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Published in: Endocrine 3/2018

01-09-2018 | Original Article

Serum calcitonin gene-related peptide facilitates adipose tissue lipolysis during exercise via PIPLC/IP3 pathways

Authors: Malihe Aveseh, Maryam Koushkie-Jahromi, Javad Nemati, Saeed Esmaeili-Mahani

Published in: Endocrine | Issue 3/2018

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Abstract

Purpose

Calcitonin gene-related peptide (CGRP) is formed by alternative transcription of the calcitonin/α-CGRP gene, which also gives rise to calcitonin (CT). Recently, CGRP has been the focus of research for its metabolic effects in vitro. In the present study, the in vivo effects of CGRP on epididymal fat pads lipolysis at rest and during exercise were investigated in trained male Wistar rats.

Methods

Male Wistar rats were assigned to control and trained groups, which underwent endurance training for 12 weeks. The control (at rest) and trained (during acute exercise) animals were subjected to an intravenous injection of rat recombinant CGRP (2 µg kg−1) and CGRP-(8–37), a competitive CGRP receptors antagonist, to evaluate if and how CGRP can affect adipose tissue lipolysis at rest and during exercise.

Results

Intravenous injection of rat CGRP recombinant at rest upregulated major lipolysis pathways (cyclic AMP (cAMP), AMP-activated protein kinase (AMPK), and phospholipase C (PIPLC/IP3)) in fat pads, causing an elevation in plasma-free fatty acid (FFA) and a decrease in plasma triglyceride (TG). All the effects were eliminated by pretreating the animals with CGRP-(8–37), suggesting that CGRP receptors were necessary for lipolytic effects of CGRP in fat pads. In trained animals, acute exercise augmented CGRP in serum, cerebrospinal fluid (CSF), and the cortex. Pretreating the animals with CGRP-(8–37) attenuated PIPLC/IP3 pathway in fat pads and had no effect on cAMP and AMPK pathways.

Conclusions

Epididymal fat pads is a metabolic target for CGRP during exercise and CGRP effects on adipose tissue metabolism during exercise could be related to PIPLC/IP3 pathway.
Literature
1.
go back to reference J.F. Horowitz, Fatty acid mobilization from adipose tissue during exercise. Trends Endocrinol. Metab. 14(8), 386–392 (2003)CrossRefPubMed J.F. Horowitz, Fatty acid mobilization from adipose tissue during exercise. Trends Endocrinol. Metab. 14(8), 386–392 (2003)CrossRefPubMed
2.
go back to reference L.L. Spriet, Regulation of skeletal muscle fat oxidation during exercise in humans. Med. Sci. Sports Exerc. 34(9), 1477–1484 (2002)CrossRefPubMed L.L. Spriet, Regulation of skeletal muscle fat oxidation during exercise in humans. Med. Sci. Sports Exerc. 34(9), 1477–1484 (2002)CrossRefPubMed
3.
go back to reference R.A. Howlett, M.L. Parolin, D.J. Dyck, E. Hultman, N.L. Jones, G.J. Heigenhauser, L.L. Spriet, Regulation of skeletal muscle glycogen phosphorylase and PDH at varying exercise power outputs. Am. J. Physiol.-Regul., Integr. Comp. Physiol. 275(2), R418–R425 (1998)CrossRef R.A. Howlett, M.L. Parolin, D.J. Dyck, E. Hultman, N.L. Jones, G.J. Heigenhauser, L.L. Spriet, Regulation of skeletal muscle glycogen phosphorylase and PDH at varying exercise power outputs. Am. J. Physiol.-Regul., Integr. Comp. Physiol. 275(2), R418–R425 (1998)CrossRef
4.
go back to reference L.L. Spriet, New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med. 44(1), 87–96 (2014)CrossRefPubMedCentral L.L. Spriet, New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med. 44(1), 87–96 (2014)CrossRefPubMedCentral
5.
