Hypothalamus-pituitary-thyroid axis activity and function of cardiac muscle in energy deficit
Katarzyna Lachowicz 1 , Ewelina Pałkowska-Goździk 1 , Danuta Rosołowska-Huszcz 1Abstract
Frequently repeated statement that energy restriction is a factor that improves cardiovascular system function seems to be not fully truth. Low energy intake modifies the hypothalamus-pituitary-thyroid axis activity and thyroid hormone peripheral metabolism. Thyroid hormones, as modulators of the expression and activity of many cardiomyocyte proteins, control heart function. Decreased thyroid hormone levels and their disturbanced conversion and action result in alternation of cardiac remodeling, disorder of calcium homeostasis and diminish myocardial contractility. This review provides a summary of the current state of knowledge about the mechanisms of energy restriction effects on thyroidal axis activity, thyroid hormone peripheral metabolism and action in target tissues, especially in cardiac myocytes. We also showed the existence of energy restriction-thyroid-heart pathway.
References
- 1. Aceves C., Escobar C., Rojas-Huidobro R., Vázquez-Martínez O., Martínez-Merlos T., Aguilar-Roblero R., Díaz-Muñoz M.: Liver 5’-deiodinase activity is modified in rats under restricted feeding schedules: evidence for post-translational regulation. J. Endocrinol., 2003; 179: 91-96
Google Scholar - 2. Afifi O.K.: Effect of long term food-restriction (low-caloric diet) on pars distalisof the anterior pituitary gland of adult male albino rats: a biochemicaland histological study. Egypt. J. Histol., 2010; 33: 236-244
Google Scholar - 3. Ahima R.S., Kelly J., Elmquist J.K., Flier J.S.: Distinct physiologic and neuronal responses to decreased leptin and mild hyperleptinemia. Endocrinology, 1999; 140: 4923-4931
Google Scholar - 4. Ahmet I., Tae H.J., de Cabo R., Lakatta E.G., Talan M.I.: Effects of calorie restriction on cardioprotection and cardiovascular health. J. Mol. Cell. Cardiol., 2011; 51: 263-271
Google Scholar - 5. Ahmet I., Tae H.J., de Cabo R., Lakatta E.G., Talan M.I.: Effects of calorie restriction on cardioprotection and cardiovascular health. J. Mol. Cell. Cardiol., 2011; 51: 263-271
Google Scholar - 6. Amin A., Dhillo W.S., Murphy K.G.: The central effect of thyroid hormones on appetite. J. Thyroid Res., 2011; 2011: 1-7
Google Scholar - 7. Araujo R.L., De Andrade B.M., Da Silva M.L., Ferreira A.C., Carvalho D.P.: Tissue-specific deiodinase regulation during food restriction and low replacement dose of leptin in rats. Am. J. Physiol. Endocrinol. Metab., 2009; 296: E1157-E1163
Google Scholar - 8. Araujo R.L., De Andrade B.M., De Figueiredo A.S., Da Silva M.L., Marassi M.P., Pereira Vdos S., Bouskela E., Carvalho D.P.: Low replacement doses of thyroxine during food restriction restores type 1 deiodinase activity in rats and promotes body protein loss. J. Endocrinol., 2008; 198: 119-125
Google Scholar - 9. Biondi B.: Heart failure and thyroid dysfunction. Eur. J. Endocrinol., 2012; 167: 609-618
Google Scholar - 10. Biondi B., Klein I.: Hypothyroidism as a risk factor for cardiovascular disease. Endocrine, 2004; 24: 1-13
Google Scholar - 11. Boelen A., Kwakkel J., Thijssen-Timmer, Alkemade A., Fliers E., Wiersinga W.M.: Simultaneous changes in central and peripheral components of the hypothalamus-pituitary-thyroid axis in lipopolysaccharide-induced acute illness in mice. J. Endocrinol., 2004; 182: 315-323
Google Scholar - 12. Boelen A., Kwakkel J., Vos X.G., Wiersinga W.M., Fliers E.: Differential effects of leptin and refeeding on the fasting-induced decrease of pituitary type 2 deiodinase and thyroid hormone receptor β2 mRNA expression in mice. J. Endocrinol., 2006; 190: 537-544
