Concise Review: Quiescence in Adult Stem Cells: Biological Significance and Relevance to Tissue Regeneration

Stem Cells

Volumn 33, Issue 10, 2015, Pages 2903-2912

  Rumman, Mohammad ^a,b   Dhawan, Jyotsna ^a,c   Kassem, Moustapha ^d,e,f  

^a Institute for Stem Cell Science and Regenerative Medicine   (India)

^b MANIPAL UNIVERSITY   (India)

^c CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

^e University of Copenhagen   (Denmark)

^f KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Adult stem cells; Cell cycle; Differentiation; Hematopoietic stem cells; Marrow stromal cells; Muscle stem cells; Quiescence

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; RETINOBLASTOMA PROTEIN;

ADULT STEM CELL; CARCINOGENESIS; CELL CYCLE ARREST; CELL DIFFERENTIATION; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; MESENCHYMAL STEM CELL; MESODERM; NONHUMAN; PROTEIN FAMILY; REGULATORY MECHANISM; REVIEW; SKELETAL MUSCLE SATELLITE CELL; TISSUE INJURY; TISSUE REGENERATION; CELL CYCLE CHECKPOINT; GENETICS; REGENERATION; WOUND HEALING;

ADULT STEM CELLS; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; HOMEOSTASIS; HUMANS; REGENERATION; WOUND HEALING;

EID: 84942319012     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2056     Document Type: Review

References (96)