go back to reference J. Romijn, E. Coyle, L. Sidossis, J. Rosenblatt, R. Wolfe, Substrate metabolism during different exercise intensities in endurance-trained women. J. Appl. Physiol. 88(5), 1707–1714 (2000)CrossRefPubMed J. Romijn, E. Coyle, L. Sidossis, J. Rosenblatt, R. Wolfe, Substrate metabolism during different exercise intensities in endurance-trained women. J. Appl. Physiol. 88(5), 1707–1714 (2000)CrossRefPubMed
6.
go back to reference A. Bolsoni-Lopes, M.I.C. Alonso-Vale, Lipolysis and lipases in white adipose tissue–An update. Arch. Endocrinol. Metab. 59(4), 335–342 (2015)CrossRefPubMed A. Bolsoni-Lopes, M.I.C. Alonso-Vale, Lipolysis and lipases in white adipose tissue–An update. Arch. Endocrinol. Metab. 59(4), 335–342 (2015)CrossRefPubMed
7.
go back to reference R. Zechner, R. Zimmermann, T.O. Eichmann, S.D. Kohlwein, G. Haemmerle, A. Lass, F. Madeo, FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15(3), 279–291 (2012)CrossRefPubMedPubMedCentral R. Zechner, R. Zimmermann, T.O. Eichmann, S.D. Kohlwein, G. Haemmerle, A. Lass, F. Madeo, FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 15(3), 279–291 (2012)CrossRefPubMedPubMedCentral
8.
go back to reference S. Bijland, S.J. Mancini, I.P. Salt, Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin. Sci. 124(8), 491–507 (2013)CrossRefPubMed S. Bijland, S.J. Mancini, I.P. Salt, Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin. Sci. 124(8), 491–507 (2013)CrossRefPubMed
9.
go back to reference S.-J. Kim, T. Tang, M. Abbott, J.A. Viscarra, Y. Wang, H.S. Sul, AMPK phosphorylates desnutrin/ATGL and hormone-sensitive lipase to regulate lipolysis and fatty acid oxidation within adipose tissue. Mol. Cell. Biol. 36(14), 1961–1976 (2016)CrossRefPubMedPubMedCentral S.-J. Kim, T. Tang, M. Abbott, J.A. Viscarra, Y. Wang, H.S. Sul, AMPK phosphorylates desnutrin/ATGL and hormone-sensitive lipase to regulate lipolysis and fatty acid oxidation within adipose tissue. Mol. Cell. Biol. 36(14), 1961–1976 (2016)CrossRefPubMedPubMedCentral
10.
go back to reference S. Luquet, C. Magnan, The central nervous system at the core of the regulation of energy homeostasis. Front. Biosci. (Sch. Ed.) 1, 448–465 (2009)CrossRef S. Luquet, C. Magnan, The central nervous system at the core of the regulation of energy homeostasis. Front. Biosci. (Sch. Ed.) 1, 448–465 (2009)CrossRef
11.
go back to reference V.-S. Moullé, A. Picard, C. Le Foll, B.-E. Levin, C. Magnan, Lipid sensing in the brain and regulation of energy balance. Diabetes Metab. 40(1), 29–33 (2014)CrossRefPubMed V.-S. Moullé, A. Picard, C. Le Foll, B.-E. Levin, C. Magnan, Lipid sensing in the brain and regulation of energy balance. Diabetes Metab. 40(1), 29–33 (2014)CrossRefPubMed
12.
go back to reference M. Meens, N. Mattheij, P. van Loenen, L. Spijkers, P. Lemkens, J. Nelissen, M. Compeer, A. Alewijnse, J. De Mey, G‐protein βγ subunits in vasorelaxing and anti‐endothelinergic effects of calcitonin gene‐related peptide. Br. J. Pharmacol. 166(1), 297–308 (2012)CrossRefPubMedPubMedCentral M. Meens, N. Mattheij, P. van Loenen, L. Spijkers, P. Lemkens, J. Nelissen, M. Compeer, A. Alewijnse, J. De Mey, G‐protein βγ subunits in vasorelaxing and anti‐endothelinergic effects of calcitonin gene‐related peptide. Br. J. Pharmacol. 166(1), 297–308 (2012)CrossRefPubMedPubMedCentral
13.
