Skip to main content

Dormancy and Quiescence of Skeletal Muscle Stem Cells

  • Chapter
  • First Online:
Vertebrate Myogenesis

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 56))

Abstract

The skeletal muscle of vertebrates has a huge regenerative capacity. When destroyed after different types of injury, this organ can regenerate very quickly (less than 20 days following myotoxin injection in the mouse) ad integrum and repeatedly. The cell responsible for this regeneration is the so-called satellite cell, the muscle stem cell that lies on top of the muscle fibre, a giant, multinucleated cell that contains the contractile material. When injected in the muscle, satellite cells can efficiently differentiate into contractile muscle fibres. The satellite cell shows great therapeutic potential; and its regenerative capacity has triggered particular interest in the field of muscular degeneration.

In this review we will focus on one particular property of the satellite cell: its quiescence and dormancy. Indeed adult satellite cells are quiescent; they lie between the basal lamina and the basement membrane of the muscle fibre, ready to proliferate, and fuse in order to regenerate myofibers upon injury. It has recently been shown that a subpopulation of satellite cells is able to enter dormancy in human and mice cadavers. Dormancy is defined by a low metabolic state, low mobility, and a long lag before division when plated in vitro, compared to quiescent cells. This definition is also based on current knowledge about long-term hematopoietic stem cells, a subpopulation of stem cells that are described as dormant based on the same criteria (rare division and low metabolism when compared to progeny which are dividing more often).

In the first part of this review, we will provide a description of satellite cells which addresses their quiescent state. We will then focus on the uneven distribution of satellite cells in the muscle and describe evidence that suggests that their dormancy differs from one muscle to the next and that one should be cautious when making generalisations regarding this cellular state.

In a second part, we will discuss the transition between active dividing cells in developing animals to quiescence. This mechanism could be used or amplified in the switch from quiescence to dormancy.

In a third part, we will review the signals and dynamics that actively maintain the satellite cell quiescent. The in-depth understanding of these mechanisms is key to describing how dormancy relies on quiescent state of the cells.

In a fourth part, we will deal with dormancy per se: how dormant satellite cells can be obtained, their characteristics, their metabolic profile, and their molecular signature as compared to quiescent cells. Here, we will highlight one of the most important recent findings: that quiescence is a prerequisite for the entry of the satellite cell into dormancy.

Since dormancy is a newly discovered phenomenon, we will review the mechanisms responsible for quiescence and activation, as these two cellular states are better known and key to understanding satellite cell dormancy. This will allow us to describe dormancy and its prerequisites.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abou-Khalil R, Brack AS (2010) Muscle stem cells and reversible quiescence: the role of sprouty. Cell Cycle 9(13):2575–2580

    PubMed  CAS  Google Scholar 

  • Abou-Khalil R, Le Grand F, Pallafacchina G, Valable S, Authier FJ, Rudnicki MA, Gherardi RK, Germain S, Chretien F, Sotiropoulos A et al (2009) Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell 5(3):298–309

    PubMed  CAS  Google Scholar 

  • Al-Kafaji G, Golbahar J (2013) High glucose-induced oxidative stress increases the copy number of mitochondrial DNA in human mesangial cells. Biomed Res Int 2013:754946

    PubMed  PubMed Central  Google Scholar 

  • Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151(6):1221–1234

    PubMed  CAS  PubMed Central  Google Scholar 

  • Becker KL, Nylen ES, White JC, Muller B, Snider RH Jr (2004) Clinical review 167: Procalcitonin and the calcitonin gene family of peptides in inflammation, infection, and sepsis: a journey from calcitonin back to its precursors. J Clin Endocrinol Metab 89(4):1512–1525

    PubMed  CAS  Google Scholar 

  • Beltran B, Mathur A, Duchen MR, Erusalimsky JD, Moncada S (2000) The effect of nitric oxide on cell respiration: A key to understanding its role in cell survival or death. Proc Natl Acad Sci U S A 97(26):14602–14607

    PubMed  CAS  PubMed Central  Google Scholar 

  • Blau HM, Webster C (1981) Isolation and characterization of human muscle cells. Proc Natl Acad Sci U S A 78(9):5623–5627

