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Published in: Diabetology & Metabolic Syndrome 1/2017

Open Access 01-12-2017 | Research

Vitamin D is associated with metabotropic but not neurotrophic effects of exercise in ovariectomized rats

Authors: Parvin Babaei, Samaneh Ghorbani Shirkouhi, Rastegar Hosseini, Bahram Soltani Tehrani

Published in: Diabetology & Metabolic Syndrome | Issue 1/2017

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Abstract

Purpose

Here, we studied the beneficial effects of aerobic exercise on metabolic syndrome components, cognitive performance, brain derived neurotrophic factor (BDNF) and irisin in ovariectomized rats with different serum vitamin D (Vit D) status.

Methods

Eighty female wistar rats were divided into 2 groups of sham operated (sham, n = 8), and ovariectomized (OVX, n = 72). Then OVX were divided into 9 groups of receiving combination of exercise protocol with low dose of Vit D (OVX + EXE + LD), high dose of Vit D (OVX + EXE + HD), Vit D deficiency (OVX + EXE − D), and (OVX + EXE + Veh). Also non exercised groups of OVX receiving high dose of Vit D (OVX + HD), low dose of Vit D (OVX + LD), Vit D deficiency (OVX − D), and Veh (OVX + Veh) were included. After 2 months of related interventions, spatial memory was assessed using Morris water maze (MWM), and then metabolic syndrome components were measured.

Results

High dose of Vit D supplementation showed significant reduction in weight (p = 0.001), lipid profiles (p = 0.001), visceral fat (p = 0.001) and waist circumference (p = 0.001) regardless of exercising or not, with no change in cognitiive function. Serum BDNF level was significantly higher in Vit D deficient group (p = 0.001), and was decreased in the OVX + HD. In contrary, irisin did not show any significant relationship with serum concentration of Vit D, while it was significantly elevated in the exercised groups compared with non-exercised counterparts.