Google Scholar - 13. Boelen A., Kwakkel J., Wiersinga W.M., Fliers E.: Chronic local inflammation in mice results in decreased TRH and type 3 deiodinase mRNA expression in the hypothalamic paraventicular nucleus independently of diminished food intake. J. Endocrinol., 2006; 191: 707-714
Google Scholar - 14. Boelen A., Van Beeren M., Vos X., Surovtseva O. Belegri E., Saaltink D.J., Vreugdenhil E., Kaksbeek A, Kwakkel J., Fliers E.: Thyroid, 2012; 22: 192-199 [15] Boelen A., Wiersinga W.M., Fliers E.: Fasting induced changes in the hypothalamus-pituitary-thyroid axis. Thyroid, 2008; 18: 123-129
Google Scholar - 15. Boelen A., Wiersinga W.M., Fliers E.: Fasting induced changes in the hypothalamus-pituitary-thyroid axis. Thyroid, 2008; 18: 123-129
Google Scholar - 16. Castello L., Froio T., Maina M., Cavallini G., Biasi F., Leonarduzzi G., Donati A., Bergamini E., Poli G., Chiarpotto E.: Alternate-day fasting protects the rat heart against age-induced inflammation and fibrosis by inhibiting oxidative damage and NF-κB activation. Free Radic. Biol. Med., 2010; 48: 47-54
Google Scholar - 17. Chan J.L., Heist K., DePaoli A.M., Veldhuis J.D., Mantzoros C.S.: The role of falling leptin levels in the neuroendocrineand metabolic adaptation to short-term starvationin healthy men. J. Clin. Invest., 2003; 111: 1409-1421
Google Scholar - 18. Chen C., Cheng X., Dieter M.Z., Tanaka Y., Klaassen C.D: Activation of cAMP-dependent signaling pathway induces mouse organic anion transporting polypeptide 2 expression. Mol. Pharmacol., 2007; 71: 1159-1164
Google Scholar - 19. Cicogna A., Padavani C.R., Okoshi K., Matsubara L.S., Aragon F.F., Okoshi M.P.: The influence of temporal food restriction on performance of isolated cardiac muscle. Nutr. Res., 2001; 21: 639-648
Google Scholar - 20. Coppola A., Hughes J., Esposito E., Schiavo L., Meli R., Diano S.: Suppression of hypothalamic deiodinase type II activity blunts TRH mRNA decline during fasting. FEBS Lett., 2005; 579: 4654-4658
Google Scholar - 21. Coppola A., Liu Z.W., Andrews Z.B., Paradis E., Roy M.C., Friedman J.M., Ricquier D., Richard D., Horvath T.L., Gao X.B, Diano S.: Central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab., 2007; 5: 21-33
Google Scholar - 22. Coppola A., Meli R., Diano S.: Inverse shift in circulating corticosterone and leptin levels elevates hypothalamic deiodinase type 2 in fasted rats. Endocrinology, 2005; 146: 2827-2833
Google Scholar - 23. Danzi S., Oamaa K., Klein I.: Triiodothyronine-mediated myosin heavy chain gene transcription in the heart. Am. J. Physiol. Heart Circ. Physiol., 2003; 288: H2255-H2262
Google Scholar - 24. Darras V.M., Cokelaere M., Dewil M., Arnouts S., Decuypere E., Kühn E.R.: Partial food restriction increases inner ring deiodinating activity in the chicken and the rat. Gen. Comp. Endocrinol., 1995; 100: 334-338
Google Scholar - 25. Darras V.M., Mol K.A., Van der Geyten S., Kühn E.R.: Control of peripheral thyroid hormone levels by activating and inactivating deiodinases. Trends Comp. Endocrinol. Neurobiol., 1998; 839: 80-86
Google Scholar - 26. De Gortari P., Alvarez-Salas E., Morales-Mulia M., AlcantaraAlonso V.: Differential adaptations of the hypothalamus-pituitarythyroid axis between food restriction and anorexia. W: Hypothyroidism – influence and treatment, red.: D. Springer. In Tech, 2012, 68-96
Google Scholar - 27. De Jong M.: Transport of T3, into the perfused rat liver and subsequent metabolism are inhibited by fasting. w: Thyroid hormone transport into liver cells: its (patho)physiological significance. Pracadoktorska, 1993; 55-74
