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Na+, K+ ATPase Activity Is Reduced in Amygdala of Rats with Chronic Stress-Induced Anxiety-Like Behavior

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Abstract

In this study, we examined the effects of two chronic stress regimens upon anxiety-like behavior, Na+, K+-ATPase activity and immunocontent, and oxidative stress parameters (antioxidant enzymes and reactive oxygen species production) in the amygdala. Male rats were subjected to chronic unpredictable and to chronic restraint stress for 40 days. Subsequently, anxiety-like behavior was examined. Both stressed groups presented increased anxiety-like behavior. Reduced amygdalal Na+, K+-ATPase activity in the synaptic plasma membranes was also observed, without alterations in the amygdala immunocontent. In addition, when analyzing oxidative stress parameters, only superoxide dismutase activity was decreased in the amygdala of animals subjected to unpredictable stress. We conclude that both models of chronic stress lead to anxiety-like behavior and decreased amygdalal Na+, K+-ATPase activity, which appears not to be related to oxidative imbalance. The relationship between this decreased activity and anxiety-like behavior remains to be studied.

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References

  1. Ericinska M, Silver IA (1994) Ions and energy in mammalian brain. Prog Neurobiol 16:37–71

    Article  Google Scholar 

  2. Shull GE, Greeb J, Lingrel JB (1986) Molecular cloning of three distinct forms of the Na+, K+-ATPase alpha-subunit from rat brain. Biochemistry 25:8125–8132

    Article  PubMed  CAS  Google Scholar 

  3. Jewell EA, Shamraj OI, Lingrel JB (1992) Isoforms of the alpha subunit of Na, K-ATPase and their significance. Acta Physiol Scand Suppl 607:161–169

    PubMed  CAS  Google Scholar 

  4. Segall L, Daly SE, Blostein R (2001) Mechanistic basis for kinetic differences between the rat alpha 1, alpha 2, and alpha 3 isoforms of the Na, K-ATPase. J Biol Chem 276:31535–31541

    Article  PubMed  CAS  Google Scholar 

  5. Streck EL, Zugno AI, Tagliari B et al (2001) Inhibition of rat brain Na+, K+-ATPase activity induced by homocysteine is probably mediated by oxidative stress. Neurochem Res 26:1195–1200

    Article  PubMed  CAS  Google Scholar 

  6. Wilhelm EA, Jesse CR, Bortolatto CF et al (2009) Anticonvulsant and antioxidant effects of 3-alkynyl selenophene in 21-day-old rats on pilocarpine model of seizures. Brain Res Bull 79:281–287

    Article  PubMed  CAS  Google Scholar 

  7. Morel P, Tallineau C, Pontcharraud R et al (1998) Effects of 4-hydroxynonenal, a lipid peroxidation product, on dopamine transport and Na+/K+ATPase in rat striatal synaptosomes. Neurochem Int 33:531–540

    Article  PubMed  CAS  Google Scholar 

  8. Petrushanko I, Bogdanov N, Bulygina E et al (2006) Na-K-ATPase in rat cerebellar granule cells is redox sensitive. Am J Physiol Regul Integr Comp Physiol 290:R916–R925

    PubMed  CAS  Google Scholar 

  9. Wang P, Zeng T, Zhang CL et al (2009) Lipid peroxidation was involved in the memory impairment of carbon monoxide-induced delayed neuron damage. Neurochem Res 34:1293–1298

    Article  PubMed  CAS  Google Scholar 

  10. Long J, Liu C, Sun L et al (2009) Neuronal mitochondrial toxicity of malondialdehyde: inhibitory effects on respiratory function and enzyme activities in rat brain mitochondria. Neurochem Res 34:786–794

    Article  PubMed  CAS  Google Scholar 

  11. Choi IY, Yan H, Park YK et al (2009) Sauchinone reduces oxygen-glucose deprivation-evoked neuronal cell death via suppression of intracellular radical production. Arch Pharm Res 32:1599–1606

    Article  PubMed  CAS  Google Scholar 

  12. Cochrane CG (1991) Mechanisms of oxidant injury of cells. Mol Aspects Med 12:137–147

    Article  PubMed  CAS  Google Scholar 

  13. Metodiewa D, Koska C (2000) Reactive oxygen species and reactive nitrogen species: relevance to cyto(neuro)toxic events and neurologic disorders. An overview. Neurotoxicity Res 1:197–233

