Gender differences in ghrelin response to chronic immobilization stress in rats: Possible role of estrogen

General Physiology and Biophysics

Volumn 33, Issue 1, 2014, Pages 111-120

  Elbassuoni, Eman A ^a  

^a MINIA UNIVERSITY   (Egypt)

Author keywords

Estrogen; Gender differences; Ghrelin; Stress

Indexed keywords

ANIMALS; BODY WEIGHT; EATING; ESTRADIOL; ESTROGENS; FEEDING BEHAVIOR; FEMALE; GHRELIN; IMMOBILIZATION; MALE; OVARIECTOMY; RATS; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84894184227     PISSN: 02315882     EISSN: 13384325     Source Type: Journal    
DOI: 10.4149/gpb_2013061     Document Type: Article

References (78)

1. Ackard D. M., Neumark-Sztainer D., Story M., Perry C. (2003): Overeating among adolescents: Prevalence and associations with weight-related characteristics and psychological health. Pediatrics 111, 67-74 http://dx.doi.org/10.1542/peds.111.1.67
2. Adam T. C., Epel E. S. (2007): Stress, eating and the reward system. Physiol.Behav. 91, 449-458 http://dx.doi.org/10.1016/j.physbeh.2007.04.011
3. Asakawa A., Inui A., Kaga T., Yuzuriha H., Nagata T., Fujimiya M. (2001): A role of ghrelin in neuroendocrine and behavioral responses to stress in mice. Neuroendocrinol. 74, 143-147 http://dx.doi.org/10.1159/000054680
4. Asarian L., Geary N. (2002): Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm. Behav. 42, 461-471 http://dx.doi.org/10.1006/hbeh.2002.1835
5. Barkan A. L., Dimaraki E. V., Jessup S. K., Symons K. V., Ermolenko M., Jaffe C. A. (2003): Ghrelin secretion in humans is sexually dimorphic, suppressed by somatostatin, and not affected by the ambient growth hormone levels. J. Clin. Endocrinol. Metab. 88, 2180-2184 http://dx.doi.org/10.1210/jc. 2002-021169
6. Bielajew C., Konkle A. T., Merali Z. (2002): The effects of chronic mild stress on male Sprague-Dawley and Long Evans rats. Biochemical and physiological analyses. Behav. Brain Res. 136, 583-592 http://dx.doi.org/10.1016/S0166- 4328(02)00222-X
7. Butera P. C. (2010): Estradiol and the control of food intake. Physiol. Behav. 99, 175-180 http://dx.doi.org/10.1016/j.physbeh.2009.06.010
8. Carey M. P., Deterd C. H., de Koning J., Helmerhorst F., de Kloet E. R. (1995): The influence of ovarian steroids on hypothalamicpituitary-adrenal regulation in the female rat. J. Endocrinol. 144, 311-321 http://dx.doi.org/10. 1677/joe.0.1440311
9. Chen Y., Heiman M. L. (2001): Increased weight gain after ovariectomy is not a consequence of leptin resistance. Am. J. Physiol. Endocrinol. Metab. 280, E315-322
10. Clegg D. J., Brown L. M., Zigman J. M., Kepm C. J., Strader A. D., Benoit S. C., Woods S. C., Mangiarancina M. M., Geary N. (2007): Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56,1051-1058 http://dx.doi.org/10.2337/db06-0015
11. Date Y., Murakami N., Toshinai K., Matsukura S., Niijima A., Matsuo H., Kangawa K., Nakazato M. (2002): The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterol. 123, 1120-1128 http://dx.doi.org/10.1053/gast.2002.35954
12. de la Cour C. D., Norlen P., Hakanson R. (2007): Secretion of ghrelin from rat stomach ghrelin cells in response to local microinfusion of candidate messenger compounds: a microdialysis study. Regul. Peptd. 143, 118-126 http://dx.doi.org/10.1016/j.regpep.2007.05.001
13. Eaton D. K., Kann L., Kinchen S., Ross J., Hawkins J., Harris W. A. (2006): Youth risk behavior surveillance-United States, 2005. MMWR Surveill. Summ. 55, 1-108
14. Eckel L. A., Houpt T. A., Geary N. (2002): Estradiol treatment increases CCKinduced c-Fos expression in the brains of ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R1378-1385
