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Molecular Regulation of Cellular Quiescence: A Perspective from Adult Stem Cells and Its Niches

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Cellular Quiescence

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1686))

Abstract

Cellular quiescence is a reversible growth arrest state. In response to extracellular environment, quiescent cells are capable of resuming proliferation for tissue homeostasis and tissue regeneration. Subpopulations of adult stem cells remain quiescent and reside in their specialized stem cell niches. Within the niche, they interact with a repertoire of niche components. Niche integrates signals to maintain quiescence or gear stem cells toward regeneration. Recent studies provide insights into the regulatory components of stem cell niche and their influence on residing stem cells. Aberrant niche activities perturb stem cell quiescence and activation, compromise stem cell functions, and contribute to tissue aging and disease pathogenesis. This review covers current knowledge regarding cellular quiescence with a focus on original and emerging concepts of how niches influence stem cell quiescence.

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References

  1. Howard A, Pelc SR (1986) Synthesis of desoxyribonucleic acid in normal and irradiated cells and its relation to chromosome breakage. Int J Radiat Biol Relat Stud Phys Chem Med 49(2):207–218. doi:10.1080/09553008514552501

    Article  CAS  Google Scholar 

  2. Hevesy G (1945) On the effect of roentgen rays on cellular division. Rev Mod Phys 17:102–111. doi:10.1103/RevModPhys.17.102

    Article  CAS  Google Scholar 

  3. Yao G (2014) Modelling mammalian cellular quiescence. Interface Focus 4(3):20130074. doi:10.1098/rsfs.2013.0074

    Article  PubMed  PubMed Central  Google Scholar 

  4. Baserga R (1968) Biochemistry of the cell cycle: A review. Cell Prolif 1(2):167–191. doi:10.1111/j.1365-2184.1968.tb00957.x

    Article  CAS  Google Scholar 

  5. Fausto N (2004) Liver regeneration and repair: hepatocytes, progenitor cells, and stem cells. Hepatol Baltim Md 39(6):1477–1487. doi:10.1002/hep.20214

    Article  Google Scholar 

  6. Bischoff R (1990) Cell cycle commitment of rat muscle satellite cells. J Cell Biol 111(1):201–207

    Article  CAS  PubMed  Google Scholar 

  7. Zetterberg A, Larsson O (1985) Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells. Proc Natl Acad Sci U S A 82(16):5365–5369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Patt HM, Quastler H (1963) Radiation effects on cell renewal and related systems. Physiol Rev 43:357–396

    CAS  PubMed  Google Scholar 

  9. Blomen VA, Boonstra J (2007) Cell fate determination during G1 phase progression. Cell Mol Life Sci 64(23):3084–3104. doi:10.1007/s00018-007-7271-z

    Article  CAS  PubMed  Google Scholar 

  10. Coller HA, Sang L, Roberts JM (2006) A new description of cellular quiescence. PLoS Biol 4(3):e83. doi:10.1371/journal.pbio.0040083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Valentin M, Yang E (2008) Autophagy is activated, but is not required for the G 0 function of BCL-2 or BCL-xL. Cell Cycle 7(17):2762–2768. doi:10.4161/cc.7.17.6595

    Article  CAS  PubMed  Google Scholar 

  12. Temin HM (1971) Stimulation by serum of multiplication of stationary chicken cells. J Cell Physiol 78(2):161–170. doi:10.1002/jcp.1040780202

    Article  CAS  PubMed  Google Scholar 

  13. Stoker MG (1972) The Leeuwenhoek lecture, 1971. Tumour viruses and the sociology of fibroblasts. Proc R Soc Lond B Biol Sci 181(1062):1–17

    Article  CAS  PubMed  Google Scholar 

  14. Polyak K, Kato JY, Solomon MJ, Sherr CJ, Massague J, Roberts JM, Koff A (1994) p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev 8(1):9–22

    Article  CAS  PubMed  Google Scholar 

  15. Benaud CM, Dickson RB (2001) Adhesion-regulated G1 cell cycle arrest in epithelial cells requires the downregulation of c-Myc. Oncogene 20(33):4554–4567. doi:10.1038/sj.onc.1204609

    Article  CAS  PubMed  Google Scholar 

  16. Fausto N (1997) Hepatocytes break the rules of senescence in serial transplantation studies. Is there a limit to their replicative capacity? Am J Pathol 151(5):1187–1189

