Aqueous Extracts of Walnut (Juglans regia L.) and Nelumbo nucifera Seeds Reduce Plasma Corticosterone Levels, Gastric Lesions, and c-fos Immunoreactivity in Chronic Restraint-stressed Mice

  • Kim, Dae-Won (Central Research Center, Natural F&P Co., Ltd.) ;
  • Hwang, In-Koo (Department of Anatomy and Cell Biology, College of Veterinary Medicine and BK21 Program for Veterinary Science, Seoul National University) ;
  • Yoo, Ki-Yeon (Department of Anatomy and Neurobiology, College of Medicine, Hallym University) ;
  • Li, Hua (Department of Anatomy and Neurobiology, College of Medicine, Hallym University) ;
  • Kang, Il-Jun (Department of Food Science and Nutrition, Division of Life Science, Hallym University) ;
  • Moon, Won-Kuk (Central Research Center, Natural F&P Co., Ltd.) ;
  • Won, Moo-Ho (Department of Anatomy and Neurobiology, College of Medicine, Hallym University) ;
  • Kim, Seok-Joong (Department of Food and Nutrition, Dongduk Women's University) ;
  • Han, Dae-Seok (Food Processing and Post-harvest Technology Division, Korea Food Research Institute) ;
  • Kim, Dong-Woo (Central Research Center, Natural F&P Co., Ltd.)
  • Published : 2008.08.31

Abstract

In the present study, chronic effects of the hot water extracts of walnut seed (Juglans regia L.) (WSE) and Nelumbo nucifera seed (NSE) were investigated in mice exposed to 2 hr of restraint stress each day for 4 weeks. Corticosterone levels in serum were significantly increased in the vehicle-treated stressed group ($25\;{\mu}g/dL$) compared to that in the control group ($13\;{\mu}g/dL$). This stress induced gastric redness and lesions. However, treatment with WSE and/or NSE significantly protected the stomach from this lesion by 50-60% compared to that in the vehicletreated group. In the amygdala, the administration of WSE and/or NSE also reduced the immediate early gene (c-fos) expression by 70-90% vs. the vehicle-treated group. These suggest that WSE and/or NSE may reduce the appearance of symptoms induced by stress and these materials are useful as anti-stress foods, as natural products tend to be relatively safe compared to chemical products.

