Murine and human myogenic cells identified by elevated aldehyde dehydrogenase activity: Implications for muscle regeneration and repair

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Vella, Joseph B ^a,b   Thompson, Seth D ^a   Bucsek, Mark J ^a,b   Song, Minjung ^a   Huard, Johnny ^a,b,c  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b University of Pittsburgh   (United States)

^c MCGOWAN INSTITUTE FOR REGENERATIVE MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; GLUTATHIONE; SUPEROXIDE DISMUTASE; ANTIOXIDANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE CONTRACTURE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MUSCLE STRESS; MYOBLAST; NONHUMAN; SKELETAL MUSCLE; ADULT; AGED; ANIMAL; BONE DEVELOPMENT; C57BL MOUSE; CELL SEPARATION; CHONDROGENESIS; CYTOLOGY; ENZYMOLOGY; FLOW CYTOMETRY; METABOLISM; MIDDLE AGED; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REGENERATION; WOUND HEALING;

ADULT; AGED; ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIOXIDANTS; CELL PROLIFERATION; CELL SEPARATION; CHONDROGENESIS; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MUSCLE CELLS; MUSCLE, SKELETAL; MYOBLASTS; OSTEOGENESIS; REGENERATION; STRESS, PHYSIOLOGICAL; WOUND HEALING;

EID: 83455213328     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029226     Document Type: Article

References (86)

1. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, et al. (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355: 696-702.
2. Zubrzycka-Gaarn EE, Bulman DE, Karpati G, Burghes AH, Belfall B, et al. (1988) The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle. Nature 333: 466-469.
3. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, et al. (2010) Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 9: 77-93.
4. Bushby K, Finkel R, Birnkrant DJ, Case LE, Clemens PR, et al. (2010) Diagnosis and management of Duchenne muscular dystrophy, part 2: implementation of multidisciplinary care. Lancet Neurol 9: 177-189.
5. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, et al. (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15: 867-877.
6. Skuk D, Paradis M, Goulet M, Tremblay JP, (2007) Ischemic central necrosis in pockets of transplanted myoblasts in nonhuman primates: implications for cell-transplantation strategies. Transplantation 84: 1307-1315.
7. Gussoni E, Blau HM, Kunkel LM, (1997) The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med 3: 970-977.
8. Skuk D, Tremblay JP, (2011) Intramuscular cell transplantation as a potential treatment of myopathies: clinical and preclinical relevant data. Expert Opinion on Biological Therapy 11: 359-374.
9. Urish KL, Vella JB, Okada M, Deasy BM, Tobita K, et al. (2009) Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol Biol Cell 20: 509-520.
10. Zheng B, Cao BH, Crisan M, Sun B, Li GH, et al. (2007) Prospective identification of myogenic endothelial cells in human skeletal muscle. Nature Biotechnology 25: 1025-1034.
11. Drowley L, Okada T, Beckman S, Vella JB, Keller BB, et al. (2010) Cellular Antioxidant Levels Influence Muscle Stem Cell Therapy. Molecular Therapy 18: 1865-1873.
12. Gharaibeh B, Lu A, Tebbets JC, Zheng B, Feduska JM, et al. (2008) Isolation of a slowly adhering cell fraction containing stems cells from murine skeletal muscle by the preplate technique. Nature Protocols 3: 1501-1509.
13. Cerletti M, Molloy MJ, Tomczak KK, Yoon S, Ramoni MF, et al. (2006) Melanoma cell adhesion molecule is a novel marker for human fetal myogenic cells and affects myoblast fusion. J Cell Sci 119: 3117-3127.
14. Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, et al. (2008) Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134: 37-47.
15. Meng J, Muntoni F, Morgan JE, (2011) Stem cells to treat muscular dystrophies- where are we? Neuromuscul Disord 21: 4-12.
16. Vauchez K, Marolleau J-P, Schmid M, Khattar P, Chapel A, et al. (2009) Aldehyde Dehydrogenase Activity Identifies a Population of Human Skeletal Muscle Cells With High Myogenic Capacities. Mol Ther 17: 1948-1958.
17. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, et al. (2002) Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 157: 851-864.
18. Beauchamp JR, Morgan JE, Pagel CN, Partridge TA, (1994) Quantitative studies of efficacy of myoblast transplantation. Muscle Nerve 18 (Suppl): 261.
