Skip to main content
SpringerLink
Log in

Asymmetric Behavior in Stem Cells

  • Chapter
Regulatory Networks in Stem Cells

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

Abstract

Asymmetry in the stem cell niche refers to the notion that daughter cells are different from each other. There is significant evidence that many stem cell divisions result in one daughter cell that is similar to the parent cell and, hence, necessarily allows for self-renewal of the stem cell phenotype, whereas the other daughter cell is a differentiated or committed cell type. In this chapter we will discuss the role of asymmetry in stem cell divisions and the evidence that supports different asymmetric scenarios in different model systems. We first present the early asymmetric divisions that have been described in first divisions of the zygote and in gametogenesis. Next, we will discuss evidence of asymmetry in postnatal stem cells. Here we will describe two systems in particular – the hematopoietic system and muscle stem cells. Lastly, we will present a theory of the immortal strand hypothesis in which the role of DNA strand segregation is discussed as it relates to asymmetry in cell divisions and the protection of the self-renewing stem cell.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
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

Similar content being viewed by others

References

  1. Spemann H. Embryonic development and induction. New Haven, London: Yale University Press; H. Milford, Oxford University Press; 1938.

    Google Scholar 

  2. Cibelli JB. Principles of cloning. Amsterdam; Boston: Academic Press; 2002.

    Google Scholar 

  3. Sell S. Stem cells handbook. Totowa, NJ: Humana Press; 2004.

    Google Scholar 

  4. Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983;100(1):64–119.

    PubMed  CAS  Google Scholar 

  5. Schnabel R, Hutter H, Moerman D, Schnabel H. Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev Biol. 1997;184(2):234–65.

    PubMed  CAS  Google Scholar 

  6. Betschinger J, Knoblich JA. Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Curr Biol. 2004;14(16):R674–85.

    PubMed  CAS  Google Scholar 

  7. Zernicka-Goetz M. Patterning of the embryo: the first spatial decisions in the life of a mouse. Development. 2002;129(4):815–29.

    PubMed  CAS  Google Scholar 

  8. Beddington RS, Robertson EJ. Axis development and early asymmetry in mammals. Cell. 1999;96(2):195–209.

    PubMed  CAS  Google Scholar 

  9. Piotrowska K, Zernicka-Goetz M. Role for sperm in spatial patterning of the early mouse embryo. Nature. 2001;409(6819): 517–21.

    PubMed  CAS  Google Scholar 

  10. Plusa B, Piotrowska K, Zernicka-Goetz M. Sperm entry position provides a surface marker for the first cleavage plane of the mouse zygote. Genesis. 2002;32(3):193–8.

    PubMed  Google Scholar 

  11. Gardner RL. The early blastocyst is bilaterally symmetrical and its axis of symmetry is aligned with the animal-vegetal axis of the zygote in the mouse. Development. 1997;124(2):289–301.

    PubMed  CAS  Google Scholar 

  12. Ciemerych MA, Mesnard D, Zernicka-Goetz M. Animal and vegetal poles of the mouse egg predict the polarity of the embryonic axis, yet are nonessential for development. Development. 2000;127(16):3467–74.

    PubMed  CAS  Google Scholar 

  13. Saffman EE, Lasko P. Germline development in vertebrates and invertebrates. Cell Mol Life Sci. 1999;55(8–9):1141–63.

    PubMed  CAS  Google Scholar 

  14. Raz E. Primordial germ-cell development: the zebrafish perspective. Nat Rev Genet. 2003;4(9):690–700.

    PubMed  CAS  Google Scholar 

  15. Mahowald AP. Polar granules of Drosophila. 3. The continuity of polar granules during the life cycle of Drosophila. J Exp Zool. 1971;176(3):329–43.

    PubMed  CAS  Google Scholar 

  16. Ham RG, Veomett MJ. Mechanisms of development. St. Louis: Mosby; 1980.

    Google Scholar 

  17. Wilson EB. The cell in development and heredity. 3rd ed. New York: Macmillan; 1925.

    Google Scholar 

  18. Underwood EM, Caulton JH, Allis CD, Mahowald AP. Developmental fate of pole cells in Drosophila melanogaster. Dev Biol. 1980;77(2):303–14.

    PubMed  CAS  Google Scholar 

  19. Wylie C. Germ cells. Cell. 1999;96(2):165–74.

    PubMed  CAS  Google Scholar 

  20. Tam PP, Zhou SX. The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol. 1996;178(1):124–32.

    PubMed  CAS  Google Scholar 

  21. Lawson KA, Dunn NR, Roelen BA, et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999;13(4):424–36.

    PubMed  CAS  Google Scholar 

  22. Hardy RW, Tokuyasu KT, Lindsley DL, Garavito M. The germinal proliferation center in the testis of Drosophila melanogaster. J Ultrastruct Res. 1979;69(2):180–90.

