Gastric inhibitory polypeptide receptor antagonism suppresses intramuscular adipose tissue accumulation and ameliorates sarcopenia.
GIP receptor
aging
fibro-adipogenic progenitors
intramuscular adipose tissue
sarcopenia
Journal
Journal of cachexia, sarcopenia and muscle
ISSN: 2190-6009
Titre abrégé: J Cachexia Sarcopenia Muscle
Pays: Germany
ID NLM: 101552883
Informations de publication
Date de publication:
27 Oct 2023
27 Oct 2023
Historique:
revised:
10
08
2023
received:
29
04
2023
accepted:
11
09
2023
medline:
28
10
2023
pubmed:
28
10
2023
entrez:
28
10
2023
Statut:
aheadofprint
Résumé
Intramuscular adipose tissue (IMAT) formation derived from muscle fibro-adipogenic progenitors (FAPs) has been recognized as a pathological feature of sarcopenia. This study aimed to explore whether genetic and pharmacological gastric inhibitory polypeptide (GIP) receptor antagonism suppresses IMAT accumulation and ameliorates sarcopenia in mice. Whole body composition, grip strength, skeletal muscle weight, tibialis anterior (TA) muscle fibre cross-sectional area (CSA) and TA muscle IMAT area were measured in young and aged male C57BL/6 strain GIP receptor (Gipr)-knockout (Gipr Body composition analysis revealed that 104-week-old Gipr GIP promotes the differentiation of muscle FAPs into adipocytes and its receptor antagonism suppresses IMAT accumulation and promotes muscle regeneration. Pharmacological GIP receptor antagonism may serve as a novel therapeutic approach for sarcopenia.
Sections du résumé
BACKGROUND
BACKGROUND
Intramuscular adipose tissue (IMAT) formation derived from muscle fibro-adipogenic progenitors (FAPs) has been recognized as a pathological feature of sarcopenia. This study aimed to explore whether genetic and pharmacological gastric inhibitory polypeptide (GIP) receptor antagonism suppresses IMAT accumulation and ameliorates sarcopenia in mice.
METHODS
METHODS
Whole body composition, grip strength, skeletal muscle weight, tibialis anterior (TA) muscle fibre cross-sectional area (CSA) and TA muscle IMAT area were measured in young and aged male C57BL/6 strain GIP receptor (Gipr)-knockout (Gipr
RESULTS
RESULTS
Body composition analysis revealed that 104-week-old Gipr
CONCLUSIONS
CONCLUSIONS
GIP promotes the differentiation of muscle FAPs into adipocytes and its receptor antagonism suppresses IMAT accumulation and promotes muscle regeneration. Pharmacological GIP receptor antagonism may serve as a novel therapeutic approach for sarcopenia.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Japan Agency for Medical Research and Development (AMED)
ID : JP20ek0210111
Organisme : Suzuken Memorial Foundation
ID : 21-092
Organisme : JSPS KAKENHI
ID : 16H06276
Organisme : JSPS KAKENHI
ID : 22H04922
Organisme : JSPS KAKENHI
ID : 23K16764
Organisme : MEXT Promotion of Distinctive Joint Research Center Program
ID : JPMXP0618217663
Organisme : MEXT Promotion of Distinctive Joint Research Center Program
ID : JPMXP0621467949
Informations de copyright
© 2023 The Authors. Journal of Cachexia, Sarcopenia and Muscle published by Wiley Periodicals LLC.
Références
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019;48:16-31.
Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, et al. Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 2020;21:300-307.e2.
Cruz-Jentoft AJ, Sayer AA. Sarcopenia. Lancet 2019;393:2636-2646.
Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007;132:2131-2157.
Seino Y, Yabe D. Glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1: incretin actions beyond the pancreas. J Diabetes Investig 2013;4:108-130.
Miyawaki K, Yamada Y, Ban N, Ihara Y, Tsukiyama K, Zhou H, et al. Inhibition of gastric inhibitory polypeptide signaling prevents obesity. Nat Med 2002;8:738-742.
