Hypoxia Increases Mouse Satellite Cell Clone Proliferation Maintaining both In Vitro and In Vivo Heterogeneity and Myogenic Potential

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Urbani, Luca ^a,b   Piccoli, Martina ^a,b   Franzin, Chiara ^a,b   Pozzobon, Michela ^a,b   de Coppi, Paolo ^b,c  

^a Fondazione Citta della Speranza   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOTOXIN; GREEN FLUORESCENT PROTEIN; MYOGENIC FACTOR; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CLONE; CELL HETEROGENEITY; CELL HYPOXIA; CELL ISOLATION; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; HINDLIMB; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MUSCLE POTENTIAL; NONHUMAN; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE SATELLITE CELL; TIBIALIS ANTERIOR MUSCLE;

ADENOSINE TRIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; CELL HYPOXIA; CELL PROLIFERATION; GREEN FLUORESCENT PROTEINS; HINDLIMB; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MICE; MICE, INBRED C57BL; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOGENIC REGULATORY FACTORS; OXYGEN; REAL-TIME POLYMERASE CHAIN REACTION; SATELLITE CELLS, SKELETAL MUSCLE;

RATTUS;

EID: 84869210326     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049860     Document Type: Article

References (75)

1. Moss FP, Leblond CP, (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170: 421-435.
2. Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, et al. (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122: 289-301.
3. Mauro A, (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495.
4. Cornelison DDW, Wold B, (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191: 270-283.
5. Hawke TJ, Garry DJ, (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-551.
6. Beauchamp G, Morgan JE, Pagel CN, Partridge TA, (1999) Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem-like properties as the myogenic source. J Cell Biol 144: 1113-1122.
7. Csete M, Walikonis J, Slawny N, Wei Y, Korsnes S, et al. (2001) Oxygen-Mediated Regulation of Skeletal Muscle Satellite Cell Proliferation and Adipogenesis in Culture. Journal of Cellular Physiology 189: 189-196.
8. Lee WY, Lui PP, Rui YF, (2012) Hypoxia-Mediated Efficient Expansion of Human Tendon-Derived Stem Cells In Vitro. Tissue Eng Part A 18(5-6): 484-98.
9. Rodrigues CA, Diogo MM, Da Silva CL, Cabral JM, (2010) Hypoxia enhances proliferation of mouse embryonic stem cell-derived neural stem cells. Biotechnol Bioeng 106(2): 260-70.
10. Ma T, Grayson WL, Frohlich M, Vunjak-Novakovic G, (2009) Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol Prog 25(1): 32-42.
11. Koning M, Werker PM, van Luyn MJ, Harmsen MC, (2011) Hypoxia promotes proliferation of human myogenic satellite cells: a potential benefactor in tissue engineering of skeletal muscle. Tissue Eng Part A 17(13-14): 1747-58.
12. Ivanovic Z, Dello Sbarba P, Trimoreau F, Faucher JL, Praloran V, (2000) Primitive human HPCs are better maintained and expanded in vitro at 1 percent oxygen than at 20 percent. Transfusion 40: 1482-1488.
13. Cipolleschi MG, Rovida E, Ivanovic Z, Praloran V, Olivotto M, et al. (2000) The expansion of murine bone marrow cells preincubated in hypoxia as an in vitro indicator of their marrowrepopulating ability. Leukemia 14: 735-739.
14. Ivanovic Z, Bartolozzi B, Bernabei PA, Cipolleschi MG, Rovida E, et al. (2000) Incubation of murine bone marrow cells in hypoxia ensures the maintenance of marrow repopulating ability together with the expansion of committed progenitors. Br J Haematol 108: 424-429.
15. Greenbaum AR, Etherington PJ, Manek S, O'Hare D, Parker KH, et al. (1997) Measurements of oxygenation and perfusion in skeletal muscle using multiple microelectrodes. J Muscle Res Cell Motil 18: 149-159.
16. Broek T, Grefte RW, Von den Hoff JW, (2010) Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 224(1): 7-16.
17. Charge SB, Rudnicki MA, (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev, Jan 84(1): 209-38.
18. Punch VG, Jones AE, Rudnicki MA, (2009) Transcriptional networks that regulate muscle stem cell function. Wiley Interdiscip Rev Syst Biol Med 1: 128-140.
19. Zammit PS, Partridge TA, Yablonka-Reuveni Z, (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54: 1177-1191.