Keywords

References

  1. Andrews G, Sanderson K, Slade T, Isakidis C. Why does the burden of disease persist? Relating the burden of anxiety and depression to effectiveness of treatment. B. World Health Organ. 78: 446-454 (2000)
  2. Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. J. Am. Med. Assoc. 267: 1244-1252 (1992) https://doi.org/10.1001/jama.267.9.1244
  3. Takahashi M, Tokuyama S, Kaneto H. Anti-stress effect of ginseng on the inhibition of the development of morphine tolerance in stressed mice. Jpn. J. Pharmacol. 59: 399-404 (1992) https://doi.org/10.1254/jjp.59.399
  4. Bhattacharya SK, Muruganandam AV. Adaptogenic activity of Withania somnifera: An experimental study using a rat model of chronic stress. Pharmacol. Biochem. Be. 75: 547-555 (2003) https://doi.org/10.1016/S0091-3057(03)00110-2
  5. Tan-Lee BS, Yu GY, Kim K, Han S, Han J, Lee GS, Kim ES, Lee CJ, Ryu JH, Cheong JH. Anti-stress effect of artichoke juice in SD rats and ICR mice. Food Sci. Biotechnol. 13: 302-308 (2004)
  6. Lee GS, Choi JY, Ko HS, Tan-Lee BS, Yu GY, Jeong CW, Park HG, Kim MK, Ryu JH, Jung IK, Cheong JH. Stree-reducing effects of brown rice koji. Food Sci. Biotechnol. 15: 63-69 (2006)
  7. Kaneko H, Nakanish K, Murakami A, Kaidoh H, Kuwashima K. The acute effects of massive dose of red ginseng on healthy adults under the condition of cold stress. Ginseng Rev. 22: 20-24 (1996)
  8. Kim DH, Jung JS, Moon YS, Sung JH, Suh HW, Kim YH, Song DK. Inhibition of intracerebroventricular injection stress-induced plasma corticosterone levels by intracerebroventricularly administered compound K, a ginseng saponin metabolite, in mice. Biol. Pharm. Bull. 26: 1035-1038 (2003) https://doi.org/10.1248/bpb.26.1035
  9. Choi SS, Lee JK, Suh HW. Effect of ginsenosides administered intrathecally on the antinociception induced by cold water swimming stress in the mouse. Biol. Pharm. Bull. 26: 858-861 (2003) https://doi.org/10.1248/bpb.26.858
  10. Xu R, Yokoyama WH, Irving D, Rein D, Walzem RL, German JB. Effect of dietary catechin and vitamin E on aortic fatty streak accumulation in hypercholesterolemic hamsters. Atherosclerosis 137: 29-36 (1998) https://doi.org/10.1016/S0021-9150(97)00248-7
  11. Davis P, Valacchi G, Pagnin E, Shao Q, Gross HB, Calo L, Yokoyama W. Walnuts reduce aortic ET-1 mRNA levels in hamsters fed a high-fat, atherogenic diet. J. Nutr. 136: 428-432 (2006) https://doi.org/10.1093/jn/136.2.428
  12. Fukuda T, Ito H, Yoshida T. Antioxidative polyphenols from walnuts (Juglans regia L.). Phytochemistry 63: 795-801 (2003) https://doi.org/10.1016/S0031-9422(03)00333-9
  13. Sohn DH, Kim YC, Oh SH, Park EJ, Li X, Lee BH.Hepatoprotective and free radical scavenging effects of Nelumbo nucifera. Phytomedicine 10: 165-169 (2003) https://doi.org/10.1078/094471103321659889
  14. Mukherjee PK, Saha K, Saha BP. Effect of Nelumbo nucifera rhizome extract on blood sugar level in rats. J. Ethnopharmacol. 58: 207-213 (1997) https://doi.org/10.1016/S0378-8741(97)00107-4
  15. Ono Y, Hattori E, Fukaya Y, Imai S, Ohizumi Y. Anti-obesity effect of Nelumbo nucifera leaves extract in mice and rats. J. Ethnopharmacol. 106: 238-244 (2006) https://doi.org/10.1016/j.jep.2005.12.036
  16. Bayne K. Revised guide for the care and use of laboratory animals available. The Physiologist 39: 208-211 (1996)
  17. Selye H. History of the stress concept. pp. 7-36. In: Handbook of Stress. Goldberg L, Brenitz S (eds). The Free Press, New York, NY, USA (1993)
  18. Hurst MW, Jenkins CD, Rose RM. The relatioin of psychological stress to onset of medical illness. Annu. Rev. Med. 27: 301-312 (1976) https://doi.org/10.1146/annurev.me.27.020176.001505
  19. Barsky AJ, Wyshak G, Klerman GL. Medical and psychiatric determinants of outpatient medical utilization. Med. Care 24: 548-560 (1986) https://doi.org/10.1097/00005650-198606000-00009
  20. Breier A, Albus M, Picker D, Zahn TP, Wolkowitz OM, Paul SM. Controllable and uncontrollable stress in humans: Alterations in mood and neuroendocrine and psychophysiological function. Am. J. Psychiat. 144: 11-19 (1987)