    PubMed  CAS  PubMed Central  Google Scholar 

  • Blazar BR, Lasky LC, Perentesis JP, Watson KV, Steinberg SE, Filipovich AH, Orr HT, Ramsay NK (1986) Successful donor cell engraftment in a recipient of bone marrow from a cadaveric donor. Blood 67(6):1655–1660

    PubMed  CAS  Google Scholar 

  • Bottinelli R (2001) Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story? Pflugers Arch 443(1):6–17

    PubMed  CAS  Google Scholar 

  • Bowie MB, McKnight KD, Kent DG, McCaffrey L, Hoodless PA, Eaves CJ (2006) Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect. J Clin Invest 116(10):2808–2816

    PubMed  CAS  PubMed Central  Google Scholar 

  • Buckingham M, Relaix F (2007) The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu Rev Cell Dev Biol 23:645–673

    PubMed  CAS  Google Scholar 

  • Buckley PA, Konigsberg IR (1977) Do myoblasts in vivo withdraw from the cell cycle? A reexamination. Proc Natl Acad Sci U S A 74(5):2031–2035

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cardasis CA, Cooper GW (1975) An analysis of nuclear numbers in individual muscle fibers during differentiation and growth: a satellite cell-muscle fiber growth unit. J Exp Zool 191(3):347–358

    PubMed  CAS  Google Scholar 

  • Charlton CA, Mohler WA, Blau HM (2000) Neural cell adhesion molecule (NCAM) and myoblast fusion. Dev Biol 221(1):112–119

    PubMed  CAS  Google Scholar 

  • Chi N, Epstein JA (2002) Getting your Pax straight: Pax proteins in development and disease. Trends Genet 18(1):41–47

    PubMed  CAS  Google Scholar 

  • Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122(2):289–301

    PubMed  CAS  Google Scholar 

  • Collins CA, Gnocchi VF, White RB, Boldrin L, Perez-Ruiz A, Relaix F, Morgan JE, Zammit PS (2009) Integrated functions of Pax3 and Pax7 in the regulation of proliferation, cell size and myogenic differentiation. PLoS One 4(2):e4475

    PubMed  PubMed Central  Google Scholar 

  • Davie JK, Cho JH, Meadows E, Flynn JM, Knapp JR, Klein WH (2007) Target gene selectivity of the myogenic basic helix-loop-helix transcription factor myogenin in embryonic muscle. Dev Biol 311(2):650–664

    PubMed  CAS  Google Scholar 

  • Davis RL, Cheng PF, Lassar AB, Weintraub H (1990) The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60(5):733–746

    PubMed  CAS  Google Scholar 

  • de Maruenda EC, Franzini-Armstrong C (1978) Satellite and invasive cells in frog sartorius muscle. Tissue Cell 10(4):749–772

    PubMed  Google Scholar 

  • Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M et al (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458(7239):780–783

    PubMed  CAS  PubMed Central  Google Scholar 

  • Erker L, Azuma H, Lee AY, Guo C, Orloff S, Eaton L, Benedetti E, Jensen B, Finegold M, Willenbring H et al (2010) Therapeutic liver reconstitution with murine cells isolated long after death. Gastroenterology 139(3):1019–1029

    PubMed  PubMed Central  Google Scholar 

  • Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St John JC (2007) Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 120(Pt 22):4025–4034

    PubMed  CAS  Google Scholar 

  • Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25(10):2448–2459

    PubMed  CAS  Google Scholar 

  • Gayraud-Morel B, Chretien F, Flamant P, Gomes D, Zammit PS, Tajbakhsh S (2007) A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev Biol 312(1):13–28

    PubMed  CAS  Google Scholar 

  • Gayraud-Morel B, Chretien F, Tajbakhsh S (2009) Skeletal muscle as a paradigm for regenerative biology and medicine. Regen Med 4(2):293–319

    PubMed  Google Scholar 

  • Ghins E, Colson-van Schoor M, Marechal G (1984) The origin of muscle stem cells in rat triceps surae regenerating after mincing. J Muscle Res Cell Motil 5(6):711–722

    PubMed  CAS  Google Scholar 

  • Gibson MC, Schultz E (1982) The distribution of satellite cells and their relationship to specific fiber types in soleus and extensor digitorum longus muscles. Anat Rec 202(3):329–337

