Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Current Osteoporosis Reports
Published in: Current Osteoporosis Reports 4/2020

01-08-2020 | Muscle and Bone (A Bonetto and M Brotto, Section Editors)

Bone-Muscle Mutual Interactions

Authors: Nuria Lara-Castillo, Mark L. Johnson

Published in: Current Osteoporosis Reports | Issue 4/2020

Login to get access

Abstract

Purpose of Review

The purpose of this review is to describe the current state of our thinking regarding bone-muscle interactions beyond the mechanical perspective.

Recent Findings

Recent and prior evidence has begun to dissect many of the molecular mechanisms that bone and muscle use to communicate with each other and to modify each other’s function. Several signaling factors produced by muscle and bone have emerged as potential mediators of these biochemical/molecular interactions. These include muscle factors such as myostatin, Irisin, BAIBA, IL-6, and the IGF family and the bone factors FGF-23, Wnt1 and Wnt3a, PGE2, FGF9, RANKL, osteocalcin, and sclerostin.

Summary

The identification of these signaling molecules and their underlying mechanisms offers the very real and exciting possibility that new pharmaceutical approaches can be developed that will permit the simultaneous treatments of diseases that often occur in combination, such as osteoporosis and sarcopenia.
Literature
1.
Gomarasca M, Banfi G, Lombardi G. Myokines: the endocrine coupling of skeletal muscle and bone. Adv Clin Chem. 2020;94:155–218.PubMedCrossRef
2.
• Trajanoska K, et al. Genetics of bone and muscle interactions in humans. Curr Osteoporos Rep. 2019;17(2):86–95 High Importance: This manuscript describes key pleiotropic loci that have been identified by multivariate GWAS studies.PubMedPubMedCentralCrossRef
3.
Bonewald L. Use it or lose it to age: a review of bone and muscle communication. Bone. 2019;120:212–8.PubMedCrossRef
4.
Karsenty G, Mera P. Molecular bases of the crosstalk between bone and muscle. Bone. 2018;115:43–9.PubMedCrossRef
5.
Tagliaferri C, Wittrant Y, Davicco MJ, Walrand S, Coxam V. Muscle and bone, two interconnected tissues. Ageing Res Rev. 2015;21:55–70.PubMedCrossRef
6.
7.
Cianferotti L, Brandi ML. Muscle-bone interactions: basic and clinical aspects. Endocrine. 2014;45(2):165–77.PubMedCrossRef
8.
9.
10.
Byrd HS, Spicer TE, Cierney G 3rd. Management of open tibial fractures. Plast Reconstr Surg. 1985;76(5):719–30.PubMedCrossRef
11.
Cierny G 3rd, Byrd HS, Jones RE. Primary versus delayed soft tissue coverage for severe open tibial fractures. A comparison of results. Clin Orthop Relat Res. 1983;178:54–63.CrossRef
12.
Richards RR, Mahoney JL, Minas T. Influence of soft tissue coverage on the healing of cortical defects in canine diaphyseal bone. Ann Plast Surg. 1986;16(4):296–304.PubMedCrossRef
13.
Godina M. Early microsurgical reconstruction of complex trauma of the extremities. Plast Reconstr Surg. 1986;78(3):285–92.PubMedCrossRef
14.
Chan JK, et al. Soft-tissue reconstruction of open fractures of the lower limb: muscle versus fasciocutaneous flaps. Plast Reconstr Surg. 2012;130(2):284e–95e.PubMedPubMedCentralCrossRef
15.
Cosman F, de Beur SJ, LeBoff M, Lewiecki EM, Tanner B, Randall S, et al. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25(10):2359–81.PubMedPubMedCentralCrossRef
16.
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(4):601.PubMedPubMedCentralCrossRef
17.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412–23.PubMedPubMedCentralCrossRef