1. Gray JV, Petsko GA, Johnston GC, et al., "Sleeping beauty": Quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2004; 68: 187-206.
2. Herman PK,. Stationary phase in yeast. Curr Opin Microbiol 2002; 5: 602-607.
3. Schultz E, Gibson MC, Champion T,. Satellite cells are mitotically quiescent in mature mouse muscle: An EM and radioautographic study. J Exp Zool 1978; 206: 451-456.
4. Shea KL, Xiang W, LaPorta VS, et al., Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 2010; 6: 117-129.
5. Arai F, Hirao A, Ohmura M, et al., Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118: 149-161.
6. Mourikis P, Sambasivan R, Castel D, et al., A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 2012; 30: 243-252.
7. Coller HA, Sang L, Roberts JM,. A new description of cellular quiescence. PLoS Biol 2006; 4: e83.
8. Lemons JM, Feng XJ, Bennett BD, et al., Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol 2010; 8: e1000514.
9. Sachidanandan C, Sambasivan R, Dhawan J,. Tristetraprolin and LPS-inducible CXC chemokine are rapidly induced in presumptive satellite cells in response to skeletal muscle injury. J Cell Sci 2002; 115: 2701-2712.
10. Subramaniam S, Sreenivas P, Cheedipudi S, et al., Distinct transcriptional networks in quiescent myoblasts: A role for Wnt signaling in reversible vs. irreversible arrest. PloS One 2013; 8: e65097.
11. Fukada S, Uezumi A, Ikemoto M, et al., Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 2007; 25: 2448-2459.
12. Murray AW,. Recycling the cell cycle: Cyclins revisited. Cell 2004; 116: 221-234.
13. Johnson A, Skotheim JM,. Start and the restriction point. Curr Opin Cell Biol 2013; 25: 717-723.
14. Hartwell L,. Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 1992; 71: 543-546.
15. Pardee AB,. A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci USA 1974; 71: 1286-1290.
16. Spencer SL, Cappell SD, Tsai FC, et al., The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell 2013; 155: 369-383.
17. Rodgers JT, King KY, Brett JO, et al., mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature 2014; 510: 393-396.
18. Bischoff R,. Cell cycle commitment of rat muscle satellite cells. J Cell Biol 1990; 111: 201-207.
19. Bravo R, Macdonald-Bravo H,. Induction of the nuclear protein 'cyclin' in quiescent mouse 3T3 cells stimulated by serum and growth factors. Correlation with DNA synthesis. EMBO J 1984; 3: 3177-3181.
20. Gerdes J, Li L, Schlueter C, et al., Immunobiochemical and molecular biologic characterization of the cell proliferation-associated nuclear antigen that is defined by monoclonal antibody Ki-67. Am J Pathol 1991; 138: 867-873.
21. Rhee WJ, Bao G,. Simultaneous detection of mRNA and protein stem cell markers in live cells. BMC Biotechnol 2009; 9: 30.
22. Kubota Y, Takubo K, Suda T,. Bone marrow long label-retaining cells reside in the sinusoidal hypoxic niche. Biochem Biophys Res Commun 2008; 366: 335-339.
23. Duvillie B, Attali M, Aiello V, et al., Label-retaining cells in the rat pancreas: Location and differentiation potential in vitro. Diabetes 2003; 52: 2035-2042.
24. Giachino C, Taylor V,. Lineage analysis of quiescent regenerative stem cells in the adult brain by genetic labelling reveals spatially restricted neurogenic niches in the olfactory bulb. Eur J Neurosci 2009; 30: 9-24.
25. Chakkalakal JV, Jones KM, Basson MA, et al., The aged niche disrupts muscle stem cell quiescence. Nature 2012; 490: 355-360.
26. Foudi A, Hochedlinger K, Van Buren D, et al., Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 2009; 27: 84-90.
27. Van Zant G,. Studies of hematopoietic stem cells spared by 5-fluorouracil. J Exp Med 1984; 159: 679-690.
28. Heslop L, Morgan JE, Partridge TA,. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 2000; 113: 2299-2308.
29. Oki T, Nishimura K, Kitaura J, et al., A novel cell-cycle-indicator, mVenus-p27K-, identifies quiescent cells and visualizes G0-G1 transition. Sci Rep 2014; 4: 4012.
30. Macpherson I, Montagnier L,. Agar Suspension Culture for the Selective Assay of Cells Transformed by Polyoma Virus. Virology 1964; 23: 291-294.
31. Benecke BJ, Ben-Ze'ev A, Penman S,. The control of mRNA production, translation and turnover in suspended and reattached anchorage-dependent fibroblasts. Cell 1978; 14: 931-939.
32. Dike LE, Farmer SR,. Cell adhesion induces expression of growth-associated genes in suspension-arrested fibroblasts. Proc Natl Acad Sci USA 1988; 85: 6792-6796.
