Modifying muscular dystrophy through transforming growth factor-β

FEBS Journal

Volumn 280, Issue 17, 2013, Pages 4198-4209

  Ceco, Ermelinda ^a   McNally, Elizabeth M ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

extracellular matrix; genetic modifier; muscular dystrophy; transforming growth factor (TGF )

Indexed keywords

DYSTROPHIN; FIBRILLIN 1; FIBRILLIN 2; SARCOGLYCAN; TRANSFORMING GROWTH FACTOR BETA;

CELL MEMBRANE; DISEASE COURSE; DISEASE SEVERITY; ENVIRONMENTAL FACTOR; EXTRACELLULAR MATRIX; GENE MAPPING; GENE MUTATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HEREDITY; HOMEOSTASIS; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; MODIFIER GENE; MUSCLE ATROPHY; MUSCLE FUNCTION; MUSCLE WEAKNESS; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; UPREGULATION;

EXTRACELLULAR MATRIX; GENETIC MODIFIER; MUSCULAR DYSTROPHY; TRANSFORMING GROWTH FACTOR-Β (TGF-Β);

ANIMALS; GENES, MODIFIER; HUMANS; MUSCULAR DYSTROPHIES; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84882734669     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12266     Document Type: Review

References (93)

1. Chen YW, Nagaraju K, Bakay M, McIntyre O, Rawat R, Shi R, &, Hoffman EP, (2005) Early onset of inflammation and later involvement of TGFbeta in Duchenne muscular dystrophy. Neurology 65, 826-834.
2. Porter JD, Khanna S, Kaminski HJ, Rao JS, Merriam AP, Richmonds CR, Leahy P, Li J, Guo W, &, Andrade FH, (2002) A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum Mol Genet 11, 263-272.
3. Flanigan KM, Dunn DM, von Niederhausern A, Soltanzadeh P, Gappmaier E, Howard MT, Sampson JB, Mendell JR, Wall C, King WM, et al,. (2009) Mutational spectrum of DMD mutations in dystrophinopathy patients: application of modern diagnostic techniques to a large cohort. Hum Mutat 30, 1657-1666.
4. Flanigan KM, Ceco E, Lamar K, Kaminoh Y, Dunn DM, Mendell JR, King WM, Pestronk A, Florence JM, Mathews KD, et al,. (2013) LTBP4 genotype predicts age of ambulatory loss in Duchenne muscular dystrophy. Ann Neurol in press.
5. Ginjaar IB, Kneppers AL, v d Meulen JD, Anderson LV, Bremmer-Bout M, van Deutekom JC, Weegenaar J, den Dunnen JT, &, Bakker E, (2000) Dystrophin nonsense mutation induces different levels of exon 29 skipping and leads to variable phenotypes within one BMD family. Eur J Hum Genet 8, 793-796.
6. Hattori N, Kaido M, Nishigaki T, Inui K, Fujimura H, Nishimura T, Naka T, &, Hazama T, (1999) Undetectable dystrophin can still result in a relatively benign phenotype of dystrophinopathy. Neuromuscul Disord 9, 220-226.
7. Noguchi S, McNally EM, Ben Othmane K, Hagiwara Y, Mizuno Y, Yoshida M, Yamamoto H, Bonnemann CG, Gussoni E, Denton PH, et al,. (1995) Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science 270, 819-822.
8. McNally EM, Passos-Bueno MR, Bonnemann CG, Vainzof M, de Sa Moreira E, Lidov HG, Othmane KB, Denton PH, Vance JM, Zatz M, et al,. (1996) Mild and severe muscular dystrophy caused by a single gamma-sarcoglycan mutation. Am J Hum Genet 59, 1040-1047.
9. Kefi M, Amouri R, Driss A, Ben Hamida C, Ben Hamida M, Kunkel LM, &, Hentati F, (2003) Phenotype and sarcoglycan expression in Tunisian LGMD 2C patients sharing the same del521-T mutation. Neuromuscul Disord 13, 779-787.
10. Piccolo F, Jeanpierre M, Leturcq F, Dode C, Azibi K, Toutain A, Merlini L, Jarre L, Navarro C, Krishnamoorthy R, et al,. (1996) A founder mutation in the gamma-sarcoglycan gene of gypsies possibly predating their migration out of India. Hum Mol Genet 5, 2019-2022.
