Resistance to early-life stress in mice: Effects of genetic background and stress duration

Frontiers in Behavioral Neuroscience

Volumn , Issue APRIL, 2011, Pages

  Savignac, Hélène M ^a,b   Dinan, Timothy G ^a,b   Cryan, John F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Anxiety; Behavior; Genetics impact; Maternal separation; Mice; Resistance; Stress

Indexed keywords

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BAGG ALBINO MOUSE; BEHAVIOR CHANGE; BRAIN GUT AXIS; C57BL 6 MOUSE; COGNITION; COLON LENGTH; CONTROLLED STUDY; DEFECATION; DEPRESSION; DIGESTIVE TRACT PARAMETERS; EARLY LIFE STRESS; FEMALE; FORCED SWIMMING TEST; MALADJUSTMENT; MALE; MATERNAL DEPRIVATION; MAZE TEST; MOUSE; NERVOUS SYSTEM FUNCTION; NEWBORN; NONHUMAN; OPEN FIELD TEST; TASK PERFORMANCE;

EID: 84855248138     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2011.00013     Document Type: Article

References (89)

1. Anisman, H., Merali, Z., and Stead, J. D. (2008). Experiential and genetic contributions to depressive-and anxiety-like disorders: clinical and experimental studies. Neurosci. Biobehav. Rev. 32, 1185-1206.
2. Anisman, H., Zaharia, M. D., Meaney, M. J., and Merali, Z. (1998). Do early-life events permanently alter behavioral and hormonal responses to stressors? Int. J. Dev. Neurosci. 16, 149-164.
3. Bair, M. J., Robinson, R. L., Katon, W., and Kroenke, K. (2003). Depression and pain comorbidity: a literature review. Arch. Intern. Med. 163, 2433-2445.
4. Barone, F. C., Barton, M. E., White, R. F., Legos, J. J., Kikkawa, H., Shimamura, M., Kuratani, K., and Kinoshita, M. (2008). Inhibition of phosphodiesterase type 4 decreases stress induced defecation in rats and mice. Pharmacology 81, 11-17.
5. Barreau, F., Ferrier, L., Fioramonti, J., and Bueno, L. (2007). New insights in the etiology and pathophysiology of irritable bowel syndrome: contribution of neonatal stress models. Pediatr. Res. 62, 240-245.
6. Bartolomucci, A., Palanza, P., Sacerdote, P., Panerai, A. E., Sgoifo, A., Dantzer, R., and Parmigiani, S. (2005). Social factors and individual vulnerability to chronic stress exposure. Neurosci. Biobehav. Rev. 29, 67-81.
7. Belzung, C., and Griebel, G. (2001). Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav. Brain Res. 125, 141-149
8. Bercik, P., Wang, L., Verdu, E. F., Mao, Y. K., Blennerhassett, P., Khan, W. I., Kean, I., Tougas, G., and Collins, S. M. (2004). Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology 127, 179-187
9. Browne, C. A., Clarke, G., Dinan, T. G., and Cryan, J. F. (2011). Differential stress induced alterations in tryptophan hydroxylase activity and serotonin turnover in two inbred mouse strains. Neuropharmacology 60, 683-691.
10. Cabib, S., Puglisi-Allegra, S., and D'Amato, F. R. (1993). Effects of postnatal stress on dopamine mesolimbic system responses to aversive experiences in adult life. Brain Res. 604, 232-239
11. Calatayud, F., and Belzung, C. (2001). Emotional reactivity in mice, a case of nongenetic heredity? Physiol. Behav. 74, 355-362.
12. Caldji, C., Diorio, J., Anisman, H., and Meaney, M. J. (2004). Maternal behavior regulates benzodiazepine/ GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology 29, 1344-1352.
13. Carpenter, L. L., Carvalho, J. P., Tyrka, A. R., Wier, L. M., Mello, A. F., Mello, M. F., Anderson, G. M., Wilkinson, C. W., and Price, L. H. (2007). Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol. Psychiatry 62, 1080-1087.