    PubMed  CAS  Google Scholar 

  23. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science. 2001;294(5551):2542–5.

    PubMed  CAS  Google Scholar 

  24. Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science. 2001;294(5551):2546–9.

    PubMed  CAS  Google Scholar 

  25. Kiger AA, White-Cooper H, Fuller MT. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature. 2000;407(6805):750–4.

    PubMed  CAS  Google Scholar 

  26. Harrison DA, McCoon PE, Binari R, Gilman M, Perrimon N. Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 1998;12(20): 3252–63.

    PubMed  CAS  Google Scholar 

  27. Yamashita YM, Fuller MT, Jones DL. Signaling in stem cell niches: lessons from the Drosophila germline. J Cell Sci. 2005;118(Pt 4):665–72.

    PubMed  CAS  Google Scholar 

  28. Tran J, Brenner TJ, DiNardo S. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature. 2000;407(6805):754–7.

    PubMed  CAS  Google Scholar 

  29. Schulz C, Wood CG, Jones DL, Tazuke SI, Fuller MT. Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development. 2002;129(19):4523–34.

    PubMed  CAS  Google Scholar 

  30. Yamashita YM, Jones DL, Fuller MT. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science. 2003;301(5639):1547–50.

    PubMed  CAS  Google Scholar 

  31. Barton SC, Surani MA, Norris ML. Role of paternal and maternal genomes in mouse development. Nature. 1984;311(5984):374–6.

    PubMed  CAS  Google Scholar 

  32. Reik W, Santos F, Mitsuya K, Morgan H, Dean W. Epigenetic asymmetry in the mammalian zygote and early embryo: relationship to lineage commitment? Philos Trans R Soc Lond B Biol Sci. 2003;358(1436):1403–9; discussion 9.

    PubMed  CAS  Google Scholar 

  33. Lane N, Dean W, Erhardt S, et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003;35(2):88–93.

    PubMed  CAS  Google Scholar 

  34. Haaf T. Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development. Curr Top Microbiol Immunol. 2006;310:13–22.

    PubMed  CAS  Google Scholar 

  35. Nakamura T, Arai Y, Umehara H, et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol. 2007;9(1):64–71.

    PubMed  CAS  Google Scholar 

  36. Chapman V, Forrester L, Sanford J, Hastie N, Rossant J. Cell lineage-specific undermethylation of mouse repetitive DNA. Nature. 1984;307(5948):284–6.

    PubMed  CAS  Google Scholar 

  37. Kalantry S, Mills KC, Yee D, Otte AP, Panning B, Magnuson T. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat Cell Biol. 2006;8(2):195–202.

    PubMed  CAS  Google Scholar 

  38. Donovan PJ. The germ cell-the mother of all stem cells. Int J Dev Biol. 1998;42(7):1043–50.

    PubMed  CAS  Google Scholar 

  39. Zhong W. Diversifying neural cells through order of birth and asymmetry of division. Neuron. 2003;37(1):11–4.

    PubMed  CAS  Google Scholar 

  40. Roegiers F, Younger-Shepherd S, Jan LY, Jan YN. Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat Cell Biol. 2001;3(1):58–67.

    PubMed  CAS  Google Scholar 

  41. Wang H, Chia W. Drosophila neural progenitor polarity and asymmetric division. Biol Cell. 2005;97(1):63–74.

    PubMed  CAS  Google Scholar 

  42. Jan YN, Jan LY. Asymmetric cell division in the Drosophila nervous system. Nat Rev Neurosci. 2001;2(11):772–9.

    PubMed  CAS  Google Scholar 

  43. Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron. 1996;17(1):43–53.

    PubMed  CAS  Google Scholar 

  44. Rhyu MS, Jan LY, Jan YN. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell. 1994;76(3):477–91.

    PubMed  CAS  Google Scholar 

  45. Orgogozo V, Schweisguth F, Bellaiche Y. Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo. Development. 2001;128(5):631–43.

    PubMed  CAS  Google Scholar 

  46. Berdnik D, Torok T, Gonzalez-Gaitan M, Knoblich JA. The endo- cytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev Cell. 2002;3(2):221–31.

    PubMed  CAS  Google Scholar 

  47. Kraut R, Chia W, Jan LY, Jan YN, Knoblich JA. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature. 1996;383(6595):50–5.

