Abstract
The present study was designed to investigate the antistress effect of furosemide (sodium potassium chloride co-transporter inhibitor) in immobilization and foot-shock stress-induced behavioral alterations in the mice. Acute stress was induced in Swiss albino mice either by applying electric foot shocks of 0.6-mA intensity of 1-s duration with 30-s inter-shock interval for 1 h or immobilizing for 150 min. The acute stress-induced behavioral changes were assessed by using actophotometer, hole board, open-field, and social interaction tests. Biochemically, the corticosterone levels were estimated in the serum as a biomarker of hypothalamus-pituitary-adrenal (HPA) axis. Acute stress resulted in the development of behavioral alterations and elevation of the corticosterone levels. Intraperitoneal administration of furosemide (25 and 50 mg/kg) significantly attenuated immobilization and foot-shock stress-induced behavioral changes along with normalization of the corticosterone levels. It may be concluded that furosemide produces beneficial effects in reestablishing the behavioral and biochemical alterations in immobilization and foot-shock-induced acute stress in mice.
Similar content being viewed by others
References
Agrawal A, Jaggi AS, Singh N (2011) Pharmacological investigations on adaptation in rats subjected to cold water immersion stress. Physiol Behav 103:321–329
Akil HA, Morano MI (1995) Stress. In: Bloom FE, Kupfer DJ (eds) Psychopharmacology: the fourth generation in progress. Raven Press, New York, pp 773–785
Aoki E, Shibasaki T, Kawana S (2003) Intermittent foot shock stress prolongs the telogen stage in the hair cycle of mice. Exp Dermatol 12:371–377
Bali A, Jaggi AS (2013) Angiotensin as stress mediator: role of its receptor and interrelationships among other stress mediators and receptors. Pharmacol Res 76:49–57
Bali A, Jaggi AS (2014) Multifunctional aspects of allopregnanolone in stress and related disorders. Prog Neuropsychopharmacol Biol Psychiatry 48:64–78
Bali A, Singh N, Jaggi AS (2013) Investigations into mild electric foot shock stress-induced cognitive enhancement: possible role of angiotens in neuropeptides. J Renin-Angiotensin-Aldosterone Syst 14(3):197–203
Bali A, Randhawa PK, Jaggi AS (2014) Interplay between RAS and opioids: opening the Pandora of complexities. Neuropeptides 48:249–256
Beck J, Lenart B, Kintner DB, Sun D (2003) Na-K-Cl cotransporter contributes to glutamate-mediated excitotoxicity. J Neurosci 23(12):5061–5068
Bhatia N, Jaggi AS, Singh N, Anand P, Dhawan R (2011) Adaptogenic potential of curcumin in experimental chronic stress and chronic unpredictable stress-induced memory deficits and alterations in functional homeostasis. J Nat Med 65:532–543
Brandt C, Nozadze M, Heuchert N, Rattka M, Loscher W (2010) disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy. The. J Neurosci 25:8602–8612
Brown GR, Nemes C (2008) The exploratory behavior of rats in the hole board apparatus: is head-dipping a valid measure of neophilia. Behav Process 78:442–448
Brumback AC, Staley DW (2008) Thermodynamic regulation of NKCC1-mediated Cl- co-transport underlies plasticity of GABAA signaling in neonatal neurons. J Neurosci 6:1301–1312
Busquet P, Nguyen NK, Schmid E, Tanimoto N, Seeliger MW, Ben-Yosef T, Mizuno F, Akopian A, Striessnig J, Singewald N (2010) CaV1.3 L-type Ca2+ channels modulate depression-like behaviour in mice independent of deaf phenotype. Int J Neuropsychopharmacol 13:499–513
Creel S, Winnie JA Jr, Christianson D (2009) Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. Proc Natl Acad Sci U S A 106(30):12388–12393
