Cytoglobin modulates myogenic progenitor cell viability and muscle regeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages

  Singh, Sarvjeet ^a   Canseco, Diana C ^a   Manda, Shilpa M ^a   Shelton, John M ^a   Chirumamilla, Rajendra R ^a   Goetsch, Sean C ^a   Ye, Qiu ^a   Gerard, Robert D ^b   Schneider, Jay W ^a   Richardson, James A ^a,b   Rothermel, Beverly A ^a,b   Mammen, Pradeep P A ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Myocyte differentiation proliferation; Myogenesis; Nuclear protein; Redox signaling

Indexed keywords

CASPASE; CYTOGLOBIN; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL NUCLEUS; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; KNOCKOUT MOUSE; MALE; MOUSE; MUSCLE CELL; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SKELETAL MUSCLE; STEM CELL;

MYOCYTE DIFFERENTIATION/PROLIFERATION; MYOGENESIS; NUCLEAR PROTEIN; REDOX SIGNALING;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION; GLOBINS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLES; REACTIVE OXYGEN SPECIES; REGENERATION; RNA, SMALL INTERFERING; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELLS; TIME FACTORS;

EID: 84891906331     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314962111     Document Type: Article

References (85)

1. Deconinck N, Dan B (2007) Pathophysiology of duchenne muscular dystrophy: Current hypotheses. Pediatr Neurol 36(1): 1-7.
2. Heslop L, Morgan JE, Partridge TA (2000) Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 113(Pt 12): 2299-2308.
3. Yokota T, et al. (2006) Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J Cell Sci 119(Pt 13): 2679-2687.
4. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: Physiology to molecular biology. J Appl Physiol (1985) 91(2): 534-551.
5. Shi X, Garry DJ (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20(13): 1692-1708.
6. Li J, et al. (2011) Evidence of heterogeneity within bovine satellite cells isolated from young and adult animals. J Anim Sci 89(6): 1751-1757.
7. Shefer G, Rauner G, Yablonka-Reuveni Z, Benayahu D (2010) Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS ONE 5(10):e13307.
8. Day K, Shefer G, Shearer A, Yablonka-Reuveni Z (2010) The depletion of skeletal muscle satellite cells with age is concomitant with reduced capacity of single progenitors to produce reserve progeny. Dev Biol 340(2): 330-343.
9. Scimè A, et al. (2010) Transcriptional profiling of skeletal muscle reveals factors that are necessary to maintain satellite cell integrity during ageing. Mech Ageing Dev 131(1): 9-20.
10. Holterman CE, Rudnicki MA (2005) Molecular regulation of satellite cell function. Semin Cell Dev Biol 16(4-5): 575-584.
11. Cossu G, Biressi S (2005) Satellite cells, myoblasts and other occasional myogenic progenitors: Possible origin, phenotypic features and role in muscle regeneration. Semin Cell Dev Biol 16(4-5): 623-631.
12. Dhawan J, Rando TA (2005) Stem cells in postnatal myogenesis: Molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15(12): 666-673.
13. Irintchev A, Wernig A (1987) Muscle damage and repair in voluntarily running mice: Strain and muscle differences. Cell Tissue Res 249(3): 509-521.
14. Wernig A, Irintchev A, Weisshaupt P (1990) Muscle injury, cross-sectional area and fibre type distribution in mouse soleus after intermittent wheel-running. J Physiol 428: 639-652.
15. Kihlström M, Salminen A, Vihko V (1988) Food deprivation decreases the exertioninduced acid hydrolase response in mouse skeletal muscle. Eur J Appl Physiol Occup Physiol 57(2): 177-180.
16. Wallace GQ, McNally EM (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71: 37-57.
17. Schultz E, Jaryszak DL (1985) Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech Ageing Dev 30(1): 63-72.
18. Schultz E, Jaryszak DL, Valliere CR (1985) Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8(3): 217-222.
19. Sheehan SM, Allen RE (1999) Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J Cell Physiol 181(3): 499-506.
20. Schultz E (1985) Satellite cells in normal, regenerating and dystrophic muscle. Adv Exp Med Biol 182: 73-84.
21. Schultz E (1996) Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol 175(1): 84-94.
22. Chargé SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84(1): 209-238.
23. Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170(4): 421-435.
24. Singh S, et al. (2009) Calcineurin activates cytoglobin transcription in hypoxic myocytes. J Biol Chem 284(16): 10409-10421.
25. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270(5639): 725-727.