15. Epel E., Jimenez S., Brownell K., Stroud L., Stoney C., Niaura R. (2004): Are stress eaters at risk for the metabolic syndrome? Ann. N. Y. Acad. Sci. 1032, 208-210 http://dx.doi.org/10.1196/annals.1314.022
16. Flores A., Gallegos A. I., Velasco J., Mendoza F. D., Montiel C., Everardo P. M., Cruz M. E., Domínguez R. (2008): The acute effects of bilateral ovariectomy or adrenalectomy on progesterone, testosterone and estradiol serum levels depend on the surgical approach and the day of the estrous cycle when they are performed. Reprod. Biol. Endocrinol. 6, 1-7 http://dx.doi.org/10.1186/1477-7827-6-48
17. Gambineri A., Pagotto U., De Lasio R., Meriggiola M. C., Costantino A., Patton L. (2005): Short-term modification of sex hormones is associated with changes in ghrelin circulating levels in healthy normal-weight men. J. Endocrinol. Invest. 28, 241-246
18. Gao Q., Mezei G., Nie Y., Rao Y., Choi C. S., Bechmann I., Leranth C., Toran-Allerand D., Priest C. A. (2007): Anorectic estrogen mimics leptin's effect on the rewiring of melanocortin cells and Stat3 signaling in obese animals. Nat. Med. 13, 89-94 http://dx.doi.org/10.1038/nm1525
19. Geary N., Asarian L. (2001): Estradiol increases glucagon's satiating potency in ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281, R1290-1294
20. Greenman Y., Golani N., Gilad S., Yaron M., Limor R., Stern N. (2004): Ghrelin secretion is modulated in a nutrient-and gender-specific manner. Clin. Endocrinol. 60, 382-388 http://dx.doi.org/10.1111/j.1365-2265.2004.01993.x
21. Johnson J. G., Cohen P., Kasen S., Brook J. S. (2002): Childhood adversities associated with risk for eating disorders or weight problems during adolescence or early adulthood. Am. J. Psychiatry 159, 394-400 http://dx.doi.org/10.1176/appi.ajp.159.3.394
22. Kajantie E., Phillips D. I. W. (2005): The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31, 151-178 http://dx.doi.org/10.1016/j.psyneuen.2005. 07.002
23. Kalin M. F., Zumoff B. (1990): Sex hormones and coronary disease: a review of the clinical studies. Steroids 55, 330-352 http://dx.doi.org/10.1016/ 0039-128X(90)90058-J
24. Kellokoski E., Poykko S. M., Karjalainen A. H., Ukkola O., Heikkinen J., Kesaniemi Y. A., Horkko S. (2005): Estrogen replacement therapy increases plasma ghrelin levels. J. Clin. Endocrinol. Metab. 90, 2954-2963 http://dx.doi.org/10. 1210/jc.2004-2016
25. Kim M. S., Yoon C. Y., Park K. H., Shin C. S., Park K. S., Kim S. Y. (2003): Changes in ghrelin and ghrelin receptor expression according to feeding status. Neuroreport 14, 1317-1320
26. Klein S. L. (2000): The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24, 627-638 http://dx.doi.org/10.1016/S0149-7634(00)00027-0
27. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. (1999): Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402, 656-660 http://dx.doi.org/10.1038/45230
28. Kojima M., Kangawa K. (2005): Ghrelin: structure and function. Physiol. Rev. 85, 495-522 http://dx.doi.org/10.1152/physrev.00012.2004
29. Kristensson E., Sundqvist M., Astin M., Kjerling M., Mattsson H., Dornonville de la Cour C. (2006): Acute psychological stress raises plasma ghrelin in the rat. Regul. Pept. 134, 114-117 http://dx.doi.org/10.1016/j. regpep.2006.02.003
30. Levine A. S, Morley J. E. (1981): Stress-induced eating in rats. Am. J. Physiol. 241, R72-76
31. Liang Y. Q., Akishta M., Kim S., Ako J., Hashimoto M., Iijima K., Ohike Y., Watanabe T., Sudoh N. (2002): Estrogen receptor b is involved in the anorectic action of estrogen. Int. J. Obes. Relat. Metab. Disord. 26, 1103-1109 http://dx.doi.org/10.1038/sj.ijo.0802054
32. Loth K., van den Berg P., Eisenberg M. E., Neumark-Sztainer D. (2008): Stressful life events and disordered eating behaviors: Findings from Project EAT. J. Adolesc. Health 43, 514-516 http://dx.doi.org/10.1016/j.jadohealth.2008. 03.007