19. Huard J, Acsadi G, Jani A, Massie B, Karpati G, (1994) Gene transfer into skeletal muscles by isogenic myoblasts. Hum Gene Ther 5: 949-958.
20. Guerette B, Skuk D, Celestin F, Huard J, Tardif F, et al. (1997) Prevention by anti-LFA-1 of acute myoblast death following transplantation. J Immunol 159: 2522-2531.
21. Skuk D, Caron NJ, Goulet M, Roy B, Tremblay JP, (2003) Resetting the problem of cell death following muscle-derived cell transplantation: detection, dynamics and mechanisms. J Neuropathol Exp Neurol 62: 951-967.
22. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, et al. (2002) A stem cell molecular signature. Science 298: 601-604.
23. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA, (2002) "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298: 597-600.
24. Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, et al. (2004) Antioxidative stress-associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104: 3591-3597.
25. Fulle S, Di Donna S, Puglielli C, Pietrangelo T, Beccafico S, et al. (2005) Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol 40: 189-197.
26. Ryan T, Liu J, Chu A, Wang L, Blais A, et al. (2011) Retinoic Acid Enhances Skeletal Myogenesis in Human Embryonic Stem Cells by Expanding the Premyogenic Progenitor Population. Stem Cell Reviews and Reports pp. 1-12.
27. Edwards M, McBurney M, (1983) The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol 98: 187-191.
28. Froeschle A, Alric S, Kitzmann M, Carnac G, Aurade F, et al. (1998) Retinoic acid receptors and muscle b-HLH proteins: partners in retinoid- induced myogenesis. Oncogene 16: 3369-3378.
29. Kennedy K, Porter T, Mehta V, Ryan S, Price F, et al. (2009) Retinoic acid enhances skeletal muscle progenitor formation and bypasses inhibition by bone morphogenetic protein 4 but not dominant negative beta-catenin. BMC Biology 7: 67.
30. Douville J, Beaulieu R, Balicki D, (2009) ALDH1 as a Functional Marker of Cancer Stem and Progenitor Cells Stem Cells and Development 18: 17-25.
31. Storms RW, Green PD, Safford KM, Niedzwiecki D, Cogle CR, et al. (2005) Distinct hematopoietic progenitor compartments are delineated by the expression of aldehyde dehydrogenase and CD34. Blood 106: 95-102.
32. Hess DA, Meyerrose TE, Wirthlin L, Craft TP, Herrbrich PE, et al. (2004) Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 104: 1648-1655.
33. Gentry T, Foster S, Winstead L, Deibert E, Fiordalisi M, et al. (2007) Simultaneous isolation of human BM hematopoietic, endothelial and mesenchymal progenitor cells by flow sorting based on aldehyde dehydrogenase activity: implications for cell therapy. Cytotherapy 9: 259-274.
34. Capoccia BJ, Robson DL, Levac KD, Maxwell DJ, Hohm SA, et al. (2009) Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity. Blood 113: 5340-5351.
35. Corti S, Locatelli F, Papadimitriou D, Donadoni C, Salani S, et al. (2006) Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cells 24: 975-985.
36. Cai J, Cheng A, Luo Y, Lu C, Mattson MP, et al. (2004) Membrane properties of rat embryonic multipotent neural stem cells. J Neurochem 88: 212-226.
37. Jean E, Laoudj-Chenivesse D, Notarnicola C, Rouger K, Serratrice N, et al. (2011) Aldehyde dehydrogenase activity promotes survival of human muscle precursor cells. J Cell Mol Med 15: 119-133.
38. Ma I, Allan, L A, (2011) The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev 7: 292-306.
39. Makia NL, Bojang P, Falkner KC, Conklin DJ, Prough RA, (2011) Murine hepatic aldehyde dehydrogenase 1a1 is a major contributor to oxidation of aldehydes formed by lipid peroxidation. Chemico-Biological Interactions 191: 278-287.
40. Ogasawara MA, Zhang H, (2008) Redox Regulation and its Emerging Roles in Stem Cells and Stem-Like Cancer Cells. Antioxid Redox Signal 11: 1107-1122.