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Wu JC, Merlino G, Cveklova K, Mosinger B, Fausto N (1994) Autonomous growth in serum-free medium and production of hepatocellular carcinomas by differentiated hepatocyte lines that overexpress transforming growth factor alpha 1. Cancer Res 54(22):5964–5973

    CAS  PubMed  Google Scholar 

  18. Zetterberg A, Larsson O (1991) Coordination between cell growth and cell cycle transit in animal cells. Cold Spring Harb Symp Quant Biol 56:137–147

    Article  CAS  PubMed  Google Scholar 

  19. Pardee AB (1974) A restriction point for control of normal animal cell proliferation. Proc Natl Acad Sci U S A 71(4):1286–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zetterberg A, Larsson O, Wiman KG (1995) What is the restriction point? Curr Opin Cell Biol 7(6):835–842

    Article  CAS  PubMed  Google Scholar 

  21. Frolov MV, Dyson NJ (2004) Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J Cell Sci 117(11):2173–2181. doi:10.1242/jcs.01227

    Article  CAS  PubMed  Google Scholar 

  22. Stein GH, Drullinger LF, Soulard A, Dulić V (1999) Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol Cell Biol 19(3):2109–2117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wang W, Martindale JL, Yang X, Chrest FJ, Gorospe M (2005) Increased stability of the p16 mRNA with replicative senescence. EMBO Rep 6(2):158–164. doi:10.1038/sj.embor.7400346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hitomi M, Stacey DW (1999) Cellular ras and cyclin D1 are required during different cell cycle periods in cycling NIH 3T3 cells. Mol Cell Biol 19(7):4623–4632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chassot A-A, Lossaint G, Turchi L, Meneguzzi G, Fisher D, Ponzio G, Dulic V (2008) Confluence-induced cell cycle exit involves pre-mitotic CDK inhibition by p27 (Kip1) and cyclin D1 downregulation. Cell Cycle Georget Tex 7(13):2038–2046. doi:10.4161/cc.7.13.6233

    Article  CAS  Google Scholar 

  26. Spencer SL, Cappell SD, Tsai F-C, Overton KW, Wang CL, Meyer T (2013) The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell 155(2):369–383. doi:10.1016/j.cell.2013.08.062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rodgers JT, King KY, Brett JO, Cromie MJ, Charville GW, Maguire KK, Brunson C, Mastey N, Liu L, Tsai C-R, Goodell MA, Rando TA (2014) mTORC1 controls the adaptive transition of quiescent stem cells from G0 to G(Alert). Nature 510(7505):393–396. doi:10.1038/nature13255

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Bradley TR, Metcalf D (1966) The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci 44(3):287–299

    Article  CAS  PubMed  Google Scholar 

  29. Dexter TM, Allen TD, Lajtha LG (1977) Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol 91(3):335–344. doi:10.1002/jcp.1040910303

    Article  CAS  PubMed  Google Scholar 

  30. Scadden DT (2006) The stem-cell niche as an entity of action. Nature 441(7097):1075–1079. doi:10.1038/nature04957

    Article  CAS  PubMed  Google Scholar 

  31. Lord BI, Testa NG, Hendry JH (1975) The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood 46(1):65–72

    CAS  PubMed  Google Scholar 

  32. Lambertsen RH, Weiss L (1984) A model of intramedullary hematopoietic microenvironments based on stereologic study of the distribution of endocloned marrow colonies. Blood 63(2):287–297

    CAS  PubMed  Google Scholar 

  33. Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4(1–2):7–25

    CAS  PubMed  Google Scholar 

  34. Kimble JE, White JG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81(2):208–219

    Article  CAS  PubMed  Google Scholar 

  35. Austin J, Kimble J (1987) glp-1 Is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51(4):589–599. doi:10.1016/0092-8674(87)90128-0

    Article  CAS  PubMed  Google Scholar 

  36. Hsu Y-C, Fuchs E (2012) A family business: stem cell progeny join the niche to regulate homeostasis. Nat Rev Mol Cell Biol 13(2):103–114. doi:10.1038/nrm3272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Scadden DT (2014) Nice neighborhood: emerging concepts of the stem cell niche. Cell 157(1):41–50. doi:10.1016/j.cell.2014.02.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Olson TS, Caselli A, Otsuru S, Hofmann TJ, Williams R, Paolucci P, Dominici M, Horwitz EM (2013) Megakaryocytes promote murine osteoblastic HSC niche expansion and stem cell engraftment after radioablative conditioning. Blood 121(26):5238–5249. doi:10.1182/blood-2012-10-463414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Heazlewood SY, Neaves RJ, Williams B, Haylock DN, Adams TE, Nilsson SK (2013) Megakaryocytes co-localise with hemopoietic stem cells and release cytokines that up-regulate stem cell proliferation. Stem Cell Res 11(2):782–792. doi:10.1016/j.scr.2013.05.007