    Article  CAS  Google Scholar 

  14. Olanow CW (1992) An introduction to the free radical hypothesis in Parkinson’s disease. Ann Neurol 32(Suppl):S2–S9

    Article  PubMed  CAS  Google Scholar 

  15. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4a edn. Oxford University Press, Oxford

    Google Scholar 

  16. Wyse ATS, Streck EL, Worm P et al (2000) Preconditioning prevents the inhibition of Na+, K+ ATPase activity after brain ischemia. Neurochem Res 25:969–973

    Google Scholar 

  17. Grisar T (1984) Glial and neuronal Na+, K+ pump in epilepsy. Ann Neurol 16:S128–S134

    Article  PubMed  CAS  Google Scholar 

  18. Pisani A, Martella G, Tscherter A et al (2006) Enhanced sensitivity of DJ-1-deficient dopaminergic neurons to energy metabolism impairment: role of Na+/K+ ATPase. Neurobiol Dis 23:54–60

    Article  PubMed  CAS  Google Scholar 

  19. Hattori N, Kitagawa K, Higashida T et al (1998) CI-ATPase and Na+/K(+)-ATPase activities in Alzheimer’s disease brains. Neurosci Lett 254:141–144

    Article  PubMed  CAS  Google Scholar 

  20. Yu SP (2003) Na+, K+ ATPase: the new face of an old player in pathogenesis and apoptotic/hybrid cell death. Biochem Pharmacol 66:1601–1609

    Article  PubMed  CAS  Google Scholar 

  21. Hokin-Neaverson M, Jefferson JW (1989) Erythrocytes sodium pump activity in bipolar affective disorder and other psychiatry disorders. Neuropsychobiology 22:1–7

    Article  PubMed  CAS  Google Scholar 

  22. Mynett-Johnson L, Murphy V, McCormack J et al (1998) Evidence for an allelic association between bipolar disorder and a Na+, K+ adenosine triphosphatase alpha subunit gene (ATP1A3). Biol Psychiatry 44:47–51

    Article  PubMed  CAS  Google Scholar 

  23. Rybakowsky J, Potok E, Strzizewski W et al (1984) Erythrocyte cation transport disturbances in patients with endogenous depression. Clinical Experim Pharmacol Phys 11:319–326

    Article  Google Scholar 

  24. Wood AJ, Smith CE, Clarke EE et al (1991) Altered in vitro adaptative responses of lymphocyte Na, K-ATPase in patients with manic depressive psychosis. J Affect Disord 21:199–206

    Article  PubMed  CAS  Google Scholar 

  25. EI-Mallakh RS, Wyatt RJ (1995) The Na+, K+ ATPase hypothesis for bipolar illness. Biol Psychiatry 37:235–244

    Article  Google Scholar 

  26. Riegel RE, Valvassori SS, Elias G et al (2009) Animal model of mania induced by ouabain: evidence of oxidative stress in submitochondrial particles of the rat brain. Neurochem Int 55:491–495

    Article  PubMed  CAS  Google Scholar 

  27. Gamaro GD, Streck EL, Matté C et al (2003) Reduction of hippocampal Na+, K+ ATPase activity in rats subjected to an experimental model of depression. Neurochem Res 28:1339–1344

    Article  PubMed  CAS  Google Scholar 

  28. de Vasconcellos AP, Tabajara AS, Ferrari C et al (2003) Effect of chronic stress on spatial memory in rats is attenuated by lithium treatment. Physiol Behav 79:143–149

    Article  PubMed  CAS  Google Scholar 

  29. Pucilowski O, Overstreet DH, Rezvani AH et al (1993) Chronic mild stress-induced anhedonia: greater effectin a genetic rat model of depression. Physiol Behav 54:1215–1220

    Article  PubMed  CAS  Google Scholar 

  30. Willner P (1991) Animal models as simulations of depression. TIPS 12:131–136

    PubMed  CAS  Google Scholar 

  31. D’Aquila PS, Brain P, Willner P (1994) Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol Behav 56:861–867

    Article  PubMed  Google Scholar 

  32. Ely DR, Dapper V, Marasca J et al (1997) Effect of restraint stress on feeding behavior of rats. Physiol Behav 61:395–398

    Article  PubMed  CAS  Google Scholar 

  33. Torres IL, Gamaro GD, Silveira-Cucco SN et al (2001) Effect of acute and repeated restraint stress on glucose oxidation to CO2 in hippocampal and cerebral cortex slices. Braz J Med Biol Res 34:111–116

