Myostatin gene inactivation prevents skeletal muscle wasting in cancer

Cancer Research

Volumn 74, Issue 24, 2014, Pages 7344-7356

  Gallot, Yann S ^a   Durieux, Anne Cécile ^a   Castells, Josiane ^a   Desgeorges, Marine M ^a   Vernus, Barbara ^b   Plantureux, Léa ^a   Rémond, Didier ^c   Jahnke, Vanessa E ^a   Lefai, Etienne ^a   Dardevet, Dominique ^c   Nemoz, Georges ^a   Schaeffer, Laurent ^d   Bonnieu, Anne ^b   Freyssenet, Damien G ^a  

^a UNIVERSITÉ DE LYON   (France)

^b University of Montpellier   (France)

^c INRA and University of Auvergne   (France)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; ATROGIN 1; MUSCLE RING FINGER 1 PROTEIN; MYOSTATIN; MSTN PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CACHEXIA; COLORECTAL CANCER; CONTROLLED STUDY; FEMALE; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; GENE INACTIVATION; GENE LOSS; INTESTINE POLYP; LEWIS LUNG CARCINOMA CELL; MAFBX GENE; MALE; MOUSE; MSTN GENE; MURF1 GENE; MUSCLE MASS; NONHUMAN; PATHOGENESIS; PHENOTYPE; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPLICATION; GENE SILENCING; GENETICS; HUMAN; LEWIS CARCINOMA; METABOLISM; MUSCLE ATROPHY; PATHOLOGY; SKELETAL MUSCLE;

ANIMALS; CACHEXIA; CARCINOMA, LEWIS LUNG; GENE SILENCING; HUMANS; MICE; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSTATIN;

EID: 84918544121     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0057     Document Type: Article

References (49)

1. Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, et al. Definition and classi fi cation of cancer cachexia: an international consensus. Lancet Oncol 2011;12:489-95.
2. Tisdale MJ. Mechanisms of cancer cachexia. Physiol Rev 2009;89:381-410.
3. Tisdale MJ. Cancer cachexia. Curr Opin Gastroenterol 2010;26:146-51.
4. Tisdale MJ. Cachexia in cancer patients. Nat Rev Cancer 2002;2:862-71.
5. Han HQ, Zhou X, Mitch WE, Goldberg AL. Myostatin/activin pathway antagonism: molecular basis and therapeutic potential. Int J Biochem Cell Biol 2013;45:2333-47.
6. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997;387:83-90.
7. Grobet L, Pirottin D, Farnir F, Poncelet D, Royo LJ, Brouwers B, et al. Modulating skeletal muscle mass by postnatal, muscle-specific inactivation of the myostatin gene. Genesis 2003;35:227-38.
8. Durieux AC, Amirouche A, Banzet S, Koulmann N, Bonnefoy R, Pasdeloup M, et al. Ectopic expression of myostatin induces atrophy of adult skeletal muscle by decreasing muscle gene expression. Endocrinology 2007;148:3140-7.
9. Amirouche A, Durieux AC, Banzet S, Koulmann N, Bonnefoy R, Mouret C, et al. Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 2009;150:286-94.
10. Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN, et al. Induction of cachexia in mice by systemically administered myostatin. Science 2002;296:1486-8.
11. Costelli P, Muscaritoli M, Bonetto A, Penna F, Reffo P, Bossola M, et al. Muscle myostatin signalling is enhanced in experimental cancer cachexia. Eur J Clin Invest 2008;38:531-8.
12. Liu CM, Yang Z, Liu CW, Wang R, Tien P, Dale R, et al. Myostatin antisense RNA-mediated muscle growth in normal and cancer cachexia mice. Gene Ther 2008;15:155-60.
13. Bonetto A, Penna F, Minero VG, Reffo P, Bonelli G, Baccino FM, et al. Deacetylase inhibitors modulate the myostatin/follistatin axis without improving cachexia in tumor-bearing mice. Curr Cancer Drug Targets 2009;9:608-16.
14. Benny Klimek ME, Aydogdu T, Link MJ, Pons M, Koniaris LG, Zimmers TA. Acute inhibition of myostatin-family proteins preserves skeletal muscle in mouse models of cancer cachexia. Biochem Biophys Res Commun 2010;391:1548-54.
15. Zhou X, Wang JL, Lu J, Song Y, Kwak KS, Jiao Q, et al. Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 2010;142:531-43.
16. Busquets S, Toledo M, Orpi M, Massa D, Porta M, Capdevila E, et al. Myostatin blockage using actRIIB antagonism in mice bearing the Lewis lung carcinoma results in the improvement of muscle wasting and physical performance. J Cachexia Sarcopenia Muscle 2012;3:37-43.
17. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990;247:322-4.
18. Baltgalvis KA, Berger FG, Pena MM, Davis JM, Muga SJ, Carson JA. Interleukin-6 and cachexia in ApcMin/+ mice. Am J Physiol Regul Integr Comp Physiol 2008;294:R393-401.
19. Berthon P, Duguez S, Favier FB, Amirouche A, Feasson L, Vico L, et al. Regulation of ubiquitin-proteasome system, caspase enzyme activities, and extracellular proteinases in rat soleus muscle in response to unloading. Pflugers Arch 2007;454:625-33.
20. Rapisarda A, Melillo G. Role of the VEGF/VEGFR axis in cancer biology and therapy. Adv Cancer Res 2012;114:237-67.
21. Macheda ML, Rogers S, Best JD. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 2005;202:654-62.
22. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 2004;19:176-82.
23. Hu-Lowe DD, Chen E, Zhang L, Watson KD, Mancuso P, Lappin P, et al. Targeting activin receptor-like kinase 1 inhibits angiogenesis and tumorigenesis through a mechanism of action complementary to anti-VEGF therapies. Cancer Res 2011;71:1362-73.
24. Antsiferova M, Werner S. The bright and the dark sides of activin in wound healing and cancer. J Cell Sci 2012;125:3929-37.
25. Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem 1997;272:32401-10.
26. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, et al. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 2001;3: 1009-13.
27. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 2001;3:1014-9.
28. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atro-gin- 1 and cause skeletal muscle atrophy. Cell 2004;117:399-412.
29. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, et al. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 2004;14:395-403.
30. Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG, et al. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 2004;119:285-98.
31. Mittal A, Bhatnagar S, Kumar A, Lach-Trifilieff E, Wauters S, Li H, et al. The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol 2010;188:833-49.
32. Paul PK, Gupta SK, Bhatnagar S, Panguluri SK, Darnay BG, Choi Y, et al. Targeted ablation of TRAF6 inhibits skeletal muscle wasting in mice. J Cell Biol 2010;191:1395-411.
33. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007;6:458-71.
34. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007;6:472-83.
35. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012;8:445-544.
36. Chen JL, Walton KL, Winbanks CE, Murphy KT, Thomson RE, Makanji Y, et al. Elevated expression of activins promotes muscle wasting and cachexia. FASEB J 2014;28:1711-23.
37. Matzuk MM, Finegold MJ, Mather JP, Krummen L, Lu H, Bradley A. Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-de ficient mice. Proc Natl Acad Sci U S A 1994;91:8817-21.
38. Groden J, Thliveris A, Samowitz W, Carlson M, Gelbert L, Albertsen H, et al. Identification and characterization of the familial adenomatous polyposis coli gene. Cell 1991;66:589-600.
39. Lokireddy S, Mouly V, Butler-Browne G, Gluckman PD, Sharma M, Kambadur R, et al. Myostatin promotes the wasting of human myoblast cultures through promoting ubiquitin-proteasome pathway-mediated loss of sarcomeric proteins. Am J Physiol Cell Physiol 2011;301:C1316-24.
40. Lee SJ, Reed LA, Davies MV, Girgenrath S, Goad ME, Tomkinson KN, et al. Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc Natl Acad Sci U S A 2005;102:18117-22.
41. Lach-Trifilieff E, Minetti GC, Sheppard K, Ibebunjo C, Feige JN, Hartmann S, et al. An antibody blocking activin type II receptors induces strong skeletal muscle hypertrophy and protects from atrophy. Mol Cell Biol 2014;34:606-18.
42. Souza TA, Chen X, Guo Y, Sava P, Zhang J, Hill JJ, et al. Proteomic identification and functional validation of activins and bone morphogenetic protein 11 as candidate novel muscle mass regulators. Mol Endocrinol 2008;22:2689-702.
43. Sartori R, Schirwis E, Blaauw B, Bortolanza S, Zhao J, Enzo E, et al. BMP signaling controls muscle mass. Nat Genet 2013;45:1309-18.
44. Winbanks CE, Chen JL, Qian H, Liu Y, Bernardo BC, Beyer C, et al. The bone morphogenetic protein axis is a positive regulator of skeletal muscle mass. J Cell Biol 2013;203:345-57.
45. Cipriano SC, Chen L, Kumar TR, Matzuk MM. Follistatin is a modulator of gonadal tumor progression and the activin-induced wasting syndrome in inhibin-defi cient mice. Endocrinology 2000; 141:2319-27.
46. Coerver KA, Woodruff TK, Finegold MJ, Mather J, Bradley A, Matzuk MM. Activin signaling through activin receptor type II causes the cachexia-like symptoms in inhibin-deficient mice. Mol Endocrinol 1996;10:534-43.
47. Li Q, Kumar R, Underwood K, O'Connor AE, Loveland KL, Seehra JS, et al. Prevention of cachexia-like syndrome development and reduction of tumor progression in inhibin-de ficient mice following administration of a chimeric activin receptor type II-murine Fc protein. Mol Hum Reprod 2007;13:675-83.
48. Kumar TR, Palapattu G, Wang P, Woodruff TK, Boime I, Byrne MC, et al. Transgenic models to study gonadotropin function: the role of follicle-stimulating hormone in gonadal growth and tumorigenesis. Mol Endocrinol 1999;13:851-65.
49. Argiles JM, Lopez-Soriano FJ. The energy state of tumor-bearing rats. J Biol Chem 1991;266:2978-82.