Focusing on fibrosis: Halofuginone-induced functional improvement in the mdx mouse model of Duchenne muscular dystrophy

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 4, 2008, Pages

  McLoon, Linda K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFIBROTIC AGENT; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CORTICOSTEROID; CREATINE; CYCLOSPORIN A; DEFLAZACORT; DYSTROPHIN; GELATINASE A; HALOFUGINONE; PREDNISOLONE; PREDNISONE; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BEHAVIOR DISORDER; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL FEATURE; CONGESTIVE CARDIOMYOPATHY; DIAPHRAGM MUSCLE; DISEASE COURSE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG INHIBITION; DRUG MECHANISM; DRUG SCREENING; DUCHENNE MUSCULAR DYSTROPHY; EDITORIAL; ENDURANCE; EXERCISE; FIBROBLAST; FUNCTIONAL STATUS; GENE; GENE MUTATION; GENETIC DISORDER; HEART DISEASE; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE FIBROSIS; HEART VENTRICLE WALL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LIMB WEAKNESS; LUNG FIBROSIS; MDX GENE; MORTALITY; MOUSE; MUSCLE FUNCTION; MYOFIBROSIS; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; RESPIRATORY FAILURE; RESPIRATORY FUNCTION; SIDE EFFECT; SINGLE DRUG DOSE; SURVIVAL; TIDAL VOLUME; WEIGHT GAIN; X CHROMOSOME LINKED DISORDER;

AGE FACTORS; ANIMALS; COLLAGEN TYPE I; COLLAGEN TYPE III; DISEASE MODELS, ANIMAL; FIBROSIS; HEART; MICE; MICE, INBRED MDX; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM; PHYSICAL ENDURANCE; PIPERIDINES; PROTEIN SYNTHESIS INHIBITORS; QUINAZOLINONES; RESPIRATORY MECHANICS; TIME FACTORS; VENTRICULAR FUNCTION, LEFT;

EID: 41749119428     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00176.2008     Document Type: Editorial

References (46)