26. Burmester T, Ebner B, Weich B, Hankeln T (2002) Cytoglobin: A novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol 19(4): 416-421.
27. Trent JT, 3rd, Hargrove MS (2002) A ubiquitously expressed human hexacoordinate hemoglobin. J Biol Chem 277(22): 19538-19545.
28. Mammen PP, et al. (2006) Cytoglobin is a stress-responsive hemoprotein expressed in the developing and adult brain. J Histochem Cytochem 54(12): 1349-1361.
29. Fordel E, Thijs L, Moens L, Dewilde S (2007) Neuroglobin and cytoglobin expression in mice. Evidence for a correlation with reactive oxygen species scavenging. FEBS J 274(5): 1312-1317.
30. Fordel E, et al. (2006) Neuroglobin and cytoglobin overexpression protects human SHSY5Y neuroblastoma cells against oxidative stress-induced cell death. Neurosci Lett 410(2): 146-151.
31. Hodges NJ, Innocent N, Dhanda S, Graham M (2008) Cellular protection from oxidative DNA damage by over-expression of the novel globin cytoglobin in vitro. Mutagenesis 23(4): 293-298.
32. Li D, et al. (2007) Cytoglobin up-regulated by hydrogen peroxide plays a protective role in oxidative stress. Neurochem Res 32(8): 1375-1380.
33. Xu R, et al. (2006) Cytoglobin overexpression protects against damage-induced fibrosis. Mol Ther 13(6): 1093-1100.
34. Stagner JI, Seelan RS, Parthasarathy RN, White K (2009) Reduction of ischemic cell death in cultured Islets of Langerhans by the induction of cytoglobin. Islets 1(1): 50-54.
35. Geuens E, et al. (2003) A globin in the nucleus!. J Biol Chem 278(33): 30417-30420.
36. Schmidt M, et al. (2004) Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia. J Biol Chem 279(9): 8063-8069.
37. Garry DJ, et al. (1996) Postnatal development and plasticity of specialized muscle fiber characteristics in the hindlimb. Dev Genet 19(2): 146-156.
38. Ordway GA, Garry DJ (2004) Myoglobin: An essential hemoprotein in striated muscle. J Exp Biol 207(Pt 20): 3441-3446.
39. Garry DJ, et al. (2000) Myogenic stem cell function is impaired in mice lacking the forkhead/winged helix protein MNF. Proc Natl Acad Sci USA 97(10): 5416-5421.
40. Hawke TJ, et al. (2007) Xin, an actin binding protein, is expressed within muscle satellite cells and newly regenerated skeletal muscle fibers. Am J Physiol Cell Physiol 293(5):C1636-C1644.
41. Hawke TJ, Jiang N, Garry DJ (2003) Absence of p21CIP rescues myogenic progenitor cell proliferative and regenerative capacity in Foxk1 null mice. J Biol Chem 278(6): 4015-4020.
42. Hawke TJ, Kanatous SB, Martin CM, Goetsch SC, Garry DJ (2006) Rad is temporally regulated within myogenic progenitor cells during skeletal muscle regeneration. Am J Physiol Cell Physiol 290(2):C379-C387.
43. Yan Z, et al. (2003) Highly coordinated gene regulation in mouse skeletal muscle regeneration. J Biol Chem 278(10): 8826-8836.
44. Hawke TJ, et al. (2003) p21 is essential for normal myogenic progenitor cell function in regenerating skeletal muscle. Am J Physiol Cell Physiol 285(5):C1019-C1027.
45. Li S, et al. (2005) Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc Natl Acad Sci USA 102(4): 1082-1087.
46. Weiland TR, Kundu S, Trent JT, 3rd, Hoy JA, Hargrove MS (2004) Bis-histidyl hexacoordination in hemoglobins facilitates heme reduction kinetics. J Am Chem Soc 126(38): 11930-11935.
47. Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75: 19-37.
48. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809): 239-247.
49. Finkel T (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15(2): 247-254.
50. Finkel T (2005) Radical medicine: Treating ageing to cure disease. Nat Rev Mol Cell Biol 6(12): 971-976.
51. Reeder BJ (2010) The redox activity of hemoglobins: From physiologic functions to pathologic mechanisms. Antioxid Redox Signal 13(7): 1087-1123.
52. Petersen MG, Dewilde S, Fago A (2008) Reactions of ferrous neuroglobin and cytoglobin with nitrite under anaerobic conditions. J Inorg Biochem 102(9): 1777-1782.
53. Kiger L, et al. (2011) Electron transfer function versus oxygen delivery: A comparative study for several hexacoordinated globins across the animal kingdom. PLoS ONE 6(6): e20478.
54. Reeder BJ, Svistunenko DA, Wilson MT (2011) Lipid binding to cytoglobin leads to a change in haem co-ordination: A role for cytoglobin in lipid signalling of oxidative stress. Biochem J 434(3): 483-492.
55. Gardner AM, Cook MR, Gardner PR (2010) Nitric-oxide dioxygenase function of human cytoglobin with cellular reductants and in rat hepatocytes. J Biol Chem 285(31): 23850-23857.
