Advertisement

The TGF-β Signalling Network in Muscle Development, Adaptation and Disease

  • Justin L. Chen
  • Timothy D. Colgan
  • Kelly L. Walton
  • Paul Gregorevic
  • Craig A. Harrison
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 900)

Abstract

Skeletal muscle possesses remarkable ability to change its size and force-producing capacity in response to physiological stimuli. Impairment of the cellular processes that govern these attributes also affects muscle mass and function in pathological conditions. Myostatin, a member of the TGF-β family, has been identified as a key regulator of muscle development, and adaptation in adulthood. In muscle, myostatin binds to its type I (ALK4/5) and type II (ActRIIA/B) receptors to initiate Smad2/3 signalling and the regulation of target genes that co-ordinate the balance between protein synthesis and degradation. Interestingly, evidence is emerging that other TGF-β proteins act in concert with myostatin to regulate the growth and remodelling of skeletal muscle. Consequently, dysregulation of TGF-β proteins and their associated signalling components is increasingly being implicated in muscle wasting associated with chronic illness, ageing, and inactivity. The growing understanding of TGF-β biology in muscle, and its potential to advance the development of therapeutics for muscle-related conditions is reviewed here.

Keywords

Skeletal muscle wasting Neuromuscular disorders Myostatin Activin TGF-β network 

Notes

Acknowledgements

This work was supported by grant funding (526648, 566820, 1006488, 1078907) from the National Health and Medical Research Council (NHMRC, Australia). JLC is supported by a postdoctoral fellowship from the Cancer Council Victoria. KLW is supported by an Early Career Seed from the Victorian Cancer Agency. PG is supported by a Career Development Fellowship (1046782) from the NHMRC. JLC and TDC were previously supported by Australian Postgraduate Awards. PG was previously supported by a Senior Research Fellowship, sponsored by Pfizer Australia. CAH was supported by a Career Development Fellowship (1013533) from the NHMRC. Hudson Institute of Medical Research and Baker IDI Heart and Diabetes Institute are supported in part by the Operational Infrastructure Support Program of the Victorian Government.

Conflict of Interest

The authors declare no conflict of interest.

References

  1. Acharyya S, Ladner KJ, Nelsen LL et al (2004) Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J Clin Invest 114:370–378PubMedPubMedCentralCrossRefGoogle Scholar
  2. Acharyya S, Villalta SA, Bakkar N et al (2007) Interplay of IKK/NF-kappa B signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest 117:889–901PubMedPubMedCentralCrossRefGoogle Scholar
  3. Akhurst RJ, Hata A (2012) Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov 11:790–811PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allen RE, Boxhorn LK (1987) Inhibition of skeletal muscle satellite cell differentiation by transforming growth factor-beta. J Cell Physiol 133:567–572PubMedCrossRefGoogle Scholar
  5. Allen DL, Unterman TG (2007) Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors. Am J Physiol Cell Physiol 292:C188–C199PubMedCrossRefGoogle Scholar
  6. Andreetta F, Bernasconi P, Baggi F et al (2006) Immunomodulation of TGF-beta1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: Implications for antifibrotic therapy. J Neuroimmunol 175:77–86PubMedCrossRefGoogle Scholar
  7. Anker SD, Negassa A, Coats AJ et al (2003) Prognostic importance of weight loss in chronic heart failure and the effect of treatment with angiotensin-converting-enzyme inhibitors: an observational study. Lancet 361:1077–1083PubMedCrossRefGoogle Scholar
  8. Annes JP, Chen Y, Munger JS et al (2004) Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J Cell Biol 165:723–734PubMedPubMedCentralCrossRefGoogle Scholar
  9. Argadine HM, Hellyer NJ, Mantilla CB et al (2009) The effect of denervation on protein synthesis and degradation in adult rat diaphragm muscle. J Appl Physiol 107:438–444PubMedPubMedCentralCrossRefGoogle Scholar
  10. Assoian RK, Komoriya A, Meyers CA et al (1983) Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization. J Biol Chem 258:7155–7160PubMedGoogle Scholar
  11. Attie KM, Borgstein NG, Yang Y et al (2013) A single ascending-dose study of muscle regulator ACE-031 in healthy volunteers. Muscle Nerve 47:416–423PubMedCrossRefGoogle Scholar
  12. Baldwin RL, Friess H, Yokoyama M et al (1996) Attenuated ALK5 receptor expression in human pancreatic cancer: correlation with resistance to growth inhibition. Int J Cancer 67:283–288PubMedCrossRefGoogle Scholar
  13. Baran W, Szepietowski JC, Mazur G et al (2007) TGF-beta(1) gene polymorphism in psoriasis vulgaris. Cytokine 38:8–11PubMedCrossRefGoogle Scholar
  14. Baumann AP, Ibebunjo C, Grasser WA et al (2003) Myostatin expression in age and denervation-induced skeletal muscle atrophy. J Musculoskelet Neuronal Interact 3:8–16PubMedGoogle Scholar
  15. Bauskin AR, Brown DA, Kuffner T et al (2006) Role of macrophage inhibitory cytokine-1 in tumorigenesis and diagnosis of cancer. Cancer Res 66:4983–4986PubMedCrossRefGoogle Scholar
  16. Behan WM, Longman C, Petty RK et al (2003) Muscle fibrillin deficiency in Marfan’s syndrome myopathy. J Neurol Neurosurg Psychiatry 74:633–638PubMedPubMedCentralCrossRefGoogle Scholar
  17. Belville C, Josso N, Picard JY (1999) Persistence of Mullerian derivatives in males. Am J Med Genet 89:218–223PubMedCrossRefGoogle Scholar
  18. Berg JN, Gallione CJ, Stenzel TT et al (1997) The activin receptor-like kinase 1 gene: genomic structure and mutations in hereditary hemorrhagic telangiectasia type 2. Am J Hum Genet 61:60–67PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bernasconi P, Di Blasi C, Mora M et al (1999) Transforming growth factor-beta 1 and fibrosis in congenital muscular dystrophies. Neuromusc Disord 9:28–33PubMedCrossRefGoogle Scholar
  20. Blobe GC, Schiemann WP, Lodish HF (2000) Role of transforming growth factor beta in human disease. N Engl J Med 342:1350–1358PubMedCrossRefGoogle Scholar
  21. Bodine SC, Stitt TN, Gonzalez M et al (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014–1019PubMedCrossRefGoogle Scholar
