Pathology is alleviated by doxycycline in a laminin-α2-null model of congenital muscular dystrophy

Annals of Neurology

Volumn 65, Issue 1, 2009, Pages 47-56

  Girgenrath, Mahasweta ^a   Beermann, Mary Lou ^b   Vishnudas, Vivek K ^b   Homma, Sachiko ^b   Miller, Jeffrey Boone ^b,c  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DNA NUCLEOTIDYLEXOTRANSFERASE; DOXYCYCLINE; LAMININ ALPHA2; MINOCYCLINE; PROTEIN BAX; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; BEHAVIOR; BIRTH; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFECT; FEMALE; GENE MUTATION; GROWTH; GROWTH RATE; HINDLIMB; HISTOLOGY; HOMOZYGOTE; INFLAMMATION; LIFESPAN; MALE; MAMMAL; MOUSE; MUSCULAR DYSTROPHY; NEUROMUSCULAR DISEASE; NEUROMUSCULAR FUNCTION; NEWBORN; NICK END LABELING; NONHUMAN; PARALYSIS; PATHOLOGY; POSTNATAL GROWTH; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN PHOSPHORYLATION;

AGE FACTORS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, CD11B; APOPTOSIS; CELL LINE, TRANSFORMED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXYCYCLINE; ENZYME INHIBITORS; IN SITU NICK-END LABELING; LAMININ; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUTATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; STAUROSPORINE; SURVIVAL ANALYSIS; THREONINE;

EID: 60849118087     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.21523     Document Type: Article

References (49)

