Table of Contents
International Scholarly Research Notices
Volume 2014, Article ID 690950, 9 pages
http://dx.doi.org/10.1155/2014/690950
Research Article

Metabolic Effects of Social Isolation in Adult C57BL/6 Mice

1Department of Molecular Virology, Immunology and Medical Genetics and the Comprehensive Cancer Center, The Ohio State University, 912 Biomedical Research Tower, 460 West 12th Avenue, Columbus, OH 43210, USA
2Functional Genomics and Translational Neuroscience Lab, Department of Molecular Medicine and Pathology, University of Auckland, Auckland 1142, New Zealand

Received 27 August 2014; Accepted 23 October 2014; Published 26 November 2014

Academic Editor: Isabel C. F. R. Ferreira

Copyright © 2014 Meng Sun et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Berry, V. Bellisario, S. Capoccia et al., “Social deprivation stress is a triggering factor for the emergence of anxiety- and depression-like behaviours and leads to reduced brain BDNF levels in C57BL/6J mice,” Psychoneuroendocrinology, vol. 37, no. 6, pp. 762–772, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Ros-Simó and O. Valverde, “Early-life social experiences in mice affect emotional behaviour and hypothalamic-pituitary-adrenal axis function,” Pharmacology Biochemistry and Behavior, vol. 102, no. 3, pp. 434–441, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. R. J. Katz, “Animal models and human depressive disorders,” Neuroscience & Biobehavioral Reviews, vol. 5, no. 2, pp. 231–246, 1981. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Bartolomucci, P. Palanza, P. Sacerdote et al., “Individual housing induces altered immuno-endocrine responses to psychological stress in male mice,” Psychoneuroendocrinology, vol. 28, no. 4, pp. 540–558, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Guidotti, E. Dong, K. Matsumoto, G. Pinna, A. M. Rasmusson, and E. Costa, “The socially-isolated mouse: A model to study the putative role of allopregnanolone and 5α-dihydroprogesterone in psychiatric disorders,” Brain Research Reviews, vol. 37, no. 1–3, pp. 110–115, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Nonogaki, K. Nozue, and Y. Oka, “Social isolation affects the development of obesity and type 2 diabetes in mice,” Endocrinology, vol. 148, no. 10, pp. 4658–4666, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Sinha and A. M. Jastreboff, “Stress as a common risk factor for obesity and addiction,” Biological Psychiatry, vol. 73, no. 9, pp. 827–835, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. W. Smith, A. Baum, and R. R. Wing, “Stress and weight gain in parents of cancer patients,” International Journal of Obesity, vol. 29, no. 2, pp. 244–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Kim, W.-W. Whang, H.-T. Kim et al., “Expression of neuropeptide Y and cholecystokinin in the rat brain by chronic mild stress,” Brain Research, vol. 983, no. 1-2, pp. 201–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. S. C. Weninger, L. J. Muglia, L. Jacobson, and J. A. Majzoub, “CRH-deficient mice have a normal anorectic response to chronic stress,” Regulatory Peptides, vol. 84, no. 1–3, pp. 69–74, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Bhatnagar and C. Vining, “Facilitation of hypothalamic-pituitary-adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm,” Hormones and Behavior, vol. 43, no. 1, pp. 158–165, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. R. S. Sherwin and L. Sacca, “Effect of epinephrine on glucose metabolism in humans: contribution of the liver,” American Journal of Physiology—Endocrinology and Metabolism, vol. 10, no. 2, pp. E157–E165, 1984. View at Google Scholar · View at Scopus