41. Lassen N, Bateman JB, Estey T, Kuszak JR, Nees DW, et al. (2007) Multiple and additive functions of ALDH3A1 and ALDH1A1: cataract phenotype and ocular oxidative damage in Aldh3a1(-/-)/Aldh1a1(-/-) knock-out mice. J Biol Chem 282: 25668-25676.
42. Kops GJPL, Dansen TB, Polderman PE, Saarloos I, Wirtz KWA, et al. (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419: 316-321.
43. Tran H, Brunet A, Grenier JM, Datta SR, Fornace AJ Jr, et al. (2002) DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296: 530-534.
44. Cai H, Gehrig P, Scott TM, Zimmermann R, Schlapbach R, et al. (2006) MnSOD marks cord blood late outgrowth endothelial cells and accompanies robust resistance to oxidative stress. Biochem Biophys Res Commun 350: 364-369.
45. Nagano M, Yamashita T, Hamada H, Ohneda K, Kimura KI, et al. (2007) Identification of functional endothelial progenitor cells suitable for the treatment of ischemic tissue using human umbilical cord blood. Blood 110: 151-160.
46. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, et al. (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells Nature 458: 780-785.
47. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
48. Ginestier C, Wicinski J, Cervera N, Monville F, Finetti P, et al. (2009) Retinoid signaling regulates breast cancer stem cell differentiation. Cell Cycle 8: 3297-3302.
49. Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, et al. (1999) Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci U S A 96: 9118-9123.
50. Qu Z, Huard J, (2000) Matching host muscle and donor myoblasts for myosin heavy chain improves myoblast transfer therapy. Gene Ther 7: 428-437.
51. Jankowski RJ, Haluszczak C, Trucco M, Huard J, (2001) Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells. Hum Gene Ther 12: 619-628.
52. Kumar V, Abbas AK, Fausto N, (2005) Acute and Chronic Inflammation. In: Kumar V, Abbas AK, Fausto N, editors. Robbins and Cotran: Pathologic Basis of Disease. 7th ed Philadelphia Elsevier pp. 48-78.
53. Guttridge DC, Mayo MW, Madrid LV, Wang C-Y Jr, ASB (2000) NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289: 2363-2366.
54. Li Y-p, Scwartz RJ, Waddell ID, Holloway BR, Reid MB, (1998) Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kB activation in response to tumor necrosis factor a Faseb J 12: 871-880.
55. Jankowski RJ, Deasy BM, Cao B, Gates C, Huard J, (2002) The role of CD34 expression and cellular fusion in the regeneration capacity of myogenic progenitor cells. J Cell Sci 115: 4361-4374.
56. Fink MP, Macias CA, Xiao J, Tyurina YY, Delude RL, et al. (2007) Hemigramicidin-TEMPO conjugates: novel mitochondria-targeted antioxidants. Crit Care Med 35: S461-467.
57. Chen Ha, Zhoua L, Lina C-Y, Beattiea MC, et al. (2010) Effect of glutathione redox state on Leydig cell susceptibility to acute oxidative stress. Molecular and Cellular Endocrinology 323: 147-154.
58. Hayes JD, McLellan LI, (1999) Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 31: 273-300.
59. Halevy O, Lerman O, (1993) Retinoic acid induces adult muscle cell differentiation mediated by the retinoic acid receptor-α. Journal of Cellular Physiology 154: 566-572.
60. Gazit D, Turgeman G, Kelley P, Wang E, Jalenak M, et al. (1999) Engineered pluripotent mesenchymal cells integrate and differentiate in regenerating bone: a novel cell-mediated gene therapy. J Gene Med 1: 121-133.
61. Zhang W, Deng Z-L, Chen L, Zuo G-W, Luo Q, et al. (2010) Retinoic Acids Potentiate BMP9-Induced Osteogenic Differentiation of Mesenchymal Progenitor Cells. PLoS ONE 5: e11917.
62. Cash DE, Bock CB, Schughart K, Linney E, Underhill TM, (1997) Retinoic Acid Receptor α Function in Vertebrate Limb Skeletogenesis: a Modulator of Chondrogenesis. Journal of Cell Biology 136: 445-457.
63. Von Schroeder HP, Hashimoto Y, Heersche JN, (1994) The effects of natural and synthetic retinoids on the differentiation of RCJ C5.18 chondrogenic cells. Teratology 50: 54-62.