go back to reference J. McCulloch, R. Uddman, T.A. Kingman, L. Edvinsson, Calcitonin gene-related peptide: functional role in cerebrovascular regulation. Proc. Natl Acad. Sci. 83(15), 5731–5735 (1986)CrossRefPubMed J. McCulloch, R. Uddman, T.A. Kingman, L. Edvinsson, Calcitonin gene-related peptide: functional role in cerebrovascular regulation. Proc. Natl Acad. Sci. 83(15), 5731–5735 (1986)CrossRefPubMed
14.
go back to reference S.-J. Smillie, R. King, X. Kodji, E. Outzen, G. Pozsgai, E. Fernandes, N. Marshall, P. De Winter, R.J. Heads, C. Dessapt-Baradez, An ongoing role of α-calcitonin gene–related peptide as part of a protective network against hypertension, vascular hypertrophy, and oxidative stress. Hypertension 63(5), 1056–1062 (2014)CrossRefPubMed S.-J. Smillie, R. King, X. Kodji, E. Outzen, G. Pozsgai, E. Fernandes, N. Marshall, P. De Winter, R.J. Heads, C. Dessapt-Baradez, An ongoing role of α-calcitonin gene–related peptide as part of a protective network against hypertension, vascular hypertrophy, and oxidative stress. Hypertension 63(5), 1056–1062 (2014)CrossRefPubMed
15.
go back to reference F. Russell, R. King, S.-J. Smillie, X. Kodji, S. Brain, Calcitonin gene-related peptide: physiology and pathophysiology. Physiol. Rev. 94(4), 1099–1142 (2014)CrossRefPubMedPubMedCentral F. Russell, R. King, S.-J. Smillie, X. Kodji, S. Brain, Calcitonin gene-related peptide: physiology and pathophysiology. Physiol. Rev. 94(4), 1099–1142 (2014)CrossRefPubMedPubMedCentral
16.
go back to reference R.N. Danaher, K.M. Loomes, B.L. Leonard, L. Whiting, D.L. Hay, L.Y. Xu, E.W. Kraegen, A.R. Phillips, G.J. Cooper, Evidence that α-calcitonin gene-related peptide is a neurohormone that controls systemic lipid availability and utilization. Endocrinology 149(1), 154–160 (2008)CrossRefPubMed R.N. Danaher, K.M. Loomes, B.L. Leonard, L. Whiting, D.L. Hay, L.Y. Xu, E.W. Kraegen, A.R. Phillips, G.J. Cooper, Evidence that α-calcitonin gene-related peptide is a neurohormone that controls systemic lipid availability and utilization. Endocrinology 149(1), 154–160 (2008)CrossRefPubMed
17.
go back to reference B. Leighton, G.J. Cooper, Pancreatic amylin and calcitonin gene-related peptide cause resistance to insulin in skeletal muscle in vitro. Nature 335(6191), 632–635 (1988)CrossRefPubMed B. Leighton, G.J. Cooper, Pancreatic amylin and calcitonin gene-related peptide cause resistance to insulin in skeletal muscle in vitro. Nature 335(6191), 632–635 (1988)CrossRefPubMed
18.
go back to reference B. Leighton, E. Foot, The role of the sensory peptide calcitonin-gene-related peptide (s) in skeletal muscle carbohydrate metabolism: effects of capsaicin and resiniferatoxin. Biochem. J. 307(3), 707–712 (1995)CrossRefPubMedPubMedCentral B. Leighton, E. Foot, The role of the sensory peptide calcitonin-gene-related peptide (s) in skeletal muscle carbohydrate metabolism: effects of capsaicin and resiniferatoxin. Biochem. J. 307(3), 707–712 (1995)CrossRefPubMedPubMedCentral
19.
