Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2017

Open Access 01-12-2017 | Research article

The effect of low intensity shockwave treatment (Li-SWT) on human myoblasts and mouse skeletal muscle

Authors: Lise K. Hansen, Henrik D. Schrøder, Lars Lund, Karthikeyan Rajagopal, Vrisha Maduri, Jeeva Sellathurai

Published in: BMC Musculoskeletal Disorders | Issue 1/2017

Login to get access

Abstract

Background

Transplanting myogenic cells and scaffolds for tissue engineering in skeletal muscle have shown inconsistent results. One of the limiting factors is neovascularization at the recipient site. Low intensity shockwave therapy (Li-SWT) has been linked to increased tissue regeneration and vascularization, both integral to survival and integration of transplanted cells. This study was conducted to demonstrate the response of myoblasts and skeletal muscle to Li-SWT.

Method

Primary isolated human myoblasts and explants were treated with low intensity shockwaves and subsequently cell viability, proliferation and differentiation were tested. Cardiotoxin induced injury was created in tibialis anterior muscles of 28 mice, and two days later, the lesions were treated with 500 impulses of Li-SWT on one of the legs. The treatment was repeated every third day of the period and ended on day 14 after cardiotoxin injection.. The animals were followed up and documented up to 21 days after cardiotoxin injury.

Results

Li-SWT had no significant effect on cell death, proliferation, differentiation and migration, the explants however showed decreased adhesion. In the animal experiments, qPCR studies revealed a significantly increased expression of apoptotic, angiogenic and myogenic genes; expression of Bax, Bcl2, Casp3, eNOS, Pax7, Myf5 and Met was increased in the early phase of regeneration in the Li-SWT treated hind limbs. Furthermore, a late accumulative angiogenic effect was demonstrated in the Li-SWT treated limbs by a significantly increased expression of Angpt1, eNOS, iNOS, Vegfa, and Pecam1.