Conclusion

Vit D insufficiency deteriorates metabolic syndrome components, and elevates serum BDNF as a compensatory metabotropic factor, and further supplementation significantly attenuates these components parallel with reduction in BDNF. In addition, aerobic exercise successfully induces various metabolic benefits, provided optimum serum level of Vit D.
Literature
1.
go back to reference Haffner SM, Valdez RA, Hazuda HP, et al. Prospective analysis of the insulin-resistance syndrome (syndrome X). Diabetes. 1992;41:715–22.CrossRefPubMed Haffner SM, Valdez RA, Hazuda HP, et al. Prospective analysis of the insulin-resistance syndrome (syndrome X). Diabetes. 1992;41:715–22.CrossRefPubMed
2.
go back to reference Meigs JB, Nathan DM, Wilson PW, et al. Metabolic risk factors worsen continuously across the spectrum of nondiabetic glucose tolerance. The Framingham offspring study. Ann Intern Med. 1998;128:524–33.CrossRefPubMed Meigs JB, Nathan DM, Wilson PW, et al. Metabolic risk factors worsen continuously across the spectrum of nondiabetic glucose tolerance. The Framingham offspring study. Ann Intern Med. 1998;128:524–33.CrossRefPubMed
3.
go back to reference Reilly MP, Rader DJ. The metabolic syndrome: more than the sum of its parts? Circulation. 2003;108:1546–51.CrossRefPubMed Reilly MP, Rader DJ. The metabolic syndrome: more than the sum of its parts? Circulation. 2003;108:1546–51.CrossRefPubMed
4.
go back to reference Rosano GMC, Vitale C, Marazzi G, et al. Menopause and cardiovascular disease: the evidence. Climacteric. 2007;10:19–24.CrossRefPubMed Rosano GMC, Vitale C, Marazzi G, et al. Menopause and cardiovascular disease: the evidence. Climacteric. 2007;10:19–24.CrossRefPubMed
8.
go back to reference Pittas AG, Lau J, Hu FB, et al. The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J Clin Endocrinol Metab. 2007;92:2017–29.CrossRefPubMedPubMedCentral Pittas AG, Lau J, Hu FB, et al. The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J Clin Endocrinol Metab. 2007;92:2017–29.CrossRefPubMedPubMedCentral
9.
go back to reference Liu S, Song Y, Ford ES, et al. Dietary calcium, vitamin D, and the prevalence of metabolic syndrome in middle-aged and older US women. Diabetes Care. 2005;28:2926–32.CrossRefPubMed Liu S, Song Y, Ford ES, et al. Dietary calcium, vitamin D, and the prevalence of metabolic syndrome in middle-aged and older US women. Diabetes Care. 2005;28:2926–32.CrossRefPubMed
10.
go back to reference Tinkler GP, Voytko ML. Estrogen modulates cognitive and cholinergic process in surgically menopausal mokeys. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29:423–31.CrossRefPubMed Tinkler GP, Voytko ML. Estrogen modulates cognitive and cholinergic process in surgically menopausal mokeys. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29:423–31.CrossRefPubMed
12.
go back to reference Annweiler C, Fantino B, Schott AM, et al. Vitamin D insufficiency and mild cognitive impairment: cross-sectional association. Eur J Neurol. 2012;19:1023–9.CrossRefPubMed Annweiler C, Fantino B, Schott AM, et al. Vitamin D insufficiency and mild cognitive impairment: cross-sectional association. Eur J Neurol. 2012;19:1023–9.CrossRefPubMed
13.
go back to reference Eyles DW, Smith S, Kinobe R, et al. Distribution of the vitamin D receptor and 1[alpha]-hydroxylase in human brain. J Chem Neuroanat. 2005;29:21–30.CrossRefPubMed Eyles DW, Smith S, Kinobe R, et al. Distribution of the vitamin D receptor and 1[alpha]-hydroxylase in human brain. J Chem Neuroanat. 2005;29:21–30.CrossRefPubMed
14.
go back to reference Babaei P, Azali AK, Soltani TB, Damirchi A. Effect of 6 weeks of endurance exercise and following detraining on serum brain derived neurotrophic factor and memory performance in middle aged males with metabolic syndrome. J Sports Med Phys Fitness. 2013;53:437–43.PubMed Babaei P, Azali AK, Soltani TB, Damirchi A. Effect of 6 weeks of endurance exercise and following detraining on serum brain derived neurotrophic factor and memory performance in middle aged males with metabolic syndrome. J Sports Med Phys Fitness. 2013;53:437–43.PubMed
15.
go back to reference Babaei P, Damirchi A, Mehdipoor M. Long term habitual exercise is associated with lower resting level of serum BDNF. Neurosci Lett. 2014;566:304–8.CrossRefPubMed Babaei P, Damirchi A, Mehdipoor M. Long term habitual exercise is associated with lower resting level of serum BDNF. Neurosci Lett. 2014;566:304–8.CrossRefPubMed
16.