33. Lu S., Guan J. L., Wang Q. P., Uehara K., Yamada S., Goto N. (2002): Immunocytochemical observation of ghrelin-containing neurons in the rat arcuate nucleus. Neurosci. Lett. 321, 157-160 http://dx.doi.org/10.1016/S0304-3940(01) 02544-7
34. Maffeis C., Bonadonna R. C., Consolaro A., Vettor R., Banzato C., Silvagni D., Bogoni G., Pellegrino M., Tato L. (2006): Ghrelin, insulin sensitivity and postprandial glucose disposal in overweight and obese children. Eur. J. Endocrinol. 154, 61-68 http://dx.doi.org/10.1530/eje.1.02055
35. Matsubara M., Sakata I., Wada R., Yamazaki M., Inoue K., Sakai T. (2004): Estrogen modulates ghrelin expression in the female rat stomach. Peptides 25, 289-297 http://dx.doi.org/10.1016/j.peptides.2003.12.020
36. McElroy J. F., Wade G. N. (1987): Short-and long-term effects of ovariectomy on food intake, body weight, carcass composition, and brown adipose tissue in rats. Physiol. Behav. 39, 361-365 http://dx.doi.org/10.1016/0031- 9384(87)90235-6
37. Morley J. E., Levine A. S., Rowland N. E. (1983): Stress induced eating. Life. Sci. 32, 2169-2182 http://dx.doi.org/10.1016/0024-3205(83)90415-0
38. Mundinger T. O., Cummings D. E., Taborsky G. J. (2006): Direct stimulation of ghrelin secretion by sympathetic nerves. Endocrinology 147, 2893-2901 http://dx.doi.org/10.1210/en.2005-1182
39. Murata M., Okimura Y., Iida K., Matsumoto M., Sowa H., Kaji H., Kojima M., Kangawa K., Chihara K. (2002): Ghrelin modulates the downstream molecules of insulin signaling in hepatoma cells. J. Biol. Chem. 15, 5667-5674 http://dx.doi.org/10.1074/jbc.M103898200
40. National Institutes of Health (1992): Institutional Animal Care and Use Committee Guidebook. NIH Publication no. 92-3415.
41. Washington, D.C.: U.S. Government Printing Office. NAL call number: HV4764.I58 1992
42. Neumark-Sztainer D., Wall M., Guo J., Story M., Haines J., Eisenberg M. (2006): Obesity, disordered eating, and eating disorders in a longitudinal study of adolescents: how do dieters fare 5 years later? J. Am. Diet Assoc. 106, 559-568 http://dx.doi.org/10.1016/j.jada.2006.01.003
43. Patel A. D., Stanley S. A., Murphy K. G., Frost G. S., Gardiner J. V., Kent A. S., White N. E., Ghatei M. A., Bloom S. R. (2006): Ghrelin stimulates insulin-induced glucose uptake in adipocytes. Regul. Pept. 134, 17-22 http://dx.doi.org/10.1016/j.regpep.2005.11.001
44. Patterson Z. R., Ducharme R., Anisman H., Abizaid A. (2010): Altered metabolic and neurochemical responses to chronic unpredictable stressors in ghrelin receptor-deficient mice. Eur. J. Neurosci. 32, 632-639 http://dx.doi.org/10.1111/j.1460-9568.2010.07310.x
45. Patton G. C., Selzer R., Coffey C., Carlin J. B., Wolfe R. (1999): Onset of adolescent eating disorders: population based cohort study over 3 years. BMJ 318, 765-768 http://dx.doi.org/10.1136/bmj.318.7186.765
46. Pelletier G., Li S., Luu-The V., Labrie F. (2007): Oestrogenic regulation of pro-opiomelanocortin, neuropeptide Y and corticotrophinreleasing hormone mRNAs in mouse hypothalamus. J. Neuroendocrinol. 19, 426-431 http://dx.doi.org/10.1111/j.1365-2826.2007.01548.x
47. Pollard I., White B. M., Bassett J. R., Cairncross K. D. (1975): Plasma glucocorticoid elevation and desynchronization of the estrous cycle following unpredictable stress in the rat. Behav. Biol. 14, 103-108 http://dx.doi.org/10. 1016/S0091-6773(75)90374-0
48. Purnell J. Q., Weigle D. S., Breen P., Cummings D. E. (2003): Ghrelin levels correlate with insulin levels, insulin resistance, and highdensity lipoprotein cholesterol, but not with gender, menopausal status, or cortisol levels in humans. J. Clin. Endocrinol. Metab. 88, 5747-5752 http://dx.doi.org/ 10.1210/jc.2003-030513