33. Yaffe D, Saxel O,. A myogenic cell line with altered serum requirements for differentiation. Differentiation 1977; 7: 159-166.
34. Frisch SM, Francis H,. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994; 124: 619-626.
35. Milasincic DJ, Dhawan J, Farmer SR,. Anchorage-dependent control of muscle-specific gene expression in C2C12 mouse myoblasts. In Vitro Cell Dev Biol Anim 1996; 32: 90-99.
36. Winer JP, Janmey PA, McCormick ME, et al., Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A 2009; 15: 147-154.
37. Dhawan J, Helfman DM,. Modulation of acto-myosin contractility in skeletal muscle myoblasts uncouples growth arrest from differentiation. J Cell Sci 2004; 117: 3735-3748.
38. Cheng T, Rodrigues N, Shen H, et al., Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000; 287: 1804-1808.
39. Bradford GB, Williams B, Rossi R, et al., Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol 1997; 25: 445-453.
40. Wilson A, Laurenti E, Oser G, et al., Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008; 135: 1118-1129.
41. Seale P, Sabourin LA, Girgis-Gabardo A, et al., Pax7 is required for the specification of myogenic satellite cells. Cell 2000; 102: 777-786.
42. Grounds MD, Garrett KL, Lai MC, et al., Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 1992; 267: 99-104.
43. Mauro A,. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961; 9: 493-495.
44. Irintchev A, Zeschnigk M, Starzinski-Powitz A, et al., Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dynam 1994; 199: 326-337.
45. Cornelison DD, Wold BJ,. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 1997; 191: 270-283.
46. Wakeford S, Watt DJ, Partridge TA,. X-irradiation improves mdx mouse muscle as a model of myofiber loss in DMD. Muscle Nerve 1991; 14: 42-50.
47. Gnocchi VF, White RB, Ono Y, et al., Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PloS One 2009; 4: e5205.
48. Friedenstein AJ, Gorskaja JF, Kulagina NN,. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976; 4: 267-274.
49. da Silva Meirelles L, Chagastelles PC, Nardi NB,. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006; 119: 2204-2213.
50. Morikawa S, Mabuchi Y, Kubota Y, et al., Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009; 206: 2483-2496.
51. Gronthos S, Zannettino AC, Hay SJ, et al., Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003; 116: 1827-1835.
52. Haas RJ, Bohne F, Fliedner TM,. On the development of slowly-turning-over cell types in neonatal rat bone marrow (studies utilizing the complete tritiated thymidine labelling method complemented by C-14 thymidine administration). Blood 1969; 34: 791-805.
53. Falla N, Van V, Bierkens J, et al., Characterization of a 5-fluorouracil-enriched osteoprogenitor population of the murine bone marrow. Blood 1993; 82: 3580-3591.
54. Worthley DL, Churchill M, Compton JT, et al., Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell 2015; 160: 269-284.
55. Fukada S,. Molecular regulation of muscle stem cells by 'quiescence genes'. Yakugaku Zasshi 2011; 131: 1329-1332.
56. Crespo JL, Hall MN,. Elucidating TOR signaling and rapamycin action: Lessons from Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2002; 66: 579-591, table of contents.
57. Voorhoeve PM, Agami R,. Unraveling human tumor suppressor pathways: A tale of the INK4A locus. Cell Cycle 2004; 3: 616-620.
58. Matsumoto A, Takeishi S, Kanie T, et al., p57 is required for quiescence and maintenance of adult hematopoietic stem cells. Cell Stem Cell 2011; 9: 262-271.
59. Weinberg RA,. The retinoblastoma protein and cell cycle control. Cell 1995; 81: 323-330.
60. LeCouter JE, Kablar B, Hardy WR, et al., Strain-dependent myeloid hyperplasia, growth deficiency, and accelerated cell cycle in mice lacking the Rb-related p107 gene. Mol Cell Biol 1998; 18: 7455-7465.
61. Viatour P, Somervaille TC, Venkatasubrahmanyam S, et al., Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 2008; 3: 416-428.
62. Sankaran VG, Orkin SH, Walkley CR,. Rb intrinsically promotes erythropoiesis by coupling cell cycle exit with mitochondrial biogenesis. Genes Dev 2008; 22: 463-475.
63. Hosoyama T, Nishijo K, Prajapati SI, et al., Rb1 gene inactivation expands satellite cell and postnatal myoblast pools. J Biol Chem 2011; 286: 19556-19564.
64. Huh MS, Parker MH, Scime A, et al., Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J Cell Biol 2004; 166: 865-876.
65. Carnac G, Fajas L, L'Honore A, et al., The retinoblastoma-like protein p130 is involved in the determination of reserve cells in differentiating myoblasts. Curr Biol 2000; 10: 543-546.