go back to reference Vaynman S, Ying Z, Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. EJN. 2004;20:2580–90.PubMed Vaynman S, Ying Z, Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. EJN. 2004;20:2580–90.PubMed
17.
go back to reference Boström P, Wu J, Jedrychowski MP, et al. A PGC1-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463–8.CrossRefPubMedPubMedCentral Boström P, Wu J, Jedrychowski MP, et al. A PGC1-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463–8.CrossRefPubMedPubMedCentral
18.
go back to reference Coelho FG, Vital TM, Stein AM, et al. Acute aerobic exercise increases brain-derived neurotrophic factor levels in elderly with Alzheimer’s disease. J Alzheimer’s Dis. 2014;39:401–8. Coelho FG, Vital TM, Stein AM, et al. Acute aerobic exercise increases brain-derived neurotrophic factor levels in elderly with Alzheimer’s disease. J Alzheimer’s Dis. 2014;39:401–8.
19.
21.
go back to reference Kumar S, Parkash J, Kataria H, et al. Interactive effect of excitotoxic injury and dietary restriction on neurogenesis and neurotrophic factors in adult male rat brain. Neurosci Res. 2009;65:367–74.CrossRefPubMed Kumar S, Parkash J, Kataria H, et al. Interactive effect of excitotoxic injury and dietary restriction on neurogenesis and neurotrophic factors in adult male rat brain. Neurosci Res. 2009;65:367–74.CrossRefPubMed
22.
go back to reference Gomez PF, Ying Z, Roy RR, Edgerton VR, et al. Voluntary exercise induces aBDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol. 2002;88:2187–95.CrossRef Gomez PF, Ying Z, Roy RR, Edgerton VR, et al. Voluntary exercise induces aBDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol. 2002;88:2187–95.CrossRef
23.
go back to reference Vaynman S, Ying Z, Gomez PF. Interplay between brain derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience. 2003;122:647–57.CrossRefPubMed Vaynman S, Ying Z, Gomez PF. Interplay between brain derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience. 2003;122:647–57.CrossRefPubMed
25.
go back to reference Nakagawa T, Kishino MO, Sugar E. Brain-derived neurotrophic factor (BDNF) regulates glucose and energy metabolism in diabetic mice. Diabetes Metab Res Rev. 2002;18:185–91.CrossRefPubMed Nakagawa T, Kishino MO, Sugar E. Brain-derived neurotrophic factor (BDNF) regulates glucose and energy metabolism in diabetic mice. Diabetes Metab Res Rev. 2002;18:185–91.CrossRefPubMed
26.
go back to reference Pontzer H, Durazo AR, Dugas LR, et al. Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Curr Biol. 2016;26:1–8.CrossRef Pontzer H, Durazo AR, Dugas LR, et al. Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Curr Biol. 2016;26:1–8.CrossRef
27.
go back to reference Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev. 2015;43:110–6.CrossRefPubMed Pontzer H. Constrained total energy expenditure and the evolutionary biology of energy balance. Exerc Sport Sci Rev. 2015;43:110–6.CrossRefPubMed
28.
go back to reference Saadati H, Babri SH, Ahmadiasl N, et al. Effects of exercise on memory consolidation and retrieval of passive avoidance learning in young male rats. Asian J Sports Med. 2010;1:137–42.CrossRefPubMedPubMedCentral Saadati H, Babri SH, Ahmadiasl N, et al. Effects of exercise on memory consolidation and retrieval of passive avoidance learning in young male rats. Asian J Sports Med. 2010;1:137–42.CrossRefPubMedPubMedCentral
29.
go back to reference Okura T, Nakata Y, Ohkawara K, et al. Effects of aerobic exercise on metabolic syndrome improvement in response to weight reduction. Obesity. 2007;15:2478–84.CrossRefPubMed Okura T, Nakata Y, Ohkawara K, et al. Effects of aerobic exercise on metabolic syndrome improvement in response to weight reduction. Obesity. 2007;15:2478–84.CrossRefPubMed
30.
go back to reference Damirchi A, Mehdizade R, Ansar MM, et al. Effects of aerobic exercise training on visceral fat and serum adiponectin concentration in ovariectomized rats. Climacteric. 2010;13:171–8.CrossRefPubMed Damirchi A, Mehdizade R, Ansar MM, et al. Effects of aerobic exercise training on visceral fat and serum adiponectin concentration in ovariectomized rats. Climacteric. 2010;13:171–8.CrossRefPubMed
31.
go back to reference Shinoda M, Latour M, Lavoie J. Effects of physical training on body composition and organ weights in ovariectomized and hyperestrogenic rats. Int J Obes Relat Metab Disord. 2002;26:335–43.CrossRefPubMed Shinoda M, Latour M, Lavoie J. Effects of physical training on body composition and organ weights in ovariectomized and hyperestrogenic rats. Int J Obes Relat Metab Disord. 2002;26:335–43.CrossRefPubMed