go back to reference C.S. Walker, D.L. Hay, S.M. Fitzpatrick, G.J. Cooper, K.M. Loomes, α-Calcitonin gene related peptide (α-CGRP) mediated lipid mobilization in 3T3-L1 adipocytes. Peptides 58, 14–19 (2014)CrossRefPubMed C.S. Walker, D.L. Hay, S.M. Fitzpatrick, G.J. Cooper, K.M. Loomes, α-Calcitonin gene related peptide (α-CGRP) mediated lipid mobilization in 3T3-L1 adipocytes. Peptides 58, 14–19 (2014)CrossRefPubMed
20.
go back to reference K. Chatzipanteli, R.B. Goldbergt, G.A. Howard, B.A. Roos, Calcitonin gene-related peptide is an adipose-tissue neuropeptide with lipolytic actions. Endocrinol. Metab. 3(4), 235–242 (1996) K. Chatzipanteli, R.B. Goldbergt, G.A. Howard, B.A. Roos, Calcitonin gene-related peptide is an adipose-tissue neuropeptide with lipolytic actions. Endocrinol. Metab. 3(4), 235–242 (1996)
21.
go back to reference P. Linscheid, D. Seboek, H. Zulewski, U. Keller, B. Muller, Autocrine/paracrine role of inflammation-mediated calcitonin gene-related peptide and adrenomedullin expression in human adipose tissue. Endocrinology 146(6), 2699–2708 (2005)CrossRefPubMed P. Linscheid, D. Seboek, H. Zulewski, U. Keller, B. Muller, Autocrine/paracrine role of inflammation-mediated calcitonin gene-related peptide and adrenomedullin expression in human adipose tissue. Endocrinology 146(6), 2699–2708 (2005)CrossRefPubMed
22.
go back to reference T. Liu, A. Kamiyoshi, T. Sakurai, Y. Ichikawa-Shindo, H. Kawate, L. Yang, M. Tanaka, X. Xian, A. Imai, L. Zhai, Endogenous calcitonin gene-related peptide regulates lipid metabolism and energy homeostasis in male mice. Endocrinology 158(5), 1194–1206 (2017)CrossRefPubMed T. Liu, A. Kamiyoshi, T. Sakurai, Y. Ichikawa-Shindo, H. Kawate, L. Yang, M. Tanaka, X. Xian, A. Imai, L. Zhai, Endogenous calcitonin gene-related peptide regulates lipid metabolism and energy homeostasis in male mice. Endocrinology 158(5), 1194–1206 (2017)CrossRefPubMed
23.
go back to reference C.S. Walker, X. Li, L. Whiting, S. Glyn-Jones, S. Zhang, A.J. Hickey, M.A. Sewell, K. Ruggiero, A.R. Phillips, E.W. Kraegen, Mice lacking the neuropeptide α-calcitonin gene-related peptide are protected against diet-induced obesity. Endocrinology 151(9), 4257–4269 (2010)CrossRefPubMed C.S. Walker, X. Li, L. Whiting, S. Glyn-Jones, S. Zhang, A.J. Hickey, M.A. Sewell, K. Ruggiero, A.R. Phillips, E.W. Kraegen, Mice lacking the neuropeptide α-calcitonin gene-related peptide are protected against diet-induced obesity. Endocrinology 151(9), 4257–4269 (2010)CrossRefPubMed
24.
go back to reference M. Kjær, T. Mohr, F. Dela, N. Secher, H. Galbo, H.L. Olesen, F.B. Sørensen, S. Schifter, Leg uptake of calcitonin gene‐related peptide during exercise in spinal cord injured humans. Clin. Physiol. Funct. Imaging 21(1), 32–38 (2001)CrossRef M. Kjær, T. Mohr, F. Dela, N. Secher, H. Galbo, H.L. Olesen, F.B. Sørensen, S. Schifter, Leg uptake of calcitonin gene‐related peptide during exercise in spinal cord injured humans. Clin. Physiol. Funct. Imaging 21(1), 32–38 (2001)CrossRef
25.