  22. Bogdanovich S, Krag TO, Barton ER et al (2002) Functional improvement of dystrophic muscle by myostatin blockade. Nature 420:418–421PubMedCrossRefGoogle Scholar
  23. Bogdanovich S, Perkins KJ, Krag TO et al (2005) Myostatin propeptide-mediated amelioration of dystrophic pathophysiology. FASEB J 19:543–549PubMedCrossRefGoogle Scholar
  24. Booth FW, Seider MJ (1979) Early change in skeletal muscle protein synthesis after limb immobilization of rats. J Appl Physiol 47:974–977PubMedGoogle Scholar
  25. Border WA, Noble NA (1994) Transforming growth factor beta in tissue fibrosis. N Engl J Med 331:1286–1292PubMedCrossRefGoogle Scholar
  26. Bosaeus I, Daneryd P, Svanberg E et al (2001) Dietary intake and resting energy expenditure in relation to weight loss in unselected cancer patients. Int J Cancer 93:380–383PubMedCrossRefGoogle Scholar
  27. Bottinger EP, Factor VM, Tsang ML et al (1996) The recombinant proregion of transforming growth factor beta1 (latency-associated peptide) inhibits active transforming growth factor beta1 in transgenic mice. Proc Natl Acad Sci U S A 93:5877–5882PubMedPubMedCentralCrossRefGoogle Scholar
  28. Brown DJ, Kim TB, Petty EM et al (2002) Autosomal dominant stapes ankylosis with broad thumbs and toes, hyperopia, and skeletal anomalies is caused by heterozygous nonsense and frameshift mutations in NOG, the gene encoding noggin. Am J Hum Genet 71:618–624PubMedPubMedCentralCrossRefGoogle Scholar
  29. Brunner AM, Marquardt H, Malacko AR et al (1989) Site-directed mutagenesis of cysteine residues in the pro region of the transforming growth factor beta 1 precursor. Expression and characterization of mutant proteins. J Biol Chem 264:13660–13664PubMedGoogle Scholar
  30. Buijs JT, Henriquez NV, Van Overveld PG et al (2007) TGF-beta and BMP7 interactions in tumour progression and bone metastasis. Clin Exp Metastasis 24:609–617PubMedCrossRefGoogle Scholar
  31. Burks TN, Andres-Mateos E, Marx R et al. (2011) Losartan restores skeletal muscle remodeling and protects against disuse atrophy in sarcopenia. Sci Transl Med 3:82ra37Google Scholar
  32. Campbell KP, Kahl SD (1989) Association of dystrophin and an integral membrane glycoprotein. Nature 338:259–262PubMedCrossRefGoogle Scholar
  33. Carlson ME, Conboy MJ, Hsu M et al (2009) Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 8:676–689PubMedPubMedCentralCrossRefGoogle Scholar
  34. Chang H, Brown CW, Matzuk MM (2002) Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev 23:787–823PubMedCrossRefGoogle Scholar
  35. Cheifetz S, Hernandez H, Laiho M et al (1990) Distinct transforming growth factor-beta (TGF-beta) receptor subsets as determinants of cellular responsiveness to three TGF-beta isoforms. J Biol Chem 265:20533–20538PubMedGoogle Scholar
  36. Chen YW, Nagaraju K, Bakay M et al (2005) Early onset of inflammation and later involvement of TGF beta in Duchenne muscular dystrophy. Neurology 65:826–834PubMedCrossRefGoogle Scholar
  37. Chen H, Brady Ridgway J, Sai T et al (2013) Context-dependent signaling defines roles of BMP9 and BMP10 in embryonic and postnatal development. Proc Natl Acad Sci U S A 110:11887–11892PubMedPubMedCentralCrossRefGoogle Scholar
  38. Chen JL, Walton KL, Winbanks CE et al (2014) Elevated expression of activins promotes muscle wasting and cachexia. FASEB J 28:1711–1723PubMedCrossRefGoogle Scholar
  39. Chen JL, Walton KL, Al-Musawi SL et al (2015) Development of novel activin-targeted therapeutics. Mol Ther 23:434–444PubMedPubMedCentralCrossRefGoogle Scholar
  40. Chiu CS, Peekhaus N, Weber H et al (2013) Increased muscle force production and bone mineral density in ActRIIB-Fc-treated mature rodents. J Gerontol A Biol Sci Med Sci 68:1181–1192PubMedCrossRefGoogle Scholar
  41. Ciciliot S, Rossi AC, Dyar KA et al (2013) Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 45:2191–2199PubMedCrossRefGoogle Scholar
  42. Clement JH, Raida M, Sanger J et al (2005) Bone morphogenetic protein 2 (BMP-2) induces in vitro invasion and in vivo hormone independent growth of breast carcinoma cells. Int J Oncol 27:401–407PubMedGoogle Scholar
  43. Cohn RD, Campbell KP (2000) Molecular basis of muscular dystrophies. Muscle Nerve 23:1456–1471PubMedCrossRefGoogle Scholar
  44. Cohn RD, Van Erp C, Habashi JP et al (2007) Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat Med 13:204–210PubMedPubMedCentralCrossRefGoogle Scholar
  45. Collins-Hooper H, Sartori R, Macharia R et al. (2014) Propeptide-mediated inhibition of myostatin increases muscle mass through inhibiting proteolytic pathways in aged mice. J Gerontol A Biol Sci Med Sci 69(9):1049–1059Google Scholar
  46. Constantin B (2014) Dystrophin complex functions as a scaffold for signalling proteins. Biochim Biophys Acta-Biomembr 1838:635–642CrossRefGoogle Scholar
  47. Cornelison DD, Olwin BB, Rudnicki MA et al (2000) MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol 224:122–137PubMedCrossRefGoogle Scholar
  48. Cusella-De Angelis MG, Molinari S, Le Donne A et al (1994) Differential response of embryonic and fetal myoblasts to TGF beta: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120:925–933PubMedGoogle Scholar
  49. D’abronzo FH, Swearingen B, Klibanski A et al (1999) Mutational analysis of activin/transforming growth factor-beta type I and type II receptor kinases in human pituitary tumors. J Clin Endocrinol Metab 84:1716–1721PubMedCrossRefGoogle Scholar
  50. Dam TT, Peters KW, Fragala M et al (2014) An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol A Biol Sci Med Sci 69:584–590PubMedPubMedCentralCrossRefGoogle Scholar
  51. De Boer MD, Selby A, Atherton P et al (2007) The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. J Physiol 585:241–251PubMedPubMedCentralCrossRefGoogle Scholar
  52. De Crescenzo G, Grothe S, Zwaagstra J et al (2001) Real-time monitoring of the interactions of transforming growth factor-beta (TGF-beta) isoforms with latency-associated protein and the ectodomains of the TGF-beta type II and III receptors reveals different kinetic models and stoichiometries of binding. J Biol Chem 276:29632–29643PubMedCrossRefGoogle Scholar
