Hypoxia Promotes Proliferation of Human Myogenic Satellite Cells: A Potential Benefactor in Tissue Engineering of Skeletal Muscle
Publication: Tissue Engineering Part A
Volume 17, Issue Number 13-14
Abstract
Facial paralysis is a physically, psychologically, and socially disabling condition. Innovative treatment strategies based on regenerative medicine, in particular tissue engineering of skeletal muscle, are promising for treatment of patients with facial paralysis. The natural source for tissue-engineered muscle would be muscle stem cells, that is, human satellite cells (SC). In vivo, SC respond to hypoxic, ischemic muscle damage by activation, proliferation, differentiation to myotubes, and maturation to muscle fibers, while maintaining their reserve pool of SC. Therefore, our hypothesis is that hypoxia improves proliferation and differentiation of SC. During tissue engineering, a three-dimensional construct, or implanting SC in vivo, SC will encounter hypoxic environments. Thus, we set out to test our hypothesis on SC in vitro. During the first five passages, hypoxically cultured SC proliferated faster than their counterparts under normoxia. Moreover, also at higher passages, a switch from normoxia to hypoxia enhanced proliferation of SC. Hypoxia did not affect the expression of SC markers desmin and NCAM. However, the average surface expression per cell of NCAM was downregulated by hypoxia, and it also downregulated the gene expression of NCAM. The gene expression of the myogenic transcription factors PAX7, MYF5, and MYOD was upregulated by hypoxia. Moreover, gene expression of structural proteins α-sarcomeric actin, and myosins MYL1 and MYL3 was upregulated by hypoxia during differentiation. This indicates that hypoxia promotes a promyogenic shift in SC. Finally, Pax7 expression was not influenced by hypoxia and maintained in a subset of mononucleated cells, whereas these cells were devoid of structural muscle proteins. This suggests that during myogenesis in vitro, at least part of the SC adopt a quiescent, that is, reserve cells, phenotype. In conclusion, tissue engineering under hypoxic conditions would seem favorable in terms of myogenic proliferation, while maintaining the quiescent SC pool.
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References
1.
Terng S.C.Rijnders W.Kon M.Werker P.M. [Custom-made gold plate prosthesis in the upper eyelid in patients with facial paralysis: improved eyelid closure with less effects on other eye complaints]Nederlands tijdschrift voor geneeskunde1448002000. 1. Terng, S.C., Rijnders, W., Kon, M., and Werker, P.M. [Custom-made gold plate prosthesis in the upper eyelid in patients with facial paralysis: improved eyelid closure with less effects on other eye complaints]. Nederlands tijdschrift voor geneeskunde 144, 800, 2000.
2.
Werker P.M. [Plastic surgery in patients with facial palsy]Nederlands tijdschrift voor geneeskunde1512872007. 2. Werker, P.M. [Plastic surgery in patients with facial palsy]. Nederlands tijdschrift voor geneeskunde 151, 287, 2007.
3.
Terzis J.K.Karypidis D. Blink restoration in adult facial paralysisPlast Reconstr Surg1261262010. 3. Terzis, J.K., and Karypidis, D. Blink restoration in adult facial paralysis. Plast Reconstr Surg 126, 126, 2010.
4.
May M.Klein S.R. Differential diagnosis of facial nerve palsyOtolaryngol Clin North Am246131991. 4. May, M., and Klein, S.R. Differential diagnosis of facial nerve palsy. Otolaryngol Clin North Am 24, 613, 1991.
5.
Nicolai J.P. Autostatic syndrome in association with facial nerve transplantationPlast Reconstr Surg11219632003. 5. Nicolai, J.P. Autostatic syndrome in association with facial nerve transplantation. Plast Reconstr Surg 112, 1963, 2003.
6.
Borschel G.H.Dow D.E.Dennis R.G.Brown D.L. Tissue-engineered axially vascularized contractile skeletal musclePlast Reconstr Surg11722352006. 6. Borschel, G.H., Dow, D.E., Dennis, R.G., and Brown, D.L. Tissue-engineered axially vascularized contractile skeletal muscle. Plast Reconstr Surg 117, 2235, 2006.
7.
