Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors

Regenerative efforts typically focus on the delivery of single factors, but it is likely that multiple factors regulating distinct aspects of the regenerative process (e.g., vascularization and stem cell activation) can be used in parallel to affect regeneration of functional tissues. This possibility was addressed in the context of ischemic muscle injury, which typically leads to necrosis and loss of tissue and function. The role of sustained delivery, via injectable gel, of a combination of VEGF to promote angiogenesis and insulin-like growth factor-1 (IGF1) to directly promote muscle regeneration and the return of muscle function in ischemic rodent hindlimbs was investigated. Sustained VEGF delivery alone led to neoangiogenesis in ischemic limbs, with complete return of tissue perfusion to normal levels by 3 weeks, as well as protection from hypoxia and tissue necrosis, leading to an improvement in muscle contractility. Sustained IGF1 delivery alone was found to enhance muscle fiber regeneration and protected cells from apoptosis. However, the combined delivery of VEGF and IGF1 led to parallel angiogenesis, reinnervation, and myogenesis; as satellite cell activation and proliferation was stimulated, cells were protected from apoptosis, the inflammatory response was muted, and highly functional muscle tissue was formed. In contrast, bolus delivery of factors did not have any benefit in terms of neoangiogenesis and perfusion and had minimal effect on muscle regeneration. These results support the utility of simultaneously targeting distinct aspects of the regenerative process.

[1]  A. Wagers,et al.  Cellular and Molecular Signatures of Muscle Regeneration: Current Concepts and Controversies in Adult Myogenesis , 2005, Cell.

[2]  F. Booth,et al.  IGF‐I restores satellite cell proliferative potential in immobilized old skeletal muscle , 2000, Journal of applied physiology.

[3]  D. Mooney,et al.  Polymeric system for dual growth factor delivery , 2001, Nature Biotechnology.

[4]  Richard P. Harvey,et al.  Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway , 1999, Nature.

[5]  T. Hawke,et al.  Myogenic satellite cells: physiology to molecular biology. , 2001, Journal of applied physiology.

[6]  J. Alroy,et al.  Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy , 2000, Nature Medicine.

[7]  D. Lubeck The costs of musculoskeletal disease: health needs assessment and health economics. , 2003, Best practice & research. Clinical rheumatology.

[8]  H. Vandenburgh,et al.  Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture. , 1991, The American journal of physiology.

[9]  C. Lang,et al.  Increased protein synthesis after acute IGF-I or insulin infusion is localized to muscle in mice. , 1998, American journal of physiology. Endocrinology and metabolism.

[10]  Helen M. Blau,et al.  Biological Progression from Adult Bone Marrow to Mononucleate Muscle Stem Cell to Multinucleate Muscle Fiber in Response to Injury , 2002, Cell.

[11]  G. Adams,et al.  Localized infusion of IGF-I results in skeletal muscle hypertrophy in rats. , 1998, Journal of applied physiology.

[12]  R. Ribchester,et al.  Programmed axon death, synaptic dysfunction and the ubiquitin proteasome system. , 2004, Current drug targets. CNS and neurological disorders.

[13]  A. Musarò,et al.  Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model , 2005, The Journal of cell biology.

[14]  B. Zheng,et al.  Prospective identification of myogenic endothelial cells in human skeletal muscle , 2007, Nature Biotechnology.

[15]  S. Price,et al.  Insulin-like growth factor I: the yin and yang of muscle atrophy. , 2004, Endocrinology.

[16]  M. Rudnicki,et al.  Cellular and molecular regulation of muscle regeneration. , 2004, Physiological reviews.

[17]  G H Willital,et al.  Skeletal muscle tissue engineering using isolated myoblasts on synthetic biodegradable polymers: preliminary studies. , 1999, Tissue engineering.

[18]  M. Turunen,et al.  Vascular endothelial growth factor-D transgenic mice show enhanced blood capillary density, improved postischemic muscle regeneration, and increased susceptibility to tumor formation. , 2009, Blood.

[19]  A. Musarò,et al.  IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1 , 1999, Nature.

[20]  J. Sanes,et al.  Watching the neuromuscular junction , 2003, Journal of neurocytology.

[21]  N. Rosenthal,et al.  Proliferation precedes differentiation in IGF-I-stimulated myogenesis , 1996, The Journal of cell biology.

[22]  J. Tidball Biomechanics and Mechanotransduction in Cells and Tissues Mechanical signal transduction in skeletal muscle growth and adaptation , 2005 .

[23]  A. Mauro SATELLITE CELL OF SKELETAL MUSCLE FIBERS , 1961, The Journal of biophysical and biochemical cytology.