18.
Kull M, Kallikorm R, Lember M. Impact of a new sarco-osteopenia definition on health-related quality of life in a population-based cohort in Northern Europe. J Clin Densitom. 2012;15(1):32–8.PubMedCrossRef
19.
Binkley N, Buehring B. Beyond FRAX: it’s time to consider “sarco-osteopenia”. J Clin Densitom. 2009;12(4):413–6.PubMedCrossRef
20.
Sepulveda-Loyola W, et al. The joint occurrence of osteoporosis and sarcopenia (osteosarcopenia): definitions and characteristics. J Am Med Dir Assoc. 2020;21(2):220–5.PubMedCrossRef
21.
Kirk B, Al Saedi A, Duque G. Osteosarcopenia: a case of geroscience. Aging Med (Milton). 2019;2(3):147–56.CrossRef
22.
Fatima M, Brennan-Olsen SL, Duque G. Therapeutic approaches to osteosarcopenia: insights for the clinician. Ther Adv Musculoskelet Dis. 2019;11:1759720x19867009.PubMedPubMedCentralCrossRef
23.
Huo YR, Suriyaarachchi P, Gomez F, Curcio CL, Boersma D, Muir SW, et al. Phenotype of osteosarcopenia in older individuals with a history of falling. J Am Med Dir Assoc. 2015;16(4):290–5.PubMedCrossRef
24.
Ho-Pham LT, Nguyen UD, Nguyen TV. Association between lean mass, fat mass, and bone mineral density: a meta-analysis. J Clin Endocrinol Metab. 2014;99(1):30–8.PubMedCrossRef
25.
Huh JH, Song MK, Park KH, Kim KJ, Kim JE, Rhee YM, et al. Gender-specific pleiotropic bone-muscle relationship in the elderly from a nationwide survey (KNHANES IV). Osteoporos Int. 2014;25(3):1053–61.PubMedCrossRef
26•.
. Luo Y, Jiang K, He M. Association between grip strength and bone mineral density in general US population of NHANES 2013–2014. Arch Osteoporos. 2020;15(1):47 High Importance: This manuscript describes a US population study of hand grip strength and bone mineral density of the femoral neck and total lumbar spine. They found that grip strength can be associated with nonadjacent bones and grip strength of the dominant arm was highly correlated with BMD.PubMedCrossRef
27.
Locquet M, Beaudart C, Durieux N, Reginster JY, Bruyère O. Relationship between the changes over time of bone mass and muscle health in children and adults: a systematic review and meta-analysis. BMC Musculoskelet Disord. 2019;20(1):429.PubMedPubMedCentralCrossRef
28.
29.
Huang J, Hsu YH, Mo C, Abreu E, Kiel DP, Bonewald LF, et al. METTL21C is a potential pleiotropic gene for osteoporosis and sarcopenia acting through the modulation of the NF-kappaB signaling pathway. J Bone Miner Res. 2014;29(7):1531–40.PubMedCrossRef
30.
Medina-Gomez C, Kemp JP, Dimou NL, Kreiner E, Chesi A, Zemel BS, et al. Bivariate genome-wide association meta-analysis of pediatric musculoskeletal traits reveals pleiotropic effects at the SREBF1/TOM1L2 locus. Nat Commun. 2017;8(1):121.PubMedPubMedCentralCrossRef
31.
Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, et al. Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem. 2006;281(10):6120–3.PubMedCrossRef
32.
Gorski JP, Huffman NT, Vallejo J, Brotto L, Chittur SV, Breggia A, et al. Deletion of Mbtps1 (Pcsk8, S1p, Ski-1) gene in osteocytes stimulates soleus muscle regeneration and increased size and contractile force with age. J Biol Chem. 2016;291(9):4308–22.PubMedCrossRef
33.
Gorski JP, Price JL. Bone muscle crosstalk targets muscle regeneration pathway regulated by core circadian transcriptional repressors DEC1 and DEC2. Bonekey Rep. 2016;5:850.PubMedPubMedCentralCrossRef
34.
Samsa WE, Vasanji A, Midura RJ, Kondratov RV. Deficiency of circadian clock protein BMAL1 in mice results in a low bone mass phenotype. Bone. 2016;84:194–203.PubMedPubMedCentralCrossRef