    Article  CAS  PubMed  Google Scholar 

  40. Bruns I, Lucas D, Pinho S, Ahmed J, Lambert MP, Kunisaki Y, Scheiermann C, Schiff L, Poncz M, Bergman A, Frenette PS (2014) Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat Med 20(11):1315–1320. doi:10.1038/nm.3707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zhao M, Perry JM, Marshall H, Venkatraman A, Qian P, He XC, Ahamed J, Li L (2014) Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat Med 20(11):1321–1326. doi:10.1038/nm.3706

    Article  CAS  PubMed  Google Scholar 

  42. Hsu Y-C, Pasolli HA, Fuchs E (2011) Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144(1):92–105. doi:10.1016/j.cell.2010.11.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Brownell I, Guevara E, Bai CB, Loomis CA, Joyner AL (2011) Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 8(5):552–565. doi:10.1016/j.stem.2011.02.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Plikus MV, Mayer JA, de la Cruz D, Baker RE, Maini PK, Maxson R, Chuong C-M (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451(7176):340–344. doi:10.1038/nature06457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Augustine RA, Ladyman SR, Grattan DR (2008) From feeding one to feeding many: hormone-induced changes in bodyweight homeostasis during pregnancy. J Physiol 586(2):387–397. doi:10.1113/jphysiol.2007.146316

    Article  CAS  PubMed  Google Scholar 

  46. Craven AJ, Ormandy CJ, Robertson FG, Wilkins RJ, Kelly PA, Nixon AJ, Pearson AJ (2001) Prolactin signaling influences the timing mechanism of the hair follicle: analysis of hair growth cycles in prolactin receptor knockout mice. Endocrinology 142(6):2533–2539. doi:10.1210/endo.142.6.8179

    Article  CAS  PubMed  Google Scholar 

  47. Craven AJ, Nixon AJ, Ashby MG, Ormandy CJ, Blazek K, Wilkins RJ, Pearson AJ (2006) Prolactin delays hair regrowth in mice. J Endocrinol 191(2):415–425. doi:10.1677/joe.1.06685

    Article  CAS  PubMed  Google Scholar 

  48. Goldstein J, Fletcher S, Roth E, Wu C, Chun A, Horsley V (2014) Calcineurin/Nfatc1 signaling links skin stem cell quiescence to hormonal signaling during pregnancy and lactation. Genes Dev 28(9):983–994. doi:10.1101/gad.236554.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wu X, Rathbone CR (2013) Satellite cell functional alterations following cutaneous burn in rats include an increase in their osteogenic potential. J Surg Res 184(2):e9–16. doi:10.1016/j.jss.2013.03.046

    Article  CAS  PubMed  Google Scholar 

  50. Wu X, Walters TJ, Rathbone CR (2013) Skeletal muscle satellite cell activation following cutaneous burn in rats. Burns 39(4):736–744. doi:10.1016/j.burns.2012.10.016

    Article  PubMed  Google Scholar 

  51. Cheung TH, Rando TA (2013) Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 14(6):329–340. doi:10.1038/nrm3591

    Article  CAS  PubMed  Google Scholar 

  52. Cotsarelis G, Sun TT, Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61(7):1329–1337

    Article  CAS  PubMed  Google Scholar 

  53. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118(5):635–648. doi:10.1016/j.cell.2004.08.012

    Article  CAS  PubMed  Google Scholar 

  54. Müller-Röver S, Handjiski B, van der Veen C, Eichmüller S, Foitzik K, McKay IA, Stenn KS, Paus R (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117(1):3–15. doi:10.1046/j.0022-202x.2001.01377.x

    Article  PubMed  Google Scholar 

  55. Morris RJ, Potten CS (1999) Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen. J Invest Dermatol 112(4):470–475. doi:10.1046/j.1523-1747.1999.00537.x