[24]  H. Vandenburgh,et al.  Paracrine release of insulin-like growth factor 1 from a bioengineered tissue stimulates skeletal muscle growth in vitro. , 2006, Tissue engineering.

[25]  E. Schultz,et al.  Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. , 1978, The Journal of experimental zoology.

[26]  D. Mooney,et al.  Regulating activation of transplanted cells controls tissue regeneration. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A. D. Di Giulio,et al.  Systemic administration of insulin‐like growth factor decreases motor neuron cell death and promotes muscle reinnervation , 1998, Journal of neuroscience research.

[28]  B. Zheng,et al.  Purification and culture of human blood vessel-associated progenitor cells. , 2008, Current protocols in stem cell biology.

[29]  S. Rosenthal,et al.  Opposing early and late effects of insulin-like growth factor I on differentiation and the cell cycle regulatory retinoblastoma protein in skeletal myoblasts. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  L. Zentilin,et al.  VEGF overexpression via adeno‐associated virus gene transfer promotes skeletal muscle regeneration and enhances muscle function in mdx mice , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[31]  B. Sacchetti,et al.  Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells , 2007, Nature Cell Biology.

[32]  Coleman Mp,et al.  Programmed axon death, synaptic dysfunction and the ubiquitin proteasome system. , 2004 .

[33]  H. Sweeney,et al.  Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. , 1999, Acta physiologica Scandinavica.

[34]  L. Kunkel,et al.  Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts , 1989, Nature.

[35]  N. Rosenthal,et al.  IGF-1, inflammation and stem cells: interactions during muscle regeneration. , 2005, Trends in immunology.

[36]  G Cossu,et al.  Muscle regeneration by bone marrow-derived myogenic progenitors. , 1998, Science.

[37]  N. Rosenthal,et al.  Local expression of IGF‐1 accelerates muscle regeneration by rapidly modulating inflammatory cytokines and chemokines , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[38]  M. Grounds Age‐associated Changes in the Response of Skeletal Muscle Cells to Exercise and Regeneration a , 1998, Annals of the New York Academy of Sciences.

[39]  K. Mcclatchey Musculoskeletal conditions affect millions. , 2004, Archives of pathology & laboratory medicine.

[40]  J. Oldham,et al.  Growth factors controlling muscle development. , 1999, Domestic animal endocrinology.

[41]  David J. Mooney,et al.  Spatio–temporal VEGF and PDGF Delivery Patterns Blood Vessel Formation and Maturation , 2007, Pharmaceutical Research.

[42]  F. Ambrosio,et al.  Effect of VEGF on the regenerative capacity of muscle stem cells in dystrophic skeletal muscle. , 2009, Molecular therapy : the journal of the American Society of Gene Therapy.

[43]  P. Caroni,et al.  Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors , 1990, The Journal of cell biology.

[44]  J. Isner,et al.  Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE-/- mice. , 1999, Circulation.

[45]  Gianfranco Sinagra,et al.  Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. , 2004, Molecular therapy : the journal of the American Society of Gene Therapy.

[46]  K. Jin,et al.  Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  David J. Mooney,et al.  Controlled growth factor release from synthetic extracellular matrices , 2000, Nature.

[48]  J. Tidball Inflammatory processes in muscle injury and repair. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[49]  P. Carmeliet,et al.  Molecular mechanisms of blood vessel growth. , 2001, Cardiovascular research.

[50]  A. Musarò,et al.  The neuroprotective effects of a locally acting IGF-1 isoform , 2007, Experimental Gerontology.

[51]  Robert J. Schwartz,et al.  Myogenic Vector Expression of Insulin-like Growth Factor I Stimulates Muscle Cell Differentiation and Myofiber Hypertrophy in Transgenic Mice (*) , 1995, The Journal of Biological Chemistry.

[52]  L. Kunkel,et al.  Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation. , 2002, The Journal of clinical investigation.

[53]  D. Kohane,et al.  Engineering vascularized skeletal muscle tissue , 2005, Nature Biotechnology.

[54]  V. Perry,et al.  Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene , 2001, Nature Neuroscience.

[55]  D. Allen,et al.  The distribution of intracellular calcium concentration in isolated single fibres of mouse skeletal muscle during fatiguing stimulation , 1994, Pflügers Archiv.

[56]  Michael Simons,et al.  Role of Angiogenesis in Cardiovascular Disease : a Critical Appraisal , 2022 .

[57]  A. Musarò,et al.  Local expression of mIgf-1 modulates ubiquitin, caspase and CDK5 expression in skeletal muscle of an ALS mouse model , 2008, Neurological research.

[58]  D J Mooney,et al.  Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis , 2007, Journal of thrombosis and haemostasis : JTH.

[59]  G. Bernardi,et al.  Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. , 2004, Proceedings of the National Academy of Sciences of the United States of America.