The effect of early-life stress on airway inflammation in adult mice

NeuroImmunoModulation

Volumn 17, Issue 4, 2010, Pages 229-239

  Vig, Rattanjeet ^a   Gordon, John R ^b   Thébaud, Bernard ^a   Befus, A Dean ^a   Vliagoftis, Harissios ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Airway inflammation; Asthma; Early life stress; Maternal separation; Mouse; Psychological stress

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 4; OVALBUMIN; SODIUM CHLORIDE;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EARLY LIFE STRESS; EOSINOPHIL; FEMALE; INFLAMMATORY CELL; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE;

AGING; ANIMALS; ANIMALS, NEWBORN; ASTHMA; BRONCHITIS; CYTOKINES; DISEASE MODELS, ANIMAL; EOSINOPHILS; MATERNAL DEPRIVATION; MICE; MICE, INBRED BALB C; OVALBUMIN; RESPIRATORY SYSTEM; STRESS, PSYCHOLOGICAL; TIME;

EID: 77950141201     PISSN: 10217401     EISSN: None     Source Type: Journal    
DOI: 10.1159/000290039     Document Type: Article

References (50)

1. Weil CM, Wade SL, Bauman LJ, Lynn H, Mitchell H, Lavigne J: The relationship between psychosocial factors and asthma morbidity in inner-city children with asthma. Pediatrics 1999; 104: 1274-1280.
2. Strunk RC, Mrazek DA, Fuhrmann GS, La- Brecque JF: Physiologic and psychological characteristics associated with deaths due to asthma in childhood. A case-controlled study. JAMA 1985; 254: 1193-1198.
3. Sears MR, Rea HH, Fenwick J, Beaglehole R, Gilles AJ, Holst PE, O'Donnell TV, Rothwell RP, Sutherland DC: Deaths from asthma in New Zealand. Arch Dis Child 1986; 61: 6-10.
4. Fritz GK, Overholser JC: Patterns of response to childhood asthma. Psychosom Med 1989; 51: 347-355.
5. Kaptein AA: Psychological correlates of length of hospitalization and rehospitalization in patients with acute, severe asthma. Soc Sci Med 1982; 16: 725-729.
6. Gutstadt LB, Gillette JW, Mrazek DA, Fukuhara JT, LaBrecque JF, Strunk RC: Determinants of school performance in children with chronic asthma. Am J Dis Child 1989; 143: 471-475.
7. Innes NJ, Reid A, Halstead J, Watkin SW, Harrison BD: Psychosocial risk factors in near-fatal asthma and in asthma deaths. J R Coll Physicians Lond 1998; 32: 430-434.
8. Sandberg S, Paton JY, Ahola S, McCann DC, McGuinness D, Hillary CR, Oja H: The role of acute and chronic stress in asthma attacks in children. Lancet 2000; 356: 982-987.
9. Sandberg S, Jarvenpaa S, Penttinen A, Paton JY, McCann DC: Asthma exacerbations in children immediately following stressful life events: a Cox's hierarchical regression. Thorax 2004; 59: 1046-1051.
10. Klinnert MD, Mrazek PJ, Mrazek DA: Early asthma onset: the interaction between family stressors and adaptive parenting. Psychiatry 1994; 57: 51-61.
11. Bockelbrink A, Heinrich J, Schafer I, Zutavern A, Borte M, Herbarth O, Schaaf B, von Berg A, Schafer T, the LISA Study Group: Atopic eczema in children: another harmful sequel of divorce. Allergy 2006; 61: 1397-1402.
12. Wright RJ, Finn P, Contreras JP, Cohen S, Wright RO, Staudenmayer J, Wand M, Perkins D, Weiss ST, Gold DR: Chronic caregiver stress and IgE expression, allergen-induced proliferation, and cytokine profiles in a birth cohort predisposed to atopy. J Allergy Clin Immunol 2004; 113: 1051-1057.
13. Wright RJ, Cohen S, Carey V, Weiss ST, Gold DR: Parental stress as a predictor of wheezing in infancy: a prospective birth-cohort study. Am J Respir Crit Care Med 2002; 165: 358-365.
14. Galil N: Depression and asthma in children. Curr Opin Pediatr 2000; 12: 331-335.
15. Graham YP, Heim C, Goodman SH, Miller AH, Nemeroff CB: The effects of neonatal stress on brain development: implications for psychopathology. Dev Psychopathol 1999; 11: 545-565.
16. Bolt RJ, van Weissenbruch MM, Lafeber HN, Delamarre-van de Waal HA: Glucocorticoids and lung development in the fetus and preterm infant. Pediatr Pulmonol 2001; 32: 76-91.
17. Mehls O, Himmele R, Homme M, Kiepe D, Klaus G: The interaction of glucocorticoids with the growth hormone-insulin-like growth factor axis and its effects on growth plate chondrocytes and bone cells. J Pediatr Endocrinol Metab 2001; 14(suppl 6):1475-1482.
18. Soderholm JD, Yates DA, Gareau MG, Yang PC, MacQueen G, Perdue MH: Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am J Physiol Gastrointest Liver Physiol 2002; 283:G1257-G1263.
19. Romeo RD, Mueller AD, Sisti HM, Ogawa S, McEwan BS, Brake WG: Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm Behav 2003; 43: 561-567.
20. Parfitt DB, Levin JK, Salstein KP, Klayman AS, Greer LM, Helmreich DL: Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res 2004; 1016: 111-118.
21. Romeo RD, Fossella JA, Bateup HS, Sisti HM, Brake WG, McEwan BS: Maternal separation suppresses TGF alpha mRNA expression in the prefrontal cortex of male and female neonatal C57BL/6 mice. Brain Res Dev Brain Res 2004; 152: 73-77.
22. Tschanz SA, Makanya AN, Haenni B, Burri PH: Effects of neonatal high-dose short-term glucocorticoid treatment on the lung: a morphologic and morphometric study in the rat. Pediatr Res 2003; 53: 72-80.