    PubMed  CAS  Google Scholar 

  34. Martí O, Armario A (1997) Influence of regularity of exposure to chronic stress on the pattern of habituation of pituitary-adrenal hormones, prolactin and glucose. Stress 1:179–189

    Article  PubMed  Google Scholar 

  35. Sibille E, Wang Y, Joeyen-Waldorf J et al (2009) A molecular signature of depression in the amygdala. Am J Psychiatry 166:1011–1024

    Article  PubMed  Google Scholar 

  36. Yang TT, Simmons AN, Matthews SC et al (2010) Adolescents with major depression demonstrate increased amygdala activation. J Am Acad Child Adolesc Psychiatry 49:42–51

    Article  PubMed  Google Scholar 

  37. LeDoux J (2007) The amygdala. Curr Biol 17:R868–R874

    Article  PubMed  CAS  Google Scholar 

  38. Kim MJ, Whalen PJ (2009) The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. J Neurosci 29:11614–11618

    Article  PubMed  CAS  Google Scholar 

  39. Goldin PR, Manber-Ball T, Werner K et al (2009) Neural mechanisms of cognitive reappraisal of negative self-beliefs in social anxiety disorder. Biol Psychiatry 66:1091–1099

    Article  PubMed  Google Scholar 

  40. Wolfensberger SP, Veltman DJ, Hoogendijk WJ et al (2008) Amygdala responses to emotional faces in twins discordant or concordant for the risk for anxiety and depression. Neuroimage 41:544–552

    Article  PubMed  Google Scholar 

  41. Ikeda K, Onaka T, Yamakado M et al (2003) Degeneration of the amygdala/piriform cortex and enhanced fear/anxiety behaviors in sodium pump alpha2 subunit (Atp1a2)-deficient mice. J Neurosci 23:4667–4676

    PubMed  CAS  Google Scholar 

  42. Moseley AE, Williams MT, Schaefer TL et al (2007) Deficiency in Na+, K+ ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. J Neurosci 27:616–626

    Article  PubMed  CAS  Google Scholar 

  43. Johnson LR, Farb C, Morrison JH et al (2005) Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 136:289–299

    Article  PubMed  CAS  Google Scholar 

  44. Rossie S, Jayachandran H, Meisel RL (2006) Cellular co-localization of protein phosphatase 5 and glucocorticoid receptors in rat brain. Brain Res 1111:1–11

    Article  PubMed  CAS  Google Scholar 

  45. Silveira PP, Portella AK, Clemente Z et al (2005) The effect of neonatal handling on adult feeding behavior is not an anxiety-like behavior. Int J Dev Neurosci 23:93–99

    Article  PubMed  CAS  Google Scholar 

  46. Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463:3–33

    Article  PubMed  CAS  Google Scholar 

  47. Jones DH, Matus AI (1974) Isolation of plasma synaptic membrane from brain by combination flotation-sedimentation density gradient centrifugation. Biochim Biophys Acta 356:276–287

    Article  PubMed  CAS  Google Scholar 

  48. Chan KM, Delfer D, Junger KD (1986) A direct colorimetric assay for Ca2+ -stimulated ATPase activity. Anal Biochem 157:375–380

    Article  PubMed  CAS  Google Scholar 

  49. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-die-binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  50. Delmas-Beauvieux MC, Peuchant E, Dumon MF et al (1995) Relationship between red blood cell antioxidant enzymatic system status and lipoperoxidation during the acute phase of malaria. Clin Biochem 28:163–169

    Article  PubMed  CAS  Google Scholar 

  51. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  PubMed  CAS  Google Scholar 

  52. Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333

    Article  PubMed  CAS  Google Scholar 

  53. Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by a dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27:612–616

    Article  PubMed  CAS  Google Scholar 

  54. Lowry OH, Rosebrough NJ, Farr AL et al (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  55. Katz RJ, Roth KA, Carroll BJ (1981) Acute and chronic stress effects on open field activity in the rat: Implications for a model of depression. Neurosci Biobehav Rev 5:247–251

    Article  PubMed  CAS  Google Scholar 

  56. Gamaro GD, Manoli LP, Torres IL et al (2003) Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 42:107–114

    Article  PubMed  CAS  Google Scholar 

  57. Silveira PP, Xavier MH, Souza FH et al (2000) Interaction between repeated restraint stress and concomitant midazolam administration on sweet food ingestion in rats. Braz J Med Biol Res 33:1343–1350