  53. Dean JC (2007) Marfan syndrome: clinical diagnosis and management. Eur J Hum Genet 15:724–733PubMedCrossRefGoogle Scholar
  54. Dewys WD (1986) Weight-loss and nutritional abnormalities in cancer-patients – incidence, severity and significance. Clin Oncol 5:251–261Google Scholar
  55. Dietz HC, Cutting GR, Pyeritz RE et al (1991) Marfan-syndrome caused by a recurrent denovo missense mutation in the fibrillin gene. Nature 352:337–339PubMedCrossRefGoogle Scholar
  56. Dubois CM, Laprise MH, Blanchette F et al (1995) Processing of transforming growth factor beta 1 precursor by human furin convertase. J Biol Chem 270:10618–10624PubMedCrossRefGoogle Scholar
  57. Engvall E, Wewer UM (2003) The new frontier in muscular dystrophy research: booster genes. FASEB J 17:1579–1584PubMedCrossRefGoogle Scholar
  58. Eppert K, Scherer SW, Ozcelik H et al (1996) MADR2 maps to 18q21 and encodes a TGFbeta-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86:543–552PubMedCrossRefGoogle Scholar
  59. Ervasti JM, Ohlendieck K, Kahl SD et al (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345:315–319PubMedCrossRefGoogle Scholar
  60. Fearon K, Arends J, Baracos V (2013) Understanding the mechanisms and treatment options in cancer cachexia. Nat Rev Clin Oncol 10:90–99PubMedCrossRefGoogle Scholar
  61. Franken R, Radonic T, Den Hartog AW et al (2014) The revised role of TGF-beta in aortic aneurysms in Marfan syndrome. Neth Heart JGoogle Scholar
  62. Gazzerro E, Canalis E (2006) Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord 7:51–65PubMedCrossRefGoogle Scholar
  63. Ge GX, Hopkins DR, Greenspan DS (2006) GDF11 forms a bone morphogenetic protein 1-activated latent complex that can modulate nerve growth factor-induced differentiation of PC12 cells. FASEB J 20:A515Google Scholar
  64. Gentry LE, Nash BW (1990) The pro domain of pre-pro-transforming growth factor beta 1 when independently expressed is a functional binding protein for the mature growth factor. Biochemistry 29:6851–6857PubMedCrossRefGoogle Scholar
  65. Gentry LE, Lioubin MN, Purchio AF et al (1988) Molecular events in the processing of recombinant type 1 pre-pro-transforming growth factor beta to the mature polypeptide. Mol Cell Biol 8:4162–4168PubMedPubMedCentralCrossRefGoogle Scholar
  66. Glass D, Roubenoff R (2010) Recent advances in the biology and therapy of muscle wasting. Ann N Y Acad Sci 1211:25–36PubMedCrossRefGoogle Scholar
  67. Glister C, Kemp CF, Knight PG (2004) Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction 127:239–254PubMedCrossRefGoogle Scholar
  68. Goggins M, Shekher M, Turnacioglu K et al (1998) Genetic alterations of the transforming growth factor beta receptor genes in pancreatic and biliary adenocarcinomas. Cancer Res 58:5329–5332PubMedGoogle Scholar
  69. Gong Y, Krakow D, Marcelino J et al (1999) Heterozygous mutations in the gene encoding noggin affect human joint morphogenesis. Nat Genet 21:302–304PubMedCrossRefGoogle Scholar
  70. Gordon KJ, Blobe GC (2008) Role of transforming growth factor-beta superfamily signaling pathways in human disease. Biochim Biophys Acta 1782:197–228PubMedCrossRefGoogle Scholar
  71. Gosselin LE, Martinez DA (2004) Impact of TNF-alpha blockade on TGF-beta 1 and type I collagen mRNA expression in dystrophic muscle. Muscle Nerve 30:244–246PubMedCrossRefGoogle Scholar
  72. Gosselin LE, Williams JE, Deering M et al (2004) Localization and early time course of TGF-beta 1 mRNA expression in dystrophic muscle. Muscle Nerve 30:645–653PubMedCrossRefGoogle Scholar
  73. Grady WM, Myeroff LL, Swinler SE et al (1999) Mutational inactivation of transforming growth factor beta receptor type II in microsatellite stable colon cancers. Cancer Res 59:320–324PubMedGoogle Scholar
  74. Greenwald J, Groppe J, Gray P et al (2003) The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol Cell 11:605–617PubMedCrossRefGoogle Scholar
  75. Groenink M, Den Hartog AW, Franken R et al (2013) Losartan reduces aortic dilatation rate in adults with Marfan syndrome: a randomized controlled trial. Eur Heart J 34:3491–3500PubMedCrossRefGoogle Scholar
  76. Groppe JC, Shore EM, Kaplan FS (2007) Functional modeling of the ACVR1 (R206H) mutation in FOP. Clin Orthop Relat Res 462:87–92PubMedCrossRefGoogle Scholar
  77. Habashi JP, Judge DP, Holm TM et al (2006) Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312:117–121PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hahn SA, Schutte M, Hoque AT et al (1996) DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271:350–353PubMedCrossRefGoogle Scholar
  79. Halder SK, Beauchamp RD, Datta PK (2005) A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7:509–521PubMedPubMedCentralCrossRefGoogle Scholar
  80. Hanafusa H, Ninomiya-Tsuji J, Masuyama N et al (1999) Involvement of the p38 mitogen-activated protein kinase pathway in transforming growth factor-beta-induced gene expression. J Biol Chem 274:27161–27167PubMedCrossRefGoogle Scholar
  81. Harrington AE, Morris-Triggs SA, Ruotolo BT et al (2006) Structural basis for the inhibition of activin signalling by follistatin. EMBO J 25:1035–1045PubMedPubMedCentralCrossRefGoogle Scholar
  82. Harrison CA, Gray PC, Fischer WH et al (2004) An activin mutant with disrupted ALK4 binding blocks signaling via type II receptors. J Biol Chem 279:28036–28044PubMedCrossRefGoogle Scholar
  83. Harrison CA, Al-Musawi SL, Walton KL (2011) Prodomains regulate the synthesis, extracellular localisation and activity of TGF-beta superfamily ligands. Growth Factors 29:174–186PubMedCrossRefGoogle Scholar
  84. Hill JJ, Davies MV, Pearson AA et al (2002) The myostatin propeptide and the follistatin-related gene are inhibitory binding proteins of myostatin in normal serum. J Biol Chem 277:40735–40741PubMedCrossRefGoogle Scholar
  85. Hillebrand M, Millot N, Sheikhzadeh S et al (2014) Total serum transforming growth factor-beta 1 is elevated in the entire spectrum of genetic aortic syndromes. Clin Cardiol 37:672–679PubMedCrossRefGoogle Scholar
  86. Hoffman EP, Brown RH, Kunkel LM (1987) Dystrophin – the protein product of the duchenne muscular-dystrophy locus. Cell 51:919–928PubMedCrossRefGoogle Scholar
  87. Hollister DW, Godfrey M, Sakai LY et al (1990) Immunohistologic abnormalities of the microfibrillar-fiber system in the Marfan-syndrome. N Engl J Med 323:152–159PubMedCrossRefGoogle Scholar