  21. Balzer D, Hughes D, George LK. Stress life events and the onset of a generalized anxiety syndrome. Am. J. Psychiat. 144: 9-18 (1987)
  22. Lopez-Calderon A, Ariznavarreta C, Gonzalez-Quijano MI, Tresguerres JA, Calderon MD. Stress induced changes in testis function. J. Steroid Biochem. 40: 473-479 (1991) https://doi.org/10.1016/0960-0760(91)90217-S
  23. Millan S, González-Quijano MI, Giordano M, Soto L, Martin AI, Lopez-Calderon A. Short and long restraint differentially affect humoral and cellular immune functions. Life Sci. 59: 1431-1442 (1996) https://doi.org/10.1016/0024-3205(96)00471-7
  24. Armario A, Restrepo C, Castrellanos JM, Balasch J. Dissociation between adrenocorticotropin and corticosterone responses to restraint after previous chronic exposure to stress. Life Sci. 36: 2085-2092 (1985) https://doi.org/10.1016/0024-3205(85)90304-2
  25. Djordjeviæ J, Cvijiæ G, Davidoviæ V. Different activation of ACTH and corticosterone release in response to various stressors in rats. Physiol. Res. 52: 67-72 (2003)
  26. Akpinar D, Yargicoglu P, Derin N, Aslan M, Agar A. Effect of aminoguanidine on visual evoked potentials (VEPs), antioxidant status, and lipid peroxidation in rats exposed to chronic restraint stress. Brain Res. 1186: 87-94 (2007) https://doi.org/10.1016/j.brainres.2007.09.066
  27. An SM, Park CH, Heo JC, Park JY, Woo SU, Seo JH, Lee MS, Cho KJ, Cho HS, Shin HM, Lee SH. Gastrodia elata Blume protects against stress-induced gastric mucosal lesions in mice. Int. J. Mol. Med. 20: 209-215 (2007)
  28. Ohta Y, Chiba S, Tada M, Imai Y, Kitagawa A. Development of oxidative stress and cell damage in the liver of rats with waterimmersion restraint stress. Redox Rep. 12: 139-147 (2007) https://doi.org/10.1179/135100007X200218
  29. Liu S, Zhou W, Liu H, Yang G, Zhao W. Electroacupuncture attenuates morphine withdrawal signs and c-fos expression in the central nucleus of the amygdala in freely moving rats. Brain Res. 1044: 155-163 (2005) https://doi.org/10.1016/j.brainres.2005.02.075
  30. Trneckova L, Armario A, Hynie S, Sida P, Klenerova V. Differences in the brain expression of c-fos mRNA after restraint stress in Lewis compared to Sprague-Dawley rats. Brain Res. 1077: 7-15 (2006) https://doi.org/10.1016/j.brainres.2006.01.029
  31. Badowska-Szalewska E, Ludkiewicz B, Domaradzka-Pytel B, Dziewiatkowski J, Spodnik JH, Moryœ J. The immunoreactivity of c-Fos, NGF and its receptor TrkA after open-field exposure in the central and medial nuclei of the rat amygdala. Folia Morphol. (Warsz) 65: 145-151 (2006)
  32. Rotllant D, Nadal R, Armario A. Differential effects of stress and amphetamine administration on fos-like protein expression in corticotropin releasing factor-neurons of the rat brain. Dev. Neurobiol. 67: 702-714 (2007) https://doi.org/10.1002/dneu.20345
  33. Chen X, Herbert J. Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: Correlations with cardiovascular, hypothermic, and endocrine responses. Neuroscience 64: 675-685 (1995) https://doi.org/10.1016/0306-4522(94)00532-A
  34. Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64: 477-505 (1995) https://doi.org/10.1016/0306-4522(94)00355-9
  35. Kubo T, Okatani H, Nishigori Y, Hagiwara Y, Fukumori R, Goshima Y. Involvement of the medial amygdaloid nucleus in restraint stressinduced pressor responses in rats. Neurosci. Lett. 354: 84-86 (2004) https://doi.org/10.1016/j.neulet.2003.09.061
  36. Fukuda T, Ito H, Yoshida T. Effect of the walut polyphenol fraction on oxidative stress in type 2 diabetes mice. BioFactors 21: 251-253 (2004) https://doi.org/10.1002/biof.552210148
  37. Chen Y, Fan G, Wu H, Wu Y, Mitchell A. Separation, identification, and rapid determination of liensine, isoliensinine, and neferine from embryo of the seed of Nelumbo nucifera GAERTN. by liquid chromatography coupled to diode array detector and tandem mass spectrometry. J. Pharmaceut. Biomed. 43: 99-104 (2007) https://doi.org/10.1016/j.jpba.2006.06.016