20. Tajbakhsh S, (2009) Skeletal muscle stem cells in developmental versus regenerative myogenesis. J Intern Med 266: 372-389.
21. Zammit PS, (2008) All muscle satellite cells are equal, but are some more equal than others? Journal of Cell Science 121: 2975-2982.
22. Bischoff R, Franzini-Armstrong C (2004) Satellite and stem cells in muscle regeneration. New York: McGraw Hill.
23. Rossi CA, Pozzobon M, Ditadi A, Archacka K, Gastaldello A, et al. (2010) Clonal Characterization of Rat Muscle Satellite Cells: Proliferation, Metabolism and Differentiation Define an Intrinsic Heterogeneity. PLoS ONE 5 (1): e8523.
24. Ojima K, Uezumi A, Miyoshi H, Masuda S, Morita Y, et al. (2004) Mac-1low early myeloid cells in the bone marrow-derived SP fraction migrate into injured skeletal muscle and participate in muscle regeneration. Biochemical and Biophysical Research Communications 321: 1050-1061.
25. Fukada S, Higuchi S, Segawa M, Koda K, Yamamoto Y, et al. (2004) Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp Cell Res 296: 245-255.
26. De Coppi P, Callegari A, Chiavegato A, Gasparotto L, Piccoli M, et al. (2007) Amniotic fluid and bone marrow derived mesenchymal stem cells can be converted to smooth muscle cells in the cryo-injured rat bladder and prevent compensatory hypertrophy of surviving smooth muscle cells. J Urol 177(1): 369-76.
27. Gonzalez-Roca E, Garcia-Albeniz X, Rodriguez-Mulero S, Gomis RR, Kornacker K, et al. (2010) Accurate Expression Profiling of Very Small Cell Populations. PLoS ONE 5(12): e14418.
28. Piccoli M, Franzin C, Bertin E, Urbani L, Blaauw B, et al. (2012) Amniotic Fluid Stem Cells Restore the Muscle Cell Niche in a HSA-Cre, Smn(F7/F7) Mouse Model. Stem Cells doi: 10.1002/stem.1134. [Epub ahead of print].
29. Fraley C, Raftery AE, (2002) Model-based clustering, discriminant analysis, and density estimation. Journal of the American Statistical Association 97: 611-631.
30. Gussoni E, Soneoka Y, Strickland CD, Buzney EA, Khan MK, et al. (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401: 390-394.
31. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, et al. (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301: 487-492.
32. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, et al. (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9: 255-267.
33. Torrente Y, Belicchi M, Sampaolesi M, Pisati F, Meregalli M, et al. (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114: 182-195.
34. Mitchell KJ, Pannerec A, Cadot B, Parlakian A, Besson V, et al. (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12: 257-266.
35. De Angelis L, Berghella L, Coletta M, Lattanzi L, Zanchi M, et al. (1999) Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 147: 869-878.
36. LaBarge MA, Blau HM, (2002) Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111: 589-601.
37. Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, Blasco MA, Tajbakhsh S, (2012) A Subpopulation of Adult Skeletal Muscle Stem Cells Retains All Template DNA Strands after Cell Division. Cell 148: 112-125.
38. Lepper C, Partridge TA, Fan CM, (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138: 3639-3646.
39. Sambasivan R, Yao R, Kissenpfennig A, Van Wittenberghe L, Paldi A, et al. (2011) Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138: 3647-3656.
40. Wang YX, Rudnicki MA, (2012) Satellite cells, the engines of muscle repair. Nature Reviews Molecular Cell Biology 13(2): 127-33.
41. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, et al. (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309: 2064-2067.
42. Rossi CA, Flaibani M, Blaauw B, Pozzobon M, Figallo E, et al. (2011) In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. The FASEB Journal Vol 25: 1-9.
43. Gilbert PM, Blau HM, (2011) Engineering a stem cell house into a home. Stem Cell Res Ther 2(1): 3.
44. Lutolf MP, Blau HM, (2009) Artificial stem cell niches. Adv Mater 21(32-33): 3255-68.
45. Segev E, Shefer G, Adar R, Chapal-Ilani N, Itzkovitz S, et al. (2011) Muscle-bound primordial stem cells give rise to myofibers-associated myogenic and non-myogenic progenitors. PLoS ONE 6: e25605.
46. Shinin V, Gayraud-Morel B, Gome's D, Tajbakhsh S, (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8: 677-687.
47. Ono Y, Masuda S, Nam H, Benezra R, Miyagoe-Suzuki Y, et al. (2012) Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. Journal of Cell Science 125: 1-9.