  88. Howe JR, Roth S, Ringold JC et al (1998) Mutations in the SMAD4/DPC4 gene in juvenile polyposis. Science 280:1086–1088PubMedCrossRefGoogle Scholar
  89. Howe JR, Bair JL, Sayed MG et al (2001) Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis. Nat Genet 28:184–187PubMedCrossRefGoogle Scholar
  90. Hribal ML, Nakae J, Kitamura T et al (2003) Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J Cell Biol 162:535–541PubMedPubMedCentralCrossRefGoogle Scholar
  91. Husken-Hindi P, Tsuchida K, Park M et al (1994) Monomeric activin A retains high receptor binding affinity but exhibits low biological activity. J Biol Chem 269:19380–19384PubMedGoogle Scholar
  92. Ikushima H, Miyazono K (2010) TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 10:415–424PubMedCrossRefGoogle Scholar
  93. Iwasaki S, Miyak M, Hayashi S et al (2013) Effect of myostatin on chemokine expression in regenerating skeletal muscle cells. Cells Tissues Organs 198:66–74PubMedCrossRefGoogle Scholar
  94. Iwase S, Murakami T, Saito Y et al (2004) Steep elevation of blood interleukin-6 (IL-6) associated only with late stages of cachexia in cancer patients. Eur Cytokine Netw 15:312–316PubMedGoogle Scholar
  95. Jacobs PA, Hunt PA, Mayer M et al (1981) Duchenne muscular-dystrophy (DMD) in a female with an X-autosome translocation – further evidence that the dmd locus is at Xp21. Am J Hum Genet 33:513–518PubMedPubMedCentralGoogle Scholar
  96. Javelaud D, Mauviel A (2005) Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene 24:5742–5750PubMedCrossRefGoogle Scholar
  97. Jespersen J, Kjaer M, Schjerling P (2006) The possible role of myostatin in skeletal muscle atrophy and cachexia. Scand J Med Sci Sports 16:74–82PubMedCrossRefGoogle Scholar
  98. Jiang CH, Wen YF, Kuroda K et al (2014) Notch signaling deficiency underlies age-dependent depletion of satellite cells in muscular dystrophy. Dis Model Mech 7:997–1004PubMedPubMedCentralCrossRefGoogle Scholar
  99. Jones SW, Hill RJ, Krasney PA et al (2004) Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18:1025–1027PubMedGoogle Scholar
  100. Joulia-Ekaza D, Cabello G (2006) Myostatin regulation of muscle development: molecular basis, natural mutations, physiopathological aspects. Exp Cell Res 312:2401–2414PubMedCrossRefGoogle Scholar
  101. Judge DP, Dietz HC (2005) Marfan’s syndrome. Lancet 366:1965–1976PubMedPubMedCentralCrossRefGoogle Scholar
  102. Jung B, Nougaret S, Conseil M et al (2014) Sepsis is associated with a preferential diaphragmatic atrophy a critically Ill patient study using tridimensional computed tomography. Anesthesiology 120:1182–1191PubMedCrossRefGoogle Scholar
  103. Kaartinen V, Warburton D (2003) Fibrillin controls TGF-beta activation. Nat Genet 33:331–332PubMedCrossRefGoogle Scholar
  104. Kinoshita A, Saito T, Tomita H et al (2000) Domain-specific mutations in TGFB1 result in Camurati-Engelmann disease. Nat Genet 26:19–20PubMedCrossRefGoogle Scholar
  105. Knaus PI, Lindemann D, Decoteau JF et al (1996) A dominant inhibitory mutant of the type II transforming growth factor beta receptor in the malignant progression of a cutaneous T-cell lymphoma. Mol Cell Biol 16:3480–3489PubMedPubMedCentralCrossRefGoogle Scholar
  106. Koenig M, Hoffman EP, Bertelson CJ et al (1987) Complete cloning of the Duchenne muscular-dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50:509–517PubMedCrossRefGoogle Scholar
  107. Kollias HD, Mcdermott JC (2008) Transforming growth factor-beta and myostatin signaling in skeletal muscle. J Appl Physiol 104:579–587PubMedCrossRefGoogle Scholar
  108. Kubota T, Zhang Q, Wrana JL et al (1989) Multiple forms of SppI (secreted phosphoprotein, osteopontin) synthesized by normal and transformed rat bone cell populations: regulation by TGF-beta. Biochem Biophys Res Commun 162:1453–1459PubMedCrossRefGoogle Scholar
  109. Kuroda K, Nakashima J, Kanao K et al (2007) Interleukin 6 is associated with cachexia in patients with prostate cancer. Urology 69:113–117PubMedCrossRefGoogle Scholar
  110. La Thangue NB (1996) E2F and the molecular mechanisms of early cell-cycle control. Biochem Soc Trans 24:54–59PubMedCrossRefGoogle Scholar
  111. Lach-Trifilieff E, Minetti GC, Sheppard K et al (2014) An antibody blocking activin type II receptors induces strong skeletal muscle hypertrophy and protects from atrophy. Mol Cell Biol 34:606–618PubMedPubMedCentralCrossRefGoogle Scholar
  112. Lacro RV, Guey LT, Dietz HC et al. (2013) Characteristics of children and young adults with Marfan syndrome and aortic root dilation in a randomized trial comparing atenolol and Losartan therapy. Am Heart J 165:828–835Google Scholar
  113. Lacro RV, Dietz HC, Sleeper LA et al (2014) Atenolol versus Losartan in children and young adults with Marfan’s syndrome. N Engl J Med 371:2061–2071PubMedPubMedCentralCrossRefGoogle Scholar
  114. Lam EW, La Thangue NB (1994) DP and E2F proteins: coordinating transcription with cell cycle progression. Curr Opin Cell Biol 6:859–866PubMedCrossRefGoogle Scholar
  115. Lane KB, Machado RD, Pauciulo MW et al (2000) Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. Nat Genet 26:81–84PubMedCrossRefGoogle Scholar
  116. Langley B, Thomas M, Bishop A et al (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277:49831–49840PubMedCrossRefGoogle Scholar
  117. Laping NJ, Grygielko E, Mathur A et al (2002) Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol 62:58–64PubMedCrossRefGoogle Scholar
  118. Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149:274–293PubMedPubMedCentralCrossRefGoogle Scholar
  119. Lee SJ (2007) Quadrupling muscle mass in mice by targeting TGF-beta signaling pathways. PLoS One 2, e789PubMedPubMedCentralCrossRefGoogle Scholar
  120. Lee SJ (2008) Genetic analysis of the role of proteolysis in the activation of latent myostatin. PLoS One 3, e1628PubMedPubMedCentralCrossRefGoogle Scholar
  121. Lee SJ, Mcpherron AC (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci U S A 98:9306–9311PubMedPubMedCentralCrossRefGoogle Scholar
  122. Lee SJ, Reed LA, Davies MV et al (2005) Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc Natl Acad Sci U S A 102:18117–18122PubMedPubMedCentralCrossRefGoogle Scholar
