Exercise prevents the increased anxiety-like behavior in lactational di-(2-ethylhexyl) phthalate-exposed female rats in late adolescence by improving the regulation of hypothalamus-pituitary-adrenal axis

Hormones and Behavior

Volumn 66, Issue 4, 2014, Pages 674-684

  Wang, Dean Chuan ^a   Chen, Tsan Ju ^a   Lin, Ming Lu ^a   Jhong, Yue Cih ^a   Chen, Shih Chieh ^a  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Anxiety like behavior; Di (2 ethylhexyl) phthalate; Hypothalamic pituitary adrenal axis; Treadmill

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CORTICOSTERONE; CORTICOTROPIN; GLUCOCORTICOID RECEPTOR; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; STEROID 11BETA MONOOXYGENASE;

ADOLESCENT; ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; ELEVATED PLUS MAZE TEST; FEMALE; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LACTATION; NONHUMAN; PRENATAL EXPOSURE; PROTECTION; PROTEIN EXPRESSION; RAT; STRESS; TREADMILL EXERCISE; ANIMAL; DRUG EFFECTS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; PHYSIOLOGY; PREVENTION AND CONTROL; RUNNING; SEXUAL MATURATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANXIETY; CORTICOSTERONE; DIETHYLHEXYL PHTHALATE; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LACTATION; PHYSICAL CONDITIONING, ANIMAL; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; RUNNING; SEXUAL MATURATION;

EID: 84908086090     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.09.010     Document Type: Article

References (70)