    PubMed  CAS  Google Scholar 

  48. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science. 1999;284(5415):770–6.

    PubMed  CAS  Google Scholar 

  49. Zhong W, Jiang MM, Weinmaster G, Jan LY, Jan YN. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development. 1997;124(10):1887–97.

    PubMed  CAS  Google Scholar 

  50. Johnson GR, Metcalf D. Pure and mixed erythroid colony formation in vitro stimulated by spleen conditioned medium with no detectable erythropoietin. Proc Natl Acad Sci U S A. 1977;74(9):3879–82.

    PubMed  CAS  Google Scholar 

  51. Fauser AA, Messner HA. Granuloerythropoietic colonies in human bone marrow, peripheral blood, and cord blood. Blood. 1978;52(6):1243–8.

    PubMed  CAS  Google Scholar 

  52. Suda T, Suda J, Ogawa M. Single-cell origin of mouse hemopoietic colonies expressing multiple lineages in variable combinations. Proc Natl Acad Sci U S A. 1983;80(21):6689–93.

    PubMed  CAS  Google Scholar 

  53. Suda J, Suda T, Ogawa M. Analysis of differentiation of mouse hemopoietic stem cells in culture by sequential replating of paired progenitors. Blood. 1984;64(2):393–9.

    PubMed  CAS  Google Scholar 

  54. Suda T, Suda J, Ogawa M. Disparate differentiation in mouse hemopoietic colonies derived from paired progenitors. Proc Natl Acad Sci U S A. 1984;81(8):2520–4.

    PubMed  CAS  Google Scholar 

  55. Leary AG, Ogawa M, Strauss LC, Civin CI. Single cell origin of multilineage colonies in culture. Evidence that differentiation of multipotent progenitors and restriction of proliferative potential of monopotent progenitors are stochastic processes. J Clin Invest. 1984;74(6):2193–7.

    CAS  Google Scholar 

  56. Leary AG, Strauss LC, Civin CI, Ogawa M. Disparate differentiation in hemopoietic colonies derived from human paired progenitors. Blood. 1985;66(2):327–32.

    PubMed  CAS  Google Scholar 

  57. Mayani H, Dragowska W, Lansdorp PM. Lineage commitment in human hemopoiesis involves asymmetric cell division of multipotent progenitors and does not appear to be influenced by cytokines. J Cell Physiol. 1993;157(3):579–86.

    PubMed  CAS  Google Scholar 

  58. Brummendorf TH, Dragowska W, Zijlmans J, Thornbury G, Lansdorp PM. Asymmetric cell divisions sustain long-term hematopoiesis from single-sorted human fetal liver cells. J Exp Med. 1998;188(6):1117–24.

    PubMed  CAS  Google Scholar 

  59. Healy L, May G, Gale K, Grosveld F, Greaves M, Enver T. The stem cell antigen CD34 functions as a regulator of hemopoietic cell adhesion. Proc Natl Acad Sci U S A. 1995;92(26): 12240–4.

    PubMed  CAS  Google Scholar 

  60. Hu MC, Chien SL. The cytoplasmic domain of stem cell antigen CD34 is essential for cytoadhesion signaling but not sufficient for proliferation signaling. Blood. 1998;91(4):1152–62.

    PubMed  CAS  Google Scholar 

  61. Huang S, Law P, Francis K, Palsson BO, Ho AD. Symmetry of initial cell divisions among primitive hematopoietic progenitors is independent of ontogenic age and regulatory molecules. Blood. 1999;94(8):2595–604.

    PubMed  CAS  Google Scholar 

  62. Punzel M, Zhang T, Liu D, Eckstein V, Ho AD. Functional analysis of initial cell divisions defines the subsequent fate of individual human CD34(+)CD38(–) cells. Exp Hematol. 2002;30(5): 464–72.

    PubMed  CAS  Google Scholar 

  63. Punzel M, Liu D, Zhang T, Eckstein V, Miesala K, Ho AD. The symmetry of initial divisions of human hematopoietic progenitors is altered only by the cellular microenvironment. Exp Hematol. 2003;31(4):339–47.

    PubMed  Google Scholar 

  64. Giebel B, Zhang T, Beckmann J, et al. Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division. Blood. 2006;107(5): 2146–52.

    PubMed  CAS  Google Scholar 

  65. Bullock TE, Wen B, Marley SB, Gordon MY. Potential of CD34 in the regulation of symmetrical and asymmetrical divisions by hematopoietic progenitor cells. Stem Cells. 2007;25(4):844–51.

