Functional and Morphological Improvement of Dystrophic Muscle by Interleukin 6 Receptor Blockade

EBioMedicine

Volumn 2, Issue 4, 2015, Pages 285-293

  Pelosi, Laura ^a   Berardinelli, Maria Grazia ^a   De Pasquale, Loredana ^b   Nicoletti, Carmine ^a   D'Amico, Adele ^b   Carvello, Francesco ^b   Moneta, Gian Marco ^b   Catizone, Angela ^a   Bertini, Enrico ^b   De Benedetti, Fabrizio ^b   Musarò, Antonio ^a,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

IL6; Inflammation; Muscular dystrophy; Necrosis; Therapy

Indexed keywords

CYTOKINE RECEPTOR ANTAGONIST; GLUCOCORTICOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; INTERLEUKIN 6 RECEPTOR BLOCKING AGENT; MYOD1 PROTEIN; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; WNT7A PROTEIN; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; MALE; MOUSE; MUSCLE NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; TREADMILL TEST; WESTERN BLOTTING; ANIMAL; ANIMAL MUSCULAR DYSTROPHY; ANTAGONISTS AND INHIBITORS; BLOOD; C57BL MOUSE; COMPLICATION; DISEASE MODEL; HOMEOSTASIS; INFLAMMATION; METABOLISM; MUSCLE; NECROSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; HOMEOSTASIS; INFLAMMATION; INTERLEUKIN-6; MALE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLES; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; NECROSIS; PHENOTYPE; RECEPTORS, INTERLEUKIN-6;

EID: 84949195979     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.02.014     Document Type: Article

References (75)