Conclusion

Treatment was associated with an early upregulation in expression of selected apoptotic, pro-inflammatory, angiogenic and satellite cell activating genes after muscle injury. It also showed a late incremental effect on expression of pro-angiogenic genes. However, we found no changes in the number of PAX7 positive cells or blood vessel density in Li-SWT treated and control muscle. Furthermore, Li-SWT in the selected doses did not decrease survival, proliferation or differentiation of myoblasts in vitro.
Appendix
Available only for authorised users
Literature
1.
go back to reference Skuk D, Tremblay JP. Intramuscular cell transplantation as a potential treatment of myopathies: clinical and preclinical relevant data. Expert Opin Biol Ther. 2011;11:359–74.CrossRefPubMed Skuk D, Tremblay JP. Intramuscular cell transplantation as a potential treatment of myopathies: clinical and preclinical relevant data. Expert Opin Biol Ther. 2011;11:359–74.CrossRefPubMed
2.
go back to reference Fan Y, Maley M, Beilharz M, et al. Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve. 1996;19:853–60.CrossRefPubMed Fan Y, Maley M, Beilharz M, et al. Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve. 1996;19:853–60.CrossRefPubMed
3.
go back to reference Smythe GM, Hodgetts SI, Grounds MD. Immunobiology and the future of myoblast transfer therapy. Molecular therapy : the journal of the American Society of Gene Therapy. 2000;1:304–13.CrossRef Smythe GM, Hodgetts SI, Grounds MD. Immunobiology and the future of myoblast transfer therapy. Molecular therapy : the journal of the American Society of Gene Therapy. 2000;1:304–13.CrossRef
4.
go back to reference Boldrin L, Elvassore N, Malerba A, et al. Satellite cells delivered by micro-patterned scaffolds: a new strategy for cell transplantation in muscle diseases. Tissue Eng. 2007;13:253–62.CrossRefPubMed Boldrin L, Elvassore N, Malerba A, et al. Satellite cells delivered by micro-patterned scaffolds: a new strategy for cell transplantation in muscle diseases. Tissue Eng. 2007;13:253–62.CrossRefPubMed
5.
go back to reference Wolf MT, Dearth CL, Sonnenberg SB, et al. Naturally derived and synthetic scaffolds for skeletal muscle reconstruction. Adv Drug Deliv Rev. 2014; Wolf MT, Dearth CL, Sonnenberg SB, et al. Naturally derived and synthetic scaffolds for skeletal muscle reconstruction. Adv Drug Deliv Rev. 2014;
6.
go back to reference Bramfeldt H, Sabra G, Centis V, et al. Scaffold vascularization: a challenge for three-dimensional tissue engineering. Curr Med Chem. 2010;17:3944–67.CrossRefPubMed Bramfeldt H, Sabra G, Centis V, et al. Scaffold vascularization: a challenge for three-dimensional tissue engineering. Curr Med Chem. 2010;17:3944–67.CrossRefPubMed
7.
go back to reference Suzuki K, Murtuza B, Smolenski RT, et al. Cell transplantation for the treatment of acute myocardial infarction using vascular endothelial growth factor-expressing skeletal myoblasts. Circulation. 2001;104:I207–12.CrossRefPubMed Suzuki K, Murtuza B, Smolenski RT, et al. Cell transplantation for the treatment of acute myocardial infarction using vascular endothelial growth factor-expressing skeletal myoblasts. Circulation. 2001;104:I207–12.CrossRefPubMed
8.
go back to reference Borselli C, Cezar CA, Shvartsman D, et al. The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials. 2011;32:8905–14.CrossRefPubMedPubMedCentral Borselli C, Cezar CA, Shvartsman D, et al. The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials. 2011;32:8905–14.CrossRefPubMedPubMedCentral
10.
go back to reference Wang CJ, Huang HY, Pai CH. Shock wave-enhanced neovascularization at the tendon-bone junction: an experiment in dogs. The Journal of foot and ankle surgery : official publication of the American College of Foot and Ankle Surgeons. 2002;41:16–22.CrossRef Wang CJ, Huang HY, Pai CH. Shock wave-enhanced neovascularization at the tendon-bone junction: an experiment in dogs. The Journal of foot and ankle surgery : official publication of the American College of Foot and Ankle Surgeons. 2002;41:16–22.CrossRef