66. Sherr CJ, Roberts JM,. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 1999; 13: 1501-1512.
67. Zou P, Yoshihara H, Hosokawa K, et al., p57(Kip2) and p27(Kip1) cooperate to maintain hematopoietic stem cell quiescence through interactions with Hsc70. Cell Stem Cell 2011; 9: 247-261.
68. Zhang P, Wong C, Liu D, et al., p21(CIP1) and p57(KIP2) control muscle differentiation at the myogenin step. Genes Dev 1999; 13: 213-224.
69. Fleming HE, Janzen V, Lo Celso C, et al., Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell 2008; 2: 274-283.
70. Walkley CR, Olsen GH, Dworkin S, et al., A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell 2007; 129: 1097-1110.
71. Abou-Khalil R, Le Grand F, Pallafacchina G, et al., Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell 2009; 5: 298-309.
72. Grenier G, Scime A, Le Grand F, et al., Resident endothelial precursors in muscle, adipose, and dermis contribute to postnatal vasculogenesis. Stem Cells 2007; 25: 3101-3110.
73. Trensz F, Haroun S, Cloutier A, et al., A muscle resident cell population promotes fibrosis in hindlimb skeletal muscles of mdx mice through the Wnt canonical pathway. Am J Physiol Cell physiol 2010; 299: C939-947.
74. Brack AS, Conboy MJ, Roy S, et al., Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007; 317: 807-810.
75. Calvi LM, Adams GB, Weibrecht KW, et al., Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841-846.
76. Miller KJ, Thaloor D, Matteson S, et al., Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol 2000; 278: C174-181.
77. Reya T, Duncan AW, Ailles L, et al., A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003; 423: 409-414.
78. Liu J, Sato C, Cerletti M, et al., Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 2010; 92: 367-409.
79. Varnum-Finney B, Xu L, Brashem-Stein C, et al., Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat Med 2000; 6: 1278-1281.
80. Duncan AW, Rattis FM, DiMascio LN, et al., Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 2005; 6: 314-322.
81. Li L, Milner LA, Deng Y, et al., The human homolog of rat Jagged1 expressed by marrow stroma inhibits differentiation of 32D cells through interaction with Notch1. Immunity 1998; 8: 43-55.
82. Conboy IM, Rando TA,. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 2002; 3: 397-409.
83. Wen Y, Bi P, Liu W, et al., Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cellular Biol 2012; 32: 2300-2311.
84. Bjornson CR, Cheung TH, Liu L, et al., Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 2012; 30: 232-242.
85. Pouyssegur J, Volmat V, Lenormand P,. Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling. Biochem Pharmacol 2002; 64: 755-763.
86. Shi H, Boadu E, Mercan F, et al., MAP kinase phosphatase-1 deficiency impairs skeletal muscle regeneration and exacerbates muscular dystrophy. FASEB J 2010; 24: 2985-2997.
87. Baeza-Raja B, Munoz-Canoves P,. p38 MAPK-induced nuclear factor-kappaB activity is required for skeletal muscle differentiation: Role of interleukin-6. Mol Biol Cell 2004; 15: 2013-2026.
88. Lin H,. Cell biology of stem cells: An enigma of asymmetry and self-renewal. J Cell Biol 2008; 180: 257-260.
89. Troy A, Cadwallader AB, Fedorov Y, et al., Coordination of satellite cell activation and self-renewal by Par-complex-dependent asymmetric activation of p38alpha/beta MAPK. Cell Stem Cell 2012; 11: 541-553.
90. Wilson A, Murphy MJ, Oskarsson T, et al., c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev 2004; 18: 2747-2763.
91. Will B, Vogler TO, Bartholdy B, et al., Satb1 regulates the self-renewal of hematopoietic stem cells by promoting quiescence and repressing differentiation commitment. Nat Immunol 2013; 14: 437-445.
92. Sousa-Victor P, Perdiguero E, Munoz-Canoves P,. Geroconversion of aged muscle stem cells under regenerative pressure. Cell Cycle 2014; 13: 3183-3190.
93. Cheung TH, Quach NL, Charville GW, et al., Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 2012; 482: 524-528.
94. Ikemoto M, Fukada S, Uezumi A, et al., Autologous transplantation of SM/C-2.6(+) satellite cells transduced with micro-dystrophin CS1 cDNA by lentiviral vector into mdx mice. Mol Ther 2007; 15: 2178-2185.
95. Pallafacchina G, Francois S, Regnault B, et al., 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 2010; 4: 77-91.
96. Takubo K, Goda N, Yamada W, et al., Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010; 7: 391-402.