1. Bentzinger C.F., von Maltzahn J., Dumont N.A., Stark D.A., Wang Y.X., Nhan K., Frenette J., Cornelison D.D., Rudnicki M.A. Wnt7a stimulates myogenic stem cell motility and engraftment resulting in improved muscle strength. J. Cell Biol. 2014, 205:97-111.
2. Blau H.M., Pavlath G.K., Hardeman E.C., Chiu C.P., Silberstein L., Webster S.G., Miller S.C., Webster C. Plasticity of the differentiated state. Science 1985, 230:758-766.
3. Bogdanovich S., Krag T.O., Barton E.R., Morris L.D., Whittemore L.A., Ahima R.S., Khurana T.S. Functional improvement of dystrophic muscle by myostatin blockade. Nature 2002, 420:418-421.
4. Brussee V., Tardif F., Tremblay J.P. Muscle fibers of mdx mice are more vulnerable to exercise than those of normal mice. Neuromuscul. Disord. 1997, 7:487-492.
5. Burdi R., Didonna M.P., Pignol B., Nico B., Mangieri D., Rolland J.F., Camerino C., Zallone A., Ferro P., Andreetta F., et al. First evaluation of the potential effectiveness in muscular dystrophy of a novel chimeric compound, BN 82270, acting as calpain-inhibitor and anti-oxidant. Neuromuscul. Disord. 2006, 16:237-248.
6. Carnwath J.W., Shotton D.M. Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J. Neurol. Sci. 1987, 80:39-54.
7. Cassano M., Biressi S., Finan A., Benedetti L., Omes C., Boratto R., Martin F., Allegretti M., Broccoli V., Cusella D.A., et al. Magic-factor 1, a partial agonist of Met, induces muscle hypertrophy by protecting myogenic progenitors from apoptosis. PLoS One 2008, 3:e3223.
8. Chen J.F., Tao Y., Li J., Deng Z., Yan Z., Xiao X., Wang D.Z. microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J. Cell Biol. 2010, 190:867-879.
9. Colussi C., Mozzetta C., Gurtner A., Illi B., Rosati J., Straino S., Ragone G., Pescatori M., Zaccagnini G., Antonini A., et al. HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19183-19187.
10. Consalvi S., Mozzetta C., Bettica P., Germani M., Fiorentini F., Del Bene F., Rocchetti M., Leoni F., Monzani V., Mascagni P., et al. Preclinical studies in the mdx mouse model of Duchenne muscular dystrophy with the histone deacetylase inhibitor givinostat. Mol. Med. 2013, 19:79-87.
11. Curtale G., Mirolo M., Renzi T.A., Rossato M., Bazzoni F., Locati M. Negative regulation of Toll-like receptor 4 signaling by IL-10-dependent microRNA-146b. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:11499-11504.
12. De Benedetti F., Brunner H.I., Ruperto N., Kenwright A., Wright S., Calvo I., Cuttica R., Ravelli A., Schneider R., Woo P., et al. Randomized trial of tocilizumab in systemic juvenile idiopathic arthritis. N. Engl. J. Med. 2012, 367:2385-2395.
13. De Luca A., Pierno S., Liantonio A., Conte C.D. Pre-clinical trials in Duchenne dystrophy: what animal models can tell us about potential drug effectiveness. Neuromuscul. Disord. 2002, 12(Suppl. 1):S142-S146.
14. De Luca A., Pierno S., Liantonio A., Cetrone M., Camerino C., Fraysse B., Mirabella M., Servidei S., Ruegg U.T., Conte C.D. Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulin-like growth factor-1. J. Pharmacol. Exp. Ther. 2003, 304:453-463.
15. Denti M.A., Rosa A., D'Antona G., Sthandier O., De Angelis F.G., Nicoletti C., Allocca M., Pansarasa O., Parente V., Musaro A., et al. Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3758-3763.
16. Dupont-Versteegden E.E., McCarter R.J., Katz M.S. Voluntary exercise decreases progression of muscular dystrophy in diaphragm of mdx mice. J. Appl. Physiol. 1994, 77(4):1736-1741.
17. Eisenberg I., Alexander M.S., Kunkel L.M. miRNAS in normal and diseased skeletal muscle. J. Cell. Mol. Med. 2009, 13:2-11.
18. Erriquez D., Perini G., Ferlini A. Non-coding RNAs in muscle dystrophies. Int. J. Mol. Sci. 2013, 14:19681-19704.
19. Fujita R., Kawano F., Ohira T., Nakai N., Shibaguchi T., Nishimoto N., Ohira Y. Anti-interleukin-6 receptor antibody (MR16-1) promotes muscle regeneration via modulation of gene expressions in infiltrated macrophages. Biochim. Biophys. Acta 2014, 1840:3170-3180.
20. Fuster J.J., Walsh K. The good, the bad, and the ugly of interleukin-6 signaling. EMBO J. 2014, 33:1425-1427.
21. Gabay C. Interleukin-6 and chronic inflammation. Arthritis Res. Ther. 2006, 8(Suppl. 2):S3.
22. Glass D.J. Two tales concerning skeletal muscle. J. Clin. Investig. 2007, 117:2388-2391.
23. Goodman M.N. Interleukin-6 induces skeletal muscle protein breakdown in rats. Proc. Soc. Exp. Biol. Med. 1994, 205:182-185.
24. Granchelli J.A., Pollina C., Hudecki M.S. Pre-clinical screening of drugs using the mdx mouse. Neuromuscul. Disord. 2000, 10:235-239.
25. Greco S., De S.M., Colussi C., Zaccagnini G., Fasanaro P., Pescatori M., Cardani R., Perbellini R., Isaia E., Sale P., et al. Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J. 2009, 23:3335-3346.