  13. S. C. Heinrichs, F. Menzaghi, E. M. Pich, R. L. Hauger, and G. F. Koob, “Corticotropin-releasing factor in the paraventricular nucleus modulates feeding induced by neuropeptide Y,” Brain Research, vol. 611, no. 1, pp. 18–24, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. S. C. Heinrichs and D. Richard, “The role of corticotropin-releasing factor and urocortin in the modulation of ingestive behavior,” Neuropeptides, vol. 33, no. 5, pp. 350–359, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. P. J. Currie, “Integration of hypothalamic feeding and metabolic signals: focus on neuropeptide Y,” Appetite, vol. 41, no. 3, pp. 335–337, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Richard, Q. Lin, and E. Timofeeva, “The corticotropin-releasing factor family of peptides and CRF receptors: their roles in the regulation of energy balance,” European Journal of Pharmacology, vol. 440, no. 2-3, pp. 189–197, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Maniam and M. J. Morris, “The link between stress and feeding behaviour,” Neuropharmacology, vol. 63, no. 1, pp. 97–110, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Kyrou and C. Tsigos, “Stress hormones: physiological stress and regulation of metabolism,” Current Opinion in Pharmacology, vol. 9, no. 6, pp. 787–793, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. T. W. Castonguay, “Glucocorticoids as modulators in the control of feeding,” Brain Research Bulletin, vol. 27, no. 3-4, pp. 423–428, 1991. View at Publisher · View at Google Scholar · View at Scopus
  20. M. F. Dallman, N. C. Pecoraro, S. E. la Fleur et al., “Glucocorticoids, chronic stress, and obesity,” Progress in Brain Research, vol. 153, pp. 75–105, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. M. F. Dallman, N. C. Pecoraro, and S. E. La Fleur, “Chronic stress and comfort foods: self-medication and abdominal obesity,” Brain, Behavior, and Immunity, vol. 19, no. 4, pp. 275–280, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. E. Bell, S. Bhatnagar, J. Liang, L. Soriano, T. R. Nagy, and M. F. Dallman, “Voluntary sucrose ingestion, like corticosterone replacement, prevents the metabolic deficits of adrenalectomy,” Journal of Neuroendocrinology, vol. 12, no. 5, pp. 461–470, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Bhatnagar, M. E. Bell, J. Liang, L. Soriano, T. R. Nagy, and M. F. Dallman, “Corticosterone facilitates saccharin intake in adrenalectomized rats: does corticosterone increase stimulus salience?” Journal of Neuroendocrinology, vol. 12, no. 5, pp. 453–460, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. M. F. Dallman, “Stress-induced obesity and the emotional nervous system,” Trends in Endocrinology and Metabolism, vol. 21, no. 3, pp. 159–165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. M. F. Dallman, N. Pecoraro, S. F. Akana et al., “Chronic stress and obesity: a new view of “comfort food”,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 20, pp. 11696–11701, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. E. Leigh Gibson, “Emotional influences on food choice: sensory, physiological and psychological pathways,” Physiology and Behavior, vol. 89, no. 1, pp. 53–61, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. S. J. Torres and C. A. Nowson, “Relationship between stress, eating behavior, and obesity,” Nutrition, vol. 23, no. 11-12, pp. 887–894, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. J. P. Block, Y. He, A. M. Zaslavsky, L. Ding, and J. Z. Ayanian, “Psychosocial stress and change in weight among US adults,” The American Journal of Epidemiology, vol. 170, no. 2, pp. 181–192, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Serlachius, M. Hamer, and J. Wardle, “Stress and weight change in university students in the United Kingdom,” Physiology and Behavior, vol. 92, no. 4, pp. 548–553, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. O. Martí, J. Martí, and A. Armario, “Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure,” Physiology and Behavior, vol. 55, no. 4, pp. 747–753, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Epel, S. Jimenez, K. Brownell, L. Stroud, C. Stoney, and R. Niaura, “Are stress eaters at risk for the metabolic syndrome?” Annals of the New York Academy of Sciences, vol. 1032, pp. 208–210, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. A. A. Stone and K. D. Brownell, “The stress-eating paradox: multiple daily measurements in adult males and females,” Psychology & Health, vol. 9, no. 6, pp. 425–436, 1994. View at Publisher · View at Google Scholar