49. Rouach V., Bloch M., Rosenberg N., Gilad S., Limor R., Stern N. (2007): The acute ghrelin response to a psychological stress challenge does not predict the post-stress urge to eat. Psychoneuroendocrinology 32, 693-702 http://dx.doi.org/10.1016/j.psyneuen.2007.04.010
50. Salbe A. D., De Tschop M. H. I., Parigi A., Venti C. A., Tataranni P. A. (2004): Negative relationship between fasting plasma ghrelin concentrations and ad libitum food intake. J. Clin. Endocrinol. Metabol. 89, 2951-2956 http://dx.doi.org/10.1210/jc.2003-032145
51. Santonastaso P., Friederici S., Favaro A. (1999): Full and partial syndromes in eating disorders: A 1-year prospective study of risk factors among female students. Psychopathology 32, 50-56 http://dx.doi.org/10.1159/000029067
52. Seale J. V., Wood S. A., Atkinson H. C., Bate E., Lightman S. L., Ingram C. D. (2004): Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. J. Neuroendocrinol. 16, 516-24 http://dx.doi.org/10.1111/j.1365- 2826.2004.01195.x
53. Sgoifo A., Koolhaas J., De Boer S., Musso E., Stilli D., Buwalda B., Meerlo P. (1999): Social stress, autonomic neural activation, and cardiac activity in rats. Neurosci. Biobehavioral. Rev. 23, 915-923 http://dx.doi.org/ 10.1016/S0149-7634(99)00025-1
54. Shiiya T., Nakazato M., Mizuta M., Date Y., Mondal M. S., Tanaka M., Nozoe S., Hosoda H., Kangawa K., Matsukura S. (2002): Plasma ghrelin levels in lean and obese humans and the effect of glucose on ghrelin secretion. J. Clin. Endocrinol. Metab. 87, 240-244 http://dx.doi.org/10.1210/jc.87.1.240
55. Shimomura K., Shimizu H., Tsuchiya T., Abe Y., Uehara Y., Mori M. (2002): Is leptin a key factor which develops obesity by ovariectomy? Endocr. J. 49, 417-423 http://dx.doi.org/10.1507/endocrj.49.417
56. Silva L. E. C. M., Castro M., Amara F. C., Antunes-Rodrigues J., Elias L. L. K. (2010): Estradiol-induced hypophagia is associated with the differential mRNA expression of hypothalamic neuropeptides. Braz. J. Med. Biol. Res. 43, 759-766 http://dx.doi.org/10.1590/S0100-879X2010007500059
57. Spencer S. J., Xu L., Clarke M. A., Lemus M., Reichenbach A., Geenen B., Kozicz T., Andrews Z. B. (2012): Ghrelin regulates the hypothalamic-pituitary- adrenal axis and restricts anxiety after acute stress. Biol. Psychiatry 72, 457-465 http://dx.doi.org/10.1016/j.biopsych.2012.03.010
58. Stambor Z. (2006): Stressed out nation. Monit. Psychol. 37, 28
59. Stengel A., Goebel M., Luckey A., Yuan P. Q., Wang L., Taché Y. (2010): Cold ambient temperature reverses abdominal surgeryinduced delayed gastric emptying and decreased plasma ghrelin levels in rats. Peptides 31, 2229-2235 http://dx.doi.org/10.1016/j.peptides.2010.08.026
60. Stice E., Nemeroff C., Shaw H. (1996): A test of the dual pathway model of bulimia nervosa: Evidence for restrained eating and affect regulation mechanisms. J. Soc. Clin. Psychol. 15, 140-363 http://dx.doi.org/10.1521/jscp. 1996.15.3.340
61. Stice E., Presnell K., Shaw H., Rohde P. (2005): Psychological and behavioral risk factors for obesity onset in adolescent girls: a prospective study. J. Consult. Clin. Psychol. 73, 195-202 http://dx.doi.org/10.1037/0022- 006X.73.2.195
62. Stone A. A., Brownell K. D. (1994): The stress-eating paradox: multiple daily measurements in adult males and females. Psychol. Health 9, 425-436 http://dx.doi.org/10.1080/08870449408407469
63. Torto R., Boghossian S., Dube M. G., Kalra P. S., Kalra S. P. (2006): Central leptin gene therapy blocks ovariectomy-induced adiposity. Obesity (Silver Spring) 14, 1312-1319 http://dx.doi.org/10.1038/oby.2006.149
