Effect of the estrous cycle and surgical ovariectomy on energy balance, fuel utilization, and physical activity in lean and obese female rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 6, 2010, Pages

  Giles, Erin D ^a   Jackman, Matthew R ^a   Johnson, Ginger C ^a   Schedin, Pepper J ^b   Houser, Jordan L ^a   MacLean, Paul S ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Energy expenditure; Energy intake; Indirect calorimetry; Menopause; Spontaneous activity

Indexed keywords

FUEL;

ANIMAL EXPERIMENT; ARTICLE; CALORIMETER; ENERGY BALANCE; ESTRUS CYCLE; FEMALE; LEAN BODY WEIGHT; LIPID DIET; METABOLISM; NONHUMAN; OBESITY; OVARIECTOMY; PHYSICAL ACTIVITY; POSTMENOPAUSE; PRIORITY JOURNAL; RAT; WEIGHT GAIN;

ANIMALS; BODY COMPOSITION; CALORIMETRY, INDIRECT; DIET; DIETARY FATS; ENERGY INTAKE; ENERGY METABOLISM; ESTROUS CYCLE; FEMALE; MOTOR ACTIVITY; OBESITY; OVARIECTOMY; RATS; RATS, WISTAR;

EID: 78649820153     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00219.2010     Document Type: Article

References (54)