64. Shen X, Collier JM, Hlaing M, Zhang L, Delshad EH, et al. (2003) Genome-wide examination of myoblast cell cycle withdrawal during differentiation. Developmental Dynamics 226: 128-138.
65. Wang J, Walsh K, (1996) Resistance to apoptosis conferred by cdk inhibitors during myocyte differentiation. Science 273: 359-361.
66. Bouchentouf M, Skuk D, Tremblay JP, (2007) Early and massive death of myloblasts transplanted into skeletal muscle: responsible factors and potential solutions. Current Opinion in Organ Transplantation 12: 664-667.
67. Tidball JG, (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288: R345-353.
68. Bottino R, Balamurugan AN, Bertera S, Pietropaolo M, Trucco M, et al. (2002) Preservation of human islet cell functional mass by anti-oxidative action of a novel SOD mimic compound. Diabetes 51: 2561-2567.
69. Van den Brink MRM, Burakoff SJ, (2002) Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol 2: 273-281.
70. Haider HK, Ashraf M, (2008) Strategies to promote donor cell survival: Combining preconditioning approach with stem cell transplantation. Journal of Molecular and Cellular Cardiology 45: 554-566.
71. Balber AE, (2011) Concise review: aldehyde dehydrogenase bright stem and progenitor cell populations from normal tissues: characteristics, activities, and emerging uses in regenerative medicine. Stem Cells 29: 570-575.
72. Edwards MK, McBurney MW, (1983) The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol 98: 187-191.
73. Gazit D, Ebner R, Kahn AJ, Derynck R, (1993) Modulation of expression and cell surface binding of members of the transforming growth factor-beta superfamily during retinoic acid-induced osteoblastic differentiation of multipotential mesenchymal cells. Molecular Endocrinology 7: 189-198.
74. Skillington J, Choy L, Derynck R, (2002) Bone morphogenetic protein and retinoic acid signaling cooperate to induce osteoblast differentiation of preadipocytes. J Cell Biol 159: 135-146.
75. Grossmann J, (2002) Molecular mechanisms of "detachment-induced apoptosis-Anoikis". Apoptosis 7: 247-260.
76. Qu ZQ, Balkir L, van Deutekom JCT, Robbins PD, Pruchnic R, et al. (1998) Development of approaches to improve cell survival in myoblast transfer therapy. Journal of Cell Biology 142: 1257-1267.
77. Oshima H, Payne TR, Urish KL, Sakai T, Ling Y, et al. (2005) Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Ther 12: 1130-1141.
78. Richler C, Yaffe D, (1970) The in vitro cultivation and differentiation capacities of myogenic cell lines. Dev Biol 23: 1-22.
79. Rando TA, Blau HM, (1994) Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 125: 1275-1287.
80. Deasy BM, Qu-Peterson Z, Greenberger JS, Huard J, (2002) Mechanisms of muscle stem cell expansion with cytokines. Stem Cells 20: 50-60.
81. Bahnson A, Athanassiou C, Koebler D, Qian L, Shun T, et al. (2005) Automated measurement of cell motility and proliferation. BMC Cell Biol 6: 19.
82. Macias CA, Chiao JW, Xiao J, Arora DS, Tyurina YY, et al. (2007) Treatment with a novel hemigramicidin-TEMPO conjugate prolongs survival in a rat model of lethal hemorrhagic shock. Ann Surg 245: 305-314.
83. Jiang J, Belikova NA, Hoye AT, Zhao Q, Epperly MW, et al. (2008) A mitochondria-targeted nitroxide/hemigramicidin S conjugate protects mouse embryonic cells against gamma irradiation. Int J Radiat Oncol Biol Phys 70: 816-825.
84. Mitchell JB, Russo A, Biaglow JE, McPherson S, (1983) Cellular Glutathione Depletion by Diethyl Maleate or Buthionine Sulfoximine: No Effect of Glutathione Depletion on the Oxygen Enhancement Ratio. Radiation Research 96: 422-428.
85. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, et al. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580.
86. Deasy BM, Corsi KA, Huard J, (2007) Cellular therapy can be affected by the sex of the stem cell used. M S-Medecine Sciences 23: 798-800.