64. Toshinai K., Mondal M. S., Nakazato M., Date Y., Murakami N., Kojima M. (2001): Upregulation of Ghrelin expression in the stomach upon fasting, insulin-induced hypoglycemia, and leptin administration. Biochem. Biophys. Res. Commun. 281, 1220-1225 http://dx.doi.org/10.1006/bbrc.2001.4518
65. Toth M. J., Poehlman E. T., Matthews D. E., Tchernof A., MacCoss M. J. (2001): Effects of estradiol and progesterone on body composition, protein synthesis, and lipoprotein lipase in rats. Am. J. Physiol. Endocrinol. Metab. 280, E496-501
66. Tschop M., Weyer C., Tataranni P.A., Devanarayan V., Ravussin E., Heiman M. L. (2001): Circulating ghrelin levels are decreased in human obesity. Diabetes 50, 707-709 http://dx.doi.org/10.2337/diabetes.50.4.707
67. Vendrell J., Broch M., Vilarrasa N., Molina A., Gomez J. M., Gutierrez C., Simon I., Soler J., Richart C. (2004): Resistin, adiponectin, ghrelin, leptin, and proinflammatory cytokines: relationships in obesity. Obes. Res. 12, 962-971 http://dx.doi.org/10.1038/oby.2004.118
68. Viau V., Meaney M. J. (1991): Variations in the hypothalamic-pituitary- adrenal response to stress during the estrous cycle in the rat. Endocrinol. 129, 2503-2511 http://dx.doi.org/10.1210/endo-129-5-2503
69. Vilarrasa N., Vendrell J., Maravall J., Broch M., Estepa A., Megia A., Soler J., Simon I., Richart C., Gomez J. M. (2005): Distribution and determinants of adiponectin, resistin and ghrelin in a randomly selected healthy population. Clin. Endocrinol. 63, 329-335 http://dx.doi.org/10.1111/j.1365- 2265.2005.02346.x
70. Wang L., Basa N. R., Shaikh A., Luckey A., Heber D., St-Pierre D. H. (2006): LPS inhibits fasted plasma ghrelin levels in rats: role of IL-1 and PGs and functional implications. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G611-620 http://dx.doi.org/10.1152/ajpgi.00533.2005
71. Weiss L. A., Langenberg C., Barrett-Connor E. (2006): Ghrelin and bone: is there an association in older adults? The Rancho Bernardo study. J. Bone Miner. Res. 21, 752-757 http://dx.doi.org/10.1359/jbmr.060209
72. Whitcare C. C., Reingold S. C., O'Looney P. A. (1999): The task force on gender, multiple sclerosis and autoimmunity. A gender cap in autoimmunity. Science 283, 1277-1278
73. Wren A. M., Seal L. J., Cohen M. A., Brynes A. E., Frost G. S., Murphy K. G., Dhillo W. S., Ghatei M. A., Bloom S. R. (2001): Ghrelin enhances appetite and increases food intake in humans. J. Clin. Endocrinol. Metab. 86, 5992-5995 http://dx.doi.org/10.1210/jc.86.12.5992
74. Xu G., Li Y., An W., Li S., Guan Y., Wang N. (2009): Gastric mammalian target of rapamycin signaling regulates ghrelin production and food intake. Endocrinol. 150, 3637-3644 http://dx.doi.org/10.1210/en.2009-0372
75. Yu P. L., Wu C. I., Lee T. S., Pan W. H., Wang P. S., Wang S. W. (2009): Attenuation of estradiol on the reduction of striatal dopamine by amphetamine in ovariectomized rats. J. Cell. Biochem. 108, 1318-1324 http://dx.doi.org/10. 1002/jcb.22361
76. Zellner D. A., Loaiza S., Gonzalez Z., Pita J., Morales J., Pecora D. (2006): Food selection changes under stress. Physiol. Behav. 87, 789-793 http://dx.doi.org/10.1016/j.physbeh.2006.01.014
77. Zhao T. J., Sakata I., Li R. L., Liang G., Richardson J. A., Brown M. S., Goldstein J. L., Zigman J. M. (2010): Ghrelin secretion stimulated byα-adrenergic receptors in cultured ghrelinoma cells and in fasted mice. Proc. Natl. Acad. Sci. USA 107, 15868-15873 http://dx.doi.org/10.1073/pnas. 1011116107
78. Zheng J., Dobner A., Babygirija R., Ludwig K., Takahashi T. (2009): Effects of repeated restraint stress on gastric motility in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R1358-1365 http://dx.doi.org/10. 1152/ajpregu.90928.2008