    Article  CAS  PubMed  Google Scholar 

  56. Greco V, Chen T, Rendl M, Schober M, Pasolli HA, Stokes N, Dela Cruz-Racelis J, Fuchs E (2009) A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4(2):155–169. doi:10.1016/j.stem.2008.12.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zhang YV, Cheong J, Ciapurin N, McDermitt DJ, Tumbar T (2009) Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5(3):267–278. doi:10.1016/j.stem.2009.06.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Botchkarev VA, Botchkareva NV, Roth W, Nakamura M, Chen LH, Herzog W, Lindner G, McMahon JA, Peters C, Lauster R, McMahon AP, Paus R (1999) Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat Cell Biol 1(3):158–164. doi:10.1038/11078

    Article  CAS  PubMed  Google Scholar 

  59. Oshimori N, Fuchs E (2012) Paracrine TGF-β signaling counterbalances BMP-mediated repression in hair follicle stem cell activation. Cell Stem Cell 10(1):63–75. doi:10.1016/j.stem.2011.11.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E (2008) NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132(2):299–310. doi:10.1016/j.cell.2007.11.047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kobielak K, Pasolli HA, Alonso L, Polak L, Fuchs E (2003) Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J Cell Biol 163(3):609–623. doi:10.1083/jcb.200309042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Festa E, Fretz J, Berry R, Schmidt B, Rodeheffer M, Horowitz M, Horsley V (2011) Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146(5):761–771. doi:10.1016/j.cell.2011.07.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W (2001) beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105(4):533–545

    Article  CAS  PubMed  Google Scholar 

  64. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S, Lin JS, Sawicki JA, Cotsarelis G (2004) Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22(4):411–417. doi:10.1038/nbt950

    Article  CAS  PubMed  Google Scholar 

  65. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E (2004) Defining the epithelial stem cell niche in skin. Science 303(5656):359–363. doi:10.1126/science.1092436

    Article  CAS  PubMed  Google Scholar 

  66. Van Mater D, Kolligs FT, Dlugosz AA, Fearon ER (2003) Transient activation of beta -catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev 17(10):1219–1224. doi:10.1101/gad.1076103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Lowry WE, Blanpain C, Nowak JA, Guasch G, Lewis L, Fuchs E (2005) Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev 19(13):1596–1611. doi:10.1101/gad.1324905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lien W-H, Polak L, Lin M, Lay K, Zheng D, Fuchs E (2014) In vivo transcriptional governance of hair follicle stem cells by canonical Wnt regulators. Nat Cell Biol 16(2):179–190. doi:10.1038/ncb2903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Botchkarev VA, Botchkareva NV, Nakamura M, Huber O, Funa K, Lauster R, Paus R, Gilchrest BA (2001) Noggin is required for induction of the hair follicle growth phase in postnatal skin. FASEB J 15(12):2205–2214. doi:10.1096/fj.01-0207com

    Article  CAS  PubMed  Google Scholar 

  70. Kobielak K, Stokes N, de la Cruz J, Polak L, Fuchs E (2007) Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc Natl Acad Sci U S A 104(24):10063–10068. doi:10.1073/pnas.0703004104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Lo Celso C, Prowse DM, Watt FM (2004) Transient activation of beta-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Dev Camb Engl 131(8):1787–1799. doi:10.1242/dev.01052

    CAS  Google Scholar 

  72. Tomita Y, Akiyama M, Shimizu H (2006) PDGF isoforms induce and maintain anagen phase of murine hair follicles. J Dermatol Sci 43(2):105–115. doi:10.1016/j.jdermsci.2006.03.012

    Article  CAS  PubMed  Google Scholar 

  73. Ema H, Suda T (2012) Two anatomically distinct niches regulate stem cell activity. Blood 120(11):2174–2181. doi:10.1182/blood-2012-04-424507

    Article  CAS  PubMed  Google Scholar 

  74. Suda T, Suda J, Ogawa M (1983) Proliferative kinetics and differentiation of murine blast cell colonies in culture: evidence for variable G0 periods and constant doubling rates of early pluripotent hemopoietic progenitors. J Cell Physiol 117(3):308–318. doi:10.1002/jcp.1041170305

    Article  CAS  PubMed  Google Scholar 

  75. Cheshier SH, Morrison SJ, Liao X, Weissman IL (1999) In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci U S A 96(6):3120–3125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bradford GB, Williams B, Rossi R, Bertoncello I (1997) Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol 25(5):445–453