56. Halligan KE, Jourd'heuil FL, Jourd'heuil D (2009) Cytoglobin is expressed in the vasculature and regulates cell respiration and proliferation via nitric oxide dioxygenation. J Biol Chem 284(13): 8539-8547.
57. Fago A, et al. (2004) Allosteric regulation and temperature dependence of oxygen binding in human neuroglobin and cytoglobin. Molecular mechanisms and physiological significance. J Biol Chem 279(43): 44417-44426.
58. Hamdane D, et al. (2003) The redox state of the cell regulates the ligand binding affinity of human neuroglobin and cytoglobin. J Biol Chem 278(51): 51713-51721.
59. Fang J, Ma I, Allalunis-Turner J (2011) Knockdown of cytoglobin expression sensitizes human glioma cells to radiation and oxidative stress. Radiat Res 176(2): 198-207.
60. Fordel E, et al. (2007) Anoxia or oxygen and glucose deprivation in SH-SY5Y cells: A step closer to the unraveling of neuroglobin and cytoglobin functions. Gene 398(1-2): 114-122.
61. Stagner JI, Parthasarathy SN, Wyler K, Parthasarathy RN (2005) Protection from ischemic cell death by the induction of cytoglobin. Transplant Proc 37(8): 3452-3453.
62. Sun Y, et al. (2003) Neuroglobin protects the brain from experimental stroke in vivo. Proc Natl Acad Sci USA 100(6): 3497-3500.
63. Hendgen-Cotta UB, et al. (2008) Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA 105(29): 10256-10261.
64. Li RC, Guo SZ, Lee SK, Gozal D (2010) Neuroglobin protects neurons against oxidative stress in global ischemia. J Cereb Blood Flow Metab 30(11): 1874-1882.
65. Raychaudhuri S, Skommer J, Henty K, Birch N, Brittain T (2010) Neuroglobin protects nerve cells from apoptosis by inhibiting the intrinsic pathway of cell death. Apoptosis 15(4): 401-411.
66. Wang X, et al. (2008) Effects of neuroglobin overexpression on acute brain injury and long-term outcomes after focal cerebral ischemia. Stroke 39(6): 1869-1874.
67. Li RC, et al. (2008) Neuroglobin protects PC12 cells against oxidative stress. Brain Res 1190: 159-166.
68. Mammen PP, et al. (2003) Hypoxia-induced left ventricular dysfunction in myoglobindeficient mice. Am J Physiol Heart Circ Physiol 285(5):H2132-H2141.
69. Csete M, et al. (2001) Oxygen-mediated regulation of skeletal muscle satellite cell proliferation and adipogenesis in culture. J Cell Physiol 189(2): 189-196.
70. Franco AA, Odom RS, Rando TA (1999) Regulation of antioxidant enzyme gene expression in response to oxidative stress and during differentiation of mouse skeletal muscle. Free Radic Biol Med 27(9-10): 1122-1132.
71. Hansen JM, Klass M, Harris C, CseteM (2007) A reducing redox environment promotes C2C12 myogenesis: Implications for regeneration in aged muscle. Cell Biol Int 31(6): 546-553.
72. Lee S, et al. (2006) Glutathione-peroxidase-1 null muscle progenitor cells are globally defective. Free Radic Biol Med 41(7): 1174-1184.
73. Urish KL, et al. (2009) Antioxidant levels represent a major determinant in the regenerative capacity of muscle stem cells. Mol Biol Cell 20(1): 509-520.
74. Zaccagnini G, et al. (2007) p66(ShcA) and oxidative stress modulate myogenic differentiation and skeletal muscle regeneration after hind limb ischemia. J Biol Chem 282(43): 31453-31459.
75. Armand AS, et al. (2008) Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis. J Biol Chem 283(43): 29004-29010.
76. Davies KJ, Quintanilha AT, Brooks GA, Packer L (1982) Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107(4): 1198-1205.
77. Walker PM (1991) Ischemia/reperfusion injury in skeletal muscle. Ann Vasc Surg 5(4): 399-402.
78. Bulfield G, Siller WG, Wight PA, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81(4): 1189-1192.
79. Disatnik MH, et al. (1998) Evidence of oxidative stress in mdx mouse muscle: Studies of the pre-necrotic state. J Neurol Sci 161(1): 77-84.
80. Rando TA, Disatnik MH, Yu Y, Franco A (1998) Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord 8(1): 14-21.
81. Whitehead NP, Pham C, Gervasio OL, Allen DG (2008) N-Acetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice. J Physiol 586(7): 2003-2014.
82. Lu JR, et al. (2002) Control of facial muscle development by MyoR and capsulin. Science 298(5602): 2378-2381.
83. Musarò A, Barberi L (2010) Isolation and culture of mouse satellite cells. Methods Mol Biol 633: 101-111.
84. Singh S, Khar A (2006) Activation of NFkappaB and Ub-proteasome pathway during apoptosis induced by a serum factor is mediated through the upregulation of the 26S proteasome subunits. Apoptosis 11(5): 845-859.
85. Singh S, Khar A (2005) Differential gene expression during apoptosis induced by a serum factor: Role of mitochondrial F0-F1 ATP synthase complex. Apoptosis 10(6): 1469-1482.