  33. L. E. Kuo, M. Czarnecka, J. B. Kitlinska, J. U. Tilan, R. Kvetňanský, and Z. Zukowska, “Chronic stress, combined with a high-fat/high-sugar diet, shifts sympathetic signaling toward neuropeptide Y and leads to obesity and the metabolic syndrome,” Annals of the New York Academy of Sciences, vol. 1148, pp. 232–237, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Dodt, P. Lönnroth, J. P. Wellhöner, H. L. Fehm, and M. Elam, “Sympathetic control of white adipose tissue in lean and obese humans,” Acta Physiologica Scandinavica, vol. 177, no. 3, pp. 351–357, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Sominsky and S. J. Spencer, “Eating behavior and stress: a pathway to obesity,” Frontiers in Psychology, vol. 5, p. 434, 2014. View at Publisher · View at Google Scholar
  36. T. I. Takemoto, T. Suzuki, and T. Miyama, “Effects of isolation on mice in relation to age and sex,” The Tohoku Journal of Experimental Medicine, vol. 117, no. 2, pp. 153–165, 1975. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Sakakibara, A. Suzuki, A. Kobayashi et al., “Social isolation stress induces hepatic hypertrophy in C57BL/6J mice,” Journal of Toxicological Sciences, vol. 37, no. 5, pp. 1071–1076, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. T. R. Nagy, D. Krzywanski, J. Li, S. Meleth, and R. Damond, “Effect of group vs. single housing on phenotypic variance in C57BL/6J mice,” Obesity Research, vol. 10, no. 5, pp. 412–415, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Guo, C. F. Wu, W. Liu, J. Y. Yang, and D. Chen, “Sex difference in psychological behavior changes induced by long-term social isolation in mice,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 28, no. 1, pp. 115–121, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Kaji and K. Nonogaki, “Contribution of central SGK-1 to the acute phase responses of mice to social isolation,” Frontiers in Bioscience—Elite, vol. 2, no. 4, pp. 1355–1361, 2010. View at Google Scholar · View at Scopus
  41. K. Yamada, H. Ohki-Hamazaki, and K. Wada, “Differential effects of social isolation upon body weight, food consumption, and responsiveness to novel and social environment in bombesin receptor subtype-3 (BRS-3) deficient mice,” Physiology & Behavior, vol. 68, no. 4, pp. 555–561, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Bartolomucci, A. Cabassi, P. Govoni et al., “Metabolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress,” PLoS ONE, vol. 4, no. 1, Article ID e4331, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Arita, S. Kihara, N. Ouchi et al., “Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity,” Biochemical and Biophysical Research Communications, vol. 257, no. 1, pp. 79–83, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Cao, E.-J. D. Lin, M. C. Cahill, C. Wang, X. Liu, and M. J. During, “Molecular therapy of obesity and diabetes by a physiological autoregulatory approach,” Nature Medicine, vol. 15, no. 4, pp. 447–454, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Cao, X. Liu, E.-J. D. Lin et al., “Environmental and genetic activation of a brain-adipocyte BDNF/leptin axis causes cancer remission and inhibition,” Cell, vol. 142, no. 1, pp. 52–64, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. H. Rasmussen, “Obesity, growth hormone and weight loss,” Molecular and Cellular Endocrinology, vol. 316, no. 2, pp. 147–153, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Frystyk, C. Skjaerbaek, E. Vestbo, S. Fisker, and H. Orskov, “Circulating levels of free insulin-like growth factors in obese subjects: the impact of type 2 diabetes,” Diabetes/Metabolism Research and Reviews, vol. 15, no. 5, pp. 314–322, 1999. View at Google Scholar