11.
go back to reference Hausner T, Pajer K, Halat G, et al. Improved rate of peripheral nerve regeneration induced by extracorporeal shock wave treatment in the rat. Exp Neurol. 2012;236:363–70.CrossRefPubMed Hausner T, Pajer K, Halat G, et al. Improved rate of peripheral nerve regeneration induced by extracorporeal shock wave treatment in the rat. Exp Neurol. 2012;236:363–70.CrossRefPubMed
12.
go back to reference Ogden JA, Toth-Kischkat A, Schultheiss R. Principles of shock wave therapy. Clin Orthop Relat Res. 2001:8–17. Ogden JA, Toth-Kischkat A, Schultheiss R. Principles of shock wave therapy. Clin Orthop Relat Res. 2001:8–17.
13.
go back to reference van der Worp H, van den Akker-Scheek I, van Schie H, et al. ESWT for tendinopathy: technology and clinical implications. Knee surgery, sports traumatology, arthroscopy : official journal of the ESSKA. 2013;21:1451–8.CrossRef van der Worp H, van den Akker-Scheek I, van Schie H, et al. ESWT for tendinopathy: technology and clinical implications. Knee surgery, sports traumatology, arthroscopy : official journal of the ESSKA. 2013;21:1451–8.CrossRef
14.
go back to reference Ohl CD, Wolfrum B. Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation. Biochim Biophys Acta. 2003;1624:131–8.CrossRefPubMed Ohl CD, Wolfrum B. Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation. Biochim Biophys Acta. 2003;1624:131–8.CrossRefPubMed
15.
16.
go back to reference Vetrano M, d'Alessandro F, Torrisi MR, et al. Extracorporeal shock wave therapy promotes cell proliferation and collagen synthesis of primary cultured human tenocytes. Knee surgery, sports traumatology, arthroscopy : official journal of the ESSKA. 2011;19:2159–68.CrossRef Vetrano M, d'Alessandro F, Torrisi MR, et al. Extracorporeal shock wave therapy promotes cell proliferation and collagen synthesis of primary cultured human tenocytes. Knee surgery, sports traumatology, arthroscopy : official journal of the ESSKA. 2011;19:2159–68.CrossRef
17.
go back to reference Leone L, Vetrano M, Ranieri D, et al. Extracorporeal shock wave treatment (ESWT) improves in vitro functional activities of ruptured human tendon-derived tenocytes. PLoS One. 2012;7:e49759.CrossRefPubMedPubMedCentral Leone L, Vetrano M, Ranieri D, et al. Extracorporeal shock wave treatment (ESWT) improves in vitro functional activities of ruptured human tendon-derived tenocytes. PLoS One. 2012;7:e49759.CrossRefPubMedPubMedCentral
18.
go back to reference Hofmann A, Ritz U, Hessmann MH, et al. Extracorporeal shock wave-mediated changes in proliferation, differentiation, and gene expression of human osteoblasts. J Trauma. 2008;65:1402–10.CrossRefPubMed Hofmann A, Ritz U, Hessmann MH, et al. Extracorporeal shock wave-mediated changes in proliferation, differentiation, and gene expression of human osteoblasts. J Trauma. 2008;65:1402–10.CrossRefPubMed
19.
go back to reference Zhang X, Yan X, Wang C, et al. The dose-effect relationship in extracorporeal shock wave therapy: the optimal parameter for extracorporeal shock wave therapy. J Surg Res. 2014;186:484–92.CrossRefPubMed Zhang X, Yan X, Wang C, et al. The dose-effect relationship in extracorporeal shock wave therapy: the optimal parameter for extracorporeal shock wave therapy. J Surg Res. 2014;186:484–92.CrossRefPubMed
20.
go back to reference Nurzynska D, Di Meglio F, Castaldo C, et al. Shock waves activate in vitro cultured progenitors and precursors of cardiac cell lineages from the human heart. Ultrasound Med Biol. 2008;34:334–42.CrossRefPubMed Nurzynska D, Di Meglio F, Castaldo C, et al. Shock waves activate in vitro cultured progenitors and precursors of cardiac cell lineages from the human heart. Ultrasound Med Biol. 2008;34:334–42.CrossRefPubMed