    PubMed  CAS  Google Scholar 

  • Gloire G, Legrand-Poels S, Piette J (2006) NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol 72(11):1493–1505

    PubMed  CAS  Google Scholar 

  • Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS (2009) Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One 4(4):e5205

    PubMed  PubMed Central  Google Scholar 

  • Goldring K, Partridge T, Watt D (2002) Muscle stem cells. J Pathol 197(4):457–467

    PubMed  Google Scholar 

  • Gopinath SD, Rando TA (2008) Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell 7(4):590–598

    PubMed  CAS  Google Scholar 

  • Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80(2):853–924

    PubMed  CAS  Google Scholar 

  • Grounds MD, McGeachie JK (1987) A model of myogenesis in vivo, derived from detailed autoradiographic studies of regenerating skeletal muscle, challenges the concept of quantal mitosis. Cell Tissue Res 250(3):563–569

    PubMed  CAS  Google Scholar 

  • Grounds M, Partridge TA, Sloper JC (1980) The contribution of exogenous cells to regenerating skeletal muscle: an isoenzyme study of muscle allografts in mice. J Pathol 132(4):325–341

    PubMed  CAS  Google Scholar 

  • Grounds MD, White JD, Rosenthal N, Bogoyevitch MA (2002) The role of stem cells in skeletal and cardiac muscle repair. J Histochem Cytochem 50(5):589–610

    PubMed  CAS  Google Scholar 

  • Gruber J, Ng LF, Fong S, Wong YT, Koh SA, Chen CB, Shui G, Cheong WF, Schaffer S, Wenk MR et al (2011) Mitochondrial changes in ageing Caenorhabditis elegans–what do we learn from superoxide dismutase knockouts? PLoS One 6(5):e19444

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gu W, Schneider JW, Condorelli G, Kaushal S, Mahdavi V, Nadal-Ginard B (1993) Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72(3):309–324

    PubMed  CAS  Google Scholar 

  • Gustafsson MK, Pan H, Pinney DF, Liu Y, Lewandowski A, Epstein DJ, Emerson CP Jr (2002) Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev 16(1):114–126

    PubMed  CAS  PubMed Central  Google Scholar 

  • Guth L (1973) Fact and artifact in the histochemical procedure for myofibrillar ATPase. Exp Neurol 41(2):440–450

    PubMed  CAS  Google Scholar 

  • Guth L, Yellin H (1971) The dynamic nature of the so-called “fiber types” of mammalian skeletal muscle. Exp Neurol 31(2):227–300

    PubMed  CAS  Google Scholar 

  • Holtzer H, Rubinstein N, Fellini S, Yeoh G, Chi J, Birnbaum J, Okayama M (1975) Lineages, quantal cell cycles, and the generation of cell diversity. Q Rev Biophys 8(4):523–557

    PubMed  CAS  Google Scholar 

  • Jang YY, Sharkis SJ (2007) A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110(8):3056–3063

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jones NC, Tyner KJ, Nibarger L, Stanley HM, Cornelison DD, Fedorov YV, Olwin BB (2005) The p38alpha/beta MAPK functions as a molecular switch to activate the quiescent satellite cell. J Cell Biol 169(1):105–116

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kai T, Spradling A (2004) Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428(6982):564–569

    PubMed  CAS  Google Scholar 

  • Kapelushnik J, Aker M, Pugatsch T, Samuel S, Slavin S (1998) Bone marrow transplantation from a cadaveric donor. Bone Marrow Transplant 21(8):857–858

    PubMed  CAS  Google Scholar 

  • Kelly AM (1978) Perisynaptic satellite cells in the developing and mature rat soleus muscle. Anat Rec 190(4):891–903

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kuroda K, Tani S, Tamura K, Minoguchi S, Kurooka H, Honjo T (1999) Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J Biol Chem 274(11):7238–7244

    PubMed  CAS  Google Scholar 

  • Latil M, Rocheteau P, Chatre L, Sanulli S, Memet S, Ricchetti M, Tajbakhsh S, Chretien F (2012) Skeletal muscle stem cells adopt a dormant cell state post mortem and retain regenerative capacity. Nat Commun 3:903

