Targeting β1-integrin signaling enhances regeneration in aged and dystrophic muscle in mice

Nature Medicine

Volumn 22, Issue 8, 2016, Pages 889-896

  Rozo, Michelle ^a,b   Li, Liangji ^a,b   Fan, Chen Ming ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b GEOPHYSICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; FIBROBLAST GROWTH FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; PROTEIN KINASE B;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CONTROLLED STUDY; FEMALE; HOMEOSTASIS; INTRACELLULAR SIGNALING; MALE; MOUSE; MOUSE MODEL; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; SATELLITE CELL; STEM CELL NICHE; STEM CELL SELF-RENEWAL; TIBIALIS ANTERIOR MUSCLE; AGING; ANIMAL; CELL CULTURE; CYTOLOGY; DISEASE MODEL; DUCHENNE MUSCULAR DYSTROPHY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOPRECIPITATION; INJURIES; KNOCKOUT MOUSE; METABOLISM; MUSCLE FATIGUE; MUSCLE STRENGTH; REGENERATION; SARCOPENIA; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; WESTERN BLOTTING; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

AGING; ANIMALS; ANTIGENS, CD29; BLOTTING, WESTERN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTOR 2; FLOW CYTOMETRY; IMMUNOPRECIPITATION; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MUSCLE FATIGUE; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOBLASTS; PROTO-ONCOGENE PROTEINS C-AKT; REGENERATION; SARCOPENIA; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84976871229     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4116     Document Type: Article

References (46)