go back to reference B. Schuler, G. Rieger, M. Gubser, M. Arras, M. Gianella, O. Vogel, P. Jirkof, N. Cesarovic, J. Klohs, P. Jakob, Endogenous α‐calcitonin‐gene‐related peptide promotes exercise‐induced, physiological heart hypertrophy in mice. Acta Physiol. 211(1), 107–121 (2014)CrossRef B. Schuler, G. Rieger, M. Gubser, M. Arras, M. Gianella, O. Vogel, P. Jirkof, N. Cesarovic, J. Klohs, P. Jakob, Endogenous α‐calcitonin‐gene‐related peptide promotes exercise‐induced, physiological heart hypertrophy in mice. Acta Physiol. 211(1), 107–121 (2014)CrossRef
26.
go back to reference T. Chiba, A. Yamaguchi, T. Yamatani, A. Nakamura, T. Morishita, T. Inui, M. Fukase, T. Noda, T. Fujita, Calcitonin gene-related peptide receptor antagonist human CGRP-(8–37). Am. J. Physiol.-Endocrinol. Metab. 256(2), E331–E335 (1989)CrossRef T. Chiba, A. Yamaguchi, T. Yamatani, A. Nakamura, T. Morishita, T. Inui, M. Fukase, T. Noda, T. Fujita, Calcitonin gene-related peptide receptor antagonist human CGRP-(8–37). Am. J. Physiol.-Endocrinol. Metab. 256(2), E331–E335 (1989)CrossRef
27.
go back to reference D.L. Hay, M.L. Garelja, D.R. Poyner, C.S. Walker, Update on the pharmacology of calcitonin/CGRP family of peptides: IUPHAR Review 25. Br. J. Pharmacol. 175(1), 3–17 (2018)CrossRefPubMed D.L. Hay, M.L. Garelja, D.R. Poyner, C.S. Walker, Update on the pharmacology of calcitonin/CGRP family of peptides: IUPHAR Review 25. Br. J. Pharmacol. 175(1), 3–17 (2018)CrossRefPubMed
28.
go back to reference S.P. Alexander, A.P. Davenport, E. Kelly, N. Marrion, J.A. Peters, H.E. Benson, E. Faccenda, A.J. Pawson, J.L. Sharman, C. Southan, The Concise Guide to PHARMACOLOGY 2015/16: G protein‐coupled receptors. Br. J. Pharmacol. 172(24), 5744–5869 (2015)CrossRefPubMedPubMedCentral S.P. Alexander, A.P. Davenport, E. Kelly, N. Marrion, J.A. Peters, H.E. Benson, E. Faccenda, A.J. Pawson, J.L. Sharman, C. Southan, The Concise Guide to PHARMACOLOGY 2015/16: G protein‐coupled receptors. Br. J. Pharmacol. 172(24), 5744–5869 (2015)CrossRefPubMedPubMedCentral
29.
go back to reference R. Nikooie, S. Samaneh, Exercise-induced lactate accumulation regulates intramuscular triglyceride metabolism via transforming growth factor-β1 mediated pathways. Mol. Cell. Endocrinol. 419, 244–251 (2016)CrossRefPubMed R. Nikooie, S. Samaneh, Exercise-induced lactate accumulation regulates intramuscular triglyceride metabolism via transforming growth factor-β1 mediated pathways. Mol. Cell. Endocrinol. 419, 244–251 (2016)CrossRefPubMed
30.
go back to reference M. Mansouri, R. Nikooie, A. Keshtkar, B. Larijani, K. Omidfar, Effect of endurance training on retinol‐binding protein 4 gene expression and its protein level in adipose tissue and the liver in diabetic rats induced by a high‐fat diet and streptozotocin. J. Diabetes Investig. 5(5), 484–491 (2014)CrossRefPubMedPubMedCentral M. Mansouri, R. Nikooie, A. Keshtkar, B. Larijani, K. Omidfar, Effect of endurance training on retinol‐binding protein 4 gene expression and its protein level in adipose tissue and the liver in diabetic rats induced by a high‐fat diet and streptozotocin. J. Diabetes Investig. 5(5), 484–491 (2014)CrossRefPubMedPubMedCentral
31.