Google Scholar - 28. De Tomasi L.C., Sugizaki M.M., Lima-Leopoldo A.P., Nascimento A.F., De Oliveira A., Pinotti M.F., Padovani C.R., Leopoldo A.S., Cicogna A.C.: Food restriction promotes downregulation of myocardial L-type Ca2+ channels. Can. J. Physiol. Pharmacol., 2009; 87: 426-431
Google Scholar - 29. De Vries E.M., van Beeren H.C., Ackermans M.T., Kalsbeek A., Fliers E., Boelen A.: Differential effects of fasting vs food restriction on liver thyroid hormone metabolism in male rats. J. Endocrinol., 2015; 224: 25-35
Google Scholar - 30. DeLany J.P., Hansen B.C., Bodkin N.L., Hannah J., Bray G.A.: Longterm calorie restriction reduces energy expenditure in aging monkeys. J. Gerontol. A Biol. Sci. Med. Sci., 1999; 54A: B5-B11
Google Scholar - 31. Diano S., Naftolin F., Goglia F., Horvath T.L.: Fasting-induced increase in type II iodothyronine deiodinase activity and messenger ribonucleic acid levels is not reversed by thyroxine in the rat hypothalamus. Endocrinology, 1998; 139: 2879-2884
Google Scholar - 32. Dillmann W.H.: Cardiac hypertrophy and thyroid hormone signaling. Heart Fail. Rev., 2010; 15: 125-132
Google Scholar - 33. Docter R., De Jong M.: Inhibition of computed liver T4 uptake during caloric deprivation and after fructose administration in humans and in perfused (recirculating) rat liver. Ann.Endocrinol. (Paris), 1988; 49: 183
Google Scholar - 34. Fekete C., Lechan R.M.: Central regulation of hypothalamicpituitary-thyroid axis under physiological and pathophysiological conditions. Endocr. Rev., 2014; 35: 159-194
Google Scholar - 35. Fekete C., Légrádi G.,Mihály E., Huang Q.H., Tatro J.B., Rand W.M., Emerson C.H., Lechan R.M.: α-melanocyte-stimulating hormone is contained in nerve terminals innervating thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus and prevents fasting-induced suppression of prothyrotropin-releasing hormone gene expression. J. Neurosc., 2000; 20: 1550-1558
Google Scholar - 36. Filaire E., Degoutte F., Jouanel P., Dabonneville M., Duchamp C., Lac G., Duchamp C., Pequignit J.M.: Biological alternations after food restriction and training in rats. J. Exerc. Physiol. Online, 2004; 7: 37-44
Google Scholar - 37. Fontana L., Klein S., Holloszy J.O., Premachandra B.N.: Effect of long-term calorie restriction with adequate protein and macronutrients on thyroid hormones. J. Clin. Endocrinol. Metab., 2006; 91: 3232-3235
Google Scholar - 38. Galton V.A., Hernandez A., GermainD.L.St.: The 5’-deiodinases are not essential for the fasting induced decrease in circulating thyroid hormone levels in male mice: possible roles of the type 3 deiodinase and tissue sequestration of hormone. Endocrinology, 2014; 155: 3172-3181
Google Scholar - 39. Ghamari-Langroudi M., Vella K.R., Srisai D., Sugrue M.L., Hollenberg A.N., Cone R.D.: Regulation of thyrotropin-releasing hormoneexpressing neurons in paraventricular nucleus of the hypothalamus by signals of adiposity. Mol. Endocrinol., 2010; 24: 2366-2381
Google Scholar - 40. Giordano F.J.: Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest., 2005; 115: 500-508
Google Scholar - 41. Gromakova I.A., Konovalenko O.A.: Effects of aging and lifeprolonging diet on thyroid regulation of protein synthesis. Bull. Exp. Biol. Med., 2004; 137: 276-279
Google Scholar - 42. Gruber C., Nink N., Nikam S., Magdowski G., Kripp G., Voswinckel R., Mühlfeld C.: Myocardial remodeling in left ventricular atrophy induced by caloric restriction. J. Anat., 2012; 220: 179-185
Google Scholar - 43. Guo Z.M., Mitchell-Raymundo F., Yang H., Ikeno Y., Nelson J., Diaz V., Richardson A., Reddick R.: Dietary restriction reduces atherosclerosis and oxidative stress in the aorta of apolipoprotein E-deficient mice. Mech. Ageing Dev., 2002; 123: 1121-1131