35.
Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G. The molecular clock mediates leptin-regulated bone formation. Cell. 2005;122(5):803–15.PubMedCrossRef
36.
Andrews JL, Zhang X, McCarthy JJ, McDearmon EL, Hornberger TA, Russell B, et al. CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. Proc Natl Acad Sci U S A. 2010;107(44):19090–5.PubMedPubMedCentralCrossRef
37.
Riley LA, Esser KA. The role of the molecular clock in skeletal muscle and what it is teaching us about muscle-bone crosstalk. Curr Osteoporos Rep. 2017;15(3):222–30.PubMedPubMedCentralCrossRef
38•.
. Qin W, Dallas SL. Exosomes and extracellular RNA in muscle and bone aging and crosstalk. Curr Osteoporos Rep. 2019; High Importance: This review discusses the role of extracellular vesicles in bone-muscle crosstalk.
39.
Ge M, Ke R, Cai T, Yang J, Mu X. Identification and proteomic analysis of osteoblast-derived exosomes. Biochem Biophys Res Commun. 2015;467(1):27–32.PubMedCrossRef
40.
Cui Y, Luan J, Li H, Zhou X, Han J. Exosomes derived from mineralizing osteoblasts promote ST2 cell osteogenic differentiation by alteration of microRNA expression. FEBS Lett. 2016;590(1):185–92.PubMedCrossRef
41.
Deng L, Wang Y, Peng Y, Wu Y, Ding Y, Jiang Y, et al. Osteoblast-derived microvesicles: a novel mechanism for communication between osteoblasts and osteoclasts. Bone. 2015;79:37–42.PubMedCrossRef
42.
Huynh N, VonMoss L, Smith D, Rahman I, Felemban MF, Zuo J, et al. Characterization of regulatory extracellular vesicles from osteoclasts. J Dent Res. 2016;95(6):673–9.PubMedPubMedCentralCrossRef
43.
Li D, Liu J, Guo B, Liang C, Dang L, Lu C, et al. Osteoclast-derived exosomal miR-214-3p inhibits osteoblastic bone formation. Nat Commun. 2016;7(1):10872.PubMedPubMedCentralCrossRef
44.
Sun W, Zhao C, Li Y, Wang L, Nie G, Peng J, et al. Osteoclast-derived microRNA-containing exosomes selectively inhibit osteoblast activity. Cell Discov. 2016;2:16015.PubMedPubMedCentralCrossRef
45.
Qin Y, Peng Y, Zhao W, Pan J, Ksiezak-Reding H, Cardozo C, et al. Myostatin inhibits osteoblastic differentiation by suppressing osteocyte-derived exosomal microRNA-218: a novel mechanism in muscle-bone communication. J Biol Chem. 2017;292(26):11021–33.PubMedPubMedCentralCrossRef
46.
Veno PPM, Dusevich V, Bonewald L, Dallas S. Osteocytes release microvesicles that regulate osteoblast function. J Bone Miner Res. 2013;28(Suppl 1):S253.
47.
Sato M, Suzuki T, Kawano M, Tamura M. Circulating osteocyte-derived exosomes contain miRNAs which are enriched in exosomes from MLO-Y4 cells. Biomed Rep. 2017;6(2):223–31.PubMedCrossRef
48.
Lai X, Price C, Lu X(L), Wang L. Imaging and quantifying solute transport across periosteum: implications for muscle-bone crosstalk. Bone. 2014;66:82–9.PubMedPubMedCentralCrossRef
49.
Pedersen BK, Febbraio M. Muscle-derived interleukin-6--a possible link between skeletal muscle, adipose tissue, liver, and brain. Brain Behav Immun. 2005;19(5):371–6.PubMedCrossRef
50.
Pedersen BK, et al. Role of myokines in exercise and metabolism. J Appl Physiol (1985). 2007;103(3):1093–8.CrossRef
51.
Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev. 2008;88(4):1379–406.PubMedCrossRef
52.
McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387(6628):83–90.PubMedCrossRef
53.
Hamrick MW, McPherron AC, Lovejoy CO. Bone mineral content and density in the humerus of adult myostatin-deficient mice. Calcif Tissue Int. 2002;71(1):63–8.PubMedCrossRef