Yamada C, Yamada Y, Tsukiyama K, Yamada K, Yamane S, Harada N, et al. Genetic inactivation of GIP signaling reverses aging-associated insulin resistance through body composition changes. Biochem Biophys Res Commun 2007;364:175-180.
Goodpaster BH, Bergman BC, Brennan AM, Sparks LM. Intermuscular adipose tissue in metabolic disease. Nat Rev Endocrinol 2022;19:285-298.
Ogawa M, Belavy DL, Yoshiko A, Armbrecht G, Miokovic T, Felsenberg D, et al. Effects of 8 weeks of bed rest with or without resistance exercise intervention on the volume of the muscle tissue and the adipose tissues of the thigh. Physiol Rep 2020;8:e14560.
Biltz NK, Collins KH, Shen KC, Schwartz K, Harris CA, Meyer GA. Infiltration of intramuscular adipose tissue impairs skeletal muscle contraction. J Physiol 2020;598:2669-2683.
Goodpaster BH, Krishnaswami S, Resnick H, Kelley DE, Haggerty C, Harris TB, et al. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 2003;26:372-379.
Waters DL. Intermuscular adipose tissue: a brief review of etiology, association with physical function and weight loss in older adults. Ann Geriatr Med Res 2019;23:3-8.
Marcus RL, Addison O, Kidde JP, Dibble LE, Lastayo PC. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging 2010;14:362-366.
Pagano AF, Brioche T, Arc-Chagnaud C, Demangel R, Chopard A, Py G. Short-term disuse promotes fatty acid infiltration into skeletal muscle. J Cachexia Sarcopenia Muscle 2018;9:335-347.
Chen W, You W, Valencak TG, Shan T. Bidirectional roles of skeletal muscle fibro-adipogenic progenitors in homeostasis and disease. Ageing Res Rev 2022;80:101682.
Giuliani G, Rosina M, Reggio A. Signaling pathways regulating the fate of fibro/adipogenic progenitors (FAPs) in skeletal muscle regeneration and disease. FEBS J 2022;289:6484-6517.
Wosczyna MN, Konishi CT, Perez Carbajal EE, Wang TT, Walsh RA, Gan Q, et al. Mesenchymal stromal cells are required for regeneration and homeostatic maintenance of skeletal muscle. Cell Rep 2019;27:2029-2035.e5.
Miyawaki K, Yamada Y, Yano H, Niwa H, Ban N, Ihara Y, et al. Glucose intolerance caused by a defect in the entero-insular axis: a study in gastric inhibitory polypeptide receptor knockout mice. Proc Natl Acad Sci U S A 1999;96:14843-14847.
Beaucage KL, Pollmann SI, Sims SM, Dixon SJ, Holdsworth DW. Quantitative in vivo micro-computed tomography for assessment of age-dependent changes in murine whole-body composition. Bone Rep 2016;5:70-80.
Takahashi Y, Shimizu T, Kato S, Nara M, Suganuma Y, Sato T, et al. Reduction of superoxide dismutase 1 delays regeneration of cardiotoxin-injured skeletal muscle in KK/Ta-Ins2Akita mice with progressive diabetic nephropathy. Int J Mol Sci 2021;22:5491.
Fujita H, Morii T, Fujishima H, Sato T, Shimizu T, Hosoba M, et al. The protective roles of GLP-1R signaling in diabetic nephropathy: possible mechanism and therapeutic potential. Kidney Int 2014;85:579-589.
Heredia JE, Mukundan L, Chen FM, Mueller AA, Deo RC, Locksley RM, et al. Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 2013;153:376-388.
Nakamura T, Tanimoto H, Mizuno Y, Okamoto M, Takeuchi M, Tsubamoto Y, et al. Gastric inhibitory polypeptide receptor antagonist, SKL-14959, suppressed body weight gain on diet-induced obesity mice. Obes Sci Pract 2018;4:194-203.