Google Scholar - 44. Hammer S., Snel M., Lamb H.J., Jazet I.M., Van der Meer R.W., Pijl H., Meinders E.A., Romijn J.A., De Ross A., Smit J.W.: Prolonged caloric restriction in obese patients with type 2 diabetes mellitus decreases myocardial triglyceride content and improves myocardial function. J. Am. Coll. Cardiol., 2008; 52: 1006-1012
Google Scholar - 45. Han X., Turdi S., Hu N., Guo R., Zhang Y., Ren J.: Influence of long-term caloric restriction on myocardial and cardiomyocyte contractile function and autophagy in mice. J. Nutr. Biochem., 2012; 23: 1592-1599 [46] Heemstra K.A., Soeters M.R., Fliers E., Serlie M.J., Burggraaf
Google Scholar - 46. Heemstra K.A., Soeters M.R., Fliers E., Serlie M.J., Burggraaf J., Van Doorn M.B., Van der Klaauw A.A., Romijn J.A., Smit J.W., Cors-smit E.P., Visser T.J.: RomType 2 iodothyronine deiodinase in skeletal muscle: effects of hypothyroidism and fasting. J. Clin. Endocrinol. Metab., 2009; 94: 2144-2150
Google Scholar - 47. Heilbronn L.K., De Jonge L., Frisard M.I., DeLany J.P., Larson-Meyer D.E., Rood J., Nguyen T., Martin C.K., Volaufova J., Most M.M., Greenway F.L., Smith S.R., Deutsch W.A., Wiliamson D.A., Ravussin E. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals. A randomized controlled trial. JAMA, 2006; 295: 1539-1548
Google Scholar - 48. Heilbronn L.K., Ravussin E.: Calorie restriction and aging: review of the literature and implications for studies in humans. Am. J. Clin. Nutr., 2003; 78: 361-369
Google Scholar - 49. Holtorf K.: Thyroid hormone transport into cellular tissue. J. Restorative Med., 2014; 3: 53-68
Google Scholar - 50. Jennings A.S., Duncan C.F., Utiger R.D.: Regulation of the conversion of thyroxine to triiodothyronine in the perfused rat liver. J. Clin. Invest., 1979; 64: 1614-1624
Google Scholar - 51. Kahaly G.J., Dillmann W.H.: Thyroid hormone action in the heart. Endocr. Rev., 2005; 26: 704-728
Google Scholar - 52. Katzeff H.L., Powell S.R., Ojamaa K.: Alterations in cardiac contractility and gene expression during low-T3 syndrome: prevention with T3. Am. J. Physiol., 1997; 273: E951-E956
Google Scholar - 53. Kester M.L., Kaptein E. Roest T.J., Van Dijk C.H., Tibboel D., Meinl W., Glatt H., Coughtire M.W., Visser T.J.: Characterization of rat iodothyronine sulfotransferases. Am. J. Endocrinol. Metab., 2003; 285: E592-E598
Google Scholar - 54. Klebanov S., Herlihy J.T.: Effect of long-life restriction on cardiac myosin composition. J. Gerontol., 1997; 52A: B184-B189
Google Scholar - 55. Klein I., Danzi S.: Thyroid disease and heart. Circulation, 2007; 116: 1725-1735
Google Scholar - 56. Kmieć Z., Kotlarz G., Śmiechowska B., Myśliwski A.: The effect of fasting and refeeding on thyroid follicle structure and thyroid hormone levels in young and old rats. Arch. Gerontol. Geriatr., 1998; 26: 161-175
Google Scholar - 57. Kobori H., Ichihara A., Miyashita Y., Hayashi M., Saruta T.: Local renin–angiotensin system contributes to hyperthyroidism inducedcardiac hypertrophy. J. Endocrinol., 1999; 160: 43-47
Google Scholar - 58. Kodde I.F., van der Stok J., Smolenski R.T., de Jong J.W.: Metabolic and genetic regulation of cardiac energy substrate preference. Comp. Biochem. Physiol. A Mol. Integr. Physiol, 2007; 146: 26-39
Google Scholar - 59. Kok S.W., Roelfsema F., Langendonk J.G., Frölich M., Burggraaf J., Meinders A.E., Pijl H.: High circulating thyrotropin levels in obese women are reduced after body weight loss induced by caloric restriction. J. Clin. Endocrinol. Metab., 2005; 90: 4659-4663