Bach A.D.Arkudas A.Tjiawi J.Polykandriotis E.Kneser U.Horch R.E.Beier J.P. A new approach to tissue engineering of vascularized skeletal muscleJ Cell Mol Med107162006. 7. Bach, A.D., Arkudas, A., Tjiawi, J., Polykandriotis, E., Kneser, U., Horch, R.E., and Beier, J.P. A new approach to tissue engineering of vascularized skeletal muscle. J Cell Mol Med 10, 716, 2006.
8.
Yang J.Yamato M.Shimizu T.Sekine H.Ohashi K.Kanzaki M.Ohki T.Nishida K.Okano T. Reconstruction of functional tissues with cell sheet engineeringBiomaterials2850332007. 8. Yang, J., Yamato, M., Shimizu, T., Sekine, H., Ohashi, K., Kanzaki, M., Ohki, T., Nishida, K., and Okano, T. Reconstruction of functional tissues with cell sheet engineering. Biomaterials 28, 5033, 2007.
9.
Shimizu T.Sekine H.Yang J.Isoi Y.Yamato M.Kikuchi A.Kobayashi E.Okano T. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissuesThe FASEB J207082006. 9. Shimizu, T., Sekine, H., Yang, J., Isoi, Y., Yamato, M., Kikuchi, A., Kobayashi, E., and Okano, T. Polysurgery of cell sheet grafts overcomes diffusion limits to produce thick, vascularized myocardial tissues. The FASEB J 20, 708, 2006.
10.
Levenberg S.Rouwkema J.Macdonald M.Garfein E.S.Kohane D.S.Darland D.C.Marini R.van Blitterswijk C.A.Mulligan R.C.D'Amore P.A.Langer R. Engineering vascularized skeletal muscle tissueNat Biotechnol238792005. 10. Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E.S., Kohane, D.S., Darland, D.C., Marini, R., van Blitterswijk, C.A., Mulligan, R.C., D'Amore, P.A., and Langer, R. Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23, 879, 2005.
11.
Wagner S.Dorchies O.M.Stoeckel H.Warter J.M.Poindron P.Takeda K. Functional maturation of nicotinic acetylcholine receptors as an indicator of murine muscular differentiation in a new nerve-muscle co-culture systemPflugers Arch447142003. 11. Wagner, S., Dorchies, O.M., Stoeckel, H., Warter, J.M., Poindron, P., and Takeda, K. Functional maturation of nicotinic acetylcholine receptors as an indicator of murine muscular differentiation in a new nerve-muscle co-culture system. Pflugers Arch 447, 14, 2003.
12.
Larkin L.M.Van der Meulen J.H.Dennis R.G.Kennedy J.B. Functional evaluation of nerve-skeletal muscle constructs engineered in vitroIn Vitro Cell Dev Biol Anim42752006. 12. Larkin, L.M., Van der Meulen, J.H., Dennis, R.G., and Kennedy, J.B. Functional evaluation of nerve-skeletal muscle constructs engineered in vitro. In Vitro Cell Dev Biol Anim 42, 75, 2006.
13.
Liao H.Zhou G.Q. Development and progress of engineering of skeletal muscle tissueTissue Eng B Rev153192009. 13. Liao, H., and Zhou, G.Q. Development and progress of engineering of skeletal muscle tissue. Tissue Eng B Rev 15, 319, 2009.
14.
Koning M.Harmsen M.C.van Luyn M.J.Werker P.M. Current opportunities and challenges in skeletal muscle tissue engineeringJ Tissue Eng Regen Med34072009. 14. Koning, M., Harmsen, M.C., van Luyn, M.J., and Werker, P.M. Current opportunities and challenges in skeletal muscle tissue engineering. J Tissue Eng Regen Med 3, 407, 2009.
15.
Le G.F.Rudnicki M.A. Skeletal muscle satellite cells and adult myogenesisCurr Opin Cell Biol196282007. 15. Le, G.F., and Rudnicki, M.A. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19, 628, 2007.
16.
Ten Broek R.W.Grefte S.Von den Hoff J.W. Regulatory factors and cell populations involved in skeletal muscle regenerationJ Cell Physiol22472010. 16. Ten Broek, R.W., Grefte, S., and Von den Hoff, J.W. Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 224, 7, 2010.
17.
Buckingham M.Montarras D. Skeletal muscle stem cellsCurr Opin Genet Dev183302008. 17. Buckingham, M., and Montarras, D. Skeletal muscle stem cells. Curr Opin Genet Dev 18, 330, 2008.
18.