go back to reference M. Aveseh, R. Nikooie, M. Aminaie, Exercise‐induced changes in tumour LDH‐B and MCT1 expression are modulated by oestrogen‐related receptor alpha in breast cancer‐bearing BALB/c mice. J. Physiol. 593(12), 2635–2648 (2015)CrossRefPubMedPubMedCentral M. Aveseh, R. Nikooie, M. Aminaie, Exercise‐induced changes in tumour LDH‐B and MCT1 expression are modulated by oestrogen‐related receptor alpha in breast cancer‐bearing BALB/c mice. J. Physiol. 593(12), 2635–2648 (2015)CrossRefPubMedPubMedCentral
32.
go back to reference P.C. Emson, M. Zaidi, Further evidence for the origin of circulating calcitonin gene‐related peptide in the rat. J. Physiol. 412(1), 297–308 (1989)CrossRefPubMedPubMedCentral P.C. Emson, M. Zaidi, Further evidence for the origin of circulating calcitonin gene‐related peptide in the rat. J. Physiol. 412(1), 297–308 (1989)CrossRefPubMedPubMedCentral
33.
go back to reference M.A. Patestas, L.P. Gartner. A Textbook of Neuroanatomy John Wiley & Sons, New Jersey (2016) M.A. Patestas, L.P. Gartner. A Textbook of Neuroanatomy John Wiley & Sons, New Jersey (2016)
34.
go back to reference M.J. Watt, G.R. Steinberg, Z.P. Chen, B.E. Kemp, M.A. Febbraio, Fatty acids stimulate AMP‐activated protein kinase and enhance fatty acid oxidation in L6 myotubes. J. Physiol. 574(1), 139–147 (2006)CrossRefPubMedPubMedCentral M.J. Watt, G.R. Steinberg, Z.P. Chen, B.E. Kemp, M.A. Febbraio, Fatty acids stimulate AMP‐activated protein kinase and enhance fatty acid oxidation in L6 myotubes. J. Physiol. 574(1), 139–147 (2006)CrossRefPubMedPubMedCentral
35.
go back to reference H. Drissi, F. Lasmoles, V. Le Mellay, P.J. Marie, M. Lieberherr, Activation of phospholipase C-β1 via Gαq/11during calcium mobilization by calcitonin gene-related peptide. J. Biol. Chem. 273(32), 20168–20174 (1998)CrossRefPubMed H. Drissi, F. Lasmoles, V. Le Mellay, P.J. Marie, M. Lieberherr, Activation of phospholipase C-β1 via Gαq/11during calcium mobilization by calcitonin gene-related peptide. J. Biol. Chem. 273(32), 20168–20174 (1998)CrossRefPubMed
36.
go back to reference N. Fukai, T. Yoshimoto, T. Sugiyama, N. Ozawa, R. Sato, M. Shichiri, Y. Hirata, Concomitant expression of adrenomedullin and its receptor components in rat adipose tissues. Am. J. Physiol.-Endocrinol. Metab. 288(1), E56–E62 (2005)CrossRefPubMed N. Fukai, T. Yoshimoto, T. Sugiyama, N. Ozawa, R. Sato, M. Shichiri, Y. Hirata, Concomitant expression of adrenomedullin and its receptor components in rat adipose tissues. Am. J. Physiol.-Endocrinol. Metab. 288(1), E56–E62 (2005)CrossRefPubMed
37.