    PubMed  Google Scholar 

  • Lee HU, Kaufman SJ, Coleman JR (1984) Expression of myoblast and myocyte antigens in relation to differentiation and the cell cycle. Exp Cell Res 152(2):331–347

    PubMed  CAS  Google Scholar 

  • Lee HC, Yin PH, Lu CY, Chi CW, Wei YH (2000) Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 348(Pt 2):425–432

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lepper C, Conway SJ, Fan CM (2009) Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460(7255):627–631

    PubMed  CAS  PubMed Central  Google Scholar 

  • Liu X, Zhu Y, Gao W (2006) Isolation of neural stem cells from the spinal cords of low temperature preserved abortuses. J Neurosci Methods 157(1):64–70

    PubMed  Google Scholar 

  • Lonergan T, Brenner C, Bavister B (2006) Differentiation-related changes in mitochondrial properties as indicators of stem cell competence. J Cell Physiol 208(1):149–153

    PubMed  CAS  Google Scholar 

  • Lu J, Webb R, Richardson JA, Olson EN (1999) MyoR: a muscle-restricted basic helix-loop-helix transcription factor that antagonizes the actions of MyoD. Proc Natl Acad Sci U S A 96(2):552–557

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lunt SY, Vander Heiden MG (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27:441–464

    PubMed  CAS  Google Scholar 

  • Machalinski B, Paczkowski M, Kawa M, Paczkowska E, Ostrowski M (2003) An optimization of isolation of early hematopoietic cells from heparinized cadaveric organ donors. Transplant Proc 35(8):3096–3100

    PubMed  CAS  Google Scholar 

  • Mahdavi V, Strehler EE, Periasamy M, Wieczorek DF, Izumo S, Nadal-Ginard B (1986) Sarcomeric myosin heavy chain gene family: organization and pattern of expression. Med Sci Sports Exerc 18(3):299–308

    PubMed  CAS  Google Scholar 

  • Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40(2):294–309

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mankoo BS, Skuntz S, Harrigan I, Grigorieva E, Candia A, Wright CV, Arnheiter H, Pachnis V (2003) The concerted action of Meox homeobox genes is required upstream of genetic pathways essential for the formation, patterning and differentiation of somites. Development 130(19):4655–4664

    PubMed  CAS  Google Scholar 

  • Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    PubMed  CAS  PubMed Central  Google Scholar 

  • McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162(6):1135–1147

    PubMed  CAS  PubMed Central  Google Scholar 

  • Meadows E, Cho JH, Flynn JM, Klein WH (2008) Myogenin regulates a distinct genetic program in adult muscle stem cells. Dev Biol 322(2):406–414

    PubMed  CAS  Google Scholar 

  • Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF (1993) Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 34(4):609–616

    PubMed  CAS  Google Scholar 

  • Morgan JE, Coulton GR, Partridge TA (1987) Muscle precursor cells invade and repopulate freeze-killed muscles. J Muscle Res Cell Motil 8(5):386–396

    PubMed  CAS  Google Scholar 

  • Moss FP, Leblond CP (1970) Nature of dividing nuclei in skeletal muscle of growing rats. J Cell Biol 44(2):459–462

    PubMed  CAS  PubMed Central  Google Scholar 

  • Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170(4):421–435

    PubMed  CAS  Google Scholar 

  • Muller J, Vayssiere N, Royuela M, Leger ME, Muller A, Bacou F, Pons F, Hugon G, Mornet D (2001) Comparative evolution of muscular dystrophy in diaphragm, gastrocnemius and masseter muscles from old male mdx mice. J Muscle Res Cell Motil 22(2):133–139

    PubMed  CAS  Google Scholar 

  • Nagata Y, Partridge TA, Matsuda R, Zammit PS (2006) Entry of muscle satellite cells into the cell cycle requires sphingolipid signaling. J Cell Biol 174(2):245–253

    PubMed  CAS  PubMed Central  Google Scholar 

  • Niu R, Yoshida M, Ling F (2012) Increases in mitochondrial DNA content and 4977-bp deletion upon ATM/Chk2 checkpoint activation in HeLa cells. PLoS One 7(7):e40572

    PubMed  CAS  PubMed Central  Google Scholar 

  • Olguin HC, Olwin BB (2004) Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol 275(2):375–388