    PubMed  CAS  Google Scholar 

  66. Mauro A. Satellite cells of skeletal muscle fibers. J Biochem Biophys Cytol. 1961;9:493–8.

    CAS  Google Scholar 

  67. Leblond CP. Classification of cell populations on the basis of their proliferative behavior. Natl Cancer Inst Monogr. 1964;14: 119–50.

    PubMed  CAS  Google Scholar 

  68. Cossu G, Zani B, Coletta M, Bouche M, Pacifici M, Molinaro M. In vitro differentiation of satellite cells isolated from normal and dystrophic mammalian muscles. A comparison with embryonic myogenic cells. Cell Differ. 1980;9(6):357–68.

    CAS  Google Scholar 

  69. Bischoff R. The satellite cell and muscle regeneration. In: Engel AG, Franzini-Armstrong C, eds. Myology: basic and clinical. 2nd ed. New York: McGraw-Hill; 1994. pp. 97–118.

    Google Scholar 

  70. Cornelison DD, Wold BJ. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol. 1997;191(2):270–83.

    PubMed  CAS  Google Scholar 

  71. Yablonka-Reuveni Z, Rivera AJ. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol. 1994;164(2): 588–603.

    PubMed  CAS  Google Scholar 

  72. Beauchamp JR, Heslop L, Yu DS, et al. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol. 2000;151(6):1221–34.

    PubMed  CAS  Google Scholar 

  73. Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates “reserve cells”. J Cell Sci. 1998;111(Pt 6):769–79.

    PubMed  CAS  Google Scholar 

  74. Miller JB, Schaefer L, Dominov JA. Seeking muscle stem cells. Curr Top Dev Biol. 1999;43:191–219.

    PubMed  CAS  Google Scholar 

  75. Seale P, Rudnicki MA. A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev Biol. 2000;218(2):115–24.

    PubMed  CAS  Google Scholar 

  76. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000;102(6):777–86.

    PubMed  CAS  Google Scholar 

  77. Covault J, Sanes JR. Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J Cell Biol. 1986;102(3):716–30.

    PubMed  CAS  Google Scholar 

  78. Asakura A, Komaki M, Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 2001;68(4–5):245–53.

    PubMed  CAS  Google Scholar 

  79. Partridge TA, Morgan JE, Coulton GR, Hoffman EP, Kunkel LM. Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature. 1989;337 (6203):176–9.

    PubMed  CAS  Google Scholar 

  80. Huard J, Acsadi G, Jani A, Massie B, Karpati G. Gene transfer into skeletal muscles by isogenic myoblasts. Hum Gene Ther. 1994;5(8):949–58.

    PubMed  CAS  Google Scholar 

  81. Gussoni E, Soneoka Y, Strickland CD, et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 1999;401(6751):390–4.

    PubMed  CAS  Google Scholar 

  82. Kinoshita I, Vilquin JT, Guerette B, Asselin I, Roy R, Tremblay JP. Very efficient myoblast allotransplantation in mice under FK506 immunosuppression. Muscle Nerve. 1994;17(12): 1407–15.

    PubMed  CAS  Google Scholar 

  83. Vilquin JT, Wagner E, Kinoshita I, Roy R, Tremblay JP. Suc- cessful histocompatible myoblast transplantation in dystrophin- deficient mdx mouse despite the production of antibodies against dystrophin. J Cell Biol. 1995;131 (4):975–88.

    PubMed  CAS  Google Scholar 

  84. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci U S A. 2002;99(3):1341–6.

    PubMed  CAS  Google Scholar 

  85. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA. Myogenic specification of side population cells in skeletal muscle. J Cell Biol. 2002;159(1):123–34.

    PubMed  CAS  Google Scholar 

  86. Montanaro F, Liadaki K, Schienda J, Flint A, Gussoni E, Kunkel LM. Demystifying SP cell purification: viability, yield, and phenotype are defined by isolation parameters. Exp Cell Res. 2004;298(1):144–54.

    PubMed  CAS  Google Scholar 

  87. Jackson KA, Mi T, Goodell MA. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci U S A. 1999;96(25):14482–6.

    PubMed  CAS  Google Scholar 

  88. Liadaki K, Kho AT, Sanoudou D, et al. Side population cells isolated from different tissues share transcriptome signatures and express tissue-specific markers. Exp Cell Res. 2005;303(2): 360–74.

    PubMed  CAS  Google Scholar 

  89. Schienda J, Engleka KA, Jun S, et al. Somitic origin of limb muscle satellite and side population cells. Proc Natl Acad Sci U S A. 2006;103(4):945–50.

