Endomysial fibrosis in duchenne muscular dystrophy: A marker of poor outcome associated with macrophage alternative activation

Journal of Neuropathology and Experimental Neurology

Volumn 68, Issue 7, 2009, Pages 762-773

  Desguerre, Isabelle ^a,b,c   Mayer, Michelle ^d   Leturcq, France ^e   Barbet, Jacques Patrick ^e   Gherardi, Romain K ^b,c,f,g   Christov, Christo ^c,f,g  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^d ARMAND TROUSSEAU HOSPITAL   (France)

^e Pathology Department ^*  (France)

^f HENRI MONDOR HOSPITAL   (France)

^g INSERM U955   (France)

Author keywords

Duchenne muscular dystrophy; Macrophages; Muscle fibrosis; Satellite cells; Vessels

Indexed keywords

COLLAGEN; DYSTROPHIN; MANNOSE RECEPTOR; CD56 ANTIGEN; CELL SURFACE RECEPTOR; LECTIN; MANNOSE BINDING LECTIN;

ADOLESCENT; ARM; ARTICLE; BASOPHIL; CAPILLARY; CELL SIZE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE MARKER; DUCHENNE MUSCULAR DYSTROPHY; ENDOMYSIUM; GENE MUTATION; GENOTYPE; HISTOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LEG; MACROPHAGE ACTIVATION; MOBILIZATION; MORPHOMETRICS; MOTOR PERFORMANCE; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE NECROSIS; MUSCLE STRENGTH; MYOFIBROSIS; OXIDATIVE STRESS; PERIMYSIUM; PRESCHOOL CHILD; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; SCHOOL CHILD; WESTERN BLOTTING; FIBROSIS; FOLLOW UP; GENETICS; INFANT; MACROPHAGE; MALE; METABOLISM; MOTOR ACTIVITY; MUSCLE FIBRIL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROGNOSIS; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; VASCULARIZATION;

ANTIGENS, CD56; CAPILLARIES; CHILD; CHILD, PRESCHOOL; DYSTROPHIN; FIBROSIS; FOLLOW-UP STUDIES; HUMANS; INFANT; LECTINS, C-TYPE; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MANNOSE-BINDING LECTINS; MOTOR ACTIVITY; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOFIBRILS; OXIDATIVE STRESS; PROGNOSIS; RECEPTORS, CELL SURFACE; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 68249155413     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181aa31c2     Document Type: Article

References (59)