26. Grounds M.D., Torrisi J. Anti-TNFalpha (Remicade) therapy protects dystrophic skeletal muscle from necrosis. FASEB J. 2004, 18:676-682.
27. Grounds M.D., Radley H.G., Lynch G.S., Nagaraju K., De Luca A. Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis. 2008, 31:1-19.
28. Haddad F., Zaldivar F., Cooper D.M., Adams G.R. IL-6-induced skeletal muscle atrophy. J. Appl. Physiol. 2005, 98(3):911-917.
29. Hasty P., Bradley A., Morris J.H., Edmondson D.G., Venuti J.M., Olson E.N., Klein W.H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 1993, 364:501-506.
30. Heinrich P.C., Behrmann I., Muller-Newen G., Schaper F., Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 1998, 334(Pt 2):297-314.
31. Hirai H., Verma M., Watanabe S., Tastad C., Asakura Y., Asakura A. MyoD regulates apoptosis of myoblasts through microRNA-mediated down-regulation of Pax3. J. Cell Biol. 2010, 191:347-365.
32. Horber F.F., Haymond M.W. Human growth hormone prevents the protein catabolic side effects of prednisone in humans. J. Clin. Investig. 1990, 86:265-272.
33. Horsley V., Jansen K.M., Mills S.T., Pavlath G.K. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 2003, 113:483-494.
34. Jiang C., Wen Y., Kuroda K., Hannon K., Rudnicki M.A., Kuang S. Notch signaling deficiency underlies age-dependent depletion of satellite cells in muscular dystrophy. Dis. Model. Mech. 2014, 7:997-1004.
35. Juan A.H., Kumar R.M., Marx J.G., Young R.A., Sartorelli V. Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. Mol. Cell 2009, 36:61-74.
36. Kainulainen H., Papaioannou K.G., Silvennoinen M., Autio R., Saarela J., Oliveira B.M., Nyqvist M., Pasternack A., 't Hoen P.A., Kujala U.M., et al. Myostatin/activin blocking combined with exercise reconditions skeletal muscle expression profile of mdx mice. Mol. Cell. Endocrinol. 2015, 399:131-142.
37. Kohlhaas S., Garden O.A., Scudamore C., Turner M., Okkenhaug K., Vigorito E. Cutting edge: the Foxp3 target miR-155 contributes to the development of regulatory T cells. J. Immunol. 2009, 182:2578-2582.
38. Kostek M.C., Nagaraju K., Pistilli E., Sali A., Lai S.H., Gordon B., Chen Y.W. IL-6 signaling blockade increases inflammation but does not affect muscle function in the mdx mouse. BMC Musculoskelet. Disord. 2012, 13:106.
39. Kurek J.B., Nouri S., Kannourakis G., Murphy M., Austin L. Leukemia inhibitory factor and interleukin-6 are produced by diseased and regenerating skeletal muscle. Muscle Nerve 1996, 19:1291-1301.
40. Le G.F., Jones A.E., Seale V., Scime A., Rudnicki M.A. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 2009, 4:535-547.
41. Liu J., Luo X.J., Xiong A.W., Zhang Z.D., Yue S., Zhu M.S., Cheng S.Y. MicroRNA-214 promotes myogenic differentiation by facilitating exit from mitosis via down-regulation of proto-oncogene N-ras. J. Biol. Chem. 2010, 285:26599-26607.
42. Lu L.F., Thai T.H., Calado D.P., Chaudhry A., Kubo M., Tanaka K., Loeb G.B., Lee H., Yoshimura A., Rajewsky K., et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 2009, 30:80-91.
43. Minetti G.C., Colussi C., Adami R., Serra C., Mozzetta C., Parente V., Fortuni S., Straino S., Sampaolesi M., Di Padova M., et al. Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat. Med. 2006, 12:1147-1150.
44. Munoz-Canoves P., Scheele C., Pedersen B.K., Serrano A.L. Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword?. FEBS J. 2013, 280:4131-4148.
45. Musaro A. The basis of muscle regeneration. Adv. Biol. 2014, 2014:1-16.
46. Nabeshima Y., Hanaoka K., Hayasaka M., Esumi E., Li S., Nonaka I., Nabeshima Y. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 1993, 364:532-535.
47. Okano T., Yoshida K., Nakamura A., Sasazawa F., Oide T., Takeda S., Ikeda S. Chronic exercise accelerates the degeneration-regeneration cycle and downregulates insulin-like growth factor-1 in muscle of mdx mice. Muscle Nerve 2005, 32:191-199.
48. Okazaki M., Yamada Y., Nishimoto N., Yoshizaki K., Mihara M. Characterization of anti-mouse interleukin-6 receptor antibody. Immunol. Lett. 2002, 84:231-240.
49. Pedersen B.K., Febbraio M.A. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev. 2008, 88:1379-1406.
50. Pelosi M., De R.M., Barberi L., Musaro A. IL-6 impairs myogenic differentiation by downmodulation of p90RSK/eEF2 and mTOR/p70S6K axes, without affecting AKT activity. BioMed Res. Int. 2014, 2014:206026.
51. Pescatori M., Broccolini A., Minetti C., Bertini E., Bruno C., D'amico A., Bernardini C., Mirabella M., Silvestri G., Giglio V., et al. Gene expression profiling in the early phases of DMD: a constant molecular signature characterizes DMD muscle from early postnatal life throughout disease progression. FASEB J. 2007, 21:1210-1226.