54.
Hamrick MW, Samaddar T, Pennington C, McCormick J. Increased muscle mass with myostatin deficiency improves gains in bone strength with exercise. J Bone Miner Res. 2006;21(3):477–83.PubMedCrossRef
55.
Grobet L, Royo Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, et al. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet. 1997;17(1):71–4.PubMedCrossRef
56.
Kambadur R, Sharma M, Smith TPL, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res. 1997;7(9):910–6.PubMedCrossRef
57.
Smith TP, et al. Myostatin maps to the interval containing the bovine mh locus. Mamm Genome. 1997;8(10):742–4.PubMedCrossRef
58.
Schuelke M, Wagner KR, Stolz LE, Hübner C, Riebel T, Kömen W, et al. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med. 2004;350(26):2682–8.PubMedCrossRef
59.
Hamrick MW, Shi X, Zhang W, Pennington C, Thakore H, Haque M, et al. Loss of myostatin (GDF8) function increases osteogenic differentiation of bone marrow-derived mesenchymal stem cells but the osteogenic effect is ablated with unloading. Bone. 2007;40(6):1544–53.PubMedPubMedCentralCrossRef
60.
Dankbar B, Fennen M, Brunert D, Hayer S, Frank S, Wehmeyer C, et al. Myostatin is a direct regulator of osteoclast differentiation and its inhibition reduces inflammatory joint destruction in mice. Nat Med. 2015;21(9):1085–90.PubMedCrossRef
61.
Chen Y-S, Guo Q, Guo LJ, Liu T, Wu XP, Lin ZY, et al. GDF8 inhibits bone formation and promotes bone resorption in mice. Clin Exp Pharmacol Physiol. 2017;44(4):500–8.PubMedCrossRef
62.
Campbell C, McMillan HJ, Mah JK, Tarnopolsky M, Selby K, McClure T, et al. Myostatin inhibitor ACE-031 treatment of ambulatory boys with Duchenne muscular dystrophy: results of a randomized, placebo-controlled clinical trial. Muscle Nerve. 2017;55(4):458–64.PubMedCrossRef
63.
Long KK, O’Shea KM, Khairallah RJ, Howell K, Paushkin S, Chen KS, et al. Specific inhibition of myostatin activation is beneficial in mouse models of SMA therapy. Hum Mol Genet. 2019;28(7):1076–89.PubMedCrossRef
64.
Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481(7382):463–8.PubMedPubMedCentralCrossRef
65.
Colaianni G, et al. Irisin enhances osteoblast differentiation in vitro. Int J Endocrinol. 2014;2014:–902186.
66.
67.
Thomas T, Burguera B. Is leptin the link between fat and bone mass? J Bone Miner Res. 2002;17(9):1563–9.PubMedCrossRef
68.
Gimble JM, Nuttall ME. Bone and fat: old questions, new insights. Endocrine. 2004;23(2–3):183–8.PubMedCrossRef
69.
Confavreux CB, Levine RL, Karsenty G. A paradigm of integrative physiology, the crosstalk between bone and energy metabolisms. Mol Cell Endocrinol. 2009;310(1–2):21–9.PubMedPubMedCentralCrossRef
70.
Colaianni G, Cuscito C, Mongelli T, Pignataro P, Buccoliero C, Liu P, et al. The myokine irisin increases cortical bone mass. Proc Natl Acad Sci U S A. 2015;112(39):12157–62.PubMedPubMedCentralCrossRef
71.
Qiao X, Nie Y, Ma Y, Chen Y, Cheng R, Yin W, et al. Irisin promotes osteoblast proliferation and differentiation via activating the MAP kinase signaling pathways. Sci Rep. 2016;6:18732.PubMedCrossRef
72.
Zhang J, Valverde P, Zhu X, Murray D, Wu Y, Yu L, et al. Exercise-induced irisin in bone and systemic irisin administration reveal new regulatory mechanisms of bone metabolism. Bone research. 2017;5:–16056.
73.
Colaianni G, Mongelli T, Cuscito C, Pignataro P, Lippo L, Spiro G, et al. Irisin prevents and restores bone loss and muscle atrophy in hind-limb suspended mice. Sci Rep. 2017;7(1):2811.PubMedPubMedCentralCrossRef