  48. S. Y. Nam, E. J. Lee, K. R. Kim et al., “Effect of obesity on total and free insulin-like growth factor (IGF)-1, and their relationship to IGF-binding protein (BP)-1, IGFBP-2, IGFBP-3, insulin, and growth hormone,” International Journal of Obesity, vol. 21, no. 5, pp. 355–359, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. J. M. Gómez, F. J. Maravall, N. Gómez, M. Á. Navarro, R. Casamitjana, and J. Soler, “The IGF-I system component concentrations that decrease with ageing are lower in obesity in relationship to body mass index and body fat,” Growth Hormone and IGF Research, vol. 14, no. 2, pp. 91–96, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. M. H. Rasmussen, J. Frystyk, T. Andersen, L. Breum, J. S. Christiansen, and J. Hilsted, “The impact of obesity, fat distribution, and energy restriction on insulin-like growth factor-1 (IGF-1), IGF-binding protein-3, insulin, and growth hormone,” Metabolism: Clinical and Experimental, vol. 43, no. 3, pp. 315–319, 1994. View at Publisher · View at Google Scholar · View at Scopus
  51. E. S. Epel, “Psychological and metabolic stress: a recipe for accelerated cellular aging?” Hormones, vol. 8, no. 1, pp. 7–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Bernton, D. Hoover, R. Galloway, and K. Popp, “Adaptation to chronic stress in military trainees. Adrenal androgens, testosterone, glucocorticoids, IGF-1, and immune function,” Annals of the New York Academy of Sciences, vol. 774, pp. 217–231, 1995. View at Google Scholar · View at Scopus
  53. N. Uschold-Schmidt, K. D. Nyuyki, A. M. Füchsl, I. D. Neumann, and S. O. Reber, “Chronic psychosocial stress results in sensitization of the HPA axis to acute heterotypic stressors despite a reduction of adrenal in vitro ACTH responsiveness,” Psychoneuroendocrinology, vol. 37, no. 10, pp. 1676–1687, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. S. O. Reber, L. Birkeneder, A. H. Veenema et al., “Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: Implications and mechanisms,” Endocrinology, vol. 148, no. 2, pp. 670–682, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. E. J. Lin, M. Sun, E. Y. Choi, D. Magee, C. W. Stets, and M. J. During, “Social overcrowding as a chronic stress model that increases adiposity in mice,” Psychoneuroendocrinology, vol. 51, pp. 318–330, 2015. View at Publisher · View at Google Scholar
  56. B. O. V. Shum, C. R. Mackay, C. Z. Gorgun et al., “The adipocyte fatty acid-binding protein aP2 is required in allergic airway inflammation,” The Journal of Clinical Investigation, vol. 116, no. 8, pp. 2183–2192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. K. E. Wellen and G. S. Hotamisligil, “Obesity-induced inflammatory changes in adipose tissue,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1785–1788, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Cvijic, I. Lakic, P. Vujovic et al., “Single and combined effects of acute and chronic non-thermal stressors on rat interscapular brown adipose tissue metabolic activity,” Archives of Biological Science Belgrade, vol. 65, no. 3, pp. 919–927, 2013. View at Google Scholar
  59. T. Oka, K. Oka, and T. Hori, “Mechanisms and mediators of psychological stress-induced rise in core temperature,” Psychosomatic Medicine, vol. 63, no. 3, pp. 476–486, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Motoyama, Y. Nakai, T. Miyashita et al., “Isolation stress for 30 days alters hepatic gene expression profiles, especially with reference to lipid metabolism in mice,” Physiological Genomics, vol. 37, no. 2, pp. 79–87, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. P. A. Volden, E. L. Wonder, M. N. Skor et al., “Chronic social isolation is associated with metabolic gene expression changes specific to mammary adipose tissue,” Cancer Prevention Research, vol. 6, no. 7, pp. 634–645, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. L. A. Hilakivi, M. Ota, and R. G. Lister, “Effect of isolation on brain monoamines and the behavior of mice in tests of exploration, locomotion, anxiety and behavioral “despair”,” Pharmacology Biochemistry and Behavior, vol. 33, no. 2, pp. 371–374, 1989. View at Publisher · View at Google Scholar · View at Scopus