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ono Y, Boldrin L, Knopp P, Morgan JE, Zammit PS (2010) Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol 337(1):29–41

    PubMed  CAS  PubMed Central  Google Scholar 

  • Oustanina S, Hause G, Braun T (2004) Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 23(16):3430–3439

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pallafacchina G, Francois S, Regnault B, Czarny B, Dive V, Cumano A, Montarras D, Buckingham M (2010) An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res 4(2):77–91

    PubMed  CAS  Google Scholar 

  • Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH (2001) Cell culture. Progenitor cells from human brain after death. Nature 411(6833):42–43

    PubMed  CAS  Google Scholar 

  • Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD (2007) Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 104(13):5431–5436

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50(6):500–509

    PubMed  CAS  Google Scholar 

  • Phillips GD, Hoffman JR, Knighton DR (1990) Migration of myogenic cells in the rat extensor digitorum longus muscle studied with a split autograft model. Cell Tissue Res 262(1):81–88

    PubMed  CAS  Google Scholar 

  • Piccoli C, Ria R, Scrima R, Cela O, D'Aprile A, Boffoli D, Falzetti F, Tabilio A, Capitanio N (2005) Characterization of mitochondrial and extra-mitochondrial oxygen consuming reactions in human hematopoietic stem cells. Novel evidence of the occurrence of NAD(P)H oxidase activity. J Biol Chem 280(28):26467–26476

    PubMed  CAS  Google Scholar 

  • Pisconti A, Brunelli S, Di Padova M, De Palma C, Deponti D, Baesso S, Sartorelli V, Cossu G, Clementi E (2006) Follistatin induction by nitric oxide through cyclic GMP: a tightly regulated signaling pathway that controls myoblast fusion. J Cell Biol 172(2):233–244

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pownall ME, Gustafsson MK, Emerson CP Jr (2002) Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu Rev Cell Dev Biol 18:747–783

    PubMed  CAS  Google Scholar 

  • Quinn LS, Holtzer H, Nameroff M (1985) Generation of chick skeletal muscle cells in groups of 16 from stem cells. Nature 313(6004):692–694

    PubMed  CAS  Google Scholar 

  • Rawls A, Valdez MR, Zhang W, Richardson J, Klein WH, Olson EN (1998) Overlapping functions of the myogenic bHLH genes MRF4 and MyoD revealed in double mutant mice. Development 125(13):2349–2358

    PubMed  CAS  Google Scholar 

  • Relaix F, Montarras D, Zaffran S, Gayraud-Morel B, Rocancourt D, Tajbakhsh S, Mansouri A, Cumano A, Buckingham M (2006) Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J Cell Biol 172(1):91–102

    PubMed  CAS  PubMed Central  Google Scholar 

  • Reshef R, Maroto M, Lassar AB (1998) Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. Genes Dev 12(3):290–303

    PubMed  CAS  PubMed Central  Google Scholar 

  • 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(1–2):112–125

    PubMed  CAS  Google Scholar 

  • Rudnicki MA, Braun T, Hinuma S, Jaenisch R (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71(3):383–390

    PubMed  CAS  Google Scholar 

  • Saito Y (1985) Muscle fibre type differentiation and satellite cell population in Werdnig-Hoffmann disease. J Neurol Sci 68(1):75–87

    PubMed  CAS  Google Scholar 

  • Salleo A, La Spada G, Falzea G, Denaro MG, Cicciarello R (1983) Response of satellite cells and muscle fibers to long-term compensatory hypertrophy. J Submicrosc Cytol 15(4):929–940

    PubMed  CAS  Google Scholar 

  • Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76(2):371–423

    PubMed  CAS  Google Scholar 

  • Schmalbruch H, Hellhammer U (1977) The number of nuclei in adult rat muscles with special reference to satellite cells. Anat Rec 189(2):169–175

    PubMed  CAS  Google Scholar 

  • Schultz E, Gibson MC, Champion T (1978) Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206(3):451–456

    PubMed  CAS  Google Scholar 

  • Schultz E, Jaryszak DL, Gibson MC, Albright DJ (1986) Absence of exogenous satellite cell contribution to regeneration of frozen skeletal muscle. J Muscle Res Cell Motil 7(4):361–367