  123. Leger B, Derave W, De Bock K et al (2008) Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of akt phosphorylation. Rejuvenation Res 11:163–175PubMedCrossRefGoogle Scholar
  124. Lehmann K, Seemann P, Stricker S et al (2003) Mutations in bone morphogenetic protein receptor 1B cause brachydactyly type A2. Proc Natl Acad Sci U S A 100:12277–12282PubMedPubMedCentralCrossRefGoogle Scholar
  125. Lehmann K, Seemann P, Silan F et al (2007) A new subtype of brachydactyly type B caused by point mutations in the bone morphogenetic protein antagonist NOGGIN. Am J Hum Genet 81:388–396PubMedPubMedCentralCrossRefGoogle Scholar
  126. Lewis KA, Gray PC, Blount AL et al (2000) Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 404:411–414PubMedCrossRefGoogle Scholar
  127. Li B, Khanna A, Sharma V et al (1999) TGF-beta1 DNA polymorphisms, protein levels, and blood pressure. Hypertension 33:271–275PubMedCrossRefGoogle Scholar
  128. Li Y, Foster W, Deasy BM et al (2004) Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am J Pathol 164:1007–1019PubMedPubMedCentralCrossRefGoogle Scholar
  129. Li S, Shimono C, Norioka N et al (2010) Activin A binds to perlecan through its pro-region that has heparin/heparan sulfate binding activity. J Biol Chem 285:36645–36655PubMedPubMedCentralCrossRefGoogle Scholar
  130. Lipina C, Kendall H, Mcpherron AC et al (2010) Mechanisms involved in the enhancement of mammalian target of rapamycin signalling and hypertrophy in skeletal muscle of myostatin-deficient mice. FEBS Lett 584:2403–2408PubMedPubMedCentralCrossRefGoogle Scholar
  131. Liu D, Black BL, Derynck R (2001) TGF-beta inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes Dev 15:2950–2966PubMedPubMedCentralCrossRefGoogle Scholar
  132. Loeys BL, Chen J, Neptune ER et al (2005) A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat Genet 37:275–281PubMedCrossRefGoogle Scholar
  133. Lokireddy S, Mcfarlane C, Ge X et al (2011) Myostatin induces degradation of sarcomeric proteins through a Smad3 signaling mechanism during skeletal muscle wasting. Mol Endocrinol 25:1936–1949PubMedCrossRefGoogle Scholar
  134. Lokireddy S, Wijesoma IW, Bonala S et al (2012) Myostatin is a novel tumoral factor that induces cancer cachexia. Biochem J 446:23–36PubMedPubMedCentralCrossRefGoogle Scholar
  135. Loscalzo J (2001) Genetic clues to the cause of primary pulmonary hypertension. N Engl J Med 345:367–371PubMedCrossRefGoogle Scholar
  136. Luo K (2003) Negative regulation of BMP signaling by the ski oncoprotein. J Bone Joint Surg Am 85-A(Suppl 3):39–43PubMedGoogle Scholar
  137. Maehara Y, Kakeji Y, Kabashima A et al (1999) Role of transforming growth factor-beta 1 in invasion and metastasis in gastric carcinoma. J Clin Oncol 17:607–614PubMedGoogle Scholar
  138. Massague J (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6:597–641PubMedCrossRefGoogle Scholar
  139. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753–791PubMedCrossRefGoogle Scholar
  140. Massague J, Gomis RR (2006) The logic of TGFbeta signaling. FEBS Lett 580:2811–2820PubMedCrossRefGoogle Scholar
  141. Massague J, Cheifetz S, Endo T et al (1986) Type beta transforming growth factor is an inhibitor of myogenic differentiation. Proc Natl Acad Sci U S A 83:8206–8210PubMedPubMedCentralCrossRefGoogle Scholar
  142. Matyas G, Arnold E, Carrel T et al (2006) Identification and in silico analyses of novel TGFBR1 and TGFBR2 mutations in Marfan syndrome-related disorders. Hum Mutat 27:760–769PubMedCrossRefGoogle Scholar
  143. Matzuk MM, Finegold MJ, Su JG et al (1992) Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360:313–319PubMedCrossRefGoogle Scholar
  144. Matzuk MM, Finegold MJ, Mather JP et al (1994) Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-deficient mice. Proc Natl Acad Sci U S A 91:8817–8821PubMedPubMedCentralCrossRefGoogle Scholar
  145. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495Google Scholar
  146. Mcallister KA, Grogg KM, Johnson DW et al (1994) Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 8:345–351PubMedCrossRefGoogle Scholar
  147. Mccaffrey TA, Du B, Consigli S et al (1997) Genomic instability in the type II TGF-beta1 receptor gene in atherosclerotic and restenotic vascular cells. J Clin Invest 100:2182–2188PubMedPubMedCentralCrossRefGoogle Scholar
  148. Mccroskery S, Thomas M, Maxwell L et al (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162:1135–1147PubMedPubMedCentralCrossRefGoogle Scholar
  149. Mcpherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83–90PubMedCrossRefGoogle Scholar
  150. Megeney LA, Kablar B, Garrett K et al (1996) MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev 10:1173–1183PubMedCrossRefGoogle Scholar
  151. Mendell JR, Sahenk Z, Malik V et al (2015) A phase 1/2a follistatin gene therapy trial for Becker muscular dystrophy. Mol Ther 23:192–201PubMedPubMedCentralCrossRefGoogle Scholar
  152. Mondello P, Mian M, Aloisi C et al (2015) Cancer cachexia syndrome: pathogenesis, diagnosis, and new therapeutic options. Nutr Cancer 67:12–26PubMedCrossRefGoogle Scholar
  153. Morine KJ, Bish LT, Selsby JT et al (2010) Activin IIB receptor blockade attenuates dystrophic pathology in a mouse model of Duchenne muscular dystrophy. Muscle Nerve 42:722–730PubMedPubMedCentralCrossRefGoogle Scholar
  154. Morissette MR, Cook SA, Buranasombati C et al (2009) Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am J Physiol Cell Physiol 297:C1124–C1132PubMedCrossRefGoogle Scholar
  155. Morley JE, Thomas DR, Wilson MM (2006) Cachexia: pathophysiology and clinical relevance. Am J Clin Nutr 83:735–743PubMedGoogle Scholar
  156. Moses AG, Maingay J, Sangster K et al (2009) Pro-inflammatory cytokine release by peripheral blood mononuclear cells from patients with advanced pancreatic cancer: relationship to acute phase response and survival. Oncol Rep 21:1091–1095PubMedGoogle Scholar
  157. Mulder KM (2000) Role of Ras and Mapks in TGFbeta signaling. Cytokine Growth Factor Rev 11:23–35PubMedCrossRefGoogle Scholar
  158. Murphy KT, Koopman R, Naim T et al (2010) Antibody-directed myostatin inhibition in 21-mo-old mice reveals novel roles for myostatin signaling in skeletal muscle structure and function. FASEB J 24:4433–4442PubMedCrossRefGoogle Scholar