    Article  PubMed  CAS  Google Scholar 

  58. Alves R, Barbosa de Carvalho JG, Benedito MA (2005) High and low rearing subgroups of rats selected in the open field differ in the activity of K+ -stimulated p-nitrophenylphosphatase in the hippocampus. Brain Res 1058:178–182

    Article  PubMed  CAS  Google Scholar 

  59. Mineur YS, Belzung C, Crusio WE (2006) Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav Brain Res 175:43–50

    Article  PubMed  Google Scholar 

  60. Joo Y, Choi KM, Lee YH et al (2009) Chronic immobilization stress induces anxiety- and depression-like behaviors and decreases transthyretin in the mouse cortex. Neurosci Lett 461:121–125

    Article  PubMed  CAS  Google Scholar 

  61. Noschang CG, Pettenuzzo LF, Toigo EV et al (2009) Sex-specific differences on caffeine consumption and chronic stress-induced anxiety-like behavior and DNA breaks in the hippocampus. Pharmacol Biochem Behav 94:63–69

    Article  PubMed  CAS  Google Scholar 

  62. Rodrigues SM, LeDoux JE, Sapolsky RM (2009) The influence of stress hormones on fear circuitry. Annu Rev Neurosci 32:289–313

    Article  PubMed  CAS  Google Scholar 

  63. Vyas A, Mitra R, Shankaranarayana Rao BS et al (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–6818

    PubMed  CAS  Google Scholar 

  64. Vyas A, Jadhav S, Chattarji S (2006) Prolonged behavioral stress enhances synaptic connectivity in the basolateral amydala. Neuroscience 143:387–393

    Article  PubMed  CAS  Google Scholar 

  65. de Vasconcellos AP, Zugno AI, Dos Santos AH et al (2005) Na+, K(+)-ATPase activity is reduced in hippocampus of rats submitted to an experimental model of depression: effect of chronic lithium treatment and possible involvement in learning deficits. Neurobiol Learn Mem 84:102–110

    Article  PubMed  CAS  Google Scholar 

  66. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397–409

    Article  PubMed  CAS  Google Scholar 

  67. Westenberg HG (2009) Recent advances in understanding and treating social anxiety disorder. CNS Spectr 14(2 Suppl 3):24–33

    PubMed  Google Scholar 

  68. Papaleo F, Crawley JN, Song J et al (2008) Genetic dissection of the role of catechol-O-methyltransferase in cognition and stress reactivity in mice. J Neurosci 28:8709–8723

    Article  PubMed  CAS  Google Scholar 

  69. Paul C, Schöberl F, Weinmeister P et al (2008) Signaling through cGMP-dependent protein kinase I in the amygdala is critical for auditory-cued fear memory and long-term potentiation. J Neurosci 28:14202–14212

    Article  PubMed  CAS  Google Scholar 

  70. Farman N, Bonvalet JP, Seckl JR (1994) Aldosterone selectively increases Na+, K+ ATPase alpha 3-subunit mRNA expression in rat hippocampus. Am J Physiol 266(2 Pt 1):C423–C428

    PubMed  CAS  Google Scholar 

  71. Awaiss D, Shao Y, Isamil-Beigi F (2000) Thyroid hormone regulation of myocardial Na+, K+ ATPase gene expression. J Mol Cell Cardiol 32:1969–1980

    Article  CAS  Google Scholar 

  72. Hernandez RJ (1992) Na+, K+ ATPase regulation by neurotransmitters. Neurochem Int 20:1–10

    Article  Google Scholar 

  73. Swann AC (1983) Stimulation of brain Na+, K+ ATPase by norepinephrine in vivo: prevention by receptor antagonists and enhancement by repeated stimulation. Brain Res 260:338–341

    Article  PubMed  CAS  Google Scholar 

  74. Peña-Rangel MT, Rosalio MC, Hernandez-Rodriguez J (1999) Regulation of glial Na+, K+ ATPase by serotonin: identification of participating receptors. Neurochem Res 24:643–649

    Article  PubMed  Google Scholar 

  75. Rose EM, Koo JC, Antflick JE et al (2009) Glutamate transporter coupling to Na, K-ATPase. J Neurosci 29:8143–8155

    Article  PubMed  CAS  Google Scholar 

  76. Dobretsov M, Stimers JR (2005) Neuronal function and alpha3 isoform of the Na/K-ATPase. Front Biosci 10:2373–2396

    Article  PubMed  CAS  Google Scholar 

  77. Taguchi K, Kumanogoh H, Nakamura S et al (2007) Ouabain-induced isoform-specific localization change of the Na+, K+ -ATPase alpha subunit in the synaptic plasma membrane of rat brain. Neurosci Lett 413:42–45

