Streptozotocin-induced diabetes disrupts the body temperature daily rhythm in rats

Diabetology and Metabolic Syndrome

Volumn 7, Issue 1, 2015, Pages

  Ramos Lobo, Angela M ^a   Buonfiglio, Daniella C ^a   Cipolla Neto, José ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Daily rhythms; Insulin; Melatonin; Type 1 diabetes mellitus

Indexed keywords

GLUCOSE; HUMAN INSULIN; INSULIN GLARGINE; MELATONIN;

ACROPHASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY TEMPERATURE; BODY WEIGHT; CIRCADIAN RHYTHM; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; HIGH TEMPERATURE; HYPERGLYCEMIA; HYPOTHERMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; LOW TEMPERATURE; MALE; METABOLISM; NONHUMAN; PRIORITY JOURNAL; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; WEIGHT GAIN; WISTAR RAT;

EID: 84929090340     PISSN: None     EISSN: 17585996     Source Type: Journal    
DOI: 10.1186/s13098-015-0035-2     Document Type: Article

References (58)

1. Karatsoreos IN, Bhagat S, Bloss EB, Morrison JH, McEwen BS. Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci U S A. 2011;108(4):1657-62.
2. Minors DS, Folkard S, Waterhouse JM. The shape of the endogenous circadian rhythm of rectal temperature in humans. Chronobiol Int. 1996;13(4):261-71.
3. Hanneman SK. Measuring circadian temperature rhythm. Biol Res Nurs. 2001;2(4):236-48.
4. Kelly G. Body temperature variability (Part 1): a review of the history of body temperature and its variability due to site selection, biological rhythms, fitness, and aging. Altern Med Rev. 2006;11(4):278-93.
5. Scheer FA, Pirovano C, Van Someren EJ, Buijs RM. Environmental light and suprachiasmatic nucleus interact in the regulation of body temperature. Neuroscience. 2005;132(2):465-77.
6. la Fleur SE, Kalsbeek A, Wortel J, Fekkes ML, Buijs RM. A daily rhythm in glucose tolerance: a role for the suprachiasmatic nucleus. Diabetes. 2001;50(6):1237-43.
7. la Fleur SE, Kalsbeek A, Wortel J, van der Vliet J, Buijs RM. Role for the pineal and melatonin in glucose homeostasis: pinealectomy increases night-time glucose concentrations. J Neuroendocrinol. 2001;13(12):1025-32.
8. Reiter RJ, Tan DX, Korkmaz A. The circadian melatonin rhythm and its modulation: possible impact on hypertension. J Hypertens Suppl. 2009;27(6):S17-20.
9. Peschke E, Frese T, Chankiewitz E, Peschke D, Preiss U, Schneyer U, et al. Diabetic Goto Kakizaki rats as well as type 2 diabetic patients show a decreased diurnal serum melatonin level and an increased pancreatic melatonin-receptor status. J Pineal Res. 2006;40(2):135-43.
10. Peschke E, Stumpf I, Bazwinsky I, Litvak L, Dralle H, Muhlbauer E. Melatonin and type 2 diabetes - a possible link? J Pineal Res. 2007;42(4):350-8.
11. Goncharova ND, Vengerin AA, Khavinson V, Lapin BA. Pineal peptides restore the age-related disturbances in hormonal functions of the pineal gland and the pancreas. Exp Gerontol. 2005;40(1-2):51-7.
12. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci U S A. 2009;106(11):4453-8.
13. Boden G, Chen X, Polansky M. Disruption of circadian insulin secretion is associated with reduced glucose uptake in first-degree relatives of patients with type 2 diabetes. Diabetes. 1999;48(11):2182-8.
14. Scott EM, Carter AM, Grant PJ. Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man. Int J Obes (Lond). 2008;32(4):658-62.
15. Woon PY, Kaisaki PJ, Braganca J, Bihoreau MT, Levy JC, Farrall M, et al. Aryl hydrocarbon receptor nuclear translocator-like (BMAL1) is associated with susceptibility to hypertension and type 2 diabetes. Proc Natl Acad Sci U S A. 2007;104(36):14412-7.
16. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature. 2010;466(7306):627-31.
17. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science. 2005;308(5724):1043-5.
18. Yoon JA, Han DH, Noh JY, Kim MH, Son GH, Kim K, et al. Meal time shift disturbs circadian rhythmicity along with metabolic and behavioral alterations in mice. PLoS One. 2012;7(8), e44053.