    PubMed  CAS  Google Scholar 

  90. Galvez BG, Sampaolesi M, Brunelli S, et al. Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. J Cell Biol. 2006;174(2):231–43.

    PubMed  CAS  Google Scholar 

  91. Minasi MG, Riminucci M, De Angelis L, et al. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development. 2002;129(11):2773–83.

    PubMed  CAS  Google Scholar 

  92. Sampaolesi M, Torrente Y, Innocenzi A, et al. Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science. 2003;301(5632): 487–92.

    PubMed  CAS  Google Scholar 

  93. Dellavalle A, Sampaolesi M, Tonlorenzi R, et al. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007;9(3):255–67.

    PubMed  CAS  Google Scholar 

  94. Andreeva ER, Pugach IM, Gordon D, Orekhov AN. Continuous subendothelial network formed by pericyte-like cells in human vascular bed. Tissue Cell. 1998;30(1):127–35.

    PubMed  CAS  Google Scholar 

  95. Di Rocco G, Iachininoto MG, Tritarelli A, et al. Myogenic potential of adipose-tissue-derived cells. J Cell Sci. 2006;119(Pt 14):2945–52.

    PubMed  Google Scholar 

  96. Gavina M, Belicchi M, Rossi B, et al. VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133+ stem cells after intra-arterial transplantation. Blood. 2006;108(8):2857–66.

    PubMed  CAS  Google Scholar 

  97. Torrente Y, Belicchi M, Sampaolesi M, et al. Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest. 2004;114(2):182–95.

    PubMed  CAS  Google Scholar 

  98. Sarig R, Baruchi Z, Fuchs O, Nudel U, Yaffe D. Regeneration and transdifferentiation potential of muscle-derived stem cells propagated as myospheres. Stem Cells. 2006;24(7):1769–78.

    PubMed  Google Scholar 

  99. Lee JY, Qu-Petersen Z, Cao B, et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol. 2000;150(5):1085–100.

    PubMed  CAS  Google Scholar 

  100. Winitsky SO, Gopal TV, Hassanzadeh S, et al. Adult murine skeletal muscle contains cells that can differentiate into beating cardiomyocytes in vitro. PLoS Biol. 2005;3(4):e87.

    PubMed  Google Scholar 

  101. Zheng B, Cao B, Crisan M, et al. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol. 2007;25(9):1025–34.

    PubMed  CAS  Google Scholar 

  102. Peault B, Rudnicki M, Torrente Y, et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther. 2007;15(5):867–77.

    PubMed  CAS  Google Scholar 

  103. Olguin HC, Olwin BB. Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol. 2004;275(2):375–88.

    PubMed  CAS  Google Scholar 

  104. Qu-Petersen Z, Deasy B, Jankowski R, et al. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol. 2002;157(5):851–64.

    PubMed  CAS  Google Scholar 

  105. Deasy BM, Qu-Peterson Z, Greenberger JS, Huard J. Mechanisms of muscle stem cell expansion with cytokines. Stem Cells. 2002;20(1):50–60.

    PubMed  CAS  Google Scholar 

  106. Deasy BM, Jankowski RJ, Payne TR, et al. Modeling stem cell population growth: incorporating terms for proliferative heterogeneity. Stem Cells. 2003;21(5):536–45.

    PubMed  CAS  Google Scholar 

  107. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol. 2004;166(3):347–57.

    PubMed  CAS  Google Scholar 

  108. Halevy O, Piestun Y, Allouh MZ, et al. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn. 2004;231(3):489–502.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  110. Beauchamp JR, Morgan JE, Pagel CN, Partridge TA. Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J Cell Biol. 1999;144(6):1113–22.

    PubMed  CAS  Google Scholar 

  111. Baroffio A, Hamann M, Bernheim L, Bochaton-Piallat ML, Gabbiani G, Bader CR. Identification of self-renewing myoblasts in the progeny of single human muscle satellite cells. Differentiation. 1996;60(1):47–57.

    PubMed  CAS  Google Scholar 

  112. Collins CA, Olsen I, Zammit PS, et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005;122(2):289–301.

    PubMed  CAS  Google Scholar 

  113. Collins CA. Satellite cell self-renewal. Curr Opin Pharmacol. 2006;6(3):301–6.

    PubMed  CAS  Google Scholar 

  114. Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007;129(5):999–1010.

    PubMed  CAS  Google Scholar 

  115. Cossu G, Tajbakhsh S. Oriented cell divisions and muscle satellite cell heterogeneity. Cell. 2007;129(5):859–61.

    PubMed  