1. Anda R.F., Whitfield C.L., Felitti V.J., Chapman D., Edwards V.J., Dube S.R., Williamson D.F. Adverse childhood experiences, alcoholic parents, and later risk of alcoholism and depression. Psychiatr. Serv. 2002, 53:1001-1009.
2. Andrade A.J., Grande S.W., Talsness C.E., Grote K., Chahoud I. A dose-response study following in utero and lactational exposure to di-(2-ethylhexyl)-phthalate (DEHP): non-monotonic dose-response and low dose effects on rat brain aromatase activity. Toxicology 2006, 227:185-192.
3. Appenrodt E., Kröning G., Schwarzberg H. Increased plasma ACTH in rats exposed to the elevated plus-maze is independent of the pineal gland. Psychoneuroendocrinology 1999, 24:833-838.
4. Baek S.S., Jun T.W., Kim K.J., Shin M.S., Kang S.Y., Kim C.J. Effects of postnatal treadmill exercise on apoptotic neuronal cell death and cell proliferation of maternal-separated rat pups. Brain Dev. 2012, 34:45-56.
5. Blumenthal J.A., Babyak M.A., Doraiswamy P.M., Watkins L., Hoffman B.M., Barbour K.A., Herman S., Craighead W.E., Brosse A.L., Waugh R., Hinderliter A., Sherwood A. Exercise and pharmacotherapy in the treatment of major depressive disorder. Psychosom. Med. 2007, 69:587-596.
6. Blystone C.R., Kissling G.E., Bishop J.B., Chapin R.E., Wolfe G.W., Foster P.M. Determination of the di-(2-ethylhexyl) phthalate NOAEL for reproductive development in the rat: importance of the retention of extra animals to adulthood. Toxicol. Sci. 2010, 116:640-646.
7. Brocardo P.S., Boehme F., Patten A., Cox A., Gil-Mohapel J., Christie B.R. Anxiety- and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: Protective effects of voluntary physical exercise. Neuropharmacology 2012, 62:1607-1618.
8. Brown A.P., Dinger N., Levine B.S. Stress produced by gavage administration in the rat. Contemp. Top. Lab. Anim. Sci. 2000, 39:17-21.
9. Brummelte S., Lieblich S.E., Galea L.A. Gestational and postpartum corticosterone exposure to the dam affects behavioral and endocrine outcome of the offspring in a sexually-dimorphic manner. Neuropharmacology 2012, 62:406-418.
10. Campbell J.E., Rakhshani N., Fediuc S., Bruni S., Riddell M.C. Voluntary wheel running initially increases adrenal sensitivity to adrenocorticotrophic hormone, which is attenuated with long-term training. J. Appl. Physiol. 2009, 106:66-72.
11. Carbone S., Ponzo O.J., Gobetto N., Samaniego Y.A., Reynoso R., Scacchi P., Moguilevsky J.A., Cutrera R. Antiandrogenic effect of perinatal exposure to the endocrine disruptor di-(2-ethylhexyl) phthalate increases anxiety-like behavior in male rats during sexual maturation. Horm. Behav. 2013, 63:692-699.
12. Chang Y.T., Chen Y.C., Wu C.W., Yu L., Chen H.I., Jen C.J., Kuo Y.M. Glucocorticoid signaling and exercise-induced downregulation of the mineralocorticoid receptor in the induction of adult mouse dentate neurogenesis by treadmill running. Psychoneuroendocrinology 2008, 33:1173-1182.
13. Chennaoui M., Gomez Merino D., Lesage J., Drogou C., Guezennec C.Y. Effects of moderate and intensive training on the hypothalamo-pituitary-adrenal axis in rats. Acta Physiol. Scand. 2002, 175:113-121.
14. Cullen C.L., Burne T.H., Lavidis N.A., Moritz K.M. Low dose prenatal ethanol exposure induces anxiety-like behaviour and alters dendritic morphology in the basolateral amygdala of rat offspring. PLoS One 2013, 8:e54924.
15. Droste S.K., Chandramohan Y., Hill L.E., Linthorst A.C., Reul J.M. Voluntary exercise impacts on the rat hypothalamic-pituitary-adrenocortical axis mainly at the adrenal level. Neuroendocrinology 2007, 86:26-37.
16. Duman C.H., Schlesinger L., Russell D.S., Duman R.S. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res. 2008, 1199:148-158.
17. Figueiredo H.F., Dolgas C.M., Herman J.P. Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology 2002, 143:2534-2540.
18. Foilb A.R., Lui P., Romeo R.D. The transformation of hormonal stress responses throughout puberty and adolescence. J. Endocrinol. 2011, 210:391-398.
19. 2 anesthesia in the collection of samples for serum corticosterone analysis from Fischer 344 rats. Contemp. Top. Lab. Anim. Sci. 2004, 43:8-12.
20. 2 in swine. Acta Physiol. Scand. 1988, 132:223-231.
21. Galper D.I., Trivedi M.H., Barlow C.E., Dunn A.L., Kampert J.B. Inverse association between physical inactivity and mental health in men and women. Med. Sci. Sports Exerc. 2006, 38:173-178.
22. Gaston A., Prapavessis H. Tired, moody and pregnant? Exercise may be the answer. Psychol. Health 2013, 28:1353-1369.
23. Goggin S.L., Labrecque M.T., Allan A.M. Perinatal exposure to 50ppb sodium arsenate induces hypothalamic-pituitary-adrenal axis dysregulation in male C57BL/6 mice. Neurotoxicology 2012, 33:1338-1345.
24. Grande S.W., Andrade A.J., Talsness C.E., Grote K., Golombiewski A., Sterner-Kock A., Chahoud I. A dose-response study following in utero and lactational exposure to di-(2-ethylhexyl) phthalate (DEHP): reproductive effects on adult female offspring rats. Toxicology 2007, 229:114-122.