48. De Coppi P, Milan G, Scarda A, Boldrin L, Centobene C, et al. (2006) Rosiglitazone modifies the adipogenic potential of human muscle satellite cells. Diabetologia 49: 1962-1973.
49. Singh NK, Chae HS, Hwang IH, Yoo IM, Ahn CN, et al. (2007) Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. J Anim Sci 85: 1126-1135.
50. Rouger K, Brault M, Daval N, Leroux I, Guigand L, et al. (2004) Muscle satellite cell heterogeneity: in vitro and in vivo evidences for populations that fuse differently. Cell Tissue Res 317: 319-326.
51. Molnar G, Ho ML, Schroedl NA, (1996) Evidence for a multiple satellite cell population and a non-myogenic cell type that is regulated differently in regenerating and growing skeletal muscle. Tissue Cell 28: 547-556.
52. Rantanen J, Hurme T, Lukka R, Heino J, Kalimo H, (1995) Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab Invest 72: 341-347.
53. Schultz E, (1996) Satellite cell proliferative compartments in growing skeletal muscle. Dev Biol 175: 84-94.
54. Sherwood RI, Christensen JL, Conboy IM, Conboy MJ, Rando TA, et al. (2004) Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119: 543-554.
55. 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(1): 37-47.
56. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM, (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456(7221): 502-506.
57. Dupas T, Rouaud T, Rouger K, Lieubeau B, Cario-Toumaniantz C, et al. (2011) Fetal muscle contains different CD34+cell subsets that distinctly differentiate into adipogenic, angiogenic and myogenic lineages. Stem Cell Research 7: 230-243.
58. Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, et al. (2007) Molecular Signature of Quiescent Satellite Cells in Adult Skeletal Muscle. Stem Cells 25: 2448-2459.
59. Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G, (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. The Journal of Clinical Investigation 120 (1): 11-19.
60. Fukada S, Yamaguchi M, Kokubo H, Ogawa R, Uezumi A, et al. (2011) Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development 138: 4609-4619.
61. Csete M, (2005) Oxygen in the cultivation of stem cells. Ann N Y Acad Sci, May 1049: 1-8.
62. Shefer G, Wleklinski-Lee M, Yablonka-Reuveni Z, (2004) Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. Journal of Cell Science 117(22): 5393-5404.
63. Beauchamp JR, Heslop L, Yu DSW, Tajbakhsh S, Kelly RG, et al. (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. The Journal of Cell Biology 151: 1221-1233.
64. Kuang S, Kuroda K, Le Grand F, Rudnicki MA, (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129(5): 999-1010.
65. Gayraud-Morel B, Chrétien F, Jory A, Sambasivan R, Negroni E, et al. (2012) Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells. J Cell Sci, 2012 Feb 24.
66. Ieronimakis N, Balasundaram G, Rainey S, Srirangam K, Yablonka-Reuveni Z, et al. (2010) Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during scute injury. PLoS ONE 5: e10920.
67. Alfaro LAS, Dick SA, Siegel AL, Anonuevo AS, McNagny KM, et al. (2011) CD34 Promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration. Stem Cells Dec 29(12): 2030-41.
68. Conboy MJ, Karasov AO, Rando TA, (2007) High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol 5: e102.
69. Semenza GL, (2000) HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 88: 1474-1480.
70. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, et al. (2001) Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
71. Kubis HP, Hanke N, Scheibe RJ, Gros G, (2005) Accumulation and nuclear import of HIF1 alpha during high and low oxygen concentration in skeletal muscle cells in primary culture. Biochim Biophys Acta 1745: 187-195.
72. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, et al. (2001) HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J 15: 2445-2453.
73. Wagatsuma A, Kotake N, Yamada S, (2010) Spatial and temporal expression of hypoxia-inducible factor-1α during myogenesis in vivo and in vitro. Mol Cell Biochem 347(1-2): 145-55.
74. Pisani DF, Dechesne CA, (2005) Skeletal muscle HIF-1α expression is dependent on muscle fiber type. J Gen Physiol 126(2): 173-8.
75. Tanaka KK, Hall JK, Troy AA, Cornelison DDW, Majka SM, et al. (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4(3): 217-225.