11. Glover L, &, Brown RH Jr, (2007) Dysferlin in membrane trafficking and patch repair. Traffic 8, 785-794.
12. Mastaglia FL, Lamont PJ, &, Laing NG, (2005) Distal myopathies. Curr Opin Neurol 18, 504-510.
13. Weiler T, Bashir R, Anderson LV, Davison K, Moss JA, Britton S, Nylen E, Keers S, Vafiadaki E, Greenberg CR, et al,. (1999) Identical mutation in patients with limb girdle muscular dystrophy type 2B or Miyoshi myopathy suggests a role for modifier gene(s). Hum Mol Genet 8, 871-877.
14. Illarioshkin SN, Ivanova-Smolenskaya IA, Greenberg CR, Nylen E, Sukhorukov VS, Poleshchuk VV, Markova ED, &, Wrogemann K, (2000) Identical dysferlin mutation in limb-girdle muscular dystrophy type 2B and distal myopathy. Neurology 55, 1931-1933.
15. Bonne G, Mercuri E, Muchir A, Urtizberea A, Becane HM, Recan D, Merlini L, Wehnert M, Boor R, Reuner U, et al,. (2000) Clinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Ann Neurol 48, 170-180.
16. Granger B, Gueneau L, Drouin-Garraud V, Pedergnana V, Gagnon F, Ben Yaou R, Tezenas du Montcel S, &, Bonne G, (2011) Modifier locus of the skeletal muscle involvement in Emery-Dreifuss muscular dystrophy. Hum Genet 129, 149-159.
17. Goldfarb LG, Park KY, Cervenakova L, Gorokhova S, Lee HS, Vasconcelos O, Nagle JW, Semino-Mora C, Sivakumar K, &, Dalakas MC, (1998) Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat Genet 19, 402-403.
18. Zucconi E, Valadares MC, Vieira NM, Bueno CR Jr, Secco M, Jazedje T, da Silva HC, Vainzof M, &, Zatz M, (2010) Ringo: discordance between the molecular and clinical manifestation in a golden retriever muscular dystrophy dog. Neuromuscul Disord 20, 64-70.
19. Fukada S, Morikawa D, Yamamoto Y, Yoshida T, Sumie N, Yamaguchi M, Ito T, Miyagoe-Suzuki Y, Takeda S, Tsujikawa K, et al,. (2010) Genetic background affects properties of satellite cells and mdx phenotypes. Am J Pathol 176, 2414-2424.
20. Kucherenko MM, Pantoja M, Yatsenko AS, Shcherbata HR, Fischer KA, Maksymiv DV, Chernyk YI, &, Ruohola-Baker H, (2008) Genetic modifier screens reveal new components that interact with the Drosophila dystroglycan-dystrophin complex. PLoS One 3, e2418.
21. Guyon JR, Steffen LS, Howell MH, Pusack TJ, Lawrence C, &, Kunkel LM, (2007) Modeling human muscle disease in zebrafish. Biochim Biophys Acta 1772, 205-215.
22. Hack AA, Ly CT, Jiang F, Clendenin CJ, Sigrist KS, Wollmann RL, &, McNally EM, (1998) Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J Cell Biol 142, 1279-1287.
23. Heydemann A, Huber JM, Demonbreun A, Hadhazy M, &, McNally EM, (2005) Genetic background influences muscular dystrophy. Neuromuscul Disord 15, 601-609.
24. Heydemann A, Ceco E, Lim JE, Hadhazy M, Ryder P, Moran JL, Beier DR, Palmer AA, &, McNally EM, (2009) Latent TGF-beta-binding protein 4 modifies muscular dystrophy in mice. J Clin Invest 119, 3703-3712.
25. Swaggart KA, Heydemann A, Palmer AA, &, McNally EM, (2011) Distinct genetic regions modify specific muscle groups in muscular dystrophy. Physiol Genomics 43, 24-31.
26. Hersh CP, Demeo DL, Lazarus R, Celedon JC, Raby BA, Reilly JJ, &, Silverman EK, (2006) Genetic association analysis of functional impairment in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 173, 977-984.