    CAS  PubMed  Google Scholar 

  77. Morrison SJ, Scadden DT (2014) The bone marrow niche for haematopoietic stem cells. Nature 505(7483):327–334. doi:10.1038/nature12984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar JC, Bergman A, Frenette PS (2013) Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502(7473):637–643. doi:10.1038/nature12612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, Côté D, Rowe DW, Lin CP, Scadden DT (2009) Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457(7225):92–96. doi:10.1038/nature07434

    Article  CAS  PubMed  Google Scholar 

  80. Xie Y, Yin T, Wiegraebe W, He XC, Miller D, Stark D, Perko K, Alexander R, Schwartz J, Grindley JC, Park J, Haug JS, Wunderlich JP, Li H, Zhang S, Johnson T, Feldman RA, Li L (2009) Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457(7225):97–101. doi:10.1038/nature07639

    Article  CAS  PubMed  Google Scholar 

  81. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425(6960):841–846. doi:10.1038/nature02040

    Article  CAS  PubMed  Google Scholar 

  82. Zhang J, Niu C, Ye L, Huang H, He X, Tong W-G, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425(6960):836–841. doi:10.1038/nature02041

    Article  CAS  PubMed  Google Scholar 

  83. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118(2):149–161. doi:10.1016/j.cell.2004.07.004

    Article  CAS  PubMed  Google Scholar 

  84. Yamazaki S, Ema H, Karlsson G, Yamaguchi T, Miyoshi H, Shioda S, Taketo MM, Karlsson S, Iwama A, Nakauchi H (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147(5):1146–1158. doi:10.1016/j.cell.2011.09.053

    Article  CAS  PubMed  Google Scholar 

  85. Dirckx N, Van Hul M, Maes C (2013) Osteoblast recruitment to sites of bone formation in skeletal development, homeostasis, and regeneration. Birth Defects Res C Embryo Today Rev 99(3):170–191. doi:10.1002/bdrc.21047

    Article  CAS  Google Scholar 

  86. Visnjic D, Kalajzic Z, Rowe DW, Katavic V, Lorenzo J, Aguila HL (2004) Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 103(9):3258–3264. doi:10.1182/blood-2003-11-4011

    Article  CAS  PubMed  Google Scholar 

  87. El-Badri NS, Wang BY, Cherry, Good RA (1998) Osteoblasts promote engraftment of allogeneic hematopoietic stem cells. Exp Hematol 26(2):110–116

    Google Scholar 

  88. Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grünewald E, Cheng T, Dombkowski D, Calvi LM, Rittling SR, Scadden DT (2005) Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 201(11):1781–1791. doi:10.1084/jem.20041992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT, Bertoncello I, Bendall LJ, Simmons PJ, Haylock DN (2005) Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 106(4):1232–1239. doi:10.1182/blood-2004-11-4422

    Article  CAS  PubMed  Google Scholar 

  90. Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, Gomei Y, Iwasaki H, Matsuoka S, Miyamoto K, Miyazaki H, Takahashi T, Suda T (2007) Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1(6):685–697. doi:10.1016/j.stem.2007.10.020

    Article  CAS  PubMed  Google Scholar 

  91. Qian H, Buza-Vidas N, Hyland CD, Jensen CT, Antonchuk J, Månsson R, Thoren LA, Ekblom M, Alexander WS, Jacobsen SEW (2007) Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 1(6):671–684. doi:10.1016/j.stem.2007.10.008

    Article  CAS  PubMed  Google Scholar 

  92. Grotewold L, Theil T, Rüther U (1999) Expression pattern of Dkk-1 during mouse limb development. Mech Dev 89(1–2):151–153

    Article  CAS  PubMed  Google Scholar 

  93. MacDonald BT, Adamska M, Meisler MH (2004) Hypomorphic expression of Dkk1 in the doubleridge mouse: dose dependence and compensatory interactions with Lrp6. Development 131(11):2543–2552. doi:10.1242/dev.01126

    Article  CAS  PubMed  Google Scholar 

  94. Fleming HE, Janzen V, Lo Celso C, Guo J, Leahy KM, Kronenberg HM, Scadden DT (2008) Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell 2(3):274–283. doi:10.1016/j.stem.2008.01.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Cobas M, Wilson A, Ernst B, Mancini SJC, MacDonald HR, Kemler R, Radtke F (2004) Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 199(2):221–229. doi:10.1084/jem.20031615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL (2003) A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423(6938):409–414. doi:10.1038/nature01593