Charge S.B.Rudnicki M.A. Cellular and molecular regulation of muscle regenerationPhysiol Rev842092004. 18. Charge, S.B., and Rudnicki, M.A. Cellular and molecular regulation of muscle regeneration. Physiol Rev 84, 209, 2004.
19.
Bouchentouf M.Benabdallah B.F.Bigey P.Yau T.M.Scherman D.Tremblay J.P. Vascular endothelial growth factor reduced hypoxia-induced death of human myoblasts and improved their engraftment in mouse musclesGene Ther154042008. 19. Bouchentouf, M., Benabdallah, B.F., Bigey, P., Yau, T.M., Scherman, D., and Tremblay, J.P. Vascular endothelial growth factor reduced hypoxia-induced death of human myoblasts and improved their engraftment in mouse muscles. Gene Ther 15, 404, 2008.
20.
Hayot M.Rodriguez J.Vernus B.Carnac G.Jean E.Allen D.Goret L.Obert P.Candau R.Bonnieu A. Myostatin up-regulation is associated with the skeletal muscle response to hypoxic stimuliMol Cell Endocrinol332382011. 20. Hayot, M., Rodriguez, J., Vernus, B., Carnac, G., Jean, E., Allen, D., Goret, L., Obert, P., Candau, R., and Bonnieu, A. Myostatin up-regulation is associated with the skeletal muscle response to hypoxic stimuli. Mol Cell Endocrinol 332, 38, 2011.
21.
Hu X.Yu S.P.Fraser J.L.Lu Z.Ogle M.E.Wang J.A.Wei L. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesisJ Thorac Cardiovasc Surg1357992008. 21. Hu, X., Yu, S.P., Fraser, J.L., Lu, Z., Ogle, M.E., Wang, J.A., and Wei, L. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg 135, 799, 2008.
22.
Kook S.H.Son Y.O.Lee K.Y.Lee H.J.Chung W.T.Choi K.C.Lee J.C. Hypoxia affects positively the proliferation of bovine satellite cells and their myogenic differentiation through up-regulation of MyoDCell Biol Int328712008. 22. Kook, S.H., Son, Y.O., Lee, K.Y., Lee, H.J., Chung, W.T., Choi, K.C., and Lee, J.C. Hypoxia affects positively the proliferation of bovine satellite cells and their myogenic differentiation through up-regulation of MyoD. Cell Biol Int 32, 871, 2008.
23.
Menasche P.Alfieri O.Janssens S.McKenna W.Reichenspurner H.Trinquart L.Vilquin J.T.Marolleau J.P.Seymour B.Larghero J.Lake S.Chatellier G.Solomon S.Desnos M.Hagege A.A. The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantationCirculation11711892008. 23. Menasche, P., Alfieri, O., Janssens, S., McKenna, W., Reichenspurner, H., Trinquart, L., Vilquin, J.T., Marolleau, J.P., Seymour, B., Larghero, J., Lake, S., Chatellier, G., Solomon, S., Desnos, M., and Hagege, A.A. The myoblast autologous grafting in ischemic cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117, 1189, 2008.
24.
Csete M.Walikonis J.Slawny N.Wei Y.Korsnes S.Doyle J.C.Wold B. Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in cultureJ Cell Physiol1891892001. 24. Csete, M., Walikonis, J., Slawny, N., Wei, Y., Korsnes, S., Doyle, J.C., and Wold, B. Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J Cell Physiol 189, 189, 2001.
25.
Chakravarthy M.V.Spangenburg E.E.Booth F.W. Culture in low levels of oxygen enhances in vitro proliferation potential of satellite cells from old skeletal musclesCell Mol Life Sci5811502001. 25. Chakravarthy, M.V., Spangenburg, E.E., and Booth, F.W. Culture in low levels of oxygen enhances in vitro proliferation potential of satellite cells from old skeletal muscles. Cell Mol Life Sci 58, 1150, 2001.
26.
Sinanan A.C.Hunt N.P.Lewis M.P. Human adult craniofacial muscle-derived cells: neural-cell adhesion-molecule (NCAM; CD56)-expressing cells appear to contain multipotential stem cellsBiotechnol Appl Biochem40252004. 26. Sinanan, A.C., Hunt, N.P., and Lewis, M.P. Human adult craniofacial muscle-derived cells: neural-cell adhesion-molecule (NCAM; CD56)-expressing cells appear to contain multipotential stem cells. Biotechnol Appl Biochem 40, 25, 2004.
27.