1. Miyagoe-Suzuki Y, Nakagawa M, Takeda I. Merosin and congenital muscular dystrophy. Microsc Res Tech 2000;48: 181-191.
2. Allamand V, Guicheney P. Merosin-deficient congenital muscular dystrophy, autosomal recessive (MDC1A, MIM#156225, LAMA2 gene coding for alpha2 chain of laminin). Eur J Hum Genet 2002;10:91-94.
3. Khurana TS, Davies KE. Pharmacological strategies for muscular dystrophy. Nat Rev Drug Discov 2003;2:379-390.
4. Gawlik KI, Li JY, Petersen A, Durbeej M. Laminin alpha1 chain improves laminin alpha2 chain deficient peripheral neuropathy. Hum Mol Genet 2006;15:2690-2700.
5. Kuang W, Xu H, Vachon PH, et al. Merosin-deficient congenital muscular dystrophy: partial genetic correction in two mouse models. J Clin Invest 1999;102:844-852.
6. Girgenrath M, Dominov JA, Kostek CA, Miller JB. Inhibition of apoptosis improves outcome in a model of congenital muscular dystrophy. J Clin Invest 2004;114:1635-1639.
7. Dominov JA, Kravetz AJ, Ardelt M, et al. Muscle-specific BCL2 expression ameliorates muscle disease in laminin-α2- deficient, but not dystrophin-deficient, mice. Hum Mol Genet 2005;14:1029-1040.
8. Miyagoe Y, Hanaoka K, Nonaka I, et al. Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin laminin 2-deficient congenital muscular dystrophy. FEBS Lett 1997;415:33-39.
9. Mukasa T, Momoi T, Momoi MY. Activation of caspase-3 apoptotic pathways in skeletal muscle fibers in laminin alpha2-deficient mice. Biochem Biophys Res Commun 1999;260: 139-142.
10. Hayashi YK, Tezak Z, Momoi T, et al. Massive muscle cell degeneration in the early stage of merosin-deficient congenital muscular dystrophy. Neuromuscul Disord 2001;11:350-359.
11. Kriz J, Nguyen MD, Julien JP. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 2002;10:268-278.
12. Zhu S, Stavrovskaya IG, Drozda M, et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002;417:74-78.
13. Pi R, Li W, Lee NT, et al. Minocycline prevents glutamate- induced apoptosis of cerebellar granule neurons by differential regulation of p38 and Akt pathways. J Neurochem 2004;91: 1219-1230.
14. Wang J, Wei Q, Wang CY, et al. Minocycline up-regulates Bcl-2 and protects against cell death in mitochondria. J Biol Chem 2004;279:9948-9954.
15. Davies JE, Wang L, Garcia-Oroz L, et al. Doxycycline attenuates and delays toxicity of the oculopharyngeal muscular dystrophy mutation in transgenic mice. Nat Med 2005;11: 672-677.
16. Alano CC, Kauppinen TM, Valls AV, Swanson RA. Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations. Proc Natl Acad Sci USA 2006;103: 9685-9690.
17. Girgenrath M, Kostek CA, Miller JB. Diseased muscles that lack dystrophin or laminin-alpha2 have altered compositions and proliferation of mononucleate cells. BMC Neurol 2005;5:7.
18. Moll J, Barzaghi P, Lin S, et al. An agrin minigene rescues dystrophic symptoms in a mouse model for congenital muscular dystrophy. Nature 2001;413:302-307.
19. ARF, or p53 and is accelerated by inactivation of Bax. BMC Cell Biol 2004;5:1.
20. Jacobsen MD, Weil M, Raff MC. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J Cell Biol 1996;133:1041-1051.
21. Dominov JA, Dunn JJ, Miller JB. Bcl-2 expression identifies an early stage of myogenesis and promotes clonal expansion of muscle cells. J Cell Biol 1998;142:537-544.
22. Shen Q, Zhang Y, Uray IP, et al. The AP-1 transcription factor regulates postnatal mammary gland development. Dev Biol 2006;295:589-603.
23. Nakagawa M, Miyagoe-Suzuki Y, Ikezoe K, et al. Schwann cell myelination occurred without basal lamina formation in laminin alpha2 chain-null mutant (dy3K/dy3K) mice. Glia 2001; 35:101-110.
24. Meinen S, Barzaghi P, Lin S, et al. Linker molecules between laminins and dystroglycan ameliorate laminin-alpha2-deficient muscular dystrophy at all disease stages. J Cell Biol 2007;176: 979-993.
25. Kuang W, Xu H, Vilquin JT, Engvall E. Activation of the Lama2 gene in muscle regeneration: abortive regeneration in laminin alpha2-deficiency. Lab Invest 1999;79:1601-1613.
26. 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-, and laminin alpha2-deflcient mice. Neuromuscul Disord 2001;11:703-712.
27. Vachon PH, Loechel F, Xu H, et al. Merosin and laminin in myogenesis; specific requirement for merosin in myotube stability and survival. J Cell Biol 1996;134:1483-1497.
28. Li ZF, Shelton GD, Engvall E. Elimination of myostatin does not combat muscular dystrophy in dy mice but increases postnatal lethality. Am J Pathol 2005;166:491-497.
29. Jannapureddy SR, Patel ND, Hwang W, Boriek AM. Merosin deficiency leads to alterations in passive and active skeletal muscle mechanics. J Appl Physiol 2003;94:2524-2533.
30. Langenbach KJ, Rando TA. Inhibition of dystroglycan binding to laminin disrupts the PI3K/AKT pathway and survival signaling in muscle cells. Muscle Nerve 2002;26:644-653.
31. Miller JB, Girgenrath M. Role of apoptosis in neuromuscular diseases and potential usefulness of anti-apoptosis therapy. Trends Mol Med 2006;12:279-286.
32. Tsai MS, Chiu YT, Wang SH, et al. Abolishing Bax-dependent apoptosis shows beneficial effects on spinal muscular atrophy model mice. Mol Ther 2006;13:1149-1155.
33. Kostic V, Jackson-Lewis V, de Bilbao F, et al. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 1997;277:559-562.
34. Friedlander RM, Brown RH, Gagliardini V, et al. Inhibition of ICE slows ALS in mice. Nature 1997;388:31.
35. Irwin WA, Bergamin N, Sabatelli P, et al. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat Genet 2003;35:367-371.
36. Abmayr S, Crawford RW, Chamberlain JS. Characterization of ARC, apoptosis repressor interacting with CARD, in normal and dystrophin-deficient skeletal muscle. Hum Mol Genet 2004;13:213-221.
37. Sapadin AN, Fleischmajer R. Tetracyclines: nonantibiotic properties and their clinical implications. J Am Acad Dermatol 2006;54:258-265.
38. Connolly AM, Keeling RM, Streif EM, et al. Complement 3 deficiency and oral prednisolone improve strength and prolong survival of laminin alpha2-deficient mice. J Neuroimmunol 2002;127:80-87.
39. Girgenrath M, Weng S, Kostek CA, et al. TWEAK, via its receptor Fn14, is a novel regulator of mesenchymal progenitor cells and skeletal muscle regeneration. EMBO J 2006;25: 5826-5839.
40. Alessi DR, Andjelkovic M, Caudwell B, et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 1996;15:6541-6551.
41. Kondapaka SB, Zarnowski M, Yver DR, et al. 7-hydroxy-staurosporine (UCN-01) inhibition of Akt Thr308 but not Ser473 phosphorylation: a basis for decreased insulin-stimulated glucose transport. Clin Cancer Res 2004;10: 7192-7198.
42. Ouyang YB, Zhang XH, He QP, et al. Differential phosphorylation at Ser473 and Thr308 of Akt-1 in rat brain following hypoglycemic coma. Brain Res 2000;876:191-195.
43. Zdanowicz MM, Slonim AE, Bilaniuk I, et al. High protein diet has beneficial effects in murine muscular dystrophy. J Nutr 1995;125:1150-1158.
44. Hayes A, Williams DA. Examining potential drug therapies for muscular dystrophy utilising the dy/dy mouse: I. Clenbuterol. J Neurol Sci 1998;157:122-128.
45. Lynch GS, Cuffe SA, Plant DR, Gregorevic P. IGF-I treatment improves the functional properties of fast- and slow-twitch skeletal muscles from dystrophic mice. Neuromuscul Disord 2001; 11:260-268.
46. Yao JS, Shen F, Young WL, Yang GY. Comparison of doxycycline and minocycline in the inhibition of VEGF-induced smooth muscle cell migration. Neurochem Int 2007;50:524-530.
47. Messina S, Mazzeo A, Bitto A, et al. VEGF overexpression via adeno-associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice. FASEB J 2007;21:3737-3746.
48. Gordon PH, Moore DH, Miller RG, et al; Western ALS Study Group. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol 2007;6:1045-1053.
49. Minagar A, Alexander JS, Schwendimann RN, et al. Combination Therapy With Interferon Beta-1a and Doxycycline in Multiple Sclerosis: an Open-Label Trial. Arch Neurol 2008;65: 199-204.