21.
go back to reference Yan X, Zeng B, Chai Y, et al. Improvement of blood flow, expression of nitric oxide, and vascular endothelial growth factor by low-energy shockwave therapy in random-pattern skin flap model. Ann Plast Surg. 2008;61:646–53.CrossRefPubMed Yan X, Zeng B, Chai Y, et al. Improvement of blood flow, expression of nitric oxide, and vascular endothelial growth factor by low-energy shockwave therapy in random-pattern skin flap model. Ann Plast Surg. 2008;61:646–53.CrossRefPubMed
22.
go back to reference Mittermayr R, Hartinger J, Antonic V, et al. Extracorporeal shock wave therapy (ESWT) minimizes ischemic tissue necrosis irrespective of application time and promotes tissue revascularization by stimulating angiogenesis. Ann Surg. 2011;253:1024–32.CrossRefPubMed Mittermayr R, Hartinger J, Antonic V, et al. Extracorporeal shock wave therapy (ESWT) minimizes ischemic tissue necrosis irrespective of application time and promotes tissue revascularization by stimulating angiogenesis. Ann Surg. 2011;253:1024–32.CrossRefPubMed
23.
go back to reference Stojadinovic A, Elster EA, Anam K, et al. Angiogenic response to extracorporeal shock wave treatment in murine skin isografts. Angiogenesis. 2008;11:369–80.CrossRefPubMed Stojadinovic A, Elster EA, Anam K, et al. Angiogenic response to extracorporeal shock wave treatment in murine skin isografts. Angiogenesis. 2008;11:369–80.CrossRefPubMed
24.
go back to reference Tepekoylu C, Wang FS, Kozaryn R, et al. Shock wave treatment induces angiogenesis and mobilizes endogenous CD31/CD34-positive endothelial cells in a hindlimb ischemia model: implications for angiogenesis and vasculogenesis. J Thorac Cardiovasc Surg. 2013;146:971–8.CrossRefPubMed Tepekoylu C, Wang FS, Kozaryn R, et al. Shock wave treatment induces angiogenesis and mobilizes endogenous CD31/CD34-positive endothelial cells in a hindlimb ischemia model: implications for angiogenesis and vasculogenesis. J Thorac Cardiovasc Surg. 2013;146:971–8.CrossRefPubMed
25.
go back to reference Krokowicz L, Mielniczuk M, Drews M, et al. Long-term follow up of the effects of extracorporeal shockwave therapy (ESWT) on microcirculation in a denervated muscle flap. Polski przeglad chirurgiczny. 2011;83:325–33.CrossRefPubMed Krokowicz L, Mielniczuk M, Drews M, et al. Long-term follow up of the effects of extracorporeal shockwave therapy (ESWT) on microcirculation in a denervated muscle flap. Polski przeglad chirurgiczny. 2011;83:325–33.CrossRefPubMed
26.
go back to reference Krokowicz L, Cwykiel J, Klimczak A, et al. Pulsed acoustic cellular treatment induces expression of proangiogenic factors and chemokines in muscle flaps. J Trauma. 2010;69:1448–56.CrossRefPubMed Krokowicz L, Cwykiel J, Klimczak A, et al. Pulsed acoustic cellular treatment induces expression of proangiogenic factors and chemokines in muscle flaps. J Trauma. 2010;69:1448–56.CrossRefPubMed
28.
go back to reference Kraus M, Reinhart E, Krause H, et al. Low energy extracorporeal shockwave therapy (ESWT) for treatment of myogelosis of the masseter muscle. Mund-, Kiefer- und Gesichtschirurgie : MKG. 1999;3:20–3.CrossRefPubMed Kraus M, Reinhart E, Krause H, et al. Low energy extracorporeal shockwave therapy (ESWT) for treatment of myogelosis of the masseter muscle. Mund-, Kiefer- und Gesichtschirurgie : MKG. 1999;3:20–3.CrossRefPubMed
29.
go back to reference Gonkova MI, Ilieva EM, Ferriero G, et al. Effect of radial shock wave therapy on muscle spasticity in children with cerebral palsy. International journal of rehabilitation research Internationale Zeitschrift fur Rehabilitationsforschung Revue internationale de recherches de readaptation. 2013;36:284–90.CrossRefPubMed Gonkova MI, Ilieva EM, Ferriero G, et al. Effect of radial shock wave therapy on muscle spasticity in children with cerebral palsy. International journal of rehabilitation research Internationale Zeitschrift fur Rehabilitationsforschung Revue internationale de recherches de readaptation. 2013;36:284–90.CrossRefPubMed