74.
Kim H, et al. Irisin mediates effects on bone and fat via αV integrin receptors, 1756. Cell. 2018;175(7):–1768.e17.
75.
76.
Maisonneuve C, Igoudjil A, Begriche K, Lettéron P, Guimont MC, Bastin J, et al. Effects of zidovudine, stavudine and beta-aminoisobutyric acid on lipid homeostasis in mice: possible role in human fat wasting. Antivir Ther. 2004;9(5):801–10.PubMedCrossRef
77.
Note R, Maisonneuve C, Lettéron P, Peytavin G, Djouadi F, Igoudjil A, et al. Mitochondrial and metabolic effects of nucleoside reverse transcriptase inhibitors (NRTIs) in mice receiving one of five single- and three dual-NRTI treatments. Antimicrob Agents Chemother. 2003;47(11):3384–92.PubMedPubMedCentralCrossRef
78.
Igoudjil A, Abbey-Toby A, Begriche K, Grodet A, Chataigner K, Peytavin G, et al. High doses of stavudine induce fat wasting and mild liver damage without impairing mitochondrial respiration in mice. Antivir Ther. 2007;12(3):389–400.PubMedCrossRef
79.
Begriche K, et al. Beta-aminoisobutyric acid prevents diet-induced obesity in mice with partial leptin deficiency. Obesity (Silver Spring, Md). 2008, 2053-2067;(16):9.
80.
Begriche K, Massart J, Fromenty B. Effects of β-aminoisobutyric acid on leptin production and lipid homeostasis: mechanisms and possible relevance for the prevention of obesity. Fundam Clin Pharmacol. 2010;24(3):269–82.PubMedCrossRef
81.
Calvo JA, et al. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J Appl Physiol (1985). 2008;104(5):1304–12.CrossRef
82.
Roberts LD, Boström P, O’Sullivan JF, Schinzel RT, Lewis GD, Dejam A, et al. beta-Aminoisobutyric acid induces browning of white fat and hepatic beta-oxidation and is inversely correlated with cardiometabolic risk factors. Cell Metab. 2014;19(1):96–108.PubMedPubMedCentralCrossRef
83.
Kitase Y, Vallejo JA, Gutheil W, Vemula H, Jähn K, Yi J, et al. beta-Aminoisobutyric acid, l-BAIBA, is a muscle-derived osteocyte survival factor. Cell Rep. 2018;22(6):1531–44.PubMedPubMedCentralCrossRef
84.
85.
Shi CX, Zhao MX, Shu XD, Xiong XQ, Wang JJ, Gao XY, et al. beta-Aminoisobutyric acid attenuates hepatic endoplasmic reticulum stress and glucose/lipid metabolic disturbance in mice with type 2 diabetes. Sci Rep. 2016;6:21924.PubMedPubMedCentralCrossRef
86.
Wang H, Qian J, Zhao X, Xing C, Sun B. beta-Aminoisobutyric acid ameliorates the renal fibrosis in mouse obstructed kidneys via inhibition of renal fibroblast activation and fibrosis. J Pharmacol Sci. 2017;133(4):203–13.PubMedCrossRef
87.
Wang Z, Bian L, Mo C, Shen H, Zhao LJ, Su KJ, et al. Quantification of aminobutyric acids and their clinical applications as biomarkers for osteoporosis. Commun Biol. 2020;3(1):39.PubMedPubMedCentralCrossRef
88.
Ostrowski K, Rohde T, Zacho M, Asp S, Pedersen BK. Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J Physiol. 1998;508(Pt 3):949–53.PubMedPubMedCentralCrossRef
89.
Nehlsen-Cannarella SL, et al. Carbohydrate and the cytokine response to 2.5 h of running. J Appl Physiol (1985). 1997;82(5):1662–7.CrossRef
90.
Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Pedersen BK. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol. 2000;529(Pt 1):237–42.PubMedPubMedCentralCrossRef
91.
Hiscock N, Chan MHS, Bisucci T, Darby IA, Febbraio MA. Skeletal myocytes are a source of interleukin-6 mRNA expression and protein release during contraction: evidence of fiber type specificity. FASEB J. 2004;18(9):992–4.PubMedCrossRef
92.