    Article  CAS  PubMed  Google Scholar 

  97. Kirstetter P, Anderson K, Porse BT, Jacobsen SEW, Nerlov C (2006) Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 7(10):1048–1056. doi:10.1038/ni1381

    Article  CAS  PubMed  Google Scholar 

  98. Scheller M, Huelsken J, Rosenbauer F, Taketo MM, Birchmeier W, Tenen DG, Leutz A (2006) Hematopoietic stem cell and multilineage defects generated by constitutive beta-catenin activation. Nat Immunol 7(10):1037–1047. doi:10.1038/ni1387

    Article  CAS  PubMed  Google Scholar 

  99. Reya T, O’Riordan M, Okamura R, Devaney E, Willert K, Nusse R, Grosschedl R (2000) Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity 13(1):15–24

    Article  CAS  PubMed  Google Scholar 

  100. Nemeth MJ, Topol L, Anderson SM, Yang Y, Bodine DM (2007) Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci U S A 104(39):15436–15441. doi:10.1073/pnas.0704747104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Murdoch B, Chadwick K, Martin M, Shojaei F, Shah KV, Gallacher L, Moon RT, Bhatia M (2003) Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci U S A 100(6):3422–3427. doi:10.1073/pnas.0130233100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Yamazaki S, Iwama A, Takayanagi S, Eto K, Ema H, Nakauchi H (2009) TGF-β as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 113(6):1250–1256. doi:10.1182/blood-2008-04-146480

    Article  CAS  PubMed  Google Scholar 

  103. Scandura JM, Boccuni P, Massagué J, Nimer SD (2004) Transforming growth factor beta-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc Natl Acad Sci U S A 101(42):15231–15236. doi:10.1073/pnas.0406771101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Jung Y, Wang J, Schneider A, Sun Y-X, Koh-Paige AJ, Osman NI, McCauley LK, Taichman RS (2006) Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone 38(4):497–508. doi:10.1016/j.bone.2005.10.003

    Article  CAS  PubMed  Google Scholar 

  105. Dar A, Goichberg P, Shinder V, Kalinkovich A, Kollet O, Netzer N, Margalit R, Zsak M, Nagler A, Hardan I, Resnick I, Rot A, Lapidot T (2005) Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat Immunol 6(10):1038–1046. doi:10.1038/ni1251

    Article  CAS  PubMed  Google Scholar 

  106. Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977–988. doi:10.1016/j.immuni.2006.10.016

    Article  CAS  PubMed  Google Scholar 

  107. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9(2):493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 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. doi:10.1016/j.cell.2005.05.010

    Article  CAS  PubMed  Google Scholar 

  109. Gilbert PM, Havenstrite KL, Magnusson KEG, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329(5995):1078–1081. doi:10.1126/science.1191035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Relaix F, Rocancourt D, Mansouri A, Buckingham M (2005) A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435(7044):948–953. doi:10.1038/nature03594

    Article  CAS  PubMed  Google Scholar 

  111. Boppart MD, Burkin DJ, Kaufman SJ (2006) α7β1-Integrin regulates mechanotransduction and prevents skeletal muscle injury. Am J Physiol Cell Physiol 290(6):C1660–C1665. doi:10.1152/ajpcell.00317.2005

    Article  CAS  PubMed  Google Scholar 

  112. Shea KL, Xiang W, LaPorta VS, Licht JD, Keller C, Basson MA, Brack AS (2010) Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6(2):117–129. doi:10.1016/j.stem.2009.12.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Jones NC, Tyner KJ, Nibarger L, Stanley HM, Cornelison DDW, 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. doi:10.1083/jcb.200408066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Urciuolo A, Quarta M, Morbidoni V, Gattazzo F, Molon S, Grumati P, Montemurro F, Tedesco FS, Blaauw B, Cossu G, Vozzi G, Rando TA, Bonaldo P (2013) Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat Commun 4:1964. doi:10.1038/ncomms2964

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Bischoff R (1986) A satellite cell mitogen from crushed adult muscle. Dev Biol 115(1):140–147

    Article  CAS  PubMed  Google Scholar 

  116. Bischoff R (1990) Interaction between satellite cells and skeletal muscle fibers. Dev Camb Engl 109(4):943–952

    CAS  Google Scholar 

  117. Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302(5650):1575–1577. doi:10.1126/science.1087573