McLoon L.K.Wirtschafter J.D. N-CAM is expressed in mature extraocular muscles in a pattern conserved among three speciesInvest Ophthalmol Vis Sci373181996. 27. McLoon, L.K., and Wirtschafter, J.D. N-CAM is expressed in mature extraocular muscles in a pattern conserved among three species. Invest Ophthalmol Vis Sci 37, 318, 1996.
28.
Brady M.A.Lewis M.P.Mudera V. Synergy between myogenic and non-myogenic cells in a 3D tissue-engineered craniofacial skeletal muscle constructJ Tissue Eng Regen Med24082008. 28. Brady, M.A., Lewis, M.P., and Mudera, V. Synergy between myogenic and non-myogenic cells in a 3D tissue-engineered craniofacial skeletal muscle construct. J Tissue Eng Regen Med 2, 408, 2008.
29.
Yun Z.Lin Q.Giaccia A.J. Adaptive myogenesis under hypoxiaMol Cell Biol2530402005. 29. Yun, Z., Lin, Q., and Giaccia, A.J. Adaptive myogenesis under hypoxia. Mol Cell Biol 25, 3040, 2005.
30.
Di C.A.De M.R.Martelli F.Pompilio G.Capogrossi M.C.Germani A. Hypoxia inhibits myogenic differentiation through accelerated MyoD degradationJ Biol Chem279163322004. 30. Di, C.A., De, M.R., Martelli, F., Pompilio, G., Capogrossi, M.C., and Germani, A. Hypoxia inhibits myogenic differentiation through accelerated MyoD degradation. J Biol Chem 279, 16332, 2004.
31.
Kuang S.Rudnicki M.A. The emerging biology of satellite cells and their therapeutic potentialTrends Mol Med14822008. 31. Kuang, S., and Rudnicki, M.A. The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14, 82, 2008.
32.
Kallestad K.M.McLoon L.K. Defining the heterogeneity of skeletal muscle-derived side and main population cells isolated immediately ex vivoJ Cell Physiol2226762010. 32. Kallestad, K.M., and McLoon, L.K. Defining the heterogeneity of skeletal muscle-derived side and main population cells isolated immediately ex vivo. J Cell Physiol 222, 676, 2010.
33.
Biressi S.Rando T.A. Heterogeneity in the muscle satellite cell populationSemin Cell Dev Biol218452010. 33. Biressi, S., and Rando, T.A. Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 21, 845, 2010.
34.
McLoon L.K.Thorstenson K.M.Solomon A.Lewis M.P. Myogenic precursor cells in craniofacial musclesOral Dis131342007. 34. McLoon, L.K., Thorstenson, K.M., Solomon, A., and Lewis, M.P. Myogenic precursor cells in craniofacial muscles. Oral Dis 13, 134, 2007.
35.
Gopinath S.D.Rando T.A. Stem cell review series: aging of the skeletal muscle stem cell nicheAging Cell75902008. 35. Gopinath, S.D., and Rando, T.A. Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell 7, 590, 2008.
36.
Corbu A.Scaramozza A.Badiali-DeGiorgi L.Tarantino L.Papa V.Rinaldi R.D'Alessandro R.Zavatta M.Laus M.Lattanzi G.Cenacchi G. Satellite cell characterization from aging human muscleNeurol Res32632010. 36. Corbu, A., Scaramozza, A., Badiali-DeGiorgi, L., Tarantino, L., Papa, V., Rinaldi, R., D'Alessandro, R., Zavatta, M., Laus, M., Lattanzi, G., and Cenacchi, G. Satellite cell characterization from aging human muscle. Neurol Res 32, 63, 2010.
37.
Carosio S.Berardinelli M.G.Aucello M.Musaro A. Impact of ageing on muscle cell regenerationAgeing Res Rev10352011. 37. Carosio, S., Berardinelli, M.G., Aucello, M., and Musaro, A. Impact of ageing on muscle cell regeneration. Ageing Res Rev 10, 35, 2011.
38.
Carnac G.Fajas L.L'honore A.Sardet C.Lamb N.J.Fernandez A. The retinoblastoma-like protein p130 is involved in the determination of reserve cells in differentiating myoblastsCurr Biol105432000. 38. Carnac, G., Fajas, L., L'honore, A., Sardet, C., Lamb, N.J., and Fernandez, A. The retinoblastoma-like protein p130 is involved in the determination of reserve cells in differentiating myoblasts. Curr Biol 10, 543, 2000.