32.
go back to reference Gauthier MS, Couturier K, Latour J-G, Lavoie J-M. Concurrent exercise prevents high-fat-diet-induced macrovesicular hepatic steatosis. J Appl Physiol. 2003;94:2127–34.CrossRefPubMed Gauthier MS, Couturier K, Latour J-G, Lavoie J-M. Concurrent exercise prevents high-fat-diet-induced macrovesicular hepatic steatosis. J Appl Physiol. 2003;94:2127–34.CrossRefPubMed
33.
go back to reference Latour MG, Shinoda M, Lavoie J-M. Metabolic effects of physical training in ovariectomized and hyperestrogenic rats. J Appl Physiol. 2001;90:235–41.PubMed Latour MG, Shinoda M, Lavoie J-M. Metabolic effects of physical training in ovariectomized and hyperestrogenic rats. J Appl Physiol. 2001;90:235–41.PubMed
34.
go back to reference Hooge RD, Deyn PPD. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev. 2001;36:60–90.CrossRefPubMed Hooge RD, Deyn PPD. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev. 2001;36:60–90.CrossRefPubMed
35.
36.
go back to reference Gerbaix M, Metz L, Ringot E, et al. Visceral fat mass determination in rodent: validation of dual-energy X-ray absorptiometry and anthropometric techniques in fat and lean rats. Lipids Health Dis. 2010;9:140.CrossRefPubMedPubMedCentral Gerbaix M, Metz L, Ringot E, et al. Visceral fat mass determination in rodent: validation of dual-energy X-ray absorptiometry and anthropometric techniques in fat and lean rats. Lipids Health Dis. 2010;9:140.CrossRefPubMedPubMedCentral
37.
go back to reference Carreteroa JIB, Blasco FA, Villafruela JJ, et al. Vitamin D deficiency is associated with the metabolic syndrome in morbid obesity. Clin Nutr. 2007;26:573–80.CrossRef Carreteroa JIB, Blasco FA, Villafruela JJ, et al. Vitamin D deficiency is associated with the metabolic syndrome in morbid obesity. Clin Nutr. 2007;26:573–80.CrossRef
38.
go back to reference Trowman R, Dumville JC, Hahn S, et al. Asystematic review of the effects of calcium supplementation on body weight. Br J Nutr. 2006;95:1033–8.CrossRefPubMed Trowman R, Dumville JC, Hahn S, et al. Asystematic review of the effects of calcium supplementation on body weight. Br J Nutr. 2006;95:1033–8.CrossRefPubMed
39.
go back to reference Szafran H, Smielak KW. The role of estrogens in hormonal regulation of lipid metabolism in women. Prz Lek. 1998;55:266–70.PubMed Szafran H, Smielak KW. The role of estrogens in hormonal regulation of lipid metabolism in women. Prz Lek. 1998;55:266–70.PubMed
40.
go back to reference Yoshida T, Takahashi K, Yamatani H, et al. Impact of surgical menopause on lipid and bone metabolism. Climacteric. 2011;14:445–52.CrossRefPubMed Yoshida T, Takahashi K, Yamatani H, et al. Impact of surgical menopause on lipid and bone metabolism. Climacteric. 2011;14:445–52.CrossRefPubMed
41.
go back to reference Weinberg ME, Manson JE, Buring JE, et al. Low sex hormone-binding globulin is associated with the metabolic syndrome in postmenopausal women. Metabolism. 2006;55:1473–80.CrossRefPubMedPubMedCentral Weinberg ME, Manson JE, Buring JE, et al. Low sex hormone-binding globulin is associated with the metabolic syndrome in postmenopausal women. Metabolism. 2006;55:1473–80.CrossRefPubMedPubMedCentral
42.
go back to reference Ford ES, Ajani UA, McGuire LC, et al. Concentrations of serum vitamin D and the metabolic syndrome among U.S. adults. Diabetes Care. 2005;28:1228–30.CrossRefPubMed Ford ES, Ajani UA, McGuire LC, et al. Concentrations of serum vitamin D and the metabolic syndrome among U.S. adults. Diabetes Care. 2005;28:1228–30.CrossRefPubMed
43.
go back to reference Chen HI, Lin LC, Yu L, et al. Treadmill exercise enhances passive avoidance learning in rats: the role of downregulated serotonin system in the limbic system. Neurobiol Learn Mem. 2008;89:489–96.CrossRefPubMed Chen HI, Lin LC, Yu L, et al. Treadmill exercise enhances passive avoidance learning in rats: the role of downregulated serotonin system in the limbic system. Neurobiol Learn Mem. 2008;89:489–96.CrossRefPubMed
44.
go back to reference Rastegar H, Damirchi A, Babaei P. Vitamin D increases PPARg expression and promotes beneficial effects of physical activity in metabolic syndrome. Nutrition. 2017;36(54–5919):173–82. Rastegar H, Damirchi A, Babaei P. Vitamin D increases PPARg expression and promotes beneficial effects of physical activity in metabolic syndrome. Nutrition. 2017;36(54–5919):173–82.
46.
