces Changes in the Cerebral Galpha 12/13 and Rho-GTPase Signaling Network. Pharmacol. Rep. 2021, 73, 1179–1187. [Google Scholar] [CrossRef]
- Sheline, Y.I.; Wang, P.W.; Gado, M.H.; Csernansky, J.G.; Vannier, M.W. Hippocampal Atrophy in Recurrent Major Depression. Proc. Natl. Acad. Sci. USA 1996, 93, 3908–3913. [Google Scholar] [CrossRef]
- Lacerda, A.L.; Keshavan, M.S.; Hardan, A.Y.; Yorbik, O.; Brambilla, P.; Sassi, R.B.; Nicoletti, M.; Mallinger, A.G.; Frank, E.; Kupfer, D.J.; et al. Anatomic Evaluation of the Orbitofrontal Cortex in Major Depressive Disorder. Biol. Psychiatry 2004, 55, 353–358. [Google Scholar] [CrossRef] [PubMed]
- Botteron, K.N.; Raichle, M.E.; Drevets, W.C.; Heath, A.C.; Todd, R.D. Volumetric Reduction in Left Subgenual Prefrontal Cortex in Early Onset Depression. Biol. Psychiatry 2002, 51, 342–344. [Google Scholar] [CrossRef] [PubMed]
- Musazzi, L.; Treccani, G.; Popoli, M. Functional and Structural Remodeling of Glutamate Synapses in Prefrontal and Frontal Cortex Induced by Behavioral Stress. Front. Psychiatry 2015, 6, 60. [Google Scholar] [CrossRef] [PubMed]
- Zelek-Molik, A.; Bobula, B.; Gądek-Michalska, A.; Chorązka, K.; Bielawski, A.; Kuśmierczyk, J.; Siwiec, M.; Wilczkowski, M.; Hess, G.; Nalepa, I. Psychosocial Crowding Stress-Induced Changes in Synaptic Transmission and Glutamate Receptor Expression in the Rat Frontal Cortex. Biomolecules 2021, 11, 294. [Google Scholar] [CrossRef]
- Papp, M.; Willner, P. Models of Affective Illness: Chronic Mild Stress in the Rat. Curr. Protoc. 2023, 3, e712. [Google Scholar] [CrossRef]
- Zelek-Molik, A.; Costanzi, M.; Rafa-Zabłocka, K.; Kreiner, G.; Roman, A.; Vetulani, J.; Rossi-Arnaud, C.; Cestari, V.; Nalepa, I. Fear Memory-Induced Alterations in the mRNA Expression of G Proteins in the Mouse Brain and the Impact of Immediate Posttraining Treatment with Morphine. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2019, 93, 221–231. [Google Scholar] [CrossRef]
Brain Structure/ Treatment | Level of mRNAs [% of Sham Control ± SEM] 1 | |||
---|---|---|---|---|
HSP72 | HSC70 | HSP90A | HSP90B | |
A. PFC | ||||
Sham | 100.00 ± 10.98 | 100.00 ± 7.91 | 100.00 ± 5.86 | 100.00 ± 7.70 |
Stress-reactive | 93.63 ± 10.57 | 96.64 ± 6.89 | 96.84 ± 5.97 | 94.30 ± 5.92 |
Stress-nonreactive | 92.76 ± 8.94 | 96.33 ± 3.96 | 100.43 ± 2.96 | 85.88 ± 3.80 |
One-way ANOVA | F(2,15) = 0.15, p > 0.05 | F(2,15) = 0.10, p > 0.05 | F(2,15) = 0.15, p > 0.05 | F(2,15) = 1.39, p > 0.05 |
B. HIP | ||||
Sham | 100.00 ± 10.58 | 100.00 ± 6.83 | 100.00 ± 3.00 | 100.00 ± 8.26 |
Stress-reactive | 89.10 ± 8.30 | 99.04 ± 3.88 | 88.06 ± 2.82 * | 100.47 ± 5.64 |
Stress-nonreactive | 81.66 ± 16.30 | 78.67 ± 12.15 | 91.93 ± 2.04 | 85.89 ± 13.92 |
One-way ANOVA | F(2,15) = 0.57, p > 0.05 | F(2,15) = 2.08, p > 0.05 | F(2,15) = 5.28, p < 0.05 | F(2,15) = 0.51, p > 0.05 |
C. Thal | ||||
Sham | 100.00 ± 14.45 | 100.00 ± 7.50 | 100.00 ± 9.72 | 100.00 ± 14.09 |
Stress-reactive | 119.54 ± 18.15 | 116.78 ± 3.39 | 127.81 ± 3.76 | 136.17 ± 7.84 |
Stress-nonreactive | 112.58 ± 15.72 | 108.21 ± 11.09 | 99.51 ± 20.64 | 121.24 ± 19.32 |
One-way ANOVA | F(2,15) = 0.31, p > 0.05 | F(2,15) = 0.98, p > 0.05 | F(2,15) = 1.37, p > 0.05 | F(2,15) = 1.37, p > 0.05 |
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Bielawski, A.; Zelek-Molik, A.; Rafa-Zabłocka, K.; Kowalska, M.; Gruca, P.; Papp, M.; Nalepa, I. Elevated Expression of HSP72 in the Prefrontal Cortex and Hippocampus of Rats Subjected to Chronic Mild Stress and Treated with Imipramine. Int. J. Mol. Sci. 2024, 25, 243. https://doi.org/10.3390/ijms25010243
Bielawski A, Zelek-Molik A, Rafa-Zabłocka K, Kowalska M, Gruca P, Papp M, Nalepa I. Elevated Expression of HSP72 in the Prefrontal Cortex and Hippocampus of Rats Subjected to Chronic Mild Stress and Treated with Imipramine. International Journal of Molecular Sciences. 2024; 25(1):243. https://doi.org/10.3390/ijms25010243
Chicago/Turabian StyleBielawski, Adam, Agnieszka Zelek-Molik, Katarzyna Rafa-Zabłocka, Marta Kowalska, Piotr Gruca, Mariusz Papp, and Irena Nalepa. 2024. "Elevated Expression of HSP72 in the Prefrontal Cortex and Hippocampus of Rats Subjected to Chronic Mild Stress and Treated with Imipramine" International Journal of Molecular Sciences 25, no. 1: 243. https://doi.org/10.3390/ijms25010243