  159. Murphy KT, Chee A, Gleeson BG et al (2011) Antibody-directed myostatin inhibition enhances muscle mass and function in tumor-bearing mice. Am J Physiol Regul Integr Comp Physiol 301:R716–R726PubMedCrossRefGoogle Scholar
  160. Myeroff LL, Parsons R, Kim SJ et al (1995) A transforming growth factor beta receptor type II gene mutation common in colon and gastric but rare in endometrial cancers with microsatellite instability. Cancer Res 55:5545–5547PubMedGoogle Scholar
  161. Nakamura T, Takio K, Eto Y et al (1990) Activin-binding protein from rat ovary is follistatin. Science 247:836–838PubMedCrossRefGoogle Scholar
  162. Neptune ER, Frischmeyer PA, Arking DE et al (2003) Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat Genet 33:407–411PubMedCrossRefGoogle Scholar
  163. Ng CM, Cheng A, Myers LA et al (2004) TGF-beta-dependent pathogenesis of mitral valve prolapse in a mouse model of Marfan syndrome. J Clin Invest 114:1586–1592PubMedPubMedCentralCrossRefGoogle Scholar
  164. Oliff A, Defeo-Jones D, Boyer M et al (1987) Tumors secreting human TNF/cachectin induce cachexia in mice. Cell 50:555–563PubMedCrossRefGoogle Scholar
  165. Olson EN, Sternberg E, Hu JS et al (1986) Regulation of myogenic differentiation by type beta transforming growth factor. J Cell Biol 103:1799–1805PubMedCrossRefGoogle Scholar
  166. Pannu H, Avidan N, Tran-Fadulu V et al (2006) Genetic basis of thoracic aortic aneurysms and dissections: potential relevance to abdominal aortic aneurysms. Ann N Y Acad Sci 1085:242–255PubMedCrossRefGoogle Scholar
  167. Pees C, Laccone F, Hagl M et al (2013) Usefulness of Losartan on the size of the ascending aorta in an unselected cohort of children, adolescents, and young adults with Marfan syndrome. Am J Cardiol 112:1477–1483PubMedCrossRefGoogle Scholar
  168. Philip B, Lu Z, Gao Y (2005) Regulation of GDF-8 signaling by the p38 MAPK. Cell Signal 17:365–375PubMedCrossRefGoogle Scholar
  169. Pirisi M, Fabris C, Luisi S et al (2000) Evaluation of circulating activin-A as a serum marker of hepatocellular carcinoma. Cancer Detect Prev 24:150–155PubMedGoogle Scholar
  170. Pistilli EE, Bogdanovich S, Goncalves MD et al (2011) Targeting the activin type IIB receptor to improve muscle mass and function in the mdx mouse model of Duchenne muscular dystrophy. Am J Pathol 178:1287–1297PubMedPubMedCentralCrossRefGoogle Scholar
  171. Puthucheary ZA, Rawal J, Mcphail M et al (2013) Acute skeletal muscle wasting in critical illness. JAMA 310:1591–1600PubMedCrossRefGoogle Scholar
  172. Rahimi RA, Leof EB (2007) TGF-beta signaling: a tale of two responses. J Cell Biochem 102:593–608PubMedCrossRefGoogle Scholar
  173. Ramirez F, Dietz HC (2007) Marfan syndrome: from molecular pathogenesis to clinical treatment. Curr Opin Genet Dev 17:252–258PubMedCrossRefGoogle Scholar
  174. Ramirez F, Rifkin DB (2009) Extracellular microfibrils: contextual platforms for TGFbeta and BMP signaling. Curr Opin Cell Biol 21:616–622PubMedPubMedCentralCrossRefGoogle Scholar
  175. Ramirez F, Carta L, Lee-Arteaga S et al (2008) Fibrillin-rich microfibrils – structural and instructive determinants of mammalian development and physiology. Connect Tissue Res 49:1–6PubMedCrossRefGoogle Scholar
  176. Reardon KA, Davis J, Kapsa RM et al (2001) Myostatin, insulin-like growth factor-1, and leukemia inhibitory factor mRNAs are upregulated in chronic human disuse muscle atrophy. Muscle Nerve 24:893–899PubMedCrossRefGoogle Scholar
  177. Reinhardt DP, Ono RN, Sakai LY (1997) Calcium stabilizes fibrillin-1 against proteolytic degradation. J Biol Chem 272:1231–1236PubMedCrossRefGoogle Scholar
  178. Ribeiro SM, Poczatek M, Schultz-Cherry S et al (1999) The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem 274:13586–13593PubMedCrossRefGoogle Scholar
  179. Rifkin DB (2005) Latent transforming growth factor-beta (TGF-beta) binding proteins: orchestrators of TGF-beta availability. J Biol Chem 280:7409–7412PubMedCrossRefGoogle Scholar
  180. Riggins GJ, Kinzler KW, Vogelstein B et al (1997) Frequency of Smad gene mutations in human cancers. Cancer Res 57:2578–2580PubMedGoogle Scholar
  181. Rios R, Carneiro I, Arce VM et al (2002) Myostatin is an inhibitor of myogenic differentiation. Am J Physiol Cell Physiol 282:C993–C999PubMedCrossRefGoogle Scholar
  182. Rodino-Klapac LR, Haidet AM, Kota J et al (2009) Inhibition of myostatin with emphasis on follistatin as a therapy for muscle disease. Muscle Nerve 39:283–296PubMedPubMedCentralCrossRefGoogle Scholar
  183. Roubenoff R (2000) Sarcopenia and its implications for the elderly. Eur J Clin Nutr 54(Suppl 3):S40–S47PubMedCrossRefGoogle Scholar
  184. Sabatelli P, Gualandi F, Gara SK et al (2012) Expression of collagen VI alpha 5 and alpha 6 chains in human muscle and in Duchenne muscular dystrophy-related muscle fibrosis. Matrix Biol 31:187–196PubMedPubMedCentralCrossRefGoogle Scholar
  185. Salam MT, Gauderman WJ, Mcconnell R et al (2007) Transforming growth factor- 1 C-509 T polymorphism, oxidant stress, and early-onset childhood asthma. Am J Respir Crit Care Med 176:1192–1199PubMedPubMedCentralCrossRefGoogle Scholar
  186. Sartori R, Milan G, Patron M et al (2009) Smad2 and 3 transcription factors control muscle mass in adulthood. Am J Physiol Cell Physiol 296:C1248–C1257PubMedCrossRefGoogle Scholar
  187. Sartori R, Schirwis E, Blaauw B et al (2013) BMP signaling controls muscle mass. Nat Genet 45:1309–1318PubMedCrossRefGoogle Scholar
  188. Schneyer AL, Sidis Y, Gulati A et al (2008) Differential antagonism of activin, myostatin and growth and differentiation factor 11 by wild-type and mutant follistatin. Endocrinology 149:4589–4595PubMedPubMedCentralCrossRefGoogle Scholar
  189. Scott HR, Mcmillan DC, Crilly A et al (1996) The relationship between weight loss and interleukin 6 in non-small-cell lung cancer. Br J Cancer 73:1560–1562PubMedPubMedCentralCrossRefGoogle Scholar
  190. Sengle G, Charbonneau NL, Ono RN et al (2008a) Targeting of bone morphogenetic protein growth factor complexes to fibrillin. J Biol Chem 283:13874–13888PubMedPubMedCentralCrossRefGoogle Scholar