    Article  CAS  PubMed  Google Scholar 

  118. Dumont NA, Wang YX, Rudnicki MA (2015) Intrinsic and extrinsic mechanisms regulating satellite cell function. Dev Camb Engl 142(9):1572–1581. doi:10.1242/dev.114223

    CAS  Google Scholar 

  119. Fukada S, Yamaguchi M, Kokubo H, Ogawa R, Uezumi A, Yoneda T, Matev MM, Motohashi N, Ito T, Zolkiewska A, Johnson RL, Saga Y, Miyagoe-Suzuki Y, Tsujikawa K, Takeda S, Yamamoto H (2011) Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development 138(21):4609–4619. doi:10.1242/dev.067165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Bjornson CRR, Cheung TH, Liu L, Tripathi PV, Steeper KM, Rando TA (2012) Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30(2):232–242. doi:10.1002/stem.773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Mourikis P, Sambasivan R, Castel D, Rocheteau P, Bizzarro V, Tajbakhsh S (2012) A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30(2):243–252. doi:10.1002/stem.775

    Article  CAS  PubMed  Google Scholar 

  122. Conboy IM, Rando TA (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3(3):397–409

    Article  CAS  PubMed  Google Scholar 

  123. 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. doi:10.1016/j.cell.2007.03.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. 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. doi:10.1634/stemcells.2007-0019

    Article  CAS  PubMed  Google Scholar 

  125. Mourikis P, Gopalakrishnan S, Sambasivan R, Tajbakhsh S (2012) Cell-autonomous Notch activity maintains the temporal specification potential of skeletal muscle stem cells. Dev Camb Engl 139(24):4536–4548. doi:10.1242/dev.084756

    CAS  Google Scholar 

  126. Kardami E, Murphy LJ, Liu L, Padua RR, Fandrich RR (1990) Characterization of two preparations of antibodies to basic fibroblast growth factor which exhibit distinct patterns of immunolocalization. Growth Factors 4(1):69–80

    Article  CAS  PubMed  Google Scholar 

  127. Kästner S, Elias MC, Rivera AJ, Yablonka-Reuveni Z (2000) Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J Histochem Cytochem 48(8):1079–1096

    Article  PubMed  Google Scholar 

  128. Johnson SE, Allen RE (1993) Proliferating cell nuclear antigen (PCNA) is expressed in activated rat skeletal muscle satellite cells. J Cell Physiol 154(1):39–43. doi:10.1002/jcp.1041540106

    Article  CAS  PubMed  Google Scholar 

  129. Yablonka-Reuveni Z, Seger R, Rivera AJ (1999) Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47(1):23–42

    Article  CAS  PubMed  Google Scholar 

  130. Cornelison DDW, Filla MS, Stanley HM, Rapraeger AC, Olwin BB (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239(1):79–94. doi:10.1006/dbio.2001.0416

    Article  CAS  PubMed  Google Scholar 

  131. Cornelison DDW, Wilcox-Adelman SA, Goetinck PF, Rauvala H, Rapraeger AC, Olwin BB (2004) Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18(18):2231–2236. doi:10.1101/gad.1214204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA (1998) sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92(2):253–263

    Article  CAS  PubMed  Google Scholar 

  133. Miller KJ, Thaloor D, Matteson S, Pavlath GK (2000) Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am J Physiol Cell Physiol 278(1):C174–C181

    CAS  PubMed  Google Scholar 

  134. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE (1998) HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol 194(1):114–128. doi:10.1006/dbio.1997.8803

    Article  CAS  PubMed  Google Scholar 

  135. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM (1995) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165(2):307–312. doi:10.1002/jcp.1041650211

    Article  CAS  PubMed  Google Scholar 

  136. Yamada M, Tatsumi R, Kikuiri T, Okamoto S, Nonoshita S, Mizunoya W, Ikeuchi Y, Shimokawa H, Sunagawa K, Allen RE (2006) Matrix metalloproteinases are involved in mechanical stretch-induced activation of skeletal muscle satellite cells. Muscle Nerve 34(3):313–319. doi:10.1002/mus.20601

    Article  CAS  PubMed  Google Scholar 

  137. Gal-Levi R, Leshem Y, Aoki S, Nakamura T, Halevy O (1998) Hepatocyte growth factor plays a dual role in regulating skeletal muscle satellite cell proliferation and differentiation. Biochim Biophys Acta 1402(1):39–51. doi:10.1016/S0167-4889(97)00124-9