30.
go back to reference Ciccone MM, Notarnicola A, Scicchitano P, et al. Shockwave therapy in patients with peripheral artery disease. Adv Ther. 2012;29:698–707.CrossRefPubMed Ciccone MM, Notarnicola A, Scicchitano P, et al. Shockwave therapy in patients with peripheral artery disease. Adv Ther. 2012;29:698–707.CrossRefPubMed
31.
go back to reference Sellathurai J, Cheedipudi S, Dhawan J, et al. A novel in vitro model for studying quiescence and activation of primary isolated human myoblasts. PLoS One. 2013;8:e64067.CrossRefPubMedPubMedCentral Sellathurai J, Cheedipudi S, Dhawan J, et al. A novel in vitro model for studying quiescence and activation of primary isolated human myoblasts. PLoS One. 2013;8:e64067.CrossRefPubMedPubMedCentral
32.
go back to reference Liu N, Nelson BR, Bezprozvannaya S, et al. Requirement of MEF2A, C, and D for skeletal muscle regeneration. Proc Natl Acad Sci U S A. 2014;111:4109–14.CrossRefPubMedPubMedCentral Liu N, Nelson BR, Bezprozvannaya S, et al. Requirement of MEF2A, C, and D for skeletal muscle regeneration. Proc Natl Acad Sci U S A. 2014;111:4109–14.CrossRefPubMedPubMedCentral
33.
go back to reference Fulda S, Gorman AM, Hori O, et al. Cellular stress responses: cell survival and cell death. International journal of cell biology. 2010;2010:214074.PubMedPubMedCentral Fulda S, Gorman AM, Hori O, et al. Cellular stress responses: cell survival and cell death. International journal of cell biology. 2010;2010:214074.PubMedPubMedCentral
34.
go back to reference Karalaki M, Fili S, Philippou A, et al. Muscle regeneration: cellular and molecular events. In vivo (Athens, Greece). 2009;23:779–96. Karalaki M, Fili S, Philippou A, et al. Muscle regeneration: cellular and molecular events. In vivo (Athens, Greece). 2009;23:779–96.
35.
go back to reference Lefaucheur JP, Sebille A. The cellular events of injured muscle regeneration depend on the nature of the injury. Neuromuscular disorders : NMD. 1995;5:501–9.CrossRefPubMed Lefaucheur JP, Sebille A. The cellular events of injured muscle regeneration depend on the nature of the injury. Neuromuscular disorders : NMD. 1995;5:501–9.CrossRefPubMed
36.
go back to reference Wang CJ, Yang YJ, Huang CC. The effects of shockwave on systemic concentrations of nitric oxide level, angiogenesis and osteogenesis factors in hip necrosis. Rheumatol Int. 2011;31:871–7.CrossRefPubMed Wang CJ, Yang YJ, Huang CC. The effects of shockwave on systemic concentrations of nitric oxide level, angiogenesis and osteogenesis factors in hip necrosis. Rheumatol Int. 2011;31:871–7.CrossRefPubMed
37.
go back to reference Seghezzi G, Patel S, Ren CJ, et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol. 1998;141:1659–73.CrossRefPubMedPubMedCentral Seghezzi G, Patel S, Ren CJ, et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol. 1998;141:1659–73.CrossRefPubMedPubMedCentral
38.
go back to reference Qiu X, Lin G, Xin Z, et al. Effects of low-energy shockwave therapy on the erectile function and tissue of a diabetic rat model. J Sex Med. 2013;10:738–46.CrossRefPubMed Qiu X, Lin G, Xin Z, et al. Effects of low-energy shockwave therapy on the erectile function and tissue of a diabetic rat model. J Sex Med. 2013;10:738–46.CrossRefPubMed
39.
go back to reference Wang CJ, Yang KD, Ko JY, et al. The effects of shockwave on bone healing and systemic concentrations of nitric oxide (NO), TGF-beta1, VEGF and BMP-2 in long bone non-unions. Nitric oxide : biology and chemistry / official journal of the Nitric Oxide Society. 2009;20:298–303.CrossRef Wang CJ, Yang KD, Ko JY, et al. The effects of shockwave on bone healing and systemic concentrations of nitric oxide (NO), TGF-beta1, VEGF and BMP-2 in long bone non-unions. Nitric oxide : biology and chemistry / official journal of the Nitric Oxide Society. 2009;20:298–303.CrossRef