Google Scholar - 60. Krenning E.P., Docter R., Bernard H.F., Visser T., Hennemann G.: Decreased transport of thyroxine (T4), 3,3’,5-triiodothyronine (T3) and 3,3’,5’-triiodothyronine (rT3) into rat hepatocytes in primary culture due to a decrease of cellular ATP content and various drugs. FEBS Lett., 1982; 140: 229-233
Google Scholar - 61. Lachowicz K., Fürstenberg E., Pałkowska E., Stachoń M., Gajewska D., Myszkowska-Ryciak J., Kozłowska L., Ciecierska A., RosołowskaHuszcz D.: The effects of caloric restriction and age on thyroid hormone signalling in the heart of rats. J. Anim. Feed Sci., 2014; 23: 97-104
Google Scholar - 62. Le Moullac B., Gouache P., Bleiberg-Daniel H.: Regulation of hepatic transthyretin messenger RNA levels during moderate protein and food restriction in rats. J. Nutr., 1992; 122: 864-870
Google Scholar - 63. Lecoultre V., Ravussin E., Redman L.M.: The fall in leptin concentration is a major determinant of the metabolic adaptation induced by caloric restriction independently of the changes in leptin circadian rhythms. J. Clin. Endocrinol. Metab., 2011; 96: E1512-E1516
Google Scholar - 64. Lefevre M., Redman L.M., Heilbronn L.K., Smith J.V., Martin C.K., Rood J.C., Greenway F.L., Williamson D.A., Smith S.R., Ravussin E.: Caloric restriction alone and with exercise improves CVD risk in healthy non-obese individuals. Atherosclerosis, 2009; 203: 206-213
Google Scholar - 65. Legradi G., Emerson c.H., Ahima R.S., Flier J.S., Lechan R.M.: Leptin prevents fasting-induced suppression of prothyrotropinreleasing hormone messenger ribonucleic acid in neurons of the hypothalamic paraventicular nucleus. Endocrinology, 1997; 138: 2569-2576
Google Scholar - 66. Lindblom J., Haitina T., Fredriksson R., Schiöth H.B.: Differential regulation of nuclear receptors, neuropeptides and peptide hormones in the hypothalamus and pituitary of food restricted rats. Mol. Brain Res., 2005; 133: 37-46
Google Scholar - 67. Macek Jilkova Z., Pavelka S., Flachs P., Hensler M., Kus V., Kopecky J.: Modulation of type I iodothyronine 5’deiodinase activity in white adipose tissue by nutrition: possible involvement of leptin. Physiol. Res., 2010; 59: 561-569
Google Scholar - 68. Maglich J.M., Watson J., McMillen P.J., Goodwin B., Willson T.M., Moore J.T.: The nuclear receptor CAR is a regulator of thyroid hormone metabolism during caloric restriction. J. Biol. Chem., 2004; 279: 19832-19838
Google Scholar - 69. Merry B.J.: Dietary restriction in rodents – delayed or retarded ageing? Mech. Ageing Dev., 2005; 126: 951-959
Google Scholar - 70. Minamiyama Y., Yasuyuki B., Takemura S., Takahashi Y., Kodai S., Mizuguchi S., Nashikawa Y., Suehiro S., Okada S.: Calorie restriction improves cardiovascular risk factors via reduction of mitochondrial reactive oxygen species in type II diabetic rats. J. Pharmacol. Exp. Ther., 2007; 320: 535-543
Google Scholar - 71. Moreira-Andres M.N., Black E.B., Ramsden D.B., Hoffenberg R.: The effect of calorie restriction on serum thyroid hormone binding proteins and free hormone in obese patients. Clin. Endocrinol., 1980; 12: 249-255
Google Scholar - 72. Niemann B., Chen Y., Issa H. Silber R.E., Rohrbach S.: Caloric restriction delays cardiac ageing in rats: role of mitochondria. Cardiovasc. Res., 2010; 88: 267-276
Google Scholar - 73. Okoshi M.P., Okoshi K., Pai V.D., Pai-Silva M.D., Matsubara L.S., Cicogna A.C.: Mechanical, biochemical, and morphological changes in the heart from chronic food-restricted rats. Can. J. Physiol. Pharmacol., 2001; 79: 754-760
Google Scholar - 74. Oliveira K.J., Ortiga-Carvalho T.M., Cabanelas A., Veiga M.A., Aoki K., Ohki-Hamazaki H., Wada K., Wada E., Pazos-Moura C.C.: Disruption of neuromedin B receptor gene results in dysregulation of the pituitary-thyroid axis. J. Mol. Endocrinol., 2006; 36: 73-80