  191. Sengle G, Ono RN, Lyons KM et al (2008b) A new model for growth factor activation: type II receptors compete with the prodomain for BMP-7. J Mol Biol 381:1025–1039PubMedPubMedCentralCrossRefGoogle Scholar
  192. Serrano AL, Munoz-Canoves P (2010) Regulation and dysregulation of fibrosis in skeletal muscle. Exp Cell Res 316:3050–3058PubMedCrossRefGoogle Scholar
  193. Shao CX, Liu M, Wu X et al (2007) Time-dependent expression of myostatin RNA transcript and protein in gastrocnemius muscle of mice after sciatic nerve resection. Microsurgery 27:487–493PubMedCrossRefGoogle Scholar
  194. Shi Y, Massague J (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685–700PubMedCrossRefGoogle Scholar
  195. Shi YQ, Katsev S, Cai C et al (2000) BMP signaling is required for heart formation in vertebrates. Dev Biol 224:226–237PubMedCrossRefGoogle Scholar
  196. Shimasaki S, Moore RK, Otsuka F et al (2004) The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25:72–101PubMedCrossRefGoogle Scholar
  197. Shore EM, Xu M, Feldman GJ et al (2006) A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and sporadic fibrodysplasia ossificans progressiva. Nat Genet 38:525–527PubMedCrossRefGoogle Scholar
  198. Shovlin CL, Hughes JM, Scott J et al (1997) Characterization of endoglin and identification of novel mutations in hereditary hemorrhagic telangiectasia. Am J Hum Genet 61:68–79PubMedPubMedCentralCrossRefGoogle Scholar
  199. Sidis Y, Mukherjee A, Keutmann H et al (2006) Biological activity of follistatin isoforms and follistatin-like-3 is dependent on differential cell surface binding and specificity for activin, myostatin, and bone morphogenetic proteins. Endocrinology 147:3586–3597PubMedCrossRefGoogle Scholar
  200. Simpson CM, Stanton PG, Walton KL et al (2012) Activation of latent human GDF9 by a single residue change (Gly 391 Arg) in the mature domain. Endocrinology 153:1301–1310PubMedCrossRefGoogle Scholar
  201. Slayton RL, Williams L, Murray JC et al (2003) Genetic association studies of cleft lip and/or palate with hypodontia outside the cleft region. Cleft Palate Craniofac J 40:274–279PubMedPubMedCentralCrossRefGoogle Scholar
  202. Spurney CF, Sali A, Guerron AD et al (2011) Losartan decreases cardiac muscle fibrosis and improves cardiac function in dystrophin-deficient Mdx mice. J Cardiovasc Pharmacol Ther 16:87–95PubMedPubMedCentralCrossRefGoogle Scholar
  203. Tan BH, Fearon KC (2008) Cachexia: prevalence and impact in medicine. Curr Opin Clin Nutr Metab Care 11:400–407PubMedCrossRefGoogle Scholar
  204. Tanabe A, Taketani S, Endo-Ichikawa Y et al (2000) Analysis of the candidate genes responsible for non-syndromic cleft lip and palate in Japanese people. Clin Sci 99:105–111PubMedCrossRefGoogle Scholar
  205. Tang AM, Forrester J, Spiegelman D et al (2002) Weight loss and survival in HIV-positive patients in the era of highly active antiretroviral therapy. J Acquir Immune Defic Syndr 31:230–236PubMedCrossRefGoogle Scholar
  206. Ten Dijke P, Arthur HM (2007) Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol 8:857–869PubMedCrossRefGoogle Scholar
  207. Thawani JP, Wang AC, Than KD et al (2010) Bone morphogenetic proteins and cancer: review of the literature. Neurosurgery 66:233–246, discussion 246PubMedCrossRefGoogle Scholar
  208. Theologides A (1979) Cancer cachexia. Cancer 43:2004–2012PubMedCrossRefGoogle Scholar
  209. Thiagalingam S, Lengauer C, Leach FS et al (1996) Evaluation of candidate tumour suppressor genes on chromosome 18 in colorectal cancers. Nat Genet 13:343–346PubMedCrossRefGoogle Scholar
  210. Thies RS, Chen T, Davies MV et al (2001) GDF-8 propeptide binds to GDF-8 and antagonizes biological activity by inhibiting GDF-8 receptor binding. Growth Factors 18:251–259PubMedCrossRefGoogle Scholar
  211. Thomas JT, Lin K, Nandedkar M et al (1996) A human chondrodysplasia due to a mutation in a TGF-beta superfamily member. Nat Genet 12:315–317PubMedCrossRefGoogle Scholar
  212. Thomas JT, Kilpatrick MW, Lin K et al (1997) Disruption of human limb morphogenesis by a dominant negative mutation in CDMP1. Nat Genet 17:58–64PubMedCrossRefGoogle Scholar
  213. Thomas M, Langley B, Berry C et al (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275:40235–40243PubMedCrossRefGoogle Scholar
  214. Thys M, Schrauwen I, Vanderstraeten K et al (2007) The coding polymorphism T263I in TGF-beta1 is associated with otosclerosis in two independent populations. Hum Mol Genet 16:2021–2030PubMedCrossRefGoogle Scholar
  215. Tisdale MJ (2002) Cachexia in cancer patients. Nat Rev Cancer 2:862–871PubMedCrossRefGoogle Scholar
  216. Tisdale MJ (2009) Mechanisms of cancer cachexia. Physiol Rev 89:381–410PubMedCrossRefGoogle Scholar
  217. Trendelenburg AU, Meyer A, Rohner D et al (2009) Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296:C1258–C1270PubMedCrossRefGoogle Scholar
  218. Tsuchida K (2006) The role of myostatin and bone morphogenetic proteins in muscular disorders. Expert Opin Biol Ther 6:147–154PubMedCrossRefGoogle Scholar
  219. Tsuchida K, Arai KY, Kuramoto Y et al (2000) Identification and characterization of a novel follistatin-like protein as a binding protein for the TGF-beta family. J Biol Chem 275:40788–40796PubMedCrossRefGoogle Scholar
  220. Tsuchida K, Nakatani M, Matsuzaki T et al (2004) Novel factors in regulation of activin signaling. Mol Cell Endocrinol 225:1–8PubMedCrossRefGoogle Scholar
  221. Vakonakis I, Campbell ID (2007) Extracellular matrix: from atomic resolution to ultrastructure. Curr Opin Cell Biol 19:578–583PubMedCrossRefGoogle Scholar
  222. Vallese D, Negroni E, Duguez S et al (2013) The Rag2(-)Il2rb(-)Dmd(-) mouse: a novel dystrophic and immunodeficient model to assess innovating therapeutic strategies for muscular dystrophies. Mol Ther 21:1950–1957PubMedPubMedCentralCrossRefGoogle Scholar
  223. Villanueva A, Garcia C, Paules AB et al (1998) Disruption of the antiproliferative TGF-beta signaling pathways in human pancreatic cancer cells. Oncogene 17:1969–1978PubMedCrossRefGoogle Scholar
  224. Visvanathan R, Chapman IM (2009) Undernutrition and anorexia in the older person. Gastroenterol Clin North Am 38:39–409Google Scholar