    PubMed  CAS  Google Scholar 

  • Schultz E, Albright DJ, Jaryszak DL, David TL (1988) Survival of satellite cells in whole muscle transplants. Anat Rec 222(1):12–17

    PubMed  CAS  Google Scholar 

  • Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102(6):777–786

    PubMed  CAS  Google Scholar 

  • Shafiq SA, Gorycki MA, Mauro A (1968) Mitosis during postnatal growth in skeletal and cardiac muscle of the rat. J Anat 103(Pt 1):135–141

    PubMed  CAS  PubMed Central  Google Scholar 

  • Siegel AL, Atchison K, Fisher KE, Davis GE, Cornelison DD (2009) 3D timelapse analysis of muscle satellite cell motility. Stem Cells 27(10):2527–2538

    PubMed  CAS  PubMed Central  Google Scholar 

  • Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, Schneider JW, Zhang CC, Sadek HA (2010) The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7(3):380–390

    PubMed  CAS  PubMed Central  Google Scholar 

  • Snow MH (1977) The effects of aging on satellite cells in skeletal muscles of mice and rats. Cell Tissue Res 185(3):399–408

    PubMed  CAS  Google Scholar 

  • Son D, Kojima I, Inagi R, Matsumoto M, Fujita T, Nangaku M (2008) Chronic hypoxia aggravates renal injury via suppression of Cu/Zn-SOD: a proteomic analysis. Am J Physiol Renal Physiol 294(1):F62–F72

    PubMed  CAS  Google Scholar 

  • Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M et al (2010) Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7(3):391–402

    PubMed  CAS  Google Scholar 

  • Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275(51):40235–40243

    PubMed  CAS  Google Scholar 

  • Valcourt JR, Lemons JM, Haley EM, Kojima M, Demuren OO, Coller HA (2012) Staying alive: metabolic adaptations to quiescence. Cell Cycle 11(9):1680–1696

    PubMed  CAS  PubMed Central  Google Scholar 

  • Valdez MR, Richardson JA, Klein WH, Olson EN (2000) Failure of Myf5 to support myogenic differentiation without myogenin, MyoD, and MRF4. Dev Biol 219(2):287–298

    PubMed  CAS  Google Scholar 

  • Van Itallie CM, Van Why S, Thulin G, Kashgarian M, Siegel NJ (1993) Alterations in mitochondrial RNA expression after renal ischemia. Am J Physiol 265(3 Pt 1):C712–C719

    PubMed  Google Scholar 

  • Walters EH, Stickland NC, Loughna PT (2000) MRF-4 exhibits fiber type- and muscle-specific pattern of expression in postnatal rat muscle. Am J Physiol Regul Integr Comp Physiol 278(5):R1381–R1384

    PubMed  CAS  Google Scholar 

  • Watt DJ, Morgan JE, Clifford MA, Partridge TA (1987) The movement of muscle precursor cells between adjacent regenerating muscles in the mouse. Anat Embryol (Berl) 175(4):527–536

    CAS  Google Scholar 

  • Wokke JH, Van den Oord CJ, Leppink GJ, Jennekens FG (1989) Perisynaptic satellite cells in human external intercostal muscle: a quantitative and qualitative study. Anat Rec 223(2):174–180

    PubMed  CAS  Google Scholar 

  • Wozniak AC, Anderson JE (2007) Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236(1):240–250

    PubMed  CAS  Google Scholar 

  • Yerushalmi GM, Leibowitz-Amit R, Shaharabany M, Tsarfaty I (2002) Met-HGF/SF signal transduction induces mimp, a novel mitochondrial carrier homologue, which leads to mitochondrial depolarization. Neoplasia 4(6):510–522

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ying W (2008) NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 10(2):179–206

    PubMed  CAS  Google Scholar 

  • Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166(3):347–357

    PubMed  CAS  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabrice Chretien .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Rocheteau, P., Vinet, M., Chretien, F. (2015). Dormancy and Quiescence of Skeletal Muscle Stem Cells. In: Brand-Saberi, B. (eds) Vertebrate Myogenesis. Results and Problems in Cell Differentiation, vol 56. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-44608-9_10

Download citation

Publish with us

Policies and ethics