19. Hasler BP, Buysse DJ, Kupfer DJ, Germain A. Phase relationships between core body temperature, melatonin, and sleep are associated with depression severity: further evidence for circadian misalignment in non-seasonal depression. Psychiatry Res. 2010;178(1):205-7.
20. Gubin DG, Gubin GD, Waterhouse J, Weinert D. The circadian body temperature rhythm in the elderly: effect of single daily melatonin dosing. Chronobiol Int. 2006;23(3):639-58.
21. Wolden-Hanson T, Mitton DR, McCants RL, Yellon SM, Wilkinson CW, Matsumoto AM, et al. Daily melatonin administration to middle-aged male rats suppresses body weight, intraabdominal adiposity, and plasma leptin and insulin independent of food intake and total body fat. Endocrinology. 2000;141(2):487-97.
22. Alonso-Vale MI, Anhe GF, Borges-Silva C, Andreotti S, Peres SB, Cipolla-Neto J, et al. Pinealectomy alters adipose tissue adaptability to fasting in rats. Metab Clin Exp. 2004;53(4):500-6.
23. Alonso-Vale MI, Borges-Silva CN, Anhe GF, Andreotti S, Machado MA, Cipolla-Neto J, et al. Light/dark cycle-dependent metabolic changes in adipose tissue of pinealectomized rats. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme. 2004;36(7):474-9.
24. Muhlbauer E, Gross E, Labucay K, Wolgast S, Peschke E. Loss of melatonin signalling and its impact on circadian rhythms in mouse organs regulating blood glucose. Eur J Pharmacol. 2009;606(1-3):61-71.
25. Cipolla-Neto J, Amaral FG, Afeche SC, Tan DX, Reiter RJ. Melatonin, energy metabolism, and obesity: a review. J Pineal Res. 2014;56(4):371-81.
26. Krauchi K, Cajochen C, Wirz-Justice A. A relationship between heat loss and sleepiness: effects of postural change and melatonin administration. J Appl Physiol (1985). 1997;83(1):134-9.
27. Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94(3):311-21.
28. King AJ. The use of animal models in diabetes research. Br J Pharmacol. 2012;166(3):877-94.
29. Howarth FC, Jacobson M, Naseer O, Adeghate E. Short-term effects of streptozotocin-induced diabetes on the electrocardiogram, physical activity and body temperature in rats. Exp Physiol. 2005;90(2):237-45.
30. Howarth FC, Jacobson M, Shafiullah M, Ljubisavljevic M, Adeghate E. Heart rate, body temperature and physical activity are variously affected during insulin treatment in alloxan-induced type 1 diabetic rat. Physiological research / Academia Scientiarum Bohemoslovaca. 2011;60(1):65-73.
31. Kilgour RD, Williams PA. Diabetes affects blood pressure and heart rate responses during acute hypothermia. Acta Physiol Scand. 1998;162(1):27-32.
32. Howarth FC, Jacobson M, Shafiullah M, Adeghate E. Long-term effects of streptozotocin-induced diabetes on the electrocardiogram, physical activity and body temperature in rats. Exp Physiol. 2005;90(6):827-35.
33. Howarth FC, Jacobson M, Shafiullah M, Adeghate E. Effects of insulin treatment on heart rhythm, body temperature and physical activity in streptozotocin-induced diabetic rat. Clin Exp Pharmacol P. 2006;33(4):327-31.
34. Seydoux J, Chinet A, Schneider-Picard G, Bas S, Imesch E, Assimacopoulos-Jeannet F, et al. Brown adipose tissue metabolism in streptozotocin-diabetic rats. Endocrinology. 1983;113(2):604-10.
35. Kilgour RD, Williams PA. Effects of diabetes and food deprivation on shivering activity during progressive hypothermia in the rat. Comp Biochem Physiol A Physiol. 1996;114(2):159-65.
36. Smith OL, Davidson SB. Shivering thermogenesis and glucose uptake by muscles of normal or diabetic rats. Am J Physiol. 1982;242(1):R109-15.
37. Peschke E, Bahr I, Muhlbauer E. Melatonin and pancreatic islets: interrelationships between melatonin, insulin and glucagon. Int J Mol Sci. 2013;14(4):6981-7015.
38. Amaral FG, Turati AO, Barone M, Scialfa JH, do Carmo Buonfiglio D, Peres R, et al. Melatonin synthesis impairment as a new deleterious outcome of diabetes-derived hyperglycemia. J Pineal Res. 2014;57(1):67-79.