Starkie RL, Angus DJ, Rolland J, Hargreaves M, Febbraio MA. Effect of prolonged, submaximal exercise and carbohydrate ingestion on monocyte intracellular cytokine production in humans. J Physiol. 2000;528(Pt 3):647–55.PubMedPubMedCentralCrossRef
93.
Starkie RL, Rolland J, Angus DJ, Anderson MJ, Febbraio MA. Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-alpha levels after prolonged running. Am J Phys Cell Phys. 2001;280(4):C769–74.
94.
Juffer P, Jaspers RT, Klein-Nulend J, Bakker AD. Mechanically loaded myotubes affect osteoclast formation. Calcif Tissue Int. 2014;94(3):319–26.PubMedCrossRef
95.
Bakker AD, Kulkarni RN, Klein-Nulend J, Lems WF. IL-6 alters osteocyte signaling toward osteoblasts but not osteoclasts. J Dent Res. 2014;93(4):394–9.PubMedCrossRef
96.
McGregor NE, Murat M, Elango J, Poulton IJ, Walker EC, Crimeen-Irwin B, et al. IL-6 exhibits both cis- and trans-signaling in osteocytes and osteoblasts, but only trans-signaling promotes bone formation and osteoclastogenesis. J Biol Chem. 2019;294(19):7850–63.PubMedPubMedCentralCrossRef
97.
Tresguerres FGF, Torres J, López-Quiles J, Hernández G, Vega JA, Tresguerres IF. The osteocyte: a multifunctional cell within the bone. Ann Anat. 2020;227:151422.PubMedCrossRef
98.
Han Y, You X, Xing W, Zhang Z, Zou W. Paracrine and endocrine actions of bone-the functions of secretory proteins from osteoblasts, osteocytes, and osteoclasts. Bone Res. 2018;6:16.PubMedPubMedCentralCrossRef
99.
100.
Schaffler MB, Cheung WY, Majeska R, Kennedy O. Osteocytes: master orchestrators of bone. Calcif Tissue Int. 2014;94(1):5–24.PubMedCrossRef
101.
102.
103.
DiGirolamo DJ, Clemens TL, Kousteni S. The skeleton as an endocrine organ. Nat Rev Rheumatol. 2012;8(11):674–83.PubMedCrossRef
104.
105.
Yamashita T, Yoshioka M, Itoh N. Identification of a novel fibroblast growth factor, FGF-23, preferentially expressed in the ventrolateral thalamic nucleus of the brain. Biochem Biophys Res Commun. 2000;277(2):494–8.PubMedCrossRef
106.
Feng JQ, Ward LM, Liu S, Lu Y, Xie Y, Yuan B, et al. Loss of DMP1 causes rickets and osteomalacia and identifies a role for osteocytes in mineral metabolism. Nat Genet. 2006;38(11):1310–5.PubMedPubMedCentralCrossRef
107.
Gattineni J, Bates C, Twombley K, Dwarakanath V, Robinson ML, Goetz R, et al. FGF23 decreases renal NaPi-2a and NaPi-2c expression and induces hypophosphatemia in vivo predominantly via FGF receptor 1. Am J Physiol Ren Physiol. 2009;297(2):F282–91.CrossRef
108.
Shimada T, Kakitani M, Yamazaki Y, Hasegawa H, Takeuchi Y, Fujita T, et al. Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J Clin Invest. 2004;113(4):561–8.PubMedPubMedCentralCrossRef
109.
Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, et al. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature. 2006;444(7120):770–4.PubMedCrossRef
110.
Richter B, Faul C. FGF23 actions on target tissues-with and without Klotho. Front Endocrinol (Lausanne). 2018;9:189.CrossRef
111.
112.
Touchberry CD, Green TM, Tchikrizov V, Mannix JE, Mao TF, Carney BW, et al. FGF23 is a novel regulator of intracellular calcium and cardiac contractility in addition to cardiac hypertrophy. Am J Physiol Endocrinol Metab. 2013;304(8):E863–73.PubMedPubMedCentralCrossRef
113.
Kido S, Hashimoto Y, Segawa H, Tatsumi S, Miyamoto KI. Muscle atrophy in patients wirh ckd results from fgf23/klotho-mediated supression of insulin/igf-i signaling. Kidney Research and Clinical Practice. 2012;31(2):A44.CrossRef
114.