27. Thompson AR, Cooper JA, Jones GT, Drenos F, van Bockxmeer FM, Biros E, Walker PJ, van Rij AM, Golledge J, Norman PE, et al,. (2010) Assessment of the association between genetic polymorphisms in transforming growth factor beta, and its binding protein (LTBP), and the presence, and expansion, of abdominal aortic aneurysm. Atherosclerosis 209, 367-373.
28. Forsti A, Li X, Wagner K, Tavelin B, Enquist K, Palmqvist R, Altieri A, Hallmans G, Hemminki K, &, Lenner P, (2010) Polymorphisms in the transforming growth factor beta 1 pathway in relation to colorectal cancer progression. Genes Chromosom Cancer 49, 270-281.
29. Sterner-Kock A, Thorey IS, Koli K, Wempe F, Otte J, Bangsow T, Kuhlmeier K, Kirchner T, Jin S, Keski-Oja J, et al,. (2002) Disruption of the gene encoding the latent transforming growth factor-beta binding protein 4 (LTBP-4) causes abnormal lung development, cardiomyopathy, and colorectal cancer. Genes Dev 16, 2264-2273.
30. Giltay R, Kostka G, &, Timpl R, (1997) Sequence and expression of a novel member (LTBP-4) of the family of latent transforming growth factor-beta binding proteins. FEBS Lett 411, 164-168.
31. Todorovic V, &, Rifkin DB, (2012) LTBPs, more than just an escort service. J Cell Biochem 113, 410-418.
32. Dallas SL, Chen Q, &, Sivakumar P, (2006) Dynamics of assembly and reorganization of extracellular matrix proteins. Curr Top Dev Biol 75, 1-24.
33. Dietz HC, Cutting GR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM, Puffenberger EG, Hamosh A, Nanthakumar EJ, Curristin SM, et al,. (1991) Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 352, 337-339.
34. Doyle JJ, Gerber EE, &, Dietz HC, (2012) Matrix-dependent perturbation of TGFbeta signaling and disease. FEBS Lett 586, 2003-2015.
35. Habashi JP, Judge DP, Holm TM, Cohn RD, Loeys BL, Cooper TK, Myers L, Klein EC, Liu G, Calvi C, et al,. (2006) Losartan, an AT1 antagonist, prevents aortic aneurysm in a mouse model of Marfan syndrome. Science 312, 117-121.
36. Brooke BS, Habashi JP, Judge DP, Patel N, Loeys B, &, Dietz HC III, (2008) Angiotensin II blockade and aortic-root dilation in Marfan's syndrome. N Engl J Med 358, 2787-2795.
37. Cohn RD, van Erp C, Habashi JP, Soleimani AA, Klein EC, Lisi MT, Gamradt M, ap Rhys CM, Holm TM, &, Loeys BL, et al. (2007) Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat Med 13, 204-210.
38. Koli K, Saharinen J, Hyytiainen M, Penttinen C, &, Keski-Oja J, (2001) Latency, activation, and binding proteins of TGF-beta. Microsc Res Tech 52, 354-362.
39. Moren A, Olofsson A, Stenman G, Sahlin P, Kanzaki T, Claesson-Welsh L, ten Dijke P, Miyazono K, &, Heldin CH, (1994) Identification and characterization of LTBP-2, a novel latent transforming growth factor-beta-binding protein. J Biol Chem 269, 32469-32478.
40. Saharinen J, Taipale J, Monni O, &, Keski-Oja J, (1998) Identification and characterization of a new latent transforming growth factor-beta-binding protein, LTBP-4. J Biol Chem 273, 18459-18469.
41. Kanzaki T, &, Otabe M, (2003) Latent transforming growth factor-beta binding protein-1, a component of latent transforming growth factor-beta complex, accelerates the migration of aortic smooth muscle cells in diabetic rats through integrin-beta3. Diabetes 52, 824-828.
42. Oklu R, Hesketh R, Wicky S, &, Metcalfe JC, (2011) Localization of latent transforming growth factor-beta binding protein-1 in human coronary atherosclerotic plaques. Circ J 75, 196-200.
43. Sharafieh R, Child AH, Khaw PT, Fleck B, &, Sarfarazi M, (2012) LTBP2 gene analysis in the GLC3C-linked family and 94 CYP1B1-negative cases with primary congenital glaucoma. Ophthalmic Genet 34, 14-20.