go back to reference Varga H, Németh H, That T, et al. Weak if any effect of estrogen on spatial memory in rats. Acta Biol Szeged. 2002;46:13–6. Varga H, Németh H, That T, et al. Weak if any effect of estrogen on spatial memory in rats. Acta Biol Szeged. 2002;46:13–6.
47.
go back to reference Latimer CS, Brewer LD, Searcy JL, et al. Vitamin D prevents cognitive decline and enhances hippocampal synaptic function in aging rats. PNAS. 2014;111:E4359–66.CrossRefPubMedPubMedCentral Latimer CS, Brewer LD, Searcy JL, et al. Vitamin D prevents cognitive decline and enhances hippocampal synaptic function in aging rats. PNAS. 2014;111:E4359–66.CrossRefPubMedPubMedCentral
48.
go back to reference Taghizadeh M, Djazayery A, Salami M, et al. Vitamin-D-free regimen intensifies the spatial learning deficit in Alzheimer’s disease. Int J Neurosci. 2011;121:16–24.CrossRefPubMed Taghizadeh M, Djazayery A, Salami M, et al. Vitamin-D-free regimen intensifies the spatial learning deficit in Alzheimer’s disease. Int J Neurosci. 2011;121:16–24.CrossRefPubMed
49.
go back to reference Adham R, Mohamed A, Gehan Y, et al. Neuroprotective role of vitamin D3 in colchicine-induced Alzheimer’s disease in rats. Alex J Med. 2014;51:127–36. Adham R, Mohamed A, Gehan Y, et al. Neuroprotective role of vitamin D3 in colchicine-induced Alzheimer’s disease in rats. Alex J Med. 2014;51:127–36.
51.
go back to reference Su J, Sripanidkulcha K, Hu Y, et al. The effect of ovariectomy on learning and memory and relationship to changes in brain volume and neuronal density. Int J Neurosci. 2012;122:549–59.CrossRefPubMed Su J, Sripanidkulcha K, Hu Y, et al. The effect of ovariectomy on learning and memory and relationship to changes in brain volume and neuronal density. Int J Neurosci. 2012;122:549–59.CrossRefPubMed
53.
go back to reference Chaldakov GN. The metabotrophic NGF and BDNF: an emerging concept. Arch Ital Biol. 2011;149:257–63.PubMed Chaldakov GN. The metabotrophic NGF and BDNF: an emerging concept. Arch Ital Biol. 2011;149:257–63.PubMed
54.
go back to reference Damirchi A, Soltani TB, Azali AK, et al. Influence of aerobic training and detraining on serum BDNF, insulin resistance, and metabolic risk factors in middle-aged men diagnosed with metabolic syndrome. Clin J Sport Med. 2013;24:513–8.CrossRef Damirchi A, Soltani TB, Azali AK, et al. Influence of aerobic training and detraining on serum BDNF, insulin resistance, and metabolic risk factors in middle-aged men diagnosed with metabolic syndrome. Clin J Sport Med. 2013;24:513–8.CrossRef
55.
go back to reference Moreno NJM, Ortega F, Serrano M, et al. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J Clin Endocrinol Metab. 2013;98:E769–78.CrossRef Moreno NJM, Ortega F, Serrano M, et al. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J Clin Endocrinol Metab. 2013;98:E769–78.CrossRef
56.
go back to reference Xin C, Liu J, Zhang J, et al. Irisin improves fatty acid oxidation and glucose utilization in type 2 diabetes by regulating the AMPK signaling pathway. Int J Obes (Lond). 2016;40:443–51.CrossRef Xin C, Liu J, Zhang J, et al. Irisin improves fatty acid oxidation and glucose utilization in type 2 diabetes by regulating the AMPK signaling pathway. Int J Obes (Lond). 2016;40:443–51.CrossRef
57.
go back to reference So WY, Leung PS. Irisin ameliorates hepatic glucose/lipid metabolism and enhances cell survival in insulin-resistant human HepG2 cells through adenosine monophosphate-activated protein kinase signaling. Int J Biochem Cell Biol. 2016;78:237–47.CrossRefPubMed So WY, Leung PS. Irisin ameliorates hepatic glucose/lipid metabolism and enhances cell survival in insulin-resistant human HepG2 cells through adenosine monophosphate-activated protein kinase signaling. Int J Biochem Cell Biol. 2016;78:237–47.CrossRefPubMed
58.
go back to reference Kaidah S, Soejono SK, Partadiredja G. Exercise improves hippocampal estrogen and spatial memory of ovariectomized rats. Bratisl Med J. 2016;117:94–9.CrossRef Kaidah S, Soejono SK, Partadiredja G. Exercise improves hippocampal estrogen and spatial memory of ovariectomized rats. Bratisl Med J. 2016;117:94–9.CrossRef
59.
Metadata
Title
Vitamin D is associated with metabotropic but not neurotrophic effects of exercise in ovariectomized rats
Authors
Parvin Babaei
Samaneh Ghorbani Shirkouhi
Rastegar Hosseini
Bahram Soltani Tehrani
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2017
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/s13098-017-0288-z

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