1. Anantharaman-Barr HG, Decombaz J. The effect of wheel running and the estrous cycle on energy expenditure in female rats. Physiol Behav 46: 259-263, 1989.
2. Anderson JW, Kendall CW, Jenkins DJ. Importance of weight management in type 2 diabetes: review with meta-analysis of clinical studies. J Am Coll Nutr 22: 331-339, 2003.
3. Arney DR, Kitwood SE, Phillips CJC. The increase in activity during estrus in dairy-cows. Appl Anim Behav Sci 40: 211-218, 1994.
4. Asarian L, Geary N. Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm Behav 42: 461-471, 2002.
5. Asarian L, Geary N. Cyclic estradiol treatment phasically potentiates endogenous cholecystokinin's satiating action in ovariectomized rats. Peptides 20: 445-450, 1999.
6. Asarian L, Geary N. Modulation of appetite by gonadal steroid hormones. Philos Trans R Soc Lond B Biol Sci 361: 1251-1263, 2006.
7. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, Herman JP, Marts S, Sadee W, Steiner M, Taylor J, Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146: 1650-1673, 2005.
8. Bouthegourd JC, Martin JC, Gripois D, Roseau S, Tome D, Even PC. Fat-depleted CLA-treated mice enter torpor after a short period of fasting. Appetite 42: 91-98, 2004.
9. Brobeck JR, Wheatland M, Strominger JL. Variations in regulation of energy exchange associated with estrus, diestrus and pseudopregnancy in rats. Endocrinology 40: 65-72, 1947.
10. Butera PC. Estradiol and the control of food intake. Physiol Behav 99: 175-180, 2010.
11. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4: 579-591, 2004.
12. Chang S, Graham B, Yakubu F, Lin D, Peters JC, Hill JO. Metabolic differences between obesity-prone and obesity-resistant rats. Am J Physiol Regul Integr Comp Physiol 259: R1103-R1110, 1990.
13. Chen Y, Heiman ML. Chronic leptin administration promotes lipid utilization until fat mass is greatly reduced and preserves lean mass of normal female rats. Regul Pept 92: 113-119, 2000.
14. Chen Y, Heiman ML. Increased weight gain after ovariectomy is not a consequence of leptin resistance. Am J Physiol Endocrinol Metab 280: E315-E322, 2001. (Pubitemid 32479661)
15. Clegg DJ, Brown LM, Zigman JM, Kemp CJ, Strader AD, Benoit SC, Woods SC, Mangiaracina M, Geary N. Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56: 1051-1058, 2007.
16. Donovan BT. Wheel-running during anoestrus and oestrus in the ferret. Physiol Behav 34: 825-829, 1985.
17. Eckel LA, Houpt TA, Geary N. Spontaneous meal patterns in female rats with and without access to running wheels. Physiol Behav 70: 397-405, 2000.
18. Flatt JP, Tremblay A. Energy expenditure and substrate oxidation. In: Handbook of Obesity, edited by Bray GA, James WPT. New York: Decker, 1998, p. 513-537.
19. Freeman ME. The neuroendocrine control of the ovarian cycle of the rat. In: The Physiology of Reproduction, edited by Knobil E, Neill JD. New York: Raven, 1994, p. 613-658.
20. Galgani J, Ravussin E. Energy metabolism, fuel selection and body weight regulation. Int J Obes (Lond) 32 Suppl 7: S109-S119, 2008.
21. Galgani JE, Moro C, Ravussin E. Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 295: E1009-E1017, 2008.
22. Gao Q, Horvath TL. Cross-talk between estrogen and leptin signaling in the hypothalamus. Am J Physiol Endocrinol Metab 294: E817-E826, 2008.
23. Geary N, Asarian L. Cyclic estradiol treatment normalizes body weight and test meal size in ovariectomized rats. Physiol Behav 67: 141-147, 1999.
24. Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health 9: 88, 2009.
25. Henry BA, Clarke IJ. Adipose tissue hormones and the regulation of food intake. J Neuroendocrinol 20: 842-849, 2008.
26. Jackman MR, MacLean PS, Bessesen DH. Energy expenditure in obesity-prone and obesity-resistant rats before and after the introduction of a high-fat diet. Am J Physiol Regul Integr Comp Physiol 299: R1097-R1105, 2010.
27. Jackman MR, Steig A, Higgins JA, Johnson GC, Fleming-Elder BK, Bessesen DH, Maclean PS. Weight regain after sustained weight reduction is accompanied by suppressed oxidation of dietary fat and adipocyte hyperplasia. Am J Physiol Regul Integr Comp Physiol 294: R1117-R1129, 2008.
28. Kelley DE. Skeletal muscle triglycerides: an aspect of regional adiposity and insulin resistance. Ann NY Acad Sci 967: 135-145, 2002.
29. Kelley DE, Goodpaster BH, Storlien L. Muscle triglyceride and insulin resistance. Annu Rev Nutr 22: 325-346, 2002.
30. Laudenslager ML, Wilkinson CW, Carlisle HJ, Hammel HT. Energy balance in ovariectomized rats with and without estrogen replacement. Am J Physiol Regul Integr Comp Physiol 238: R400-R405, 1980.
31. Levin BE, Dunn-Meynell AA, Banks WA. Obesity-prone rats have normal blood-brain barrier transport but defective central leptin signaling before obesity onset. Am J Physiol Regul Integr Comp Physiol 286: R143-R150, 2004.
32. Long JA, Evans HM. The Oestrous Cycle in the Rat and Its Associated Phenomena. Berkeley, CA: University of California Press, 1922.
33. MacLean PS, Giles ED, Johnson GC, McDaniel SM, Fleming-Elder BK, Gilman KA, Andrianakos AG, Jackman MR, Shroyer KR, Schedin PJ. A surprising link between the energetics of ovariectomy-induced weight gain and mammary tumor progression in obese rats. Obesity (Silver Spring) 18: 696-703, 2010.
34. MacLean PS, Higgins JA, Jackman MR, Johnson GC, Fleming-Elder BK, Wyatt HR, Melanson EL, Hill JO. Peripheral metabolic responses to prolonged weight reduction that promote rapid, efficient regain in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 290: R1577-R1588, 2006.
35. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Donahoo WT, Melanson EL, Hill JO. Enhanced metabolic efficiency contributes to weight regain after weight loss in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 287: R1306-R1315, 2004.
36. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Peters JC, Hill JO. Metabolic adjustments with the development, treatment, and recurrence of obesity in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 287: R288-R297, 2004.
37. Meli R, Pacilio M, Raso GM, Esposito E, Coppola A, Nasti A, Di Carlo C, Nappi C, Di Carlo R. Estrogen and raloxifene modulate leptin and its receptor in hypothalamus and adipose tissue from ovariectomized rats. Endocrinology 145: 3115-3121, 2004.
38. Moline ML, Albers HE. Response of circadian locomotor activity and the proestrous luteinizing hormone surge to phase shifts of the light-dark cycle in the hamster. Physiol Behav 43: 435-440, 1988.
39. Mori MA, Araujo RC, Pesquero JB. Kinin B1 receptor stimulation modulates leptin homeostasis. Evidence for an insulin-dependent mechanism. Int Immunopharmacol 8: 242-246, 2008.
40. Murakami DM, Horwitz BA, Fuller CA. Circadian rhythms of temperature and activity in obese and lean Zucker rats. Am J Physiol Regul Integr Comp Physiol 269: R1038-R1043, 1995.
41. Noel R, Fleming A. Effects of prefattening on ovariectomy-induced hyperphagia and weight gain in rats. Behav Biol 19: 405-410, 1977. (Pubitemid 8076187)
42. Osler M. Obesity and cancer. A review of epidemiological studies on the relationship of obesity to cancer of the colon, rectum, prostate, breast, ovaries, and endometrium. Dan Med Bull 34: 267-274, 1987.
43. Parker GC, McKee ME, Bishop C, Coscina DV. Whole-body metabolism varies across the estrous cycle in Sprague-Dawley rats. Physiol Behav 74: 399-403, 2001. (Pubitemid 33070415)
44. Pelleymounter MA, Baker MB, McCaleb M. Does estradiol mediate leptin's effects on adiposity and body weight? Am J Physiol Endocrinol Metab 276: E955-E963, 1999.
45. Reeves GK, Pirie K, Beral V, Green J, Spencer E, Bull D. Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ 335: 1134, 2007.
46. Rogers NH, Perfield JW 2nd, Strissel KJ, Obin MS, Greenberg AS. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 150: 2161-2168, 2009.
47. Schedin P, Mitrenga T, Kaeck M. Estrous cycle regulation of mammary epithelial cell proliferation, differentiation, and death in the Sprague- Dawley rat: a model for investigating the role of estrous cycling in mammary carcinogenesis. J Mammary Gland Biol Neoplasia 5: 211-225, 2000.
48. Schutz Y. Dietary fat, lipogenesis and energy balance. Physiol Behav 83: 557-564, 2004.
49. Shaw MA, Whitaker EM, Hervey E, Hervey GR. The effects of ovarian hormones on regulation of energy balance in Zucker rats. J Endocrinol 98: 165-171, 1983.
50. Teske JA, Kotz CM. Effect of acute and chronic caloric restriction and metabolic glucoprivation on spontaneous physical activity in obesity-prone and obesity-resistant rats. Am J Physiol Regul Integr Comp Physiol 297: R176-R184, 2009.
51. Vona-Davis L, Rose DP. Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr Relat Cancer 14: 189-206, 2007.
52. Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev 16: 235-272, 1992.
53. Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109: 1-9, 1949.
54. Witte MM, Resuehr D, Chandler AR, Mehle AK, Overton JM. Female mice and rats exhibit species-specific metabolic and behavioral responses to ovariectomy. Gen Comp Endocrinol 166: 520-528, 2010.