14. Cervo, L., Canetta, A., Calcagno, E., Burbassi, S., Sacchetti, G., Caccia, S., Fracasso, C., Albani, D., Forloni, G., and Invernizzi, R. W. (2005). Genotype-dependent activity of tryptophan hydroxylase-2 determines the response to citalopram in a mouse model of depression. J. Neurosci. 25, 8165-8172.
15. Charney, D. S., and Manji, H. K. (2004). Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention. Sci. STKE 2004, re5.
16. Coates, M. D., Johnson, A. C., Greenwood Van Meerveld, B., and Mawe, G. M. (2006). Effects of serotonin transporter inhibition on gastrointestinal motility and colonic sensitivity in the mouse. Neurogastroenterol. Motil. 18, 464-471.
17. Crawley, J. N. (2008). Behavioral phenotyping strategies for mutant mice. Neuron 57, 809-818.
18. Cryan, J. F., Dalvi, A., Jin, S. H., Hirsch, B. R., Lucki, I., and Thomas, S. A. (2001). Use of dopamine-beta-hydroxylase deficient mice to determine the role of norepinephrine in the mechanism of action of antidepressant drugs. J. Pharmacol. Exp. Ther. 298, 651-657
19. Cryan, J. F., and Holmes, A. (2005). The ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov. 4, 775-790.
20. Cryan, J. F., Markou, A., and Lucki, I. (2002). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci. 23, 238-245.
21. Cryan, J. F., and Mombereau, C. (2004). In search of a depressed mouse: utility of models for studying depression-related behavior in genetically modified mice. Mol. Psychiatry 9, 326-357.
22. Cryan, J. F., Valentino, R. J., and Lucki, I. (2005). Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci. Biobehav. Rev. 29, 547-569.
23. D'Amato, F. R., Cabib, S., Puglisi-Allegra, S., Patacchioli, F. R., Cigliana, G., Maccari, S., and Angelucci, L. (1992). Effects of acute and repeated exposure to stress on the hypothalamopituitary-adrenocortical activity in mice during postnatal development. Horm. Behav. 26, 474-485.
24. D'Amato, F. R., Cabib, S., Ventura, R., and Orsini, C. (1998). Long-term effects of postnatal manipulation on emotionality are prevented by maternal anxiolytic treatment in mice. Dev. Psychobiol. 32, 225-234.
25. Dinan, T. G. (2005). Stress: the shared common component in major mental illnesses. Eur. Psychiatry 20(Suppl. 3), S326-S328.
26. Dinan, T. G., Cryan, J., Shanahan, F., Keeling, P. W., and Quigley, E. M. (2010). IBS: an epigenetic perspective. Nat. Rev. Gastroenterol. Hepatol. 7, 465-471.
27. Drake, A. J., Tang, J. I., and Nyirenda, M. J. (2007). Mechanisms underlying the role of glucocorticoids in the early life programming of adult disease. Clin. Sci. 113, 219-232.
28. Engler, H., Engler, A., Bailey, M. T., and Sheridan, J. F. (2005). Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice. J. Neuroimmunol. 163, 110-119.
29. Eriksson, E. M., Andren, K. I., Eriksson, H. T., and Kurlberg, G. K. (2008). Irritable bowel syndrome subtypes differ in body awareness, psychological symptoms and biochemical stress markers. World J. Gastroenterol. 14, 4889-4896.
30. Franklin, T. B., Russig, H., Weiss, I. C., Graff, J., Linder, N., Michalon, A., Vizi, S., and Mansuy, I. M. (2010). Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68, 408-415.
31. George, E. D., Bordner, K. A., Elwafi, H. M., and Simen, A. A. (2010). Maternal separation with early weaning: a novel mouse model of early life neglect. BMC Neurosci. 11, 123. doi: 10.1186/1471-2202-11-123
32. Groer, M. W., Hill, J., Wilkinson, J. E., and Stuart, A. (2002). Effects of separation and separation with supplemental stroking in BALb/c infant mice. Biol. Res. Nurs. 3, 119-131.