Avin KG, Vallejo JA, Chen NX, Wang K, Touchberry CD, Brotto M, et al. Fibroblast growth factor 23 does not directly influence skeletal muscle cell proliferation and differentiation or ex vivo muscle contractility. Am J Physiol Endocrinol Metab. 2018;315(4):E594–e604.PubMedPubMedCentralCrossRef
115.
Wang K, le L, Chun BM, Tiede-Lewis LAM, Shiflett LA, Prideaux M, et al. A novel osteogenic cell line that differentiates into GFP-tagged osteocytes and forms mineral with a bone-like lacunocanalicular structure. J Bone Miner Res. 2019;34(6):979–95.PubMedCrossRef
116.
McCormick, L.A., et al., Role of FGF9 in promotion of early osteocyte differentiation and as a potent inducer of FGF23 expression in osteocytes. J Bone Mineral Res, 2016. American Society of Bone and Mineral Research (ASBMR Annual Meeting – Atlanta, GA 2016): p. Abstract 1122.
117.
118.
Chowdhury S, Schulz L, Palmisano B, Singh P, Berger JM, Yadav VK, et al. Muscle derived interleukin-6 increases exercise capacity by signaling in osteoblasts. J Clin Invest. 2020.
119.
Dole NS, Mazur CM, Acevedo C, Lopez JP, Monteiro DA, Fowler TW, et al. Osteocyte-intrinsic TGF-beta signaling regulates bone quality through perilacunar/canalicular remodeling. Cell Rep. 2017;21(9):2585–96.PubMedPubMedCentralCrossRef
120.
Waning DL, Mohammad KS, Reiken S, Xie W, Andersson DC, John S, et al. Excess TGF-beta mediates muscle weakness associated with bone metastases in mice. Nat Med. 2015;21(11):1262–71.PubMedPubMedCentralCrossRef
121.
122.
Kim JA, Roh E, Hong SH, Lee YB, Kim NH, Yoo HJ, et al. Association of serum sclerostin levels with low skeletal muscle mass: the Korean Sarcopenic Obesity Study (KSOS). Bone. 2019;128:115053.PubMedCrossRef
123.
Hesse E, et al. Sclerostin inhibition alleviates breast cancer-induced bone metastases and muscle weakness. JCI Insight. 2019;5.
124.
Girardi F, Le Grand F. Wnt signaling in skeletal muscle development and regeneration. Prog Mol Biol Transl Sci. 2018;153:157–79.PubMedCrossRef
125.
126.
Huang J, Romero-Suarez S, Lara N, Mo C, Kaja S, Brotto L, et al. Crosstalk between MLO-Y4 osteocytes and C2C12 muscle cells is mediated by the Wnt/beta-catenin pathway. JBMR Plus. 2017;1(2):86–100.PubMedPubMedCentralCrossRef
127.
Kamel MA, Picconi JL, Lara-Castillo N, Johnson ML. Activation of beta-catenin signaling in MLO-Y4 osteocytic cells versus 2T3 osteoblastic cells by fluid flow shear stress and PGE2: implications for the study of mechanosensation in bone. Bone. 2010;47(5):872–81.PubMedPubMedCentralCrossRef
128.
Mo C, Romero-Suarez S, Bonewald L, Johnson M, Brotto M. Prostaglandin E2: from clinical applications to its potential role in bone- muscle crosstalk and myogenic differentiation. Recent Pat Biotechnol. 2012;6(3):223–9.PubMedPubMedCentralCrossRef
129.
Mo C, Zhao R, Vallejo J, Igwe O, Bonewald L, Wetmore L, et al. Prostaglandin E2 promotes proliferation of skeletal muscle myoblasts via EP4 receptor activation. Cell Cycle. 2015;14(10):1507–16.PubMedPubMedCentralCrossRef
130.
Bothwell W, Verburg M, Wynalda M, Daniels EG, Fitzpatrick FA. A radioimmunoassay for the unstable pulmonary metabolites of prostaglandin E1 and E2: an indirect index of their in vivo disposition and pharmacokinetics. J Pharmacol Exp Ther. 1982;220(2):229–35.PubMed
131.
Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O’Brien CA. Matrix-embedded cells control osteoclast formation. Nat Med. 2011;17(10):1235–41.PubMedPubMedCentralCrossRef
132.
Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-hora M, Feng JQ, et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med. 2011;17(10):1231–4.PubMedCrossRef