23. Lomask M: Further exploration of the Penh parameter. Exp Toxicol Pathol 2006; 57 (suppl 2):13-20.
24. Forsythe P, Ebeling C, Gordon JR, Befus AD, Vliagoftis H: Opposing effects of short- and long-term stress on airway inflammation. Am J Respir Crit Care Med 2004; 169: 220-226.
25. Gordon JR, Zhang X, Stevenson K, Cosford K: Thrombin induces IL-6 but not TNF- secretion by mouse mast cells: threshold-level thrombin receptor and very low level Fc- RI signaling synergistically enhance IL-6 secretion. Cell Immunol 2000; 205: 128-135.
26. Schneider AM, Li F, Zhang X, Gordon JR: Induction of pulmonary allergen-specific IgA responses or airway hyperresponsiveness in the absence of allergic lung disease following sensitization with limiting doses of ovalbumin-alum. Cell Immunol 2001; 212: 101-109.
27. Hofer MA: Survival and recovery of physiologic functions after early maternal separation in rats. Physiol Behav 1975; 15: 475-480.
28. Knackstedt MK, Hamelmann E, Arck PC: Mothers in stress: consequences for the offspring. Am J Reprod Immunol 2005; 54: 63-69.
29. Anisman H, Zaharia MD, Meaney MJ, Merali Z: Do early-life events permanently alter behavioral and hormonal responses to stressors? Int J Dev Neurosci 1998; 16: 149-164.
30. Hodson WA: Development of the Lung. New York, Dekker, 1977.
31. Elenkov IJ, Chrousos GP: Stress system - Organization, physiology and immunoregulation. Neuroimmunomodulation 2006; 13: 257-267.
32. Joachim RA, Quarcoo D, Arck PC, Herz U, Renz H, Klapp BF: Stress enhances airway reactivity and airway inflammation in an animal model of allergic bronchial asthma. Psychosom Med 2003; 65: 811-815.
33. Millstein RA, Holmes A: Effects of repeated maternal separation on anxiety- and depression- related phenotypes in different mouse strains. Neurosci Biobehav Rev 2007; 31: 3-17.
34. Macrì S, Würbel H: Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm Behav 2006; 50: 667-680.
35. Pincus-Knackstedt MK, Joachim RA, Blois SM, Douglas AJ, Orsal AS, Klapp BF, Wahn U, Hamelmann E, Arck PC: Prenatal stress enhances susceptibility of murine adult offspring toward airway inflammation. J Immunol 2006; 177: 8484-8492.
36. Chida Y, Sudo N, Sonoda J, Hiramoto T, Kubo C: Early-life psychological stress exacerbates adult mouse asthma via the hypothalamus- pituitary-adrenal axis. Am J Respir Crit Care Med 2007; 175: 316-322.
37. Kruschinski C, Skripuletz T, Bedoui S, Raber K, Straub RH, Hoffmann T, Grote K, Jacobs R, Stephan M, Pabst R, von Hörsten S: Postnatal life events affect the severity of asthmatic airway inflammation in the adult rat. J Immunol 2008; 180: 3919-3925.
38. McEwen BS: Understanding the potency of stressful early life experiences on brain and body function. Metabolism 2008; 57(suppl 2):S11-S15.
39. McIntosh J, Anisman H, Merali Z: Shortand long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res Dev Brain Res 1999; 113: 97-106.
40. Kuhn CM, Pauk J, Schanberg SM: Endocrine responses to mother-infant separation in developing rats. Dev Psychobiol 1990; 23: 395-410.
41. D'Amore A, Mazzucchelli A, Loizzo A: Longterm changes induced by neonatal handling in the nociceptive threshold and body weight in mice. Physiol Behav 1995; 57: 1195-1197.
42. Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH: Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 2007; 56: 1522-1528.
43. Schmidt MV, Oitzl MS, Levine S, de Kloet ER: The HPA system during the postnatal development of CD1 mice and the effects of maternal deprivation. Brain Res Dev Brain Res 2002; 139: 39-49.
44. Okuyama K, Ohwada K, Sakurada S, Sato N, Sora I, Tamura G, Takayanagi M, Ohno I: The distinctive effects of acute and chronic psychological stress on airway inflammation in a murine model of allergic asthma. Allergol Int 2007; 56: 29-35.
45. Tsigos C, Chrousos GP: Hypothalamic-pituitary- adrenal axis, neuroendocrine factors and stress. J Psychosom Res 2002; 53: 865-871.
46. Singh LK, Pang X, Alexacos N, Letourneau R, Theoharides TC: Acute immobilization stress triggers skin mast cell degranulation via corticotropin releasing hormone, neurotensin, and substance P: a link to neurogenic skin disorders. Brain Behav Immun 1999; 13: 225-239.
47. Charmandari E, Tsigos C, Chrousus G: Endocrinology of the stress response. Annu Rev Physiol 2005; 67: 259-284.
48. Viveros MP, Llorente R, López-Gallardo M, Suarez J, Bermúdez-Silva F, De la Fuente M, Rodriguez de Fonseca F, Garcia-Segura LM: Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology 2009, E-pub ahead of print.
49. Luine VN, Beck KD, Bowman RE, Frankfurt M, Maclusky NJ: Chronic stress and neural function: accounting for sex and age. J Neuroendocrinol 2007; 19: 743-751.
50. Riffo-Vasquez Y, Ligeiro de Oliveira AP, Page CP, Spina D, Tavares-de-Lima W: Role of sex hormones in allergic inflammation in mice. Clin Exp Allergy 2007; 37: 459-470.