    Article  CAS  PubMed  Google Scholar 

  138. Rando TA (2006) Stem cells, ageing and the quest for immortality. Nature 441(7097):1080–1086. doi:10.1038/nature04958

    Article  CAS  PubMed  Google Scholar 

  139. Rossi DJ, Bryder D, Zahn JM, Ahlenius H, Sonu R, Wagers AJ, Weissman IL (2005) Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci U S A 102(26):9194–9199. doi:10.1073/pnas.0503280102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Conboy IM, Rando TA (2012) Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches. Cell Cycle 11(12):2260–2267. doi:10.4161/cc.20437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433(7027):760–764. doi:10.1038/nature03260

    Article  CAS  PubMed  Google Scholar 

  142. Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, Rando TA (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807–810. doi:10.1126/science.1144090

    Article  CAS  PubMed  Google Scholar 

  143. Carlson BM, Faulkner JA (1989) Muscle transplantation between young and old rats: age of host determines recovery. Am J Phys 256(6 Pt 1):C1262–C1266

    CAS  Google Scholar 

  144. Chen C-C, Murray PJ, Jiang TX, Plikus MV, Chang Y-T, Lee OK, Widelitz RB, Chuong C-M (2014) Regenerative hair waves in aging mice and extra-follicular modulators follistatin, dkk1, and sfrp4. J Invest Dermatol 134(8):2086–2096. doi:10.1038/jid.2014.139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, Mikels AJ, Agrawal S, Schaffer DV, Conboy IM (2009) Relative roles of TGF-β1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 8(6):676–689. doi:10.1111/j.1474-9726.2009.00517.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Chakkalakal JV, Jones KM, Basson MA, Brack AS (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490(7420):355–360. doi:10.1038/nature11438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Keyes BE, Segal JP, Heller E, Lien W-H, Chang C-Y, Guo X, Oristian DS, Zheng D, Fuchs E (2013) Nfatc1 orchestrates aging in hair follicle stem cells. Proc Natl Acad Sci U S A 110(51):E4950–E4959. doi:10.1073/pnas.1320301110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Doles J, Storer M, Cozzuto L, Roma G, Keyes WM (2012) Age-associated inflammation inhibits epidermal stem cell function. Genes Dev 26(19):2144–2153. doi:10.1101/gad.192294.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Adams GB, Martin RP, Alley IR, Chabner KT, Cohen KS, Calvi LM, Kronenberg HM, Scadden DT (2007) Therapeutic targeting of a stem cell niche. Nat Biotechnol 25(2):238–243. doi:10.1038/nbt1281

    Article  CAS  PubMed  Google Scholar 

  150. 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. doi:10.1083/jcb.200207056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Fowler JA, Mundy GR, Lwin ST, Edwards CM (2012) Bone marrow stromal cells create a permissive microenvironment for myeloma development: a new stromal role for Wnt inhibitor Dkk1. Cancer Res 72(9):2183–2189. doi:10.1158/0008-5472.CAN-11-2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Gómez-Gaviro MV, Scott CE, Sesay AK, Matheu A, Booth S, Galichet C, Lovell-Badge R (2012) Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis. Proc Natl Acad Sci U S A 109(4):1317–1322. doi:10.1073/pnas.1016199109

    Article  PubMed  PubMed Central  Google Scholar 

  153. Arai F, Ohneda O, Miyamoto T, Zhang XQ, Suda T (2002) Msenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp Med 195(12):1549–1563. doi:10.1084/jem.20011700

  154. Schepers K, Hsiao EC, Garg T, Scott MJ, Passegué E (2012) Activated Gs signaling in osteoblastic cells alters the hematopoietic stem cell niche in mice. Blood 120(17):3425–3435. doi:10.1182/blood-2011-11-395418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Division of Life Science, Center for Stem Cell Research, State Key Laboratory of Molecular Neuroscience, Center of Systems Biology and Human Health, Institute for Advanced Study, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China

    Wai-Kin So & Tom H. Cheung

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    H. Daniel Lacorazza

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So, WK., Cheung, T.H. (2018). Molecular Regulation of Cellular Quiescence: A Perspective from Adult Stem Cells and Its Niches. In: Lacorazza, H. (eds) Cellular Quiescence. Methods in Molecular Biology, vol 1686. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7371-2_1

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