25. Gschwind Y.J., Kressig R.W., Lacroix A., Muehlbauer T., Pfenninger B., Granacher U. A best practice fall prevention exercise program to improve balance, strength/power, and psychosocial health in older adults: study protocol for a randomized controlled trial. BMC Geriatr. 2013, 13:105.
26. Hare B.D., Beierle J.A., Toufexis D.J., Hammack S.E., Falls W.A. Exercise-associated changes in the corticosterone response to acute restraint stress: evidence for increased adrenal sensitivity and reduced corticosterone response duration. Neuropsychopharmacology 2014, 39:1262-1269.
27. Heinemeyer G., Sommerfeld C., Springer A., Heiland A., Lindtner O., Greiner M., Heuer T., Krems C., Conrad A. Estimation of dietary intake of bis(2-ethylhexyl)phthalate (DEHP) by consumption of food in the German population. Int. J. Hyg. Environ. Health 2013, 216:472-480.
28. Herreros M.A., Encinas T., Torres-Rovira L., Garcia-Fernandez R.A., Flores J.M., Ros J.M., Gonzalez-Bulnes A. Exposure to the endocrine disruptor di(2-ethylhexyl)phthalate affects female reproductive features by altering pulsatile LH secretion. Environ. Toxicol. Pharmacol. 2013, 36:1141-1149.
29. Hrubá L., Schutová B., Šlamberová R. Sex differences in anxiety-like behavior and locomotor activity following prenatal and postnatal methamphetamine exposure in adult rats. Physiol. Behav. 2012, 105:364-370.
30. Hsu Y.C., Chen H.I., Kuo Y.M., Yu L., Huang T.Y., Chen S.J., Chuang J.I., Wu F.S., Jen C.J. Chronic treadmill running in normotensive rats resets the resting blood pressure to lower levels by upregulating the hypothalamic GABAergic system. J. Hypertens. 2011, 29:2339-2348.
31. Huang C.C., Shih M.C., Hsu N.C., Chien Y., Chung B.C. Fetal glucocorticoid synthesis is required for development of fetal adrenal medulla and hypothalamus feedback suppression. Endocrinology 2012, 153:4749-4756.
32. Huang T.Y., Lin L.S., Cho K.C., Chen S.J., Kuo Y.M., Yu L., Wu F.S., Chuang J.I., Chen H.I., Jen C.J. Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum. J. Appl. Physiol. 2012, 113:889-895.
33. Huynh T.N., Krigbaum A.M., Hanna J.J., Conrad C.D. Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior. Behav. Brain Res. 2011, 222:212-222.
34. Keenan K., Hipwell A., Babinski D., Bortner J., Henneberger A., Hinze A., Klostermann S., Rischall M., Sapotichne B. Examining the developmental interface of cortisol and depression symptoms in young adolescent girls. Psychoneuroendocrinology 2013, 38:2291-2299.
35. Kim H.G., Lim E.Y., Jung W.R., Shin M.K., Ann E.S., Kim K.L. Effects of treadmill exercise on hypoactivity of the hypothalamo-pituitary-adrenal axis induced by chronic administration of corticosterone in rats. Neurosci. Lett. 2008, 434:46-49.
36. Kim B.N., Cho S.C., Kim Y., Shin M.S., Yoo H.J., Kim J.W., Yang Y.H., Kim H.W., Bhang S.Y., Hong Y.C. Phthalates exposure and attention-deficit/hyperactivity disorder in school-age children. Biol. Psychiatry 2009, 66:958-963.
37. Lalanza J.F., Sanchez-Roige S., Gagliano H., Fuentes S., Bayod S., Camins A., Pallàs M., Armario A., Escorihuela R.M. Physiological and behavioural consequences of long-term moderate treadmill exercise. Psychoneuroendocrinology 2012, 37:1745-1754.
38. Lapmanee S., Charoenphandhu J., Charoenphandhu N. Beneficial effects of fluoxetine, reboxetine, venlafaxine, and voluntary running exercise in stressed male rats with anxiety- and depression-like behaviors. Behav. Brain Res. 2013, 250:316-325.
39. Latini G., De Felice C., Presta G., Del Vecchio A., Paris I., Ruggieri F., Mazzeo P. In utero exposure to di-(2-ethylhexyl) phthalate and duration of human pregnancy. Environ. Health Perspect. 2003, 111:1783-1785.
40. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A.R., Cinque C., Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 2003, 27:119-127.
41. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus maze test. Physiol. Behav. 2001, 74:435-440.
42. Martinez-Arguelles D.B., Guichard T., Culty M., Zirkin B.R., Papadopoulos V. In utero exposure to the antiandrogen di-(2-ethylhexyl) phthalate decreases adrenal aldosterone production in the adult rat. Biol. Reprod. 2011, 85:51-61.
43. Meaney M.J., Szyf M., Seckl J.R. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol. Med. 2007, 13:269-277.
44. Mikics E., Barsy B., Barsvári B., Haller J. Behavioral specificity of non-genomic glucocorticoid effects in rats: effects on risk assessment in the elevated plus-maze and the open-field. Horm. Behav. 2005, 48:152-162.
45. Miladi-Gorji H., Rashidy-Pour A., Fathollahi Y. Anxiety profile in morphine-dependent and withdrawn rats: effect of voluntary exercise. Physiol. Behav. 2012, 105:195-202.
46. Mora S., Dussaubat N., Díaz-Véliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