39. do Carmo Buonfiglio D, Peliciari-Garcia RA, do Amaral FG, Peres R, Nogueira TCA, Afeche SC, et al. Early-stage retinal melatonin synthesis impairment in streptozotocin-induced diabetic wistar rats. Invest Ophthalmol Vis Sci. 2011;52(10):7416-22.
40. Nishida S. Metabolic effects of melatonin on oxidative stress and diabetes mellitus. Endocrine. 2005;27(2):131-6.
41. Harkin A, O'Donnell JM, Kelly JP. A study of VitalView for behavioural and physiological monitoring in laboratory rats. Physiol Behav. 2002;77(1):65-77.
42. Sochor M, Baquer NZ, Ball MR, McLean P. Regulation of enzymes of glucose metabolism and lipogenesis in diabetic rat liver by thyroid hormones. Biochem Int. 1987;15(3):619-27.
43. Sundaresan PR, Sharma VK, Gingold SI, Banerjee SP. Decreased beta-adrenergic receptors in rat heart in streptozotocin-induced diabetes: role of thyroid hormones. Endocrinology. 1984;114(4):1358-63.
44. Rodgers RL, Davidoff AJ, Mariani MJ. Cardiac function of the diabetic renovascular hypertensive rat: effects of insulin and thyroid hormone treatment. Can J Physiol Pharmacol. 1991;69(3):346-54.
45. Rondeel JM, de Greef WJ, Heide R, Visser TJ. Hypothalamo-hypophysial-thyroid axis in streptozotocin-induced diabetes. Endocrinology. 1992;130(1):216-20.
46. der Elst JP S-v, van der Heide D. Effects of streptozocin-induced diabetes and food restriction on quantities and source of T4 and T3 in rat tissues. Diabetes. 1992;41(2):147-52.
47. Katovich MJ, Marks KS, Sninsky CA. Effect of insulin on the altered thyroid function and adrenergic responsiveness in the diabetic rat. Can J Physiol Pharmacol. 1993;71(8):568-75.
48. Zhang L, Parratt JR, Beastall GH, Pyne NJ, Furman BL. Streptozotocin diabetes protects against arrhythmias in rat isolated hearts: role of hypothyroidism. Eur J Pharmacol. 2002;435(2-3):269-76.
49. Matsen ME, Thaler JP, Wisse BE, Guyenet SJ, Meek TH, Ogimoto K, et al. In uncontrolled diabetes, thyroid hormone and sympathetic activators induce thermogenesis without increasing glucose uptake in brown adipose tissue. Am J Physiol Endocrinol Metab. 2013;304(7):E734-46.
50. Yang YL, Shen ZL, Tang Y, Wang N, Sun B. [Simultaneous telemetric analyzing of the temporal relationship for the changes of the circadian rhythms of brown adipose tissue thermogenesis and core temperature in the rat]. Zhongguo ying yong sheng li xue za zhi∈=∈Zhongguo yingyong shenglixue zazhi =Chinese journal of applied physiology. 2011;27(3):348-52.
51. Havel PJ, Uriu-Hare JY, Liu T, Stanhope KL, Stern JS, Keen CL, et al. Marked and rapid decreases of circulating leptin in streptozotocin diabetic rats: reversal by insulin. Am J Physiol. 1998;274(5 Pt 2):R1482-91.
52. Rezai-Zadeh K, Munzberg H. Integration of sensory information via central thermoregulatory leptin targets. Physiol Behav. 2013;121:49-55.
53. Cagnacci A, Elliott JA, Yen SS. Melatonin: a major regulator of the circadian rhythm of core temperature in humans. J Clin Endocrinol Metab. 1992;75(2):447-52.
54. Teodoro BG, Baraldi FG, Sampaio IH, Bomfim LH, Queiroz AL, Passos MA, et al. Melatonin prevents mitochondrial dysfunction and insulin resistance in rat skeletal muscle. J Pineal Res. 2014;57(2):155-67.
55. Lin MT, Chuang JI. Melatonin potentiates 5-HT(1A) receptor activation in rat hypothalamus and results in hypothermia. J Pineal Res. 2002;33(1):14-9.
56. de Fronzo RA, Hendler R, Simonson D. Insulin resistance is a prominent feature of insulin-dependent diabetes. Diabetes. 1982;31(9):795-801.
57. Anhe GF, Caperuto LC, Pereira-Da-Silva M, Souza LC, Hirata AE, Velloso LA, et al. In vivo activation of insulin receptor tyrosine kinase by melatonin in the rat hypothalamus. J Neurochem. 2004;90(3):559-66.
58. Zanquetta MM, Seraphim PM, Sumida DH, Cipolla-Neto J, Machado UF. Calorie restriction reduces pinealectomy-induced insulin resistance by improving GLUT4 gene expression and its translocation to the plasma membrane. J Pineal Res. 2003;35(3):141-8.