44. Abu-Amero KK, Osman EA, Mousa A, Wheeler J, Whigham B, Allingham RR, Hauser MA, &, Al-Obeidan SA, (2011) Screening of CYP1B1 and LTBP2 genes in Saudi families with primary congenital glaucoma: genotype-phenotype correlation. Mol Vis 17, 2911-2919.
45. Haji-Seyed-Javadi R, Jelodari-Mamaghani S, Paylakhi SH, Yazdani S, Nilforushan N, Fan JB, Klotzle B, Mahmoudi MJ, Ebrahimian MJ, Chelich N, et al,. (2012) LTBP2 mutations cause Weill-Marchesani and Weill-Marchesani-like syndrome and affect disruptions in the extracellular matrix. Hum Mutat 33, 1182-1187.
46. Shipley JM, Mecham RP, Maus E, Bonadio J, Rosenbloom J, McCarthy RT, Baumann ML, Frankfater C, Segade F, &, Shapiro SD, (2000) Developmental expression of latent transforming growth factor beta binding protein 2 and its requirement early in mouse development. Mol Cell Biol 20, 4879-4887.
47. Colarossi C, Chen Y, Obata H, Jurukovski V, Fontana L, Dabovic B, &, Rifkin DB, (2005) Lung alveolar septation defects in Ltbp-3-null mice. Am J Pathol 167, 419-428.
48. Koli K, Ryynanen MJ, &, Keski-Oja J, (2008) Latent TGF-beta binding proteins (LTBPs)-1 and -3 coordinate proliferation and osteogenic differentiation of human mesenchymal stem cells. Bone 43, 679-688.
49. Urban Z, Hucthagowder V, Schurmann N, Todorovic V, Zilberberg L, Choi J, Sens C, Brown CW, Clark RD, Holland KE, et al,. (2009) Mutations in LTBP4 cause a syndrome of impaired pulmonary, gastrointestinal, genitourinary, musculoskeletal, and dermal development. Am J Hum Genet 85, 593-605.
50. Koli K, Wempe F, Sterner-Kock A, Kantola A, Komor M, Hofmann WK, von Melchner H, &, Keski-Oja J, (2004) Disruption of LTBP-4 function reduces TGF-beta activation and enhances BMP-4 signaling in the lung. J Cell Biol 167, 123-133.
51. Sinha S, Nevett C, Shuttleworth CA, &, Kielty CM, (1998) Cellular and extracellular biology of the latent transforming growth factor-beta binding proteins. Matrix Biol 17, 529-545.
52. Miyazono K, Thyberg J, &, Heldin CH, (1992) Retention of the transforming growth factor-beta 1 precursor in the Golgi complex in a latent endoglycosidase H-sensitive form. J Biol Chem 267, 5668-5675.
53. Miyazono K, Olofsson A, Colosetti P, &, Heldin CH, (1991) A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1. EMBO J 10, 1091-1101.
54. Taipale J, Koli K, &, Keski-Oja J, (1992) Release of transforming growth factor-beta 1 from the pericellular matrix of cultured fibroblasts and fibrosarcoma cells by plasmin and thrombin. J Biol Chem 267, 25378-25384.
55. Taipale J, Lohi J, Saarinen J, Kovanen PT, &, Keski-Oja J, (1995) Human mast cell chymase and leukocyte elastase release latent transforming growth factor-beta 1 from the extracellular matrix of cultured human epithelial and endothelial cells. J Biol Chem 270, 4689-4696.
56. Munger JS, Harpel JG, Gleizes PE, Mazzieri R, Nunes I, &, Rifkin DB, (1997) Latent transforming growth factor-beta: structural features and mechanisms of activation. Kidney Int 51, 1376-1382.
57. Olofsson A, Ichijo H, Moren A, ten Dijke P, Miyazono K, &, Heldin CH, (1995) Efficient association of an amino-terminally extended form of human latent transforming growth factor-beta binding protein with the extracellular matrix. J Biol Chem 270, 31294-31297.
58. Saharinen J, Taipale J, &, Keski-Oja J, (1996) Association of the small latent transforming growth factor-beta with an eight cysteine repeat of its binding protein LTBP-1. EMBO J 15, 245-253.