Google Scholar - 75. Omodei D., Fontana L.: Calorie restriction and prevention of ageassociated chronic disease. FEBS Lett., 2011; 585: 1537-1542
Google Scholar - 76. Ortiga-Carvalho T.M., Curty F.H., Nascimento-Saba C.C., Moura E.G., Polak J., Pazos-Moura C.C.: Pituitary neuromedin B content in experimental fasting and diabetes mellitus and correlation with thyrotropin secretion. Metabolism, 1997; 46: 149-153
Google Scholar - 77. Osman F., Gammage M.D., Franklyn J.A.: Thyroid disease and its treatment: short-term and long-term cardiovascular consequences. Curr. Opin. Pharmacol., 2001; 1: 626-631
Google Scholar - 78. Pantos C., Malliopoulou V., Varonos D.D., Cokkinos D.V.: Thyroid hormone and phenotypes of cardioprotection. Basic Res. Cardiol., 2004; 99: 101-120
Google Scholar - 79. Park S.K., Prolla T.A.: Lessons learned from gene expression profile studies of aging and caloric restriction. Ageing Res. Rev., 2005; 4: 55-65
Google Scholar - 80. Paulino E.C., Ferreira J.C., Bechara L.R., Tsutsui J.M., Mathias W., Lima F.B., Casarini D.E., Cicogna A.C., Brum P.C., Negrao C.E. Paulino E.C.: Exercise training and caloric restriction prevent reduction in cardiac Ca2+-hadling protein profile in obese rats. Hypertension, 2010; 56: 629-635
Google Scholar - 81. Pinotti M.F., Leopoldo A.S., Silva M.D., Sugizaki M.M., do Noscimento A.F., Lima-Leopoldo A.P., Aragon F.F., Padovani C.R., Cicogna A.C.: A comparative study of myocardial function and morphology during fasting/refeeding and food restriction in rats. Cardiovasc. Pathol., 2010; 19: e175-e182
Google Scholar - 82. Ramadan T., Camargo S.M., Summa V., Hunziker P., Chesnov S., Pos K.M., Verrey F.: Basolateral aromatic amino acid transporter TAT1 (Slc16A10) functions as an efflux pathway. J. Cell. Physiol., 2006; 206: 771-779
Google Scholar - 83. Ramsey J.J., Colman R.J., Binkley N.C., Christensen J.D., Gresl T.A., Kemnitz J.W., Weindruch R.: Dietary restriction and aging in rhesus monkeys: the University of Wisconsin study. Exp. Gerontol., 2000; 35: 1131-1149
Google Scholar - 84. Redman L.M., Ravussin E.: Endocrine alterations in response to caloric restriction in humans. Mol. Cell. Endocrinol., 2009; 299: 129-136
Google Scholar - 85. Reinhardt W., Holtermann D., Benker G., Olbricht T., Jaspers C., Reinwein D.: Effect of small doses of iodine on thyroid function during caloric restriction in normal subjects. FGR Horm. Res., 1993; 39: 132-137
Google Scholar - 86. Rolleman E.J., Hennemann G, Van Toor H., Schoenmakers C.H., Krenning E.P., de Jong M.: Changes in renal tri-iodothyronine and thyroxine handling during fasting. Eur. J. Endocrinol., 2000; 142: 125-130
Google Scholar - 87. Rosenbaum M., Goldsmith R., Bloomfield D., Magnano A., Weimer L., Heymsfield S., Gallagher D., Mayer L., Murphy E., Leibel R.L.: Low-dose leptin reverse skeletal muscle, autonomic and neuroendocrine adaptations to maintenance of reduced weight. J. Clin. Invest., 2005; 115: 3579-3586
Google Scholar - 88. Roth G.S., Handy A.M., Mattison J.A., Tilmont E.M., Ingram D.K., Lane M.A.: Efects of dietary caloric restriction and aging on thyroid hormones of rhesus monkeys. Horm. Metab. Res., 2002; 34: 378-382
Google Scholar - 89. Rouaze-Romet M., Savu L., Vranckx R., Bleiberg-Daniel F., Le Moullac B., Gouache P., Nunez E.A.: Re-expression of thyroxine-binding globulin in post-weaning rats during protein and energy malnutrition. Acta Endocrinol., 1992; 127: 441-448
Google Scholar - 90. Rouaze-Romet M., Savu L., Vranckx R., Bleiberg-Daniel F., Le Moullac B., Gouache P., Nunez E.A.: Re-expression of thyroxine-binding globulin in post-weaning rats during protein and energy malnutrition. Acta Endocrinol., 1992; 127: 441-448