40.
go back to reference Hausdorf J, Sievers B, Schmitt-Sody M, et al. Stimulation of bone growth factor synthesis in human osteoblasts and fibroblasts after extracorporeal shock wave application. Arch Orthop Trauma Surg. 2011;131:303–9.CrossRefPubMed Hausdorf J, Sievers B, Schmitt-Sody M, et al. Stimulation of bone growth factor synthesis in human osteoblasts and fibroblasts after extracorporeal shock wave application. Arch Orthop Trauma Surg. 2011;131:303–9.CrossRefPubMed
41.
go back to reference Chandran R, Knobloch TJ, Anghelina M, et al. Biomechanical signals upregulate myogenic gene induction in the presence or absence of inflammation. American journal of physiology Cell physiology. 2007;293:C267–76.CrossRefPubMedPubMedCentral Chandran R, Knobloch TJ, Anghelina M, et al. Biomechanical signals upregulate myogenic gene induction in the presence or absence of inflammation. American journal of physiology Cell physiology. 2007;293:C267–76.CrossRefPubMedPubMedCentral
42.
go back to reference White CR, Frangos JA. The shear stress of it all: the cell membrane and mechanochemical transduction. Philos Trans R Soc Lond Ser B Biol Sci. 2007;362:1459–67.CrossRef White CR, Frangos JA. The shear stress of it all: the cell membrane and mechanochemical transduction. Philos Trans R Soc Lond Ser B Biol Sci. 2007;362:1459–67.CrossRef
43.
go back to reference Holfeld J, Tepekoylu C, Kozaryn R, et al. Shockwave therapy differentially stimulates endothelial cells: implications on the control of inflammation via toll-like receptor 3. Inflammation. 2014;37:65–70.CrossRefPubMed Holfeld J, Tepekoylu C, Kozaryn R, et al. Shockwave therapy differentially stimulates endothelial cells: implications on the control of inflammation via toll-like receptor 3. Inflammation. 2014;37:65–70.CrossRefPubMed
44.
go back to reference Modulevsky DJ, Tremblay D, Gullekson C, et al. The physical interaction of myoblasts with the microenvironment during remodeling of the cytoarchitecture. PLoS One. 2012;7:e45329.CrossRefPubMedPubMedCentral Modulevsky DJ, Tremblay D, Gullekson C, et al. The physical interaction of myoblasts with the microenvironment during remodeling of the cytoarchitecture. PLoS One. 2012;7:e45329.CrossRefPubMedPubMedCentral
45.
go back to reference Moosavi-Nejad SF, Hosseini SH, Satoh M, et al. Shock wave induced cytoskeletal and morphological deformations in a human renal carcinoma cell line. Cancer Sci. 2006;97:296–304.CrossRefPubMed Moosavi-Nejad SF, Hosseini SH, Satoh M, et al. Shock wave induced cytoskeletal and morphological deformations in a human renal carcinoma cell line. Cancer Sci. 2006;97:296–304.CrossRefPubMed
46.
go back to reference Xu JK, Chen HJ, Li XD, et al. Optimal intensity shock wave promotes the adhesion and migration of rat osteoblasts via integrin beta1-mediated expression of phosphorylated focal adhesion kinase. J Biol Chem. 2012;287:26200–12.CrossRefPubMedPubMedCentral Xu JK, Chen HJ, Li XD, et al. Optimal intensity shock wave promotes the adhesion and migration of rat osteoblasts via integrin beta1-mediated expression of phosphorylated focal adhesion kinase. J Biol Chem. 2012;287:26200–12.CrossRefPubMedPubMedCentral
47.
go back to reference Kuo YR, Wang CT, Wang FS, et al. Extracorporeal shock wave treatment modulates skin fibroblast recruitment and leukocyte infiltration for enhancing extended skin-flap survival. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2009;17:80–7.CrossRef Kuo YR, Wang CT, Wang FS, et al. Extracorporeal shock wave treatment modulates skin fibroblast recruitment and leukocyte infiltration for enhancing extended skin-flap survival. Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society. 2009;17:80–7.CrossRef