33. Holmes, A., le Guisquet, A. M., Vogel, E., Millstein, R. A., Leman, S., and Belzung, C. (2005). Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci. Biobehav. Rev. 29, 1335-1346
34. Holmes, A., Murphy, D. L., and Crawley, J. N. (2002). Reduced aggression in mice lacking the serotonin t{stroke}ransporter. Psychopharmacology (Berl.) 161, 160-167.
35. Hotoleanu, C., Popp, R., Trifa, A. P., Nedelcu, L., and Dumitrascu, D. L. (2008). Genetic determination of irritable bowel syndrome. World J. Gastroenterol. 14, 6636-6640.
36. Jacobson, L. H., Bettler, B., Kaupmann, K., and Cryan, J. F. (2007a). Behavioral evaluation of mice deficient in GABA(B(1)) receptor isoforms in tests of unconditioned anxiety. Psychopharmacology (Berl.) 190, 541-553.
37. Jacobson, L. H., Kelly, P. H., Bettler, B., Kaupmann, K., and Cryan, J. F. (2007b). Specific roles of GABA(B(1)) receptor isoforms in cognition. Behav. Brain Res. 181, 158-162.
38. Jacobson, L. H., and Cryan, J. F. (2007). Feeling strained? Influence of genetic background on depression-related behavior in mice: a review. Behav. Genet. 37, 171-213.
39. Jaworska, N., Dwyer, S. M., and Rusak, B. (2008). Repeated neonatal separation results in different neurochemical and behavioral changes in adult male and female Mongolian gerbils. Pharmacol. Biochem. Behav. 88, 533-541.
40. Julio-Pieper, M., Hyland, N. P., Bravo, J. A., Dinan, T. G., and Cryan, J. F. (2010). A novel role for the metabotropic glutamate receptor-7: modulation of faecal water content and colonic electrolyte transport in the mouse. Br. J. Pharmacol. 160, 367-375.
41. Kimball, E. S., Palmer, J. M., D'Andrea, M. R., Hornby, P. J., and Wade, P. R. (2005). Acute colitis induction by oil of mustard results in later development of an IBS-like accelerated upper GI transit in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1266-G1273.
42. Krishnan, V., Han, M. H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., Laplant, Q., Graham, A., Lutter, M., Lagace, D. C., Ghose, S., Reister, R., Tannous, P., Green, T. A., Neve, R. L., Chakravarty, S., Kumar, A., Eisch, A. J., Self, D. W., Lee, F. S., Tamminga, C. A., Cooper, D. C., Gershenfeld, H. K., and Nestler, E. J. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404.
43. Krishnan, V., and Nestler, E. J. (2008). The molecular neurobiology of depression. Nature 455, 894-902.
44. Kulikov, A. V., Avgustinovich, D. F., Kolpakov, V. G., Maslova, G. B., and Popova, N. K. (1995). 5-HT2A serotonin receptors in the brain of rats and mice hereditarily predisposed to catalepsy. Pharmacol. Biochem. Behav. 50, 383-387.
45. Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., and Plotsky, P. M. (2004). Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry 55, 367-375.
46. Lalonde, R. (2002). The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 26, 91-104
47. Lazinski, M. J., Shea, A. K., and Steiner, M. (2008). Effects of maternal prenatal stress on offspring development: a commentary. Arch. Womens Ment. Health 11, 363-375.
48. Levine, S. (2005). Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30, 939-946.
49. Loizzo, A., Loizzo, S., Galietta, G., Caiola, S., Spampinato, S., Campana, G., Seghieri, G., Ghirlanda, G., and Franconi, F. (2006). Overweight and metabolic and hormonal parameter disruption are induced in adult male mice by manipulations during lactation period. Pediatr. Res. 59, 111-115
50. MacQueen, G. M., Ramakrishnan, K., Ratnasingan, R., Chen, B., and Young, L. T. (2003). Desipramine treatment reduces the long-term behavioural and neurochemical sequelae of early-life maternal separation. Int. J. Neuropsychopharmacol. 6, 391-396
51. Macri, S., and Laviola, G. (2004). Single episode of maternal deprivation and adult depressive profile in mice: interaction with cannabinoid exposure during adolescence. Behav. Brain Res. 154, 231-238.