52. Pierno S., Nico B., Burdi R., Liantonio A., Didonna M.P., Cippone V., Fraysse B., Rolland J.F., Mangieri D., Andreetta F., et al. Role of tumour necrosis factor alpha, but not of cyclo-oxygenase-2-derived eicosanoids, on functional and morphological indices of dystrophic progression in mdx mice: a pharmacological approach. Neuropathol. Appl. Neurobiol. 2007, 33:344-359.
53. Porter J.D., Khanna S., Kaminski H.J., Rao J.S., Merriam A.P., Richmonds C.R., Leahy P., Li J., Guo W., Andrade F.H. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 2002, 11:263-272.
54. Price F.D., von Maltzahn J., Bentzinger C.F., Dumont N.A., Yin H., Chang N.C., Wilson D.H., Frenette J., Rudnicki M.A. Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nat. Med. 2014, 20:1174-1181.
55. Radley H.G., Grounds M.D. Cromolyn administration (to block mast cell degranulation) reduces necrosis of dystrophic muscle in mdx mice. Neurobiol. Dis. 2006, 23:387-397.
56. Radley H.G., Davies M.J., Grounds M.D. Reduced muscle necrosis and long-term benefits in dystrophic mdx mice after cV1q (blockade of TNF) treatment. Neuromuscul. Disord. 2008, 18:227-238.
57. Rantanen J., Hurme T., Lukka R., Heino J., Kalimo H. Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab. Investig. 1995, 72:341-347.
58. Rose-John S. IL-6 trans-signaling via the soluble IL-6 receptor: importance for the pro-inflammatory activities of IL-6. Int. J. Biol. Sci. 2012, 8:1237-1247.
59. Scott H.R., McMillan D.C., Crilly A., McArdle C.S., Milroy R. The relationship between weight loss and interleukin 6 in non-small-cell lung cancer. Br. J. Cancer 1996, 73:1560-1562.
60. Serrano A.L., Baeza-Raja B., Perdiguero E., Jardi M., Munoz-Canoves P. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 2008, 7:33-44.
61. Shavlakadze T., White J., Hoh J.F., Rosenthal N., Grounds M.D. Targeted expression of insulin-like growth factor-I reduces early myofiber necrosis in dystrophic mdx mice. Mol. Ther. 2004, 10:829-843.
62. Stupka N., Tarnopolsky M.A., Yardley N.J., Phillips S.M. Cellular adaptation to repeated eccentric exercise-induced muscle damage. J. Appl. Physiol. 2001, 91:1669-1678.
63. Stupka N., Plant D.R., Schertzer J.D., Emerson T.M., Bassel-Duby R., Olson E.N., Lynch G.S. Activated calcineurin ameliorates contraction-induced injury to skeletal muscles of mdx dystrophic mice. J. Physiol. 2006, 575:645-656.
64. Sun Q., Zhang Y., Yang G., Chen X., Zhang Y., Cao G., Wang J., Sun Y., Zhang P., Fan M., et al. Transforming growth factor-beta-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res. 2008, 36:2690-2699.
65. Tedesco F.S., Hoshiya H., D'Antona G., Gerli M.F., Messina G., Antonini S., Tonlorenzi R., Benedetti S., Berghella L., Torrente Y., et al. Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy. Sci. Transl. Med. 2011, 3:96ra78.
66. Tidball J.G., Villalta S.A. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R1173-R1187.
67. Tierney M.T., Aydogdu T., Sala D., Malecova B., Gatto S., Puri P.L., Latella L., Sacco A. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat. Med. 2014, 20:1182-1186.
68. Tsujinaka T., Ebisui C., Fujita J., Kishibuchi M., Morimoto T., Ogawa A., Katsume A., Ohsugi Y., Kominami E., Monden M. Muscle undergoes atrophy in association with increase of lysosomal cathepsin activity in interleukin-6 transgenic mouse. Biochem. Biophys. Res. Commun. 1995, 207:168-174.
69. Vidal B., Ardite E., Suelves M., Ruiz-Bonilla V., Janue A., Flick M.J., Degen J.L., Serrano A.L., Munoz-Canoves P. Amelioration of Duchenne muscular dystrophy in mdx mice by elimination of matrix-associated fibrin-driven inflammation coupled to the alphaMbeta2 leukocyte integrin receptor. Hum. Mol. Genet. 2012, 21:1989-2004.
70. Villalta S.A., Rinaldi C., Deng B., Liu G., Fedor B., Tidball J.G. Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype. Hum. Mol. Genet. 2011, 20:790-805.
71. Villalta S.A., Rosenthal W., Martinez L., Kaur A., Sparwasser T., Tidball J.G., Margeta M., Spencer M.J., Bluestone J.A. Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy. Sci. Transl. Med. 2014, 6:258ra142.
72. von Maltzahn J., Renaud J.M., Parise G., Rudnicki M.A. Wnt7a treatment ameliorates muscular dystrophy. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:20614-20619.
73. Wehling M., Spencer M.J., Tidball J.G. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 2001, 155:123-131.
74. Willmann R., Possekel S., Dubach-Powell J., Meier T., Ruegg M.A. Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul. Disord. 2009, 19:241-249.
75. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977, 270:725-727.