go back to reference J. Hoffmann, S. Wecker, L. Neeb, U. Dirnagl, U. Reuter, Primary trigeminal afferents are the main source for stimulus-induced CGRP release into jugular vein blood and CSF. Cephalalgia 32(9), 659–667 (2012)CrossRefPubMed J. Hoffmann, S. Wecker, L. Neeb, U. Dirnagl, U. Reuter, Primary trigeminal afferents are the main source for stimulus-induced CGRP release into jugular vein blood and CSF. Cephalalgia 32(9), 659–667 (2012)CrossRefPubMed
38.
go back to reference P. Hasbak, C. Lundby, N.V. Olsen, S. Schifter, I.-L. Kanstrup, Calcitonin gene-related peptide and adrenomedullin release in humans: effects of exercise and hypoxia. Regul. Pept. 108(2), 89–95 (2002)CrossRefPubMed P. Hasbak, C. Lundby, N.V. Olsen, S. Schifter, I.-L. Kanstrup, Calcitonin gene-related peptide and adrenomedullin release in humans: effects of exercise and hypoxia. Regul. Pept. 108(2), 89–95 (2002)CrossRefPubMed
39.
go back to reference X.-J. Sun, S.-S. Pan, Role of calcitonin gene–related peptide in cardioprotection of short-term and long-term exercise preconditioning. J. Cardiovasc. Pharmacol. 64(1), 53–59 (2014)CrossRefPubMed X.-J. Sun, S.-S. Pan, Role of calcitonin gene–related peptide in cardioprotection of short-term and long-term exercise preconditioning. J. Cardiovasc. Pharmacol. 64(1), 53–59 (2014)CrossRefPubMed
40.
go back to reference R. Hu, Y.-J. Li, X.-H. Li, An overview of non-neural sources of calcitonin gene-related peptide. Curr. Med. Chem. 23(8), 763–773 (2016)CrossRefPubMed R. Hu, Y.-J. Li, X.-H. Li, An overview of non-neural sources of calcitonin gene-related peptide. Curr. Med. Chem. 23(8), 763–773 (2016)CrossRefPubMed
41.
go back to reference M. Sakaguchi, Y. Inaishi, Y. Kashihara, M. Kuno, Release of calcitonin gene‐related peptide from nerve terminals in rat skeletal muscle. J. Physiol. 434(1), 257–270 (1991)CrossRefPubMedPubMedCentral M. Sakaguchi, Y. Inaishi, Y. Kashihara, M. Kuno, Release of calcitonin gene‐related peptide from nerve terminals in rat skeletal muscle. J. Physiol. 434(1), 257–270 (1991)CrossRefPubMedPubMedCentral
42.
go back to reference M. Yamada, T. Ishikawa, A. Yamanaka, A. Fujimori, K. Goto, Local neurogenic regulation of rat hindlimb circulation: CO2‐induced release of calcitonin gene‐related peptide from sensory nerves. Br. J. Pharmacol. 122(4), 710–714 (1997)CrossRefPubMedPubMedCentral M. Yamada, T. Ishikawa, A. Yamanaka, A. Fujimori, K. Goto, Local neurogenic regulation of rat hindlimb circulation: CO2‐induced release of calcitonin gene‐related peptide from sensory nerves. Br. J. Pharmacol. 122(4), 710–714 (1997)CrossRefPubMedPubMedCentral
43.
go back to reference W. Brito Vieira, M. Halsberghe, M. Schwantes, S. Perez, V. Baldissera, J. Prestes, D. Farias, N. Parizotto, Increased lactate threshold after five weeks of treadmill aerobic training in rats. Braz. J. Biol. 74(2), 444–449 (2014)CrossRefPubMed W. Brito Vieira, M. Halsberghe, M. Schwantes, S. Perez, V. Baldissera, J. Prestes, D. Farias, N. Parizotto, Increased lactate threshold after five weeks of treadmill aerobic training in rats. Braz. J. Biol. 74(2), 444–449 (2014)CrossRefPubMed
44.