1. Alexakis C, Partridge T, Bou-Gharios G. Implication of the satellite cell in dystrophic muscle fibrosis: a self-perpetuating mechanism of collagen overproduction. Am J Physiol Cell Physiol 293: C661-C669, 2007.
2. Andreetta F, Bernasconi P, Baggi F, Ferro P, Oliva L, Arnoldi E, Cornelio F, Mantegazza R, Confalonieri P. Immunomodulation of TGF-beta1 in mdx mouse inhibits connective tissue proliferation in diaphragm but increases inflammatory response: implications for antifibrotic therapy. J Neuroimmunol 175: 77-86, 2006.
3. Baxter P. Treatment of the heart in Duchenne muscular dystrophy. Dev Med Child Neurol 48: 163, 2006.
4. Bogdanovich S, Krag TO, Barton ER, Morris LD, Whittemore LA, Ahima RS, Khurana TS. Functional improvement of dystrophic muscle by myostatin blockade. Nature 420: 418-421, 2002.
5. Chamberlain JS, Metzger J, Reyes M, Townsend D, Faulkner JA. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J 21: 2195-2204, 2007.
6. Choi ET, Callow AD, Sehgal NL, Brown DM, Ryan US. Halofuginone, a specific collagen type I inhibitor, reduced anastomotic intimal hyperplasia. Arch Surg 130: 257-261, 1995.
7. Cohen L, Morgan J, Bozyk ME. Variable effects of corticosteroid treatment of serum enzyme activities in Duchenne's muscular dystrophy. Res Commun Chem Pathol Pharmacol 17: 529-538, 1977.
8. Cohn RD, Liang HY, Shetty R, Abraham T, Wagner KR. Myostatin does not regulate cardiac hypertrophy or fibrosis. Neuromuscul Disord 17: 290-296, 2007.
9. DeLuca A, Pierno S, Liantonio A, Cetrone M, Camerino C, Fraysse B, Mirabella M, Servidei S, Ruegg UT, Camerino DC. Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulin-like growth factor-1. J Pharmacol Exp Ther 304: 453-472, 2003.
10. DeLuca A, Nico B, Liantionio A, Didonna M, Fraysse B, Pierno S, Burdi R, Mangieri D, Rolland JF, Camerino C, Zallone A, Confalionieri P, Andreetta F, Arnoldi E, Courdier-Fruh I, Magyar JP, Frigeri A, Pisoni M, Svelto M, Camerino DC. A multidisciplinary evaluation of the effectiveness of cyclosporine A in dystrophic mdx mice. Am J Pathol 166: 477-489, 2005.
11. Elkin M, Reich R, Nagler A, Aingorn E, Pines M, de-Groot N, Hochberg A, Vlodavsky I. Inhibition of matrix metalloproteinase-2 expression and bladder carcinoma metastasis by halofuginone. Clin Cancer Res 5: 1982-1988, 1999.
12. Frankel KA, Rosser RJ. The pathology of the heart in progressive muscular dystrophy: epimyocardial fibrosis. Hum Pathol 7: 375-386, 1976.
13. Gnainsky Y, Kushnirsky Z, Bilu G, Hagai Y, Genina O, Volpin H, Bruck R, Spira G, Nagler A, Kawada N, Yoshizato K, Reinhardt DP, Libermann TA, Pines M. Gene expression during chemically induced liver fibrosis: effect of halofuginone on TGF-β1 signaling. Cell Tissue Res 328: 153-166, 2007.
14. Gosselin LE, Barkley JE, Spencer MJ, McCormick KM, Farkas GA. Ventilatory dysfunction in mdx mice: impact of tumor necrosis factoralpha deletion. Muscle Nerve 29: 336-343, 2003.
15. Gosselin LE, Williams JE, Personius K, Farkas GA. A comparison of factors associated with collagen metabolism in different skeletal muscles from dystrophic (mdx) mice: impact of pirfenidone. Muscle Nerve 35: 208-216, 2007.
16. Granot I, Bartov I, Plavnik I, Wax E, Hurwitz S, Pines M. Increased skin tearing in broilers and reduced collagen synthesis in skin in vivo and in vitro in response to the coccidiostat halofuginone. Poult Sci 70: 1559-1563, 1991.
17. Granot I, Halevy O, Hurwitz S, Pines M. Halofuginone: an inhibitor of collagen type I synthesis. Biochim Biophys Acta 13: 107-112, 1993.
18. Gregorevic P, Plant DR, Leeding KS, Bach LA, Lynch GS. Improved contractile function of the mdx dystrophic mouse diaphragm muscle after insulin-like growth factor-1 administration. Am J Pathol 161: 2263-2272, 2002.
19. Halevy O, Nagler A, Levi-Schaffer F, Genina O, Pines M. Inhibition of collagen type 1 synthesis by skin fibroblasts of graft versus host disease and scleroderma patients: effect of halofuginone. Biochem Pharmacol 52: 1057-1063, 1996.
20. Hoffman EP, Brown RHJ, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928, 1987.
21. Huebner KD, Jassal DS, Halevy O, Pines M, Anderson JE. Functional resolution of fibrosis in mdx mouse dystrophic heart and skeletal muscle by halofuginone. Am J Physiol Heart Circ Physiol (February 8, 2008); doi:10:1152/ajpheart.01253-2007.
22. Hunsaker RH, Fulkerson PK, Barry FJ, Lewis RP, Leier CV, Unverferth DV. Cardiac function in Duchenne's muscular dystrophy. Results of 10-year follow-up study and non-invasive testes. Am J Med 73: 235-238, 1982.