39.
Sacco A.Doyonnas R.Kraft P.Vitorovic S.Blau H.M. Self-renewal and expansion of single transplanted muscle stem cellsNature4565022008. 39. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S., and Blau, H.M. Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502, 2008.
40.
Rossi C.A.Pozzobon M.Ditadi A.Archacka K.Gastaldello A.Sanna M.Franzin C.Malerba A.Milan G.Cananzi M.Schiaffino S.Campanella M.Vettor R.De C.P. Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneityPLoS One5e85232010. 40. Rossi, C.A., Pozzobon, M., Ditadi, A., Archacka, K., Gastaldello, A., Sanna, M., Franzin, C., Malerba, A., Milan, G., Cananzi, M., Schiaffino, S., Campanella, M., Vettor, R., and De, C.P. Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity. PLoS One 5, e8523, 2010.
41.
Friday B.B.Pavlath G.K. A calcineurin- and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cellsJ Cell Sci1143032001. 41. Friday, B.B., and Pavlath, G.K. A calcineurin- and NFAT-dependent pathway regulates Myf5 gene expression in skeletal muscle reserve cells. J Cell Sci 114, 303, 2001.
42.
Cao Y.Zhao Z.Gruszczynska-Biegala J.Zolkiewska A. Role of metalloprotease disintegrin ADAM12 in determination of quiescent reserve cells during myogenic differentiation in vitroMol Cell Biol2367252003. 42. Cao, Y., Zhao, Z., Gruszczynska-Biegala, J., and Zolkiewska, A. Role of metalloprotease disintegrin ADAM12 in determination of quiescent reserve cells during myogenic differentiation in vitro. Mol Cell Biol 23, 6725, 2003.
43.
Kitzmann M.Bonnieu A.Duret C.Vernus B.Barro M.Laoudj-Chenivesse D.Verdi J.M.Carnac G. Inhibition of notch signaling induces myotube hypertrophy by recruiting a subpopulation of reserve cellsJ Cell Physiol2085382006. 43. Kitzmann, M., Bonnieu, A., Duret, C., Vernus, B., Barro, M., Laoudj-Chenivesse, D., Verdi, J.M., and Carnac, G. Inhibition of notch signaling induces myotube hypertrophy by recruiting a subpopulation of reserve cells. J Cell Physiol 208, 538, 2006.
44.
Jacquemin V.Butler-Browne G.S.Furling D.Mouly V. IL-13 mediates the recruitment of reserve cells for fusion during IGF-1-induced hypertrophy of human myotubesJ Cell Sci1206702007. 44. Jacquemin, V., Butler-Browne, G.S., Furling, D., and Mouly, V. IL-13 mediates the recruitment of reserve cells for fusion during IGF-1-induced hypertrophy of human myotubes. J Cell Sci 120, 670, 2007.
45.
Rapizzi E.Donati C.Cencetti F.Nincheri P.Bruni P. Sphingosine 1-phosphate differentially regulates proliferation of C2C12 reserve cells and myoblastsMol Cell Biochem3141932008. 45. Rapizzi, E., Donati, C., Cencetti, F., Nincheri, P., and Bruni, P. Sphingosine 1-phosphate differentially regulates proliferation of C2C12 reserve cells and myoblasts. Mol Cell Biochem 314, 193, 2008.
46.
Stuelsatz P.Pouzoulet F.Lamarre Y.Dargelos E.Poussard S.Leibovitch S.Cottin P.Veschambre P. Down-regulation of MyoD by calpain 3 promotes generation of reserve cells in C2C12 myoblastsJ Biol Chem285126702010. 46. Stuelsatz, P., Pouzoulet, F., Lamarre, Y., Dargelos, E., Poussard, S., Leibovitch, S., Cottin, P., and Veschambre, P. Down-regulation of MyoD by calpain 3 promotes generation of reserve cells in C2C12 myoblasts. J Biol Chem 285, 12670, 2010.
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Published In
Tissue Engineering Part A
Volume 17 • Issue Number 13-14 • July 2011
Pages: 1747 - 1758
PubMed: 21438665
Copyright
Copyright 2011, Mary Ann Liebert, Inc.
History
Published in print: July 2011
Published ahead of print: 25 March 2011
Published online: 23 March 2011
Accepted: 8 February 2011
Received: 29 October 2010
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