Shoji H, Takao K, Hattori S, Miyakawa T. Age-related changes in behavior in C57BL/6J mice from young adulthood to middle age. Mol Brain 2016;9:11.
Itabe H, Yamaguchi T, Nimura S, Sasabe N. Perilipins: a diversity of intracellular lipid droplet proteins. Lipids Health Dis 2017;16:83.
Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 2010;12:143-152.
Francis GA, Fayard E, Picard F, Auwerx J. Nuclear receptors and the control of metabolism. Annu Rev Physiol 2003;65:261-311.
Lukjanenko L, Karaz S, Stuelsatz P, Gurriaran-Rodriguez U, Michaud J, Dammone G, et al. Aging disrupts muscle stem cell function by impairing matricellular WISP1 secretion from fibro-adipogenic progenitors. Cell Stem Cell 2019;24:433-446.e7.
Uezumi A, Ikemoto-Uezumi M, Zhou H, Kurosawa T, Yoshimoto Y, Nakatani M, et al. Mesenchymal Bmp3b expression maintains skeletal muscle integrity and decreases in age-related sarcopenia. J Clin Invest 2021;131.
Zhu J, Li Y, Lu A, Gharaibeh B, Ma J, Kobayashi T, et al. Follistatin improves skeletal muscle healing after injury and disease through an interaction with muscle regeneration, angiogenesis, and fibrosis. Am J Pathol 2011;179:915-930.
Pagano AF, Demangel R, Brioche T, Jublanc E, Bertrand-Gaday C, Candau R, et al. Muscle regeneration with intermuscular adipose tissue (IMAT) accumulation is modulated by mechanical constraints. PLoS ONE 2015;10:e0144230.
Zhu S, Tian Z, Torigoe D, Zhao J, Xie P, Sugizaki T, et al. Aging- and obesity-related peri-muscular adipose tissue accelerates muscle atrophy. PLoS ONE 2019;14:e0221366.
Mogi M, Kohara K, Nakaoka H, Kan-No H, Tsukuda K, Wang XL, et al. Diabetic mice exhibited a peculiar alteration in body composition with exaggerated ectopic fat deposition after muscle injury due to anomalous cell differentiation. J Cachexia Sarcopenia Muscle 2016;7:213-224.
Kang X, Yang MY, Shi YX, Xie MM, Zhu M, Zheng XL, et al. Interleukin-15 facilitates muscle regeneration through modulation of fibro/adipogenic progenitors. Cell Commun Signal 2018;16:42.
Hansotia T, Maida A, Flock G, Yamada Y, Tsukiyama K, Seino Y, et al. Extrapancreatic incretin receptors modulate glucose homeostasis, body weight, and energy expenditure. J Clin Invest 2007;117:143-152.
Seino Y, Yamazaki Y. Roles of glucose-dependent insulinotropic polypeptide in diet-induced obesity. J Diabetes Investig 2022;13:1122-1128.
Kanemaru Y, Harada N, Shimazu-Kuwahara S, Yamane S, Ikeguchi E, Murata Y, et al. Absence of GIP secretion alleviates age-related obesity and insulin resistance. J Endocrinol 2020;245:13-20.
Kim SJ, Nian C, McIntosh CH. Activation of lipoprotein lipase by glucose-dependent insulinotropic polypeptide in adipocytes. A role for a protein kinase B, LKB1, and AMP-activated protein kinase cascade. J Biol Chem 2007;282:8557-8567.
Lee SJ, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci U S A 2001;98:9306-9311.
Mendell JR, Sahenk Z, Malik V, Gomez AM, Flanigan KM, Lowes LP, et al. A phase 1/2a follistatin gene therapy trial for Becker muscular dystrophy. Mol Ther 2015;23:192-201.
von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2021. J Cachexia Sarcopenia Muscle 2021;12:2259-2261.