Doron R, Lotan D, Versano Z, Benatav L, Franko M, Armoza S, Kately N, Rehavi M (2014) Escitalopram or novel herbal mixture treatments during or following exposure to stress reduce anxiety-like behavior through corticosterone and BDNF modifications. PLoS One 9:e91455
Francis GS, Siegel RM, Goldsmith SR, Olivari MT, Levine BT, Cohn JN (1985) Acute vasoconstrictor response to intravenous furosemide in patients with chronic congestive heart failure: activation of the neurohumoral axis. Ann Intern Med 103(1):1–6
Geck PC, Pietrzyk BC, Burckhardt B (1980) Pfeiffer, Heinz E. Electrically silent cotransport of Na+, K+ and Cl- in Ehrlich cells. Biochim Biophys Acta 600:432–447
Glick D, Vonredlich D, Levine S (1964) Fluorometric determination of corticosterone and cortisol in 0.02–0.05 milliliters of plasma or submilligram samples of adrenal tissue. Endocrinology 74:653–655
Granados-Soto V, Arguelles CF, Alvarez-Leefmans FJ (2005) Peripheral and central antinociceptive action of Na–K–2Cl cotransporter blockers on formalin-induced nociception in rats. Pain 114:231–238
Haas M, Forbush B (2000) The Na-K-Cl cotransporter of secretory epithelia. Annu Rev Physiol 62:515–534
Haj-Mirzaian A, Ostadhadi S, Kordjazy N, Dehpour AR, Mehr SE (2014) Opioid/NMD A receptors blockade reverses the depressant-like behavior of foot shock stress in the mouse forced swimming test. European J Pharmacol. Article in press
Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuro-Psychopharmacol Biol Psychiatry 29:1201–1213
Jaggi AS, Bhatia N, Kumar N, Singh N, Anand P, Dhawan R (2011) A review on animal models for screening potential anti-stress agents. Neurol Sci 32:993–1005
Kasuga S, Ushijima M, Morihara N, Itakura Y, Nakata Y (1999) Effect of aged garlic extract (AGE) on hyperglycemia induced by immobilization stress in mice. Jpn J Pharmacol 114:191–197
Kaur R, Jaggi AS, Singh N (2009) Studies on effect of stress preconditioning in restrain stress induced behavioral alterations. Yakugaku Zasshi 130:215–221
Krystal AD, Sutherland J, Hochman DW (2012) Loop diuretics have anxiolytic effects in rat models of conditioned anxiety. PLoS ONE 7:e35417
Kumar N, Singh N, Jaggi AS (2012) Anti-stress effects of cilnidipine and nimodipine in immobilization subjected mice. Physiol Behav 105:1148–1155
Kvetnansky R, Mikulaj L (1970) Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology 87:738–743
Kvetnansky R, McCarty R, Thoa NB, Lake CR, Kopin IJ (1979) Sympatho-adrenal responses of spontaneously hypertensive rats to immobilization stress. Am J Physiol 236:H457–H462
Lim TS, Putt N, Safranski D, Chung C, Watson RR (1981) Effect of vitamin E on cell mediated immune responses and serum corticosterone in young and maturing mice. Immunology 44:289–295
Maguire J, Salpekar JA (2013) Stress, seizures, and hypothalamic–pituitary–adrenal axis targets for the treatment of epilepsy. Epilepsy Behav 26:352–362
Manchanda RK, Jaggi AS, Singh N (2011) Ameliorative potential of sodium cromoglycate and diethyldithiocarbamic acid in restraint stress-induced behavioral alterations in rats. Pharmacol Rep 63:54–63
Nardou R, Ben-Ari Y, Khalilov I (2009) Bumetanide, an NKCC1 antagonist, does not prevent formation of epileptogenic focus but blocks epileptic focus seizures in immature rat hippocampus. J Neurophysiol 101:2878–2888
Nugent BM, Valenzuela CV, Simons TJ, McCarthy MM (2012) Kinases SPAK and OSR1 are upregulated by estradioland activate NKCC1 in the developing hypothalamus. J Neurosci 32(2):593–598
Okabe A, Ohno K, Toyoda H, Yokokura M, Sato K, Fukuda A (2002) Amygdala kindling induces up-regulation of mRNA for Na+K+2Cl- cotransporter, in the rat piriform cortex. Neurosci Res 44:225–229
Oriaifo SE, Otokiti I, Omogbai EK (2012) The effect of furosemide on experimentally-induced seizures in mice. J Clin Med Res 4(7):89–93