    Article  PubMed  CAS  Google Scholar 

  78. Grillo C, Piroli G, González SL et al (1994) Glucocorticoid regulation of mRNA encoding (Na + K) ATPase alpha 3 and beta 1 subunits in rat brain measured by in situ hybridization. Brain Res 657:83–91

    Article  PubMed  CAS  Google Scholar 

  79. Hamid H, Gao Y, Lei Z et al (2009) Effect of ouabain on sodium pump alpha-isoform expression in an animal model of mania. Prog Neuropsychopharmacol Biol Psychiatry 33:1103–1106

    Article  PubMed  CAS  Google Scholar 

  80. de Carvalho Aguiar P, Sweadner KJ, Penniston JT et al (2004) Mutations in the Na+/K+ -ATPase alpha3 gene ATP1A3 are associated with rapid-onset dystonia parkinsonism. Neuron 43:169–175

    Article  PubMed  Google Scholar 

  81. Moseley AE, Lieske SP, Wetzel RK et al (2003) The Na, K-ATPase alpha 2 isoform is expressed in neurons, and its absence disrupts neuronal activity in newborn mice. J Biol Chem 278:5317–5324

    Article  PubMed  CAS  Google Scholar 

  82. Martín-Vasallo P, Wetzel RK, García-Segura LM et al (2000) Oligodendrocytes in brain and optic nerve express the beta3 subunit isoform of Na, K-ATPase. Glia 31:206–218

    Article  PubMed  Google Scholar 

  83. Sweadner KJ (1992) Overlapping and diverse distribution of Na-K ATPase isozymes in neurons and glia. Can J Physiol Pharmacol 70(Suppl):S255–S259

    PubMed  CAS  Google Scholar 

  84. Fontella FU, Siqueira IR, Vasconcellos AP et al (2005) Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem Res 30:105–111

    Article  PubMed  CAS  Google Scholar 

  85. Liu J, Wang X, Shigenaga MK et al (1996) Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats. FASEB J 10:1532–1538

    PubMed  CAS  Google Scholar 

  86. Namba C, Adachi N, Liu K et al (2002) Suppression of sodium pump activity and an increase in the intracellular Ca2+ concentration by dexamethasone in acidotic mouse brain. Brain Res 957:271–277

    Article  PubMed  CAS  Google Scholar 

  87. Schoner W (2000) Ouabain, a new steroid hormone of adrenal gland and hypothalamus. Exp Clin Endocrinol Diabetes 108:449–454

    Article  PubMed  CAS  Google Scholar 

  88. Bauer N, Muller-Ehmsen J, Kramer U et al (2005) Ouabain-like compound changes rapidly on physical exercise in humans and dogs-effects of β-blockade and angiotensin-converting enzyme inhibition. Hypertension 45:1024–1028

    Article  PubMed  CAS  Google Scholar 

  89. Kölbel F, Schreiber V (1996) The endogenous digitalis-like factor. Mol Cell Biochem 160–161:111–115

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Research Council of Brazil (CNPq), and FINEP/Rede IBN 01.06.0842-00. Leonardo M. Crema was the recipient of a CNPq fellowship.

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Authors and Affiliations

  1. Departamento de Bioquímica, ICBS, Universidade Federal do Rio Grande do Sul, Ramiro Barcelos, 2600, Anexo, 90035-003, Porto Alegre, RS, Brazil

    Leonardo Crema, Michele Schlabitz, Bárbara Tagliari, Aline Cunha, Fabrício Simão, Rachel Krolow, Letícia Pettenuzzo, Christianne Salbego, Deusa Vendite, Angela T. S. Wyse & Carla Dalmaz

  2. Programa de Pós-Graduação em Neurociências, ICBS, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Leonardo Crema, Deusa Vendite & Carla Dalmaz

  3. Programa de Pós-Graduação em Bioquímica, ICBS, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Bárbara Tagliari, Fabrício Simão, Rachel Krolow, Letícia Pettenuzzo, Christianne Salbego, Angela T. S. Wyse & Carla Dalmaz

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  1. Leonardo Crema
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Crema, L., Schlabitz, M., Tagliari, B. et al. Na+, K+ ATPase Activity Is Reduced in Amygdala of Rats with Chronic Stress-Induced Anxiety-Like Behavior. Neurochem Res 35, 1787–1795 (2010). https://doi.org/10.1007/s11064-010-0245-9

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