23. Ishihara T. Cardiopulmonary failure in Duchenne muscular dystrophy - pathophysiology and management. [In Japanese.] Rinsho Shinkeigaku 43: 761-764, 2003.
24. Leiba M, Cahalon L, Shimoni A, Lider O, Zanin-Zhorov A, Hecht I, Sela U, Vlodavsky I, Nagler A. Halofuginone inhibits NF-kB and p38 MAPK in activated T cells. J Leukoc Biol 80: 399-406, 2006.
25. Manzur AY, Kuntzer T, Pike M, Swan A. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev 1: CD003725, 2008.
26. Marchion DC, Weber PA, Lomnitski L, Duran CM, Cheung DT. Halofuginone inhibits serum-stimulated pericardial tissue retraction in vitro. Tissue Eng 10: 1076-1083, 2004.
27. McDonald CM, Abresch RT, Carter GT, Fowler WM, Johnson ER, Kilmer DD, Sigford BJ. Profiles of neuromuscular diseases. Duchenne muscular dystrophy. Am J Phys Med Rehabil 74: S70-S92, 1995.
28. McGaha TL, Phelps RG, Spiera H, Bona C. Halofuginone, an inhibitor of type-1 collagen synthesis and skin sclerosis, blocks transforming-growth- factor-beta-mediated Smad3 activation in fibroblasts. J Invest Dermatol 118: 461-470, 2002.
29. Melacini P, Vianello A, Villanova C, Fanin M, Miorin M, Angelini C, Dalla Volta S. Cardiac and respiratory involvement in advanced stage Duchenne muscular dystrophy. Neuromuscul Disord 6: 367-376, 1996.
30. Morrison J, Lu QL, Pastoret C, Partridge T, Bou-Gharios G. T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab Invest 80: 881-891, 2000.
31. Muller J, Vayssiere N, Royuela M, Leger ME, Muller A, Bacou F, Pons F, Hugon G, Mornet D. Comparative evolution of muscular dystrophy in diaphragm, gastrocnemius and masseter muscles from old male mdx mice. J Muscle Res Cell Motil 22: 133-139, 2001.
32. Nagler A, Firman N, Feferman R, Cotev S, Pines M, Shoshan S. Reduction in pulmonary fibrosis in vivo by halofuginone. Am J Respir Crit Care Med 154: 1082-1086, 1996.
33. Nagler A, Pines M. Topical treatment of cutaneous chronic graft versus host disease with halofuginone: a novel inhibitor of collagen type 1 synthesis. Transplantation 68: 1806-1809, 1999.
34. Passaquin AC, Renard M, Kay L, Challet C, Mokharian A, Walliman T, Ruegg UT. Creatine supplementation reduces skeletal muscle degeneration and enhances mitochondrial function in mdx mice. Neuromuscul Disord 12: 174-182, 2002.
35. Pastoret C, Sebille A. mdx mice show progressive weakness and muscle deterioration with age. J Neurol Sci 129: 97-105, 1995.
36. Perloff JK, Roberts WC, de Leon AC Jr, O'Doherty D. The distinctive electrocardiogram of Duchenne's muscular dystrophy. Am J Med 42: 179-188, 1967.
37. Phillips MF, Smith PE, Carroll N, Edwards RH, Calverley PM. Nocturnal oxygenation and prognosis in Duchenne muscular dystrophy. Am J Respir Crit Care Med 160: 198-202, 1999.
38. Pines M, Snyder D, Yarkoni S, Nagler A. Halofuginone to treat fibrosis in chronic graft-versus-host disease and scleroderma. Biol Blood Marrow Transplant 9: 417-425, 2003.
39. Quinlan JG, Hahn HS, Wong BL, Lorenz JN, Wenisch AS, Levin LS. Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscul Disord 14: 491-496, 2004.
40. Ryley JF, Wilson RG. Laboratory studies with some recent anticoccidials. Parasitology 70: 203-222, 1975.
41. Sandri M, Podhorska-Okolow M, Geromel V, Rizzi C, Arslan P, Franceschi C, Carraro U. Exercise induces myonuclear ubiquitination and apoptosis in dystrophin-deficient muscle of mice. J Neuropathol Exp Neurol 56: 45-57, 1997.
42. Stecklair KP, Hamburger DR, Egorin MJ, Parise RA, Covey JM, Eiseman JL. Pharmacokinetics and tissue distribution of halofuginone (NSC713205) in CD2F1 mice and Fischer 344 rats. Cancer Chemother Pharmacol 48: 375-382, 2001.
43. Stupka N, Gregorevic P, Plant DR, Lynch GS. The calcineurin signal transduction pathway is essential for successful muscle regeneration in mdx dystrophic mice. Acta Neuropathol 107: 299-310, 2004.
44. Von Moers A, Zwirner A, Reinhold A, Bruckmann O, van Landeghem F, Stoltenburg-Didinger G, Schuppan D, Herbst H, Schuelke M. Increased mRNA expression of tissue inhibitors of metalloproteinase-1 and -2 in Duchenne muscular dystrophy. Acta Neuropathol 109: 285-293, 2005.
45. Weller B, Massa R, Karpati G, Carpenter S. Glucocorticoids and immunosuppressants do not change the prevalence of necrosis and regeneration in mdx skeletal muscles. Muscle Nerve 14: 771-774, 1991.
46. Zanotti S, Saredi S, Ruggieri A, Fabbri M, Blasevich F, Romaggi S, Morandi L, Mora M. Altered extracellular matrix transcript expression and protein modulation in primary Duchenne muscular dystrophy myotubes. Matrix Biol 26: 615-624, 2007.