Google Scholar - 91. Sangster J.K., Panciera D.L., Abbott J.A.: Cardiovascular effects of thyroid disease. Compend. Contin. Educ. Vet., 2013; 35: E1-E10
Google Scholar - 92. Seoane L.M., Carro E., Tovar S, Casanueva F.F., Dieguez C.: Regulation of in vivo TSH secretion by leptin. Regul. Pept., 2000; 92: 25-29
Google Scholar - 93. Shinmura K., Tamaki K., Sano M., Murata M., Yamakawa H., Ishida H., Fukuda K.: Impact of long term caloric restriction on cardiac senescence: caloric restriction ameliorates cardiac diastolic dysfunction associated with aging. J. Mol. Cell. Cardiol., 2011; 50: 117-127
Google Scholar - 94. Speakman J.R., Hambly C.: Starving for life: what animal studies can and cannot tell us about the use of caloric restriction to prolong human lifespan. J. Nutr., 2007; 137: 1078-1086
Google Scholar - 95. Stachoń M., Gromadzka-Ostrowska J., Lachowicz K., Fürstenberg E., Pałkowska E., Gajewska D., Myszkowska-Ryciak J., Kozłowska L., Rosołowska-Huszcz D.; Interdependence of the peripheral metabolism of glucocorticoids and thyroid hormones under calorie deficit in rats at different ages. J. Anim. Feed Sci., 2014; 23: 167-176
Google Scholar - 96. Sugizaki M.M., Carvalho R.F., Aragon F.F., Padovani C.R., Okoshi M.P., Zanati S.G., Pai-Silva M.D., Novelli E.L., Cicogna A.C.: Myocardial dysfunction induced by food restriction is related to morphological damage in normotensive middle-aged rats. J. Biomed. Sci., 2005; 12: 641-649
Google Scholar - 97. Sugizaki M.M., Leopoldo A.S., Okoshi M.P., Bruno A., Conde S.J., Lima-Leopoldo A.P., Padovani C.R., Carvalho R.F., Nascimento A.F., De Campos D.H., Nogueira C.R., Cicogna A.C.: Severe food restriction induces myocardial dysfunction related to SERCA2 activity. Can. J. Physiol. Pharmacol., 2009; 87: 666-673
Google Scholar - 98. Sugizaki M.M., Lima-Leopoldo A.P., Conde S.J., Campos D.S, Damanto R., Leopoldo A.S., Do Nascimento A.F., De Assis Oliveira Junior, Cicogna A.C.: Upregulation of mRNA myocardium calcium handling in rats submitted to exercise and food restriction. Arq. Bras. Cardiol., 2011; 97: 46-52
Google Scholar - 99. Swindell W.R.: Dietary restriction in rats and mice: a meta-analysis and review of the evidence for genotype-dependent effects on lifespan. Ageing Res. Rev., 2012; 11: 254-270
Google Scholar - 100. Swoap S.J.: Altered leptin signaling is sufficient, but not required, for hypotension associated with caloric restriction. Am. J. Physiol. Heart Circ. Physiol., 2001; 281: H2473-H2479
Google Scholar - 101. Swoap S.J., Haddad F., Bodell P., Baldwin K.M.: Control of beta-myosin heavy chain expression in systemic hypertension and caloric restriction in the rat heart. Am. J. Physiol., 1995; 269: C1025-C1033
Google Scholar - 102. Tagami T., Nakamura H., Sasaki S., Miyoshi Y., Nakao K.: Starvation-induced decrease in the maximal binding capacity for triiodothyronine of the thyroid hormone receptor is due to decrease in the receptor ptotein. Metabolism, 1996; 45: 970-973
Google Scholar - 103. Tribulova N., Knezl V., Shainberg A., Seki S., SoukupT.: Thyroid hormones and cardiac arrhythmias. Vascular Pharmacol., 2010; 52: 102-112
Google Scholar - 104. Van den Bergh A., Vangheluwe P., Vanderper A., Carmeliet P., Wuytack F., Janssens S., Flameng W., Holvoet P., Herijgers P.: Food-restriction in obese dyslipidemic diabetic mice partially restores basal contractility but not contractile reserve. Eur. J. Heart. Failure, 2009; 11: 1118-1125