52. Macri, S., and Wurbel, H. (2006). Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 50, 667-680.
53. Mayer, E. A., Bradesi, S., Chang, L., Spiegel, B. M., Bueller, J. A., and Naliboff, B. D. (2008). Functional GI disorders: from animal models to drug development. Gut 57, 384-404.
54. McKernan, D. P., Dinan, T. G., and Cryan, J. F. (2009). "Killing the Blues": a role for cellular suicide (apoptosis) in depression and the antidepressant response? Prog. Neurobiol. 88, 246-263.
55. Mertz, H. R. (2003). Overview of functional gastrointestinal disorders: dysfunction of the brain-gut axis. Gastroenterol. Clin. North Am. 32, 463-476
56. Millstein, R. A., and Holmes, A. (2007). Effects of repeated maternal separation on anxietyand depressionrelated phenotypes in different mouse strains. Neurosci. Biobehav. Rev. 31, 3-17.
57. Moles, A., Rizzi, R., and D'Amato, F. R. (2004). Postnatal stress in mice: does "stressing" the mother have the same effect as "stressing" the pups? Dev. Psychobiol. 44, 230-237.
58. Niwa, M., Matsumoto, Y., Mouri, A., Ozaki, N., and Nabeshima, T. (2010). Vulnerability in early life to changes in the rearing environment plays a crucial role in the aetiopathology of psychiatric disorders. Int. J. Neuropsychopharmacol. 1-19. 10.1017/S1461145710001239. [Epub ahead of print]
59. North, C. S., Hong, B. A., and Alpers, D. H. (2007). Relationship of functional gastrointestinal disorders and psychiatric disorders: implications for treatment. World J. Gastroenterol. 13, 2020-2027.
60. O'Mahony, C. M., Sweeney, F. F., Daly, E., Dinan, T. G., and Cryan, J. F. (2010). Restraint stress-induced brain activation patterns in two strains of mice differing in their anxiety behaviour. Behav. Brain Res. 213, 148-154.
61. O'Mahony, S. M., Hyland, N. P., Dinan, T. G., and Cryan, J. F. (2011). Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl.) 214, 71-88.
62. O'Mahony, S. M., Marchesi, J. R., Scully, P., Codling, C., Ceolho, A. M., Quigley, E. M., Cryan, J. F., and Dinan, T. G. (2009). Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry 65, 263-267.
63. O'Malley, D., Dinan, T. G., and Cryan, J. F. (2010). Alterations in colonic corticotropin-releasing factor receptors in the maternally separated rat model of irritable bowel syndrome: differential effects of acute psychological and physical stressors. Peptides 31, 662-670.
64. Oreland, S., Pickering, C., Gokturk, C., Oreland, L., Arborelius, L., and Nylander, I. (2009). Two repeated maternal separation procedures differentially affect brain 5-hydroxytryptamine transporter and receptors in young and adult male and female rats. Brain Res. 1305(Suppl.), S37-S49.
65. Parfitt, D. B., Levin, J. K., Saltstein, K. P., Klayman, A. S., Greer, L. M., and Helmreich, D. L. (2004). Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res. 1016, 111-118.
66. Popova, N. K. (2008). From gene to aggressive behavior: the role of brain serotonin. Neurosci. Behav. Physiol. 38, 471-475.
67. Priebe, K., Romeo, R. D., Francis, D. D., Sisti, H. M., Mueller, A., McEwen, B. S., and Brake, W. G. (2005). Maternal influences on adult stress and anxietylike behavior in C57BL/6J and BALB/ cJ mice: a cross-fostering study. Dev. Psychobiol. 47, 398-407.
68. Pryce, C. R., Ruedi-Bettschen, D., Dettling, A. C., Weston, A., Russig, H., Ferger, B., and Feldon, J. (2005). Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci. Biobehav. Rev. 29, 649-674.