47. Parajes S., Chan A.O., But W.M., Rose I.T., Taylor A.E., Dhir V., Arlt W., Krone N. Delayed diagnosis of adrenal insufficiency in a patient with severe penoscrotal hypospadias due to two novel P450 side-change cleavage enzyme (CYP11A1) mutations (p.R360W; p.R405X). Eur. J. Endocrinol. 2012, 167:881-885.
48. Pastula R.M., Stopka C.B., Delisle A.T., Hass C.J. Effect of moderate-intensity exercise training on the cognitive function of young adults with intellectual disabilities. J. Strength Cond. Res. 2012, 26:3441-3448.
49. Patin V., Lordi B., Vincent A., Caston J. Effects of prenatal stress on anxiety and social interactions in adult rats. Brain Res. Dev. Brain Res. 2005, 160:265-274.
50. Penninx B.W., Beekman A.T., Bandinelli S., Corsi A.M., Bremmer M., Hoogendijk W.J., Guralnik J.M., Ferrucci L. Late-life depressive symptoms are associated with both hyperactivity and hypoactivity of the hypothalamo-pituitary-adrenal axis. Am. J. Geriatr. Psychiatr. 2007, 15:522-529.
51. Pietrelli A., Lopez-Costa J., Goñi R., Brusco A., Basso N. Aerobic exercise prevents age-dependent cognitive decline and reduces anxiety-related behaviors in middle-aged and old rats. Neuroscience 2012, 202:252-266.
52. Pocar P., Fiandanese N., Secchi C., Berrini A., Fischer B., Schmidt J.S., Schaedlich K., Borromeo V. Exposure to di(2-ethyl-hexyl) phthalate (DEHP) in utero and during lactation causes long-term pituitary-gonadal axis disruption in male and female mouse offspring. Endocrinology 2012, 153:937-948.
53. Romeo R.D., Lee S.J., McEwen B.S. Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 2004, 80:387-393.
54. Romeo R.D., Bellani R., Karatsoreos I.N., Chhua N., Vernov M., Conrad C.D., McEwen B.S. Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology 2006, 147:1664-1674.
55. Salim S., Sarraj N., Taneja M., Saha K., Tejada-Simon M.V., Chugh G. Moderate treadmill exercise prevents oxidative stress-induced anxiety-like behavior in rats. Behav. Brain Res. 2010, 208:545-552.
56. Sasaki A., de Vega W.C., St-Cyr S., Pan P., McGowan P.O. Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience 2013, 240:1-12.
57. Scott K.M., Smith D.R., Ellis P.M. Prospectively ascertained child maltreatment and its association with DSM-IV mental disorders in young adults. Arch. Gen. Psychiatry 2010, 67:712-719.
58. Shalev A.Y., Videlock E.J., Peleg T., Segman R., Pitman R.K., Yehuda R. Stress hormones and post-traumatic stress disorder in civilian trauma victims: a longitudinal study. Part I: HPA axis responses. Int. J. Neuropsychopharmacol. 2008, 11:365-372.
59. Shelby M.D. NTP-CERHR monograph on the potential human reproductive and developmental effects of di (2-ethylhexyl) phthalate (DEHP). NTP CERHR MON 18, v, vii-7, II-iii-xiii passim Available on the CERHR web site. http://cerhr.niehs.nih.gov.
60. Shih M.C., Hsu N.C., Huang C.C., Wu T.S., Lai P.Y., Chung B.C. Mutation of mouse Cyp11a1 promoter caused tissue-specific reduction of gene expression and blunted stress response without affecting reproduction. Mol. Endocrinol. 2008, 22:915-923.
61. Sontag-Padilla L.M., Dorn L.D., Tissot A., Susman E.J., Beers S.R., Rose S.R. Executive functioning, cortisol reactivity, and symptoms of psychopathology in girls with premature adrenarche. Dev. Psychopathol. 2012, 24:211-223.
62. Ströhle A., Holsboer F. Stress responsive neurohormones in depression and anxiety. Pharmacopsychiatry 2003, 36(Suppl. 3):S207-S214.
63. Supornsilchai V., Söder O., Svechnikov K. Stimulation of the pituitary-adrenal axis and of adrenocortical steroidogenesis ex vivo by administration of di-2-ethylhexyl phthalate to prepubertal male rats. J. Endocrinol. 2007, 192:33-39.
64. Trasande L., Sathyanarayana S., Jo Messito M., S Gross R., Attina T.M., Mendelsohn A.L. Phthalates and the diets of U.S. children and adolescents. Environ. Res. 2013, 126:84-90.
65. Verma P., Hellemans K.G., Choi F.Y., Yu W., Weinberg J. Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress. Physiol. Behav. 2010, 99:276-285.
66. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129:2503-2511.
67. Vollert C., Zagaar M., Hovatta I., Taneja M., Vu A., Dao A., Levine A., Alkadhi K., Salim S. Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behav. Brain Res. 2011, 224:233-240.
68. Wei Z., Song L., Wei J., Chen T., Chen J., Lin Y., Xia W., Xu B., Li X., Chen X., Li Y., Xu S. Maternal exposure to di-(2-ethylhexyl)phthalate alters kidney development through the renin-angiotensin system in offspring. Toxicol. Lett. 2012, 212:212-221.
69. Wittassek M., Heger W., Koch H.M., Becker K., Angerer J., Kolossa-Gehring M. Daily intake of di(2-ethylhexyl)phthalate (DEHP) by German children - A comparison of two estimation models based on urinary DEHP metabolite levels. Int. J. Hyg. Environ. Health 2007, 210:35-42.
70. Yi S.S., Hwang I.K., Shin J.H., Choi J.H., Lee C.H., Kim I.Y., Kim Y.N., Won M.H., Park I.S., Seong J.K., Yoon Y.S. Regulatory mechanism of hypothalamo-pituitary-adrenal (HPA) axis and neuronal changes after adrenalectomy in type 2 diabetes. J. Chem. Neuroanat. 2010, 40:130-139.