go back to reference N. Vollestad, J. Hallen, O. Sejersted, Effect of exercise intensity on potassium balance in muscle and blood of man. J. Physiol. 475(2), 359–368 (1994)CrossRefPubMedPubMedCentral N. Vollestad, J. Hallen, O. Sejersted, Effect of exercise intensity on potassium balance in muscle and blood of man. J. Physiol. 475(2), 359–368 (1994)CrossRefPubMedPubMedCentral
45.
go back to reference P. Arner, E. Kriegholm, P. Engfeldt, J. Bolinder, Adrenergic regulation of lipolysis in situ at rest and during exercise. J. Clin. Investig. 85(3), 893 (1990)CrossRefPubMed P. Arner, E. Kriegholm, P. Engfeldt, J. Bolinder, Adrenergic regulation of lipolysis in situ at rest and during exercise. J. Clin. Investig. 85(3), 893 (1990)CrossRefPubMed
46.
go back to reference H.-J. Koh, M.F. Hirshman, H. He, Y. Li, Y. Manabe, J.A. Balschi, L.J. Goodyear, Adrenaline is a critical mediator of acute exercise-induced AMP-activated protein kinase activation in adipocytes. Biochem. J. 403(3), 473–481 (2007)CrossRefPubMedPubMedCentral H.-J. Koh, M.F. Hirshman, H. He, Y. Li, Y. Manabe, J.A. Balschi, L.J. Goodyear, Adrenaline is a critical mediator of acute exercise-induced AMP-activated protein kinase activation in adipocytes. Biochem. J. 403(3), 473–481 (2007)CrossRefPubMedPubMedCentral
47.
go back to reference W.G. Aschenbach, K. Sakamoto, L.J. Goodyear, 5’adenosine monophosphate-activated protein kinase, metabolism and exercise. Sports Med. 34(2), 91–103 (2004)CrossRefPubMed W.G. Aschenbach, K. Sakamoto, L.J. Goodyear, 5’adenosine monophosphate-activated protein kinase, metabolism and exercise. Sports Med. 34(2), 91–103 (2004)CrossRefPubMed
48.
go back to reference S.Y. Chou, J.L. Kostyo, N.A. Adamafio, Growth hormone inhibits activation of phosphatidylinositol phospholipase C by insulin in ob/ob mouse adipose tissue. Endocrinology 126(1), 62–66 (1990)CrossRefPubMed S.Y. Chou, J.L. Kostyo, N.A. Adamafio, Growth hormone inhibits activation of phosphatidylinositol phospholipase C by insulin in ob/ob mouse adipose tissue. Endocrinology 126(1), 62–66 (1990)CrossRefPubMed
49.
go back to reference E. Askew, A. Hecker, V. Coppes, F. Stifel, Cyclic AMP metabolism in adipose tissue of exercise-trained rats. J. Lipid Res. 19(6), 729–736 (1978)PubMed E. Askew, A. Hecker, V. Coppes, F. Stifel, Cyclic AMP metabolism in adipose tissue of exercise-trained rats. J. Lipid Res. 19(6), 729–736 (1978)PubMed
50.
go back to reference R.J. Ho , Dependence of hormone-stimulated lipolysis on ATP and cyclic AMP levels in fat cells. Horm Metab Res 2 (Suppl 2), 83–87 (1970). R.J. Ho , Dependence of hormone-stimulated lipolysis on ATP and cyclic AMP levels in fat cells. Horm Metab Res 2 (Suppl 2), 83–87 (1970).
51.
go back to reference G. Robison, R. Butcher, E. Sutherland, in Cyclic AMP. Academic Press: New York. (1971) pp. 286–316 G. Robison, R. Butcher, E. Sutherland, in Cyclic AMP. Academic Press: New York. (1971) pp. 286–316
Metadata
Title
Serum calcitonin gene-related peptide facilitates adipose tissue lipolysis during exercise via PIPLC/IP3 pathways
Authors
Malihe Aveseh
Maryam Koushkie-Jahromi
Javad Nemati
Saeed Esmaeili-Mahani
Publication date
01-09-2018
Publisher
Springer US
Published in
Endocrine / Issue 3/2018
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-018-1640-2

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