69. Pryce, C. R., and Seifritz, E. (2011). A translational research framework for enhanced validity of mouse models of psychopathological states in depression. Psychoneuroendocrinology, 36, 308-329.
70. Reber, S. O., Birkeneder, L., Veenema, A. H., Obermeier, F., Falk, W., Straub, R. H., and Neumann, I. D. (2007). Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice: implications and mechanisms. Endocrinology 148, 670-682.
71. Reber, S. O., Obermeier, F., Straub, R. H., Falk, W., and Neumann, I. D. (2006). Chronic intermittent psychosocial stress (social defeat/overcrowding) in mice increases the severity of an acute DSS-induced colitis and impairs regeneration. Endocrinology 147, 4968-4976.
72. Romeo, R. D., Mueller, A., Sisti, H. M., Ogawa, S., McEwen, B. S., and Brake, W. G. (2003). Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm. Behav. 43, 561-567
73. Savignac, H. M., Hyland, N. P., Dinan, T. G., and Cryan, J. F. (2011). The effects of repeated social interaction stress on behavioural and physiological parameters in a stress-sensitive mouse strain. Behav. Brain Res. 216, 576-584.
74. Schmidt, M. V., Wang, X. D., and Meijer, O. C. (2011). Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl.) 214, 131-140.
75. Slattery, D. A., and Neumann, I. D. (2008). No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J. Physiol. 586, 377-385.
76. Uhelski, M. L., and Fuchs, P. N. (2010). Maternal separation stress leads to enhanced emotional responses to noxious stimuli in adult rats. Behav. Brain Res. 212, 208-212.
77. van Heerden, J. H., Russell, V., Korff, A., Stein, D. J., and Illing, N. (2010). Evaluating the behavioural consequences of early maternal separation in adult C57BL/6 mice; the importance of time. Behav. Brain Res. 207, 332-342.
78. Veenema, A. H., Blume, A., Niederle, D., Buwalda, B., and Neumann, I. D. (2006). Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 24, 1711-1720.
79. Veenema, A. H., Bredewold, R., and Neumann, I. D. (2007). Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32, 437-450.
80. Veenema, A. H., Reber, S. O., Selch, S., Obermeier, F., and Neumann, I. D. (2008). Early life stress enhances the vulnerability to chronic psychosocial stress and experimental colitis in adult mice. Endocrinology 149, 2727-2736.
81. Venerosi, A., Cirulli, F., Capone, F., and Alleva, E. (2003). Prolonged perinatal AZT administration and early maternal separation: effects on social and emotional behaviour of periadolescent mice. Pharmacol. Biochem. Behav. 74, 671-681
82. Wachs, T. D. (2009). Models linking nutritional deficiencies to maternal and child mental health. Am. J. Clin. Nutr. 89, 935S-939S.
83. Wang, L., Gourcerol, G., Yuan, P. Q., Wu, S. V., Million, M., Larauche, M., and Tache, Y. (2010). Peripheral peptide YY inhibits propulsive colonic motor function through Y2 receptor in conscious mice. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G45-G56.
84. Weaver, S. A., Diorio, J., and Meaney, M. J. (2007). Maternal separation leads to persistent reductions in pain sensitivity in female rats. J. Pain 8, 962-969
85. Wei, L., David, A., Duman, R. S., Anisman, H., and Kaffman, A. (2010). Early life stress increases anxiety-like behavior in Balbc mice despite a compensatory increase in levels of postnatal maternal care. Horm. Behav. 57, 396-404.
86. Wood, J. D. (2007). Neuropathophysiology of functional gastrointestinal disorders. World J. Gastroenterol. 13, 1313-1332.
87. Wurtman, R. J. (2005). Genes, stress, and depression. Metab. Clin. Exp. 54, 16-19
88. Young, S. N., and Leyton, M. (2002). The role of serotonin in human mood and social interaction. Insight from altered tryptophan levels. Pharmacol. Biochem. Behav. 71, 857-865.
89. Zhang, X., Beaulieu, J. M., Sotnikova, T. D., Gainetdinov, R. R., and Caron, M. G. (2004). Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305, 217.