59. Koski C, Saharinen J, &, Keski-Oja J, (1999) Independent promoters regulate the expression of two amino terminally distinct forms of latent transforming growth factor-beta binding protein-1 (LTBP-1) in a cell type-specific manner. J Biol Chem 274, 32619-32630.
60. Unsold C, Hyytiainen M, Bruckner-Tuderman L, &, Keski-Oja J, (2001) Latent TGF-beta binding protein LTBP-1 contains three potential extracellular matrix interacting domains. J Cell Sci 114, 187-197.
61. Annes JP, Munger JS, &, Rifkin DB, (2003) Making sense of latent TGFbeta activation. J Cell Sci 116, 217-224.
62. Ge G, &, Greenspan DS, (2006) BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J Cell Biol 175, 111-120.
63. Dallas SL, Rosser JL, Mundy GR, &, Bonewald LF, (2002) Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J Biol Chem 277, 21352-21360.
64. Michel K, Roth S, Trautwein C, Gong W, Flemming P, &, Gressner AM, (1998) Analysis of the expression pattern of the latent transforming growth factor beta binding protein isoforms in normal and diseased human liver reveals a new splice variant missing the proteinase-sensitive hinge region. Hepatology 27, 1592-1599.
65. Yin W, Smiley E, &, Bonadio J, (1998) Alternative splicing of LTBP-3. Biochem Biophys Res Commun 245, 454-458.
66. Saharinen J, &, Keski-Oja J, (2000) Specific sequence motif of 8-Cys repeats of TGF-beta binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-beta. Mol Biol Cell 11, 2691-2704.
67. Bujak M, &, Frangogiannis NG, (2007) The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 74, 184-195.
68. Leask A, &, Abraham DJ, (2004) TGF-beta signaling and the fibrotic response. FASEB J 18, 816-827.
69. Piek E, Heldin CH, &, Ten Dijke P, (1999) Specificity, diversity, and regulation in TGF-beta superfamily signaling. FASEB J 13, 2105-2124.
70. Taipale J, Saharinen J, &, Keski-Oja J, (1998) Extracellular matrix-associated transforming growth factor-beta: role in cancer cell growth and invasion. Adv Cancer Res 75, 87-134.
71. Kane CJ, Hebda PA, Mansbridge JN, &, Hanawalt PC, (1991) Direct evidence for spatial and temporal regulation of transforming growth factor beta 1 expression during cutaneous wound healing. J Cell Physiol 148, 157-173.
72. Chin GS, Liu W, Peled Z, Lee TY, Steinbrech DS, Hsu M, &, Longaker MT, (2001) Differential expression of transforming growth factor-beta receptors I and II and activation of Smad 3 in keloid fibroblasts. Plast Reconstr Surg 108, 423-429.
73. Schmid P, Itin P, Cherry G, Bi C, &, Cox DA, (1998) Enhanced expression of transforming growth factor-beta type I and type II receptors in wound granulation tissue and hypertrophic scar. Am J Pathol 152, 485-493.
74. Lin RY, Sullivan KM, Argenta PA, Meuli M, Lorenz HP, &, Adzick NS, (1995) Exogenous transforming growth factor-beta amplifies its own expression and induces scar formation in a model of human fetal skin repair. Ann Surg 222, 146-154.
75. Cordeiro MF, (2003) Transforming growth factor-beta function blocking already effective as therapeutic strategy. Circulation 107, E37-7; author reply E37-7.
76. Shah M, Foreman DM, &, Ferguson MW, (1995) Neutralisation of TGF-beta 1 and TGF-beta 2 or exogenous addition of TGF-beta 3 to cutaneous rat wounds reduces scarring. J Cell Sci 108 (Pt 3), 985-1002.
77. Yamazaki M, Minota S, Sakurai H, Miyazono K, Yamada A, Kanazawa I, &, Kawai M, (1994) Expression of transforming growth factor-beta 1 and its relation to endomysial fibrosis in progressive muscular dystrophy. Am J Pathol 144, 221-226.