Osterlund C, Spencer RL (2011) Corticosterone pretreatment suppresses stress-induced hypothalamic-pituitary-adrenal axis activity via multiple actions that vary with time, site of action, and de novo protein synthesis. J Endocrinol 208(3):311–322
Pacak K, Kvetnansky R, Palkovits M, Fukuhara K, Yadid G, Kopin IJ, Goldstein DS (1993) Adrenalectomy augments in-vivo release of norepinephrine in the paraventricular nucleus during immobilization stress. Endocrinology 133:1404–1410
Pedersen SF, O’Donnell ME, Anderson SE, Cala PM (2006) Physiology and pathophysiology of Na+/H+ exchange and Na + -K+ -2Cl- cotransport in the heart, brain, and blood. Am J Physiol Regul Integr Comp Physiol 291(1):R1–R25
Pitcher HM, Cervero F (2010) Role of the NKCC1 co-transporter in sensitization of spinal nociceptive neurons. Pain 151:756–762
Rabasa C, Muñoz-Abellána C, Daviua N, Nadal R, Armario A (2011) Repeated exposure to immobilization or two different foot shock intensities reveals differential adaptation of the hypothalamic–pituitary–adrenal axis. Physiol Behav 103:125–133
Ravindran R, Devi RS, Samson J, Senthilvelan M (2005) Noise-stress-induced brain neurotransmitter changes and the effect of Ocimum sanctum (Linn) treatment in albino rats. J Pharmacol Sci 98:354–360
Roberts PA, Pollay M, Engles C, Pendleton B, Reynolds E, Stevens FA (1987) Effect on intracranial pressure of furosemide combined with varying doses and administration rates of mannitol. J Neurosurg 66:440–446
Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Rev Neurosci 10:423–433
Russell JM (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80:211–276
Su G, Haworth RA, Dempsey RJ, Sun D (2000) Regulation of Na + -K + -Cl- cotransporter in primary astrocytes by dibutyryl cAMP and high [K(+)](o). Am J Physiol 279:1710–1721
Ternacle J, Gallet R, Cognet T, Gueret P, Teiger E, Dubois-Randé JL, Lim P (2013) Should furosemide be avoided in acute right ventricular myocardial infarction? Ann Cardiol Angeiol (Paris) 62(2):95–100
Thapaliya K, Bhandary A, Basnet S, Aryal B (2013) Clinical status of furosemide on liver cirrhosis with portal hypertension and ascites. J Chitwan Med Coll 3(3):65–66
Wallace BK, Jelks KA, O’Donnell ME (2012) Ischemia-induced stimulation of cerebral microvascular endothelial cell Na-K-Cl cotransport involves p38 and JNK MAP kinases. Am J Physiol Cell Physiol 302:C505–C517
Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzakia H, Ogawaa T, Moric N, Fukudab A, Satoa K (2002) Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Dev Brain Res 139:59–66
Xie Z, Currie KP, Cahill AL, Fox AP (2003) Role of Cl- co-transporters in the excitation produced by GABAA receptors in juvenile bovine adrenal chromaffin cells. J Neurophysiol 90(6):3828–3837
Ye Z, Li D, Byun HS, Li L, Pan H (2012) NKCC1 upregulation disrupts chloride homeostasis in the hypothalamus and increases neuronal activity–sympathetic drive in hypertension. J Neurosci 32(25):8560–8568
Zemkova HW, Bjelobaba I, Tomic M, Zemkova H, Stojilkovic SS (2008) Molecular, pharmacological and functional properties of GABA(A) receptors in anterior pituitary cells. J Physiol 586(13):3097–3111
Acknowledgments
The authors are grateful to the Department of Pharmaceutical Sciences and Drug Research, Punjabi University, Patiala, India, for supporting this study and providing technical facilities for the work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kaur, A., Bali, A., Singh, N. et al. Investigating the stress attenuating potential of furosemide in immobilization and electric foot-shock stress models in mice. Naunyn-Schmiedeberg's Arch Pharmacol 388, 497–507 (2015). https://doi.org/10.1007/s00210-015-1084-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00210-015-1084-7