133.
Wijenayaka AR, Kogawa M, Lim HP, Bonewald LF, Findlay DM, Atkins GJ. Sclerostin stimulates osteocyte support of osteoclast activity by a RANKL-dependent pathway. PLoS One. 2011;6(10):e25900.PubMedPubMedCentralCrossRef
134.
Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397(6717):315–23.PubMedCrossRef
135.
Bonnet N, Bourgoin L, Biver E, Douni E, Ferrari S. RANKL inhibition improves muscle strength and insulin sensitivity and restores bone mass. J Clin Invest. 2019;129(8):3214–23.PubMedPubMedCentralCrossRef
136.
Hamoudi D, Bouredji Z, Marcadet L, Yagita H, Landry LB, Argaw A, et al. Muscle weakness and selective muscle atrophy in osteoprotegerin-deficient mice. Hum Mol Genet. 2020;29(3):483–94.PubMedCrossRef
137.
Boulanger Piette A, Hamoudi D, Marcadet L, Morin F, Argaw A, Ward L, et al. Targeting the muscle-bone unit: filling two needs with one deed in the treatment of Duchenne muscular dystrophy. Curr Osteoporos Rep. 2018;16(5):541–53.PubMedCrossRef
138.
Hamoudi D, Marcadet L, Piette Boulanger A, Yagita H, Bouredji Z, Argaw A, et al. An anti-RANKL treatment reduces muscle inflammation and dysfunction and strengthens bone in dystrophic mice. Hum Mol Genet. 2019;28(18):3101–12.PubMedCrossRef
139.
Brun J, Berthou F, Trajkovski M, Maechler P, Foti M, Bonnet N. Bone regulates browning and energy metabolism through mature osteoblast/osteocyte PPARgamma expression. Diabetes. 2017;66(10):2541–54.PubMedCrossRef
140.
Mera P, Ferron M, Mosialou I. Regulation of energy metabolism by bone-derived hormones. Cold Spring Harb Perspect Med. 2018:8(6).
141.
Picca A, Calvani R, Manes-Gravina E, Spaziani L, Landi F, Bernabei R, et al. Bone-muscle crosstalk: unraveling new therapeutic targets for osteoporosis. Curr Pharm Des. 2017;23(41):6256–63.PubMedCrossRef
142.
Maurel DB, Jahn K, Lara-Castillo N. Muscle-bone crosstalk: emerging opportunities for novel therapeutic approaches to treat musculoskeletal pathologies. Biomedicines. 2017:5(4).
143.
Compston J. Emerging therapeutic concepts for muscle and bone preservation/building. Bone. 2015;80:150–6.PubMedCrossRef
144.
Girgis CM. Integrated therapies for osteoporosis and sarcopenia: from signaling pathways to clinical trials. Calcif Tissue Int. 2015;96(3):243–55.PubMedCrossRef
Metadata
Title
Bone-Muscle Mutual Interactions
Authors
Nuria Lara-Castillo
Mark L. Johnson
Publication date
01-08-2020
Publisher
Springer US
Published in
Current Osteoporosis Reports / Issue 4/2020
Print ISSN: 1544-1873
Electronic ISSN: 1544-2241
DOI
https://doi.org/10.1007/s11914-020-00602-6

Other articles of this Issue 4/2020

Current Osteoporosis Reports 4/2020 Go to the issue

Rare Bone Diseases (CB Langman and E Shore, Section Editors)

Stem Cell Therapy as a Treatment for Osteogenesis Imperfecta

Muscle and Bone (A Bonetto and M Brotto, Section Editors)

Myokines and Osteokines in the Pathogenesis of Muscle and Bone Diseases

Correction

Correction to: New Developments in Fracture Risk Assessment

Bone and Diabetes (A Schwartz and P Vestergaard, Section Editors)

The Impact of Exercise on Bone Health in Type 2 Diabetes Mellitus—a Systematic Review

Skeletal Development (R Marcucio and J Feng, Section Editors)

Polycomb Repressive Complex 2: a Dimmer Switch of Gene Regulation in Calvarial Bone Development

Muscle and Bone (A Bonetto and M Brotto, Section Editors)

Muscle, Bone, and Fat Crosstalk: the Biological Role of Myokines, Osteokines, and Adipokines