1. Kohler M, Clarenbach CF, Bahler C, et al. Disability and survival in Duchenne muscular dystrophy. J Neurol Neurosurg Psychiatry 2009;80: 320-25
2. Van Essen AJ, Verheij JBGM, Reefhuis J, et al. The natural history of Duchenne muscular dystrophy: Analysis of data from a Dutch survey and review of age-related events. 2004 Online Leiden Muscular Dystrophy pages©. Available at: http://www.dmd.nl/. Accessed May 13, 2009
3. Bushby KM. Genetic and clinical correlation of Xp21 muscular dystrophy. J Inherit Metab Dis 1992;15:551-64
4. Muntoni F, Torelli S, Ferlini A. Dystrophin and mutations: One gene, several proteins, multiple phenotypes. Lancet Neurol 2003;2:731-40
5. Nicholson LV, Johnson MA, Bushby KM, et al. Integrated study of 100 patients with Xp21 linked muscular dystrophy using clinical, genetic, immunochemical and histopathological data. Trends across the clinical groups. J Med Genet 1993;30:728-36
6. Sifringer M, Uhlenberg B, Lammel S, et al. Identification of transcripts from a subtraction library which might be responsible for the mild phenotype in an intrafamilially variable course of Duchenne muscular dystrophy. Hum Genet 2004;114:149-56
7. Escolar DM, Buyse G, Henricson E, et al. CINRG randomized controlled trial of creatine and glutamine in Duchenne muscular dystrophy. Ann Neurol 2005;58:151-55
8. Desguerre I, Christov C, Mayer M, et al. Clinical heterogeneity of Duchenne muscular dystrophy (DMD): Definition of sub-phenotypes and predictive criteria by long-term follow-up. PLoS ONE 2009;4:e4347
9. Engel AG, Osawa C. Dystrophinopathies. In: Engel AG, Franzini-Armstrong C, eds. Myology. New York, NY: McGraw Hill, 2004: 961-1020
10. Hawke TJ, Garry DJ. Myogenic satellite cells: Physiology to molecular biology. J Appl Physiol 2001;91:534-51
11. Christov C, Chretien F, Abou-Khalil R, et al. Muscle satellite cells and endothelial cells: Close neighbors and privileged partners. Mol Biol Cell 2007;18:1397-409
12. Chazaud B, Sonnet C, Lafuste P, et al. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 2003;163:1133-43
13. Arnold L, Henry A, Poron F, et al. Inflammatory monocytes recruited after skeletal muscle injury switch into anti-inflammatory macrophages to support myogenesis. J Exp Med 2007;204:1057-69
14. Wehling M, Spencer MJ, Tidball JG, et al. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 2001;155:123-31
15. Stein M, Keshav S, Harris N, et al. Interleukin 4 potently enhances murine macrophage mannose receptor activity: A marker of alternative immunologic macrophage activation. J Exp Med 1992;176:287-92
16. Vidal B, Serrano AL, Tjwa M, et al. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev 2008;22:1747-52
17. Carlson ME, Hsu M, Conboy IM. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008; 454:528-32
18. Massague J, Cheifetz S, Endo T, et al. Type beta transforming growth factor is an inhibitor of myogenic differentiation. Proc Natl Acad Sci U S A 1986;83:8206-10 (Pubitemid 17182470)
19. Li Y, Foster W, Deasy BM, et al. 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 2004; 164:1007-19
20. Alexakis C, Partridge T, Bou-Garcia G. Implication of the satellite cell in dystrophic muscle fibrosis: A self-perpetuating mechanism of collagen overproduction. Am J Physiol Cell Physiol 2007;293:661-69
21. Hussain SN, Matar G, Barreiro E, et al. Modifications of proteins by 4-hydroxy-2-nonenal in the ventilatory muscles of rats. Am J Physiol Lung Cell Mol Physiol 2006;290:996-1003
22. Uchida K. 4-Hydroxy-2-nonenal: A product and mediator of oxidative stress. Prog Lipid Res 2003;42:318-43
23. Gundersen JH, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microscopy 1987;147:227-69
24. De Leeuw J. Non-linear principal component analysis and related techniques. Available at: http//www.preprints.stat.ucla.edu. Accessed May 13, 2009
25. Meulman J, Van der Kooij AJ, Heiser WJ. Principal components analysis with nonlinear optimal scaling transformations for ordinal and nominal data. In: Kaplan D, ed. Handbook of Quantitative Methodology for the Social Sciences. Thousand Oaks, CA: Sage Publications, Inc., 2004:49-70
26. Barend PL, Engel AG. Are hypercontracted muscle fibers artifacts and do they cause rupture of the plasma membrane. Neurology 1987;37: 1466-75
27. Bell CB, Conen PE. Histopathological changes in Duchenne muscular dystrophy. J Neurol Sci 1968;7:529-40
28. Connolly AM, Keeling RM, Mehta S, et al. Three mouse models of muscular dystrophy: The natural history of strength and fatigue in dystrophin-, dystrophin/utrophin Y, and laminin alpha2-deficient mice. Neuromuscul Disord 2001;118:703-12
29. Kossakowska AE, Edwards DR, Lee SS, et al. Altered balance between matrix metalloproteinases and their inhibitors in experimental biliary fibrosis. Am J Pathol 1998;153:1895-902