  225. Wagner KR, Liu X, Chang X et al (2005) Muscle regeneration in the prolonged absence of myostatin. Proc Natl Acad Sci U S A 102:2519–2524PubMedPubMedCentralCrossRefGoogle Scholar
  226. Wall BT, Dirks ML, Snijders T et al (2014) Substantial skeletal muscle loss occurs during only 5 days of disuse. Acta Physiol (Oxf) 210:600–611CrossRefGoogle Scholar
  227. Walton KL, Makanji Y, Wilce MC et al (2009) A common biosynthetic pathway governs the dimerization and secretion of inhibin and related transforming growth factor beta (TGFbeta) ligands. J Biol Chem 284:9311–9320PubMedPubMedCentralCrossRefGoogle Scholar
  228. Walton KL, Makanji Y, Chen J et al. (2010) Two distinct regions of latency associated peptide coordinate stability of the latent TGF-{beta}1 complex. J Biol Chem 285(22):17029–17037Google Scholar
  229. Watt KI, Jaspers RT, Atherton P et al (2010) SB431542 treatment promotes the hypertrophy of skeletal muscle fibers but decreases specific force. Muscle Nerve 41:624–629PubMedGoogle Scholar
  230. Wheeler MT, Snyder EC, Patterson MN et al (1999) An E-box within the MHC IIB gene is bound by MyoD and is required for gene expression in fast muscle. Am J Physiol 276:C1069–C1078PubMedGoogle Scholar
  231. Wigmore SJ, Plester CE, Richardson RA et al (1997) Changes in nutritional status associated with unresectable pancreatic cancer. Br J Cancer 75:106–109PubMedPubMedCentralCrossRefGoogle Scholar
  232. Wildi S, Kleeff J, Maruyama H et al (2001) Overexpression of activin A in stage IV colorectal cancer. Gut 49:409–417PubMedPubMedCentralCrossRefGoogle Scholar
  233. Winbanks CE, Weeks KL, Thomson RE et al (2012) Follistatin-mediated skeletal muscle hypertrophy is regulated by Smad3 and mTOR independently of myostatin. J Cell Biol 197:997–1008PubMedPubMedCentralCrossRefGoogle Scholar
  234. Winbanks CE, Chen JL, Qian H et al (2013) The bone morphogenetic protein axis is a positive regulator of skeletal muscle mass. J Cell Biol 203:345–357PubMedPubMedCentralCrossRefGoogle Scholar
  235. Wolfman NM, Mcpherron AC, Pappano WN et al (2003) Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci U S A 100:15842–15846PubMedPubMedCentralCrossRefGoogle Scholar
  236. Wrighton KH, Lin X, Feng XH (2009a) Phospho-control of TGF-beta superfamily signaling. Cell Res 19:8–20PubMedPubMedCentralCrossRefGoogle Scholar
  237. Wrighton KH, Lin X, Yu PB et al (2009b) Transforming growth factor {beta} Can stimulate Smad1 phosphorylation independently of bone morphogenic protein receptors. J Biol Chem 284:9755–9763PubMedPubMedCentralCrossRefGoogle Scholar
  238. Wu MY, Hill CS (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16:329–343PubMedCrossRefGoogle Scholar
  239. Yaden BC, Wang YX, Wilson JM et al (2014) Inhibition of activin A ameliorates skeletal muscle injury and rescues contractile properties by inducing efficient remodeling in female mice. Am J Pathol 184:1152–1166PubMedCrossRefGoogle Scholar
  240. Yamada Y, Miyauchi A, Goto J et al (1998) Association of a polymorphism of the transforming growth factor-beta1 gene with genetic susceptibility to osteoporosis in postmenopausal Japanese women. J Bone Miner Res 13:1569–1576PubMedCrossRefGoogle Scholar
  241. Zanotti S, Gibertini S, Mora M (2010) Altered production of extra-cellular matrix components by muscle-derived Duchenne muscular dystrophy fibroblasts before and after TGF-beta 1 treatment. Cell Tissue Res 339:397–410PubMedCrossRefGoogle Scholar
  242. Zdychova J, Komers R (2005) Emerging role of Akt kinase/protein kinase B signaling in pathophysiology of diabetes and its complications. Physiol Res 54:1–16PubMedGoogle Scholar
  243. Zhang H, Bradley A (1996) Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977–2986PubMedGoogle Scholar
  244. Zhang DL, Liu M, Ding F et al (2006) Expression of myostatin RNA transcript and protein in gastrocnemius muscle of rats after sciatic nerve resection. J Muscle Res Cell Motil 27:37–44PubMedCrossRefGoogle Scholar
  245. Zhang P, Li WJ, Liu HJ et al (2014) Dystrophin involved in the susceptibility of slow muscles to hindlimb unloading via concomitant activation of TGF-beta 1/Smad3 signaling and ubiquitin-proteasome degradation in mice. Cell Biochem Biophys 70:1057–1067PubMedCrossRefGoogle Scholar
  246. Zhao J, Brault JJ, Schild A et al (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–483PubMedCrossRefGoogle Scholar
  247. Zhou XP, Woodford-Richens K, Lehtonen R et al (2001) Germline mutations in BMPR1A/ALK3 cause a subset of cases of juvenile polyposis syndrome and of Cowden and Bannayan-Riley-Ruvalcaba syndromes. Am J Hum Genet 69:704–711PubMedPubMedCentralCrossRefGoogle Scholar
  248. Zhou X, Wang JL, Lu J et al (2010) Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142:531–543PubMedCrossRefGoogle Scholar
  249. Zhu X, Topouzis S, Liang LF et al (2004) Myostatin signaling through Smad2, Smad3 and Smad4 is regulated by the inhibitory Smad7 by a negative feedback mechanism. Cytokine 26:262–272PubMedCrossRefGoogle Scholar
  250. Zimmers TA, Davies MV, Koniaris LG et al (2002) Induction of cachexia in mice by systemically administered myostatin. Science 296:1486–1488PubMedCrossRefGoogle Scholar
  251. Zugmaier G, Paik S, Wilding G et al (1991) Transforming growth factor beta 1 induces cachexia and systemic fibrosis without an antitumor effect in nude mice. Cancer Res 51:3590–3594PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Justin L. Chen
    • 1
    • 2
    • 3
    • 4
  • Timothy D. Colgan
    • 3
    • 5
  • Kelly L. Walton
    • 1
    • 2
  • Paul Gregorevic
    • 3
    • 4
    • 5
    • 6
  • Craig A. Harrison
    • 1
    • 2
    • 7
  1. 1.Centre for Endocrinology and MetabolismHudson Institute of Medical ResearchClaytonAustralia
  2. 2.Department of Molecular and Translational SciencesMonash UniversityMelbourneAustralia
  3. 3.Muscle Research and Therapeutics DevelopmentBaker IDI Heart and Diabetes InstituteMelbourneAustralia
  4. 4.Department of Biochemistry and Molecular BiologyMonash UniversityMelbourneAustralia
  5. 5.Department of PhysiologyThe University of MelbourneMelbourneAustralia
  6. 6.Department of Neurology, School of MedicineThe University of WashingtonSeattleUSA
  7. 7.Department of PhysiologyMonash UniversityMelbourneAustralia

Personalised recommendations