1. Ryall, J.G., Schertzer, J.D. & Lynch, G.S. Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology 9, 213-228 (2008).
2. Chakkalakal, J.V., Jones, K.M., Basson, M.A. & Brack, A.S. The aged niche disrupts muscle stem cell quiescence. Nature 490, 355-360 (2012).
3. Fry, C.S. et al. Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat. Med. 21, 76-80 (2015).
4. Brack, A.S. et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317, 807-810 (2007).
5. Cosgrove, B.D. et al. Rejuvenation of the muscle stem cell population restores strength to injured aged muscles. Nat. Med. 20, 255-264 (2014).
6. Conboy, I.M., Conboy, M.J., Smythe, G.M. & Rando, T.A. Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577 (2003).
7. Shea, K.L. et al. Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6, 117-129 (2010).
8. Carlson, M.E., Hsu, M. & Conboy, I.M. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454, 528-532 (2008).
9. Bernet, J.D. et al. p38 MAPK signaling underlies a cell-autonomous loss of stem cell self-renewal in skeletal muscle of aged mice. Nat. Med. 20, 265-271 (2014).
10. Price, F.D. et al. Inhibition of JAK-STAT signaling stimulates adult satellite cell function. Nat. Med. 20, 1174-1181 (2014).
11. Tierney, M.T. et al. STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat. Med. 20, 1182-1186 (2014).
12. Mori, S. & Takada, Y. Cross-talk between fibroblast growth factor (FGF) receptor and integrin through direct integrin binding to FGF and resulting integrin-FGF-FGFR ternary complex formation. Med. Sci.(Basel) 1, 20-36 (2013).
13. Assoian, R.K. & Schwartz, M.A. Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11, 48-53 (2001).
14. Hynes, R.O. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687 (2002).
15. Helbling-Leclerc, A. et al. Mutations in the laminin-α2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat. Genet. 11, 216-218 (1995).
16. Schwander, M. et al. β1-integrins regulate myoblast fusion and sarcomere assembly. Dev. Cell 4, 673-685 (2003).
17. Bulfield, G., Siller, W.G., Wight, P.A. & Moore, K.J. X-chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. USA 81, 1189-1192 (1984).
18. Lepper, C., Conway, S.J. & Fan, C.-M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627-631 (2009).
19. Raghavan, S., Bauer, C., Mundschau, G., Li, Q. & Fuchs, E. Conditional ablation of β1-integrin in skin. Severe defects in epidermal proliferation, basement membrane formation and hair follicle invagination. J. Cell Biol. 150, 1149-1160 (2000).
20. Webster, M.T. & Fan, C.-M. c-MET regulates myoblast motility and myocyte fusion during adult skeletal muscle regeneration. PLoS One 8, e81757 (2013).
21. Roovers, K., Davey, G., Zhu, X., Bottazzi, M.E. & Assoian, R.K. α5β1-integrin controls cyclin D1 expression by sustaining mitogen-activated protein kinase activity in growth-factor-treated cells. Mol. Biol. Cell 10, 3197-3204 (1999).
22. Polanska, U.M., Fernig, D.G. & Kinnunen, T. Extracellular interactome of the FGF receptor-ligand system: complexities and the relative simplicity of the worm. Dev. Dyn. 238, 277-293 (2009).
23. Murakami, M., Elfenbein, A. & Simons, M. Noncanonical fibroblast growth factor signaling in angiogenesis. Cardiovasc. Res. 78, 223-231 (2008).
24. Miyamoto, S., Teramoto, H., Gutkind, J.S. & Yamada, K.M. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J. Cell Biol. 135, 1633-1642 (1996).
25. Jones, N.C., Fedorov, Y.V., Rosenthal, R.S. & Olwin, B.B. ERK1/2 is required for myoblast proliferation but is dispensable for muscle gene expression and cell fusion. J. Cell. Physiol. 186, 104-115 (2001).
26. Siegel, A.L., Atchison, K., Fisher, K.E., Davis, G.E. & Cornelison, D.D. 3D time-lapse analysis of muscle satellite cell motility. Stem Cells 27, 2527-2538 (2009).
27. Troy, A. et al. Coordination of satellite cell activation and self-renewal by Par-complex-dependent asymmetric activation of p38-α/β MAPK. Cell Stem Cell 11, 541-553 (2012).
28. Conboy, I.M. et al. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764 (2005).
29. Kragstrup, T.W., Kjaer, M. & Mackey, A.L. Structural, biochemical, cellular and functional changes in skeletal muscle extracellular matrix with aging. Scand. J. Med. Sci. Sports 21, 749-757 (2011).
30. Wood, L.K. et al. Intrinsic stiffness of extracellular matrix increases with age in skeletal muscles of mice. J. Appl. Physiol. 117, 363-369 (2014).
31. Bazzoni, G., Shih, D.-T., Buck, C.A. & Hemler, M.E. Monoclonal antibody 9EG7 defines a novel β1-integrin epitope induced by soluble ligand and manganese, but inhibited by calcium. J. Biol. Chem. 270, 25570-25577 (1995).
32. Takagi, J. & Springer, T.A. Integrin activation and structural rearrangement. Immunol. Rev. 186, 141-163 (2002).
33. Calderwood, D.A., Shattil, S.J. & Ginsberg, M.H. Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J. Biol. Chem. 275, 22607-22610 (2000).
34. Hintermann, E., Bilban, M., Sharabi, A. & Quaranta, V. Inhibitory role of α6β4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on α3β1 integrin. J. Cell Biol. 153, 465-478 (2001).
35. Toledo, M.S., Suzuki, E., Handa, K. & Hakomori, S. Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor. J. Biol. Chem. 280, 16227-16234 (2005).
36. Sahni, A. & Francis, C.W. Stimulation of endothelial cell proliferation by FGF2 in the presence of fibrinogen requires αvβ3. Blood 104, 3635-3641 (2004).
37. Lukjanenko et al. Loss of fibronectin from the aged stem cell niche affects the regenerative capacity of skeletal muscle in mice. Nat. Med. http://dx.doi.org/10.1038/nm.4126 (2016).
38. Sicari, B.M. et al. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans, with volumetric muscle loss. Sci. Transl. Med. 6, 234ra58 (2014).
39. Fukada, S. et al. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25, 2448-2459 (2007).
40. Tanentzapf, G., Devenport, D., Godt, D. & Brown, N.H. Integrin-dependent anchoring of a stem cell niche. Nat. Cell Biol. 9, 1413-1418 (2007).
41. Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71 (1999).
42. Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001).
43. Hogan, B., Beddington, R., Costantini, F. & Lacy, E. Manipulating the Mouse Embryo: a Laboratory Manual (Cold Spring Harbor Laboratory Press, 1994).
44. Hakim, C.H., Wasala, N.B. & Duan, D. Evaluation of muscle function of the extensor digitorum longus muscle ex vivo and tibialis anterior muscle in situ in mice. J. Vis. Exp. 21, e50183 (2013).
45. Barton, E.R., Lynch, G. & Khurana, T.S. Measuring Isometric Force of Isolated Mouse Muscles In Vitro (TREAT-NMD Neuromuscular Network, 2008).
46. Trapnell, C. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31, 46-53 (2013).