30. Schnaper HW, Kopp JB, Poncelet AC, et al. Increased expression of extracellular matrix proteins and decreased expression of matrix proteases after serial passage of glomerular mesangial cells. J Cell Sci 1996;109:2521-28
31. Li YY, Feng YQ, Kadokami T, et al. Myocardial extracellular matrix remodeling in transgenic mice overexpressing tumor necrosis factor alpha can be modulated by anti-tumor necrosis factor alpha therapy. Proc Natl Acad Sci U S A 2000;97:12746-51
32. Herpel E, Pritsch M, Koch A, et al. Interstitial fibrosis in the heart: Differences in extracellular matrix proteins and matrix metalloprotei-nases in end-stage dilated, ischaemic and valvular cardiomyopathy. Histopathology 2006;48:736-37
33. Selman M, King TE, Pardo A. Idiopathic pulmonary fibrosis: Prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 2001;134:136-51
34. Nandan D, Clarke EP, Ball EH, et al. Ethyl-3,4 dihydroxybenzoate inhibits myoblast differentiation: Evidence for an essential role of collagen. J Cell Biol 1990;110:1673-79
35. Saitoh O, Periasamy M, Kan M, et al. cis-4-Hydroxy-l-proline and ethyl-3,4-dihydroxybenzoate prevent myogenesis of C2C12 muscle cells and block MyoD1 and myogenin expression. Exp Cell Res 1992;200: 70-76
36. 2 kinetics in old and young individuals. J Appl Physiol 1997;82:63-91
37. Tidball JG, Wehling-Henricks M. The role of free radicals in the pathophysiology of muscular dystrophy. J Appl Physiol 2007;102: 1677-86
38. Touboul D, Brunelle A, Halgand F, et al. Lipid imaging by gold cluster time-of-flight secondary ion mass spectrometry: Application to Duch-enne muscular dystrophy. J Lipid Res 2005;46:1388-95 (Pubitemid 43109802)
39. Grady RM, Zhou H, Cunningham JM, et al. Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro. J Physiol 2003;547:125-32
40. McLennan IS. Degenerating and regenerating skeletal muscles contain several subpopulations of macrophages with distinct spatial and temporal distributions. J Anat 1996;188:17-28
41. St Pierre BA, Tidball JG. Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J Appl Physiol 1994;77:290-97
42. Villalta SA, Nguyen HX, Deng B, et al. Shifts in macrophage phenotype and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum Mol Genet 2009;18: 482-96
43. Wakayama Y, Schotland DL, Bonilla E, et al. Quantitative ultrastructural study of muscle satellite cells in Duchenne dystrophy. Neurology 1979; 29:401-7
44. Decary S, Ben Hamida C, Mouly V, et al. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscular Disord 2000;10:113-20
45. Lund TC, Grange RW, Lowe DA. Telomere shortening in diaphragm and tibialis anterior muscles of aged mdx mice. Muscle Nerve 2007;3: 387-90
46. Mauviel A. Transforming growth factor-beta: A key mediator of fibrosis. Methods Mol Med 2007;117:69-80
47. Bernasconi P, Torchiana E, Confalonieri P, et al. Expression of transforming growth factor A1 in dystrophic patient muscles correlates with fibrosis. J Clin Invest 1995;96:1137-44
48. Sun G, Haginoya K, Wu Y, et al. Connective tissue growth factor is overexpressed in muscles of human molecular dystrophy. J Neurol Sci 2008;267:48-56
49. Fadic R, Mezzano V, Alvarez K, et al. Increase in decorin and biglycan in Duchenne muscular dystrophy: Role of fibroblasts as cell source of these proteoglycans in the disease. J Cell Mol Med 2006;10:758-69
50. Zanotti S, Saredi S, Ruggieri A, et al. Altered extracellular transcript expression and protein modulation in primary Duchenne muscular dystrophy myotubes. Matrix Biol 2007;26:615-24
51. Morrison J, Palmer DB, Cobbold S, et al. Effect of T-lymphocyte depletion on muscle fibrosis in the mdx mouse. Am J Pathol 2005;166: 1701-10
52. Wehling-Henricks M, Sokolow S, Lee JJ, et al. Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum Mol Genet 2008;17:2280-92
53. Mochizuki Y, Ojima K, Uezumi A, et al. Participation of bone marrow-derived cells in fibrotic changes in denervated skeletal muscle. Am J Pathol 2005;166:1721-32
54. Fernet M, Hall J. Predictive markers for normal tissue reactions: Fantasy or reality? Cancer Radiother 2008;12:614-18
55. Wang H, Mengsteab S, Tag CG, et al. Transforming growth factor-beta1 gene polymorphisms are associated with progression of liver fibrosis in Caucasians with chronic hepatitis C infection. World J Gastroenterol 2005;11:1929-36
56. Xaubet A, Marin-Arguedas A, Lario S, et al. TGF-A1 gene polymorphisms are associated to disease progression in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2003;168:431-35
57. Molina M, Xaubet A, Li X, et al. Angiotensinogen gene G-6A polymorphism influences idiopathic pulmonary fibrosis disease progression. Eur Respir J 2008;32:1004-8
58. Bayat A, Watson JS, Stanley JK, et al. Genetic susceptibility to Dupuytren disease: Association of Zf9 transcription factor gene. Plast Reconstr Surg 2003;111:2133-39
59. Cohn RD, van Erp C, Habashi JP, et al. Angiotensin II type 1 receptor blockade attenuate TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat Med 2007;13:204-10