78. Bernasconi P, Torchiana E, Confalonieri P, Brugnoni R, Barresi R, Mora M, Cornelio F, Morandi L, &, Mantegazza R, (1995) Expression of transforming growth factor-beta 1 in dystrophic patient muscles correlates with fibrosis. Pathogenetic role of a fibrogenic cytokine. J Clin Invest 96, 1137-1144.
79. Burks TN, &, Cohn RD, (2011) Role of TGF-beta signaling in inherited and acquired myopathies. Skelet Muscle 1, 19.
80. Barton ER, (2006) Impact of sarcoglycan complex on mechanical signal transduction in murine skeletal muscle. Am J Physiol Cell Physiol 290, C411-C419.
81. Kolodziejczyk SM, Walsh GS, Balazsi K, Seale P, Sandoz J, Hierlihy AM, Rudnicki MA, Chamberlain JS, Miller FD, &, Megeney LA, (2001) Activation of JNK1 contributes to dystrophic muscle pathogenesis. Curr Biol 11, 1278-1282.
82. Nelson CA, Hunter RB, Quigley LA, Girgenrath S, Weber WD, McCullough JA, Dinardo CJ, Keefe KA, Ceci L, Clayton NP, et al,. (2011) Inhibiting TGF-beta activity improves respiratory function in mdx mice. Am J Pathol 178, 2611-2621.
83. Lorts A, Schwanekamp JA, Baudino TA, McNally EM, &, Molkentin JD, (2012) Deletion of periostin reduces muscular dystrophy and fibrosis in mice by modulating the transforming growth factor-beta pathway. Proc Natl Acad Sci USA 109, 10978-10983.
84. Oka T, Xu J, Kaiser RA, Melendez J, Hambleton M, Sargent MA, Lorts A, Brunskill EW, Dorn GW II, Conway SJ, et al,. (2007) Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ Res 101, 313-321.
85. Vetrone SA, Montecino-Rodriguez E, Kudryashova E, Kramerova I, Hoffman EP, Liu SD, Miceli MC, &, Spencer MJ, (2009) Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J Clin Invest 119, 1583-1594.
86. Pegoraro E, Hoffman EP, Piva L, Gavassini BF, Cagnin S, Ermani M, Bello L, Soraru G, Pacchioni B, Bonifati MD, et al,. (2011) SPP1 genotype is a determinant of disease severity in Duchenne muscular dystrophy. Neurology 76, 219-226.
87. Piva L, Gavassini BF, Bello L, Fanin M, Soraru G, Barp A, Ermani M, Angelini C, Hoffman EP, &, Pegoraro E, (2012) TGFBR2 but not SPP1 genotype modulates osteopontin expression in Duchenne muscular dystrophy muscle. J Pathol 228, 251-259.
88. Hullinger TG, Pan Q, Viswanathan HL, &, Somerman MJ, (2001) TGFbeta and BMP-2 activation of the OPN promoter: roles of smad- and hox-binding elements. Exp Cell Res 262, 69-74.
89. Goldstein JA, Kelly SM, LoPresti PP, Heydemann A, Earley JU, Ferguson EL, Wolf MJ, &, McNally EM, (2011) SMAD signaling drives heart and muscle dysfunction in a Drosophila model of muscular dystrophy. Hum Mol Genet 20, 894-904.
90. Allikian MJ, Bhabha G, Dospoy P, Heydemann A, Ryder P, Earley JU, Wolf MJ, Rockman HA, &, McNally EM, (2007) Reduced life span with heart and muscle dysfunction in Drosophila sarcoglycan mutants. Hum Mol Genet 16, 2933-2943.
91. Shcherbata HR, Yatsenko AS, Patterson L, Sood VD, Nudel U, Yaffe D, Baker D, &, Ruohola-Baker H, (2007) Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J 26, 481-493.
92. Holm TM, Habashi JP, Doyle JJ, Bedja D, Chen Y, van Erp C, Lindsay ME, Kim D, Schoenhoff F, Cohn RD, et al,. (2011) Noncanonical TGFbeta signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science 332, 358-361.
93. Habashi JP, Doyle JJ, Holm TM, Aziz H, Schoenhoff F, Bedja D, Chen Y, Modiri AN, Judge DP, &, Dietz HC, (2011) Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 332, 361-365.