Google Scholar - 105. Van der Heyden J.T., Docter R., Van Toor H., Wilson J.H., Hennemann G., Krenning E.P.: Effects of caloric deprivation on thyroid hormone tissue uptake and generation of low-T3 syndrome. Am. J. Physiol., 1986; 251: E156-E163
Google Scholar - 106. Van Haastern G.A., Linkels E., Klootwijk W., Van Toor H., Rondeel J.M., Themmen A.P., De Jong F.H., Valentijn K., Vaudry H., Bauer K., Visser T.J., De Greef W.J.: Starvation-induced changes in the hypothalamic content of prothyrotrophin-releasing hormone (proTRH) mRNA and the hypothalamic release of pro-TRH-derived peptides: role of the adrenal gland. J. Endocrinol., 1995; 145: 143-153
Google Scholar - 107. Van Haasteren G.A., Linkels E., Van Toor H, Klootwijk W., Kaptein E, de Jong F.H., Reymond M.J, Visser T.J. deGreef W.J.: Effects of long-term food reduction on the hypothalamus-pituitary-thyroid axis in male and female rats. J. Endocrinol., 1996; 150: 169-178
Google Scholar - 108. Vesely D.L.: Atrial natriuretic peptides in phatophysiological diseases. Cardiovasc. Res., 2001; 51: 647-658
Google Scholar - 109. Vesely D.L.: Atrial natriuretic peptides in phatophysiological diseases. Cardiovasc. Res., 2001; 51: 647-658
Google Scholar - 110. Vizotto V.A., Carvalho R.F., Sugizaki M.M., Lima A.P., Aragon F.F., Padovani C.R., Castro A.V., Dal Pai-Silva M., Nogueira C.R., Cicogna A.C.: Down-regulation of the cardiac sarcoplasmic reticulum ryanodine channel in severely food-restricted rats. Braz. J. Med. Biol. Res., 2007; 40: 27-31
Google Scholar - 111. Wagner M.S., Morimoto R., Dora J.M., Benneman A., Pavan R., Maia A.L.: Hypothyroidism induces type 2 iodothyronine deiodinase expression in mouse heart and testis. J. Mol. Endocrinol., 2003; 31: 541-550
Google Scholar - 112. Walford R.L., Mock D., Verdery R., MacCallum T.: Calorie restriction in biosphere 2. Alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period.J. Gerontol. A. Biol. Sci. Med. Sci., 2002; 57: B211-B224
Google Scholar - 113. Wang Y.Y., Morimoto S., Du C.K., Lu Q.W., Zhan D.Y., Tsutsumi T., Ide T., Miwa Y., Takahashi-Yanaga F., Sasaguri T.: Up-regulation of type 2 iodothyronine deiodinase in dilated cardiomyopathy. Cardiovasc. Res., 2010; 87: 636-646
Google Scholar - 114. Wassen F.W., Moerings E.P., Van Toor H., Hennemann G., Everts M.E.: Thyroid hormone uptake in cultured rat anterior pituitary cells:effects of energy status and bilirubin. J. Endocrinol., 2000; 165: 599-606
Google Scholar - 115. Weiss E.P., Fontana L.: Caloric restriction – powerful protection for the aging heart and vasculature. Am. J. Physiol. Circ. Physiol., 2011; 301: H1205-H1219
Google Scholar - 116. Weiss E.P., Villareal D.T., Racette S.B., Steger-May K., Premachandra B.N., Klein S., Fontana L.: Caloric restriction but not exercise-induced reductions in fat mass decrease plasma triiodothyronine concentrations: a randomized controlled trial. Rejuvenation Res., 2008; 11: 605-609
Google Scholar - 117. Weiss E.P., Villareal D.T., Racette S.B., Steger-May K., Premachandra B.N., Klein S., Fontana L.: Caloric restriction but not exercise-induced reductions in fat mass decrease plasma triiodothyronine concentrations: a randomized controlled trial. Rejuvenation Res., 2008; 11: 605-609
Google Scholar - 118. Wolfe B.E., Jimerson D.C., Orlova C. Mantzoros C.S.: Effect of dieting on plasma leptin, soluble leptin receptor, adiponectin and resistin levels in healthy volunteers. Clin. Endocrinol., 2004; 61: 332-338
Google Scholar - 119. Zanetti M., Cappellari G.G., Burekovic I., Barazzoni R., Stebel M., Guarnieri G.: Caloric restriction improves endothelial dysfunction during vascular aging: Effect on nitric oxide synthase isoforms and oxidative stress in aorta. Exp. Gerontol., 2010; 45: 848-855
Google Scholar