48.
go back to reference Smith C, Kruger MJ, Smith RM et al. The inflammatory response to skeletal muscle injury: illuminating complexities. Sports medicine (Auckland, NZ) 2008;38:947–969. Smith C, Kruger MJ, Smith RM et al. The inflammatory response to skeletal muscle injury: illuminating complexities. Sports medicine (Auckland, NZ) 2008;38:947–969.
49.
go back to reference Silvestre JS, Smadja DM, Levy BI. Postischemic revascularization: from cellular and molecular mechanisms to clinical applications. Physiol Rev. 2013;93:1743–802.CrossRefPubMed Silvestre JS, Smadja DM, Levy BI. Postischemic revascularization: from cellular and molecular mechanisms to clinical applications. Physiol Rev. 2013;93:1743–802.CrossRefPubMed
50.
go back to reference Davis TA, Stojadinovic A, Anam K, et al. Extracorporeal shock wave therapy suppresses the early proinflammatory immune response to a severe cutaneous burn injury. Int Wound J. 2009;6:11–21.CrossRefPubMed Davis TA, Stojadinovic A, Anam K, et al. Extracorporeal shock wave therapy suppresses the early proinflammatory immune response to a severe cutaneous burn injury. Int Wound J. 2009;6:11–21.CrossRefPubMed
52.
go back to reference Wozniak AC, Anderson JE. Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Developmental dynamics : an official publication of the American Association of Anatomists. 2007;236:240–50.CrossRef Wozniak AC, Anderson JE. Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Developmental dynamics : an official publication of the American Association of Anatomists. 2007;236:240–50.CrossRef
53.
go back to reference Juffer P, Bakker AD, Klein-Nulend J, et al. Mechanical loading by fluid shear stress of myotube glycocalyx stimulates growth factor expression and nitric oxide production. Cell Biochem Biophys. 2014;69:411–9.CrossRefPubMed Juffer P, Bakker AD, Klein-Nulend J, et al. Mechanical loading by fluid shear stress of myotube glycocalyx stimulates growth factor expression and nitric oxide production. Cell Biochem Biophys. 2014;69:411–9.CrossRefPubMed
54.
go back to reference Lowry JL, Brovkovych V, Zhang Y, et al. Endothelial nitric-oxide synthase activation generates an inducible nitric-oxide synthase-like output of nitric oxide in inflamed endothelium. J Biol Chem. 2013;288:4174–93.CrossRefPubMed Lowry JL, Brovkovych V, Zhang Y, et al. Endothelial nitric-oxide synthase activation generates an inducible nitric-oxide synthase-like output of nitric oxide in inflamed endothelium. J Biol Chem. 2013;288:4174–93.CrossRefPubMed
55.
go back to reference Mariotto S, de Prati AC, Cavalieri E, et al. Extracorporeal shock wave therapy in inflammatory diseases: molecular mechanism that triggers anti-inflammatory action. Curr Med Chem. 2009;16:2366–72.CrossRefPubMed Mariotto S, de Prati AC, Cavalieri E, et al. Extracorporeal shock wave therapy in inflammatory diseases: molecular mechanism that triggers anti-inflammatory action. Curr Med Chem. 2009;16:2366–72.CrossRefPubMed
56.
go back to reference Davis ME, Grumbach IM, Fukai T, et al. Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor kappaB binding. J Biol Chem. 2004;279:163–8.CrossRefPubMed Davis ME, Grumbach IM, Fukai T, et al. Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor kappaB binding. J Biol Chem. 2004;279:163–8.CrossRefPubMed
57.
Metadata
Title
The effect of low intensity shockwave treatment (Li-SWT) on human myoblasts and mouse skeletal muscle
Authors
Lise K. Hansen
Henrik D. Schrøder
Lars Lund
Karthikeyan Rajagopal
Vrisha Maduri
Jeeva Sellathurai
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2017
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-017-1879-4

Other articles of this Issue 1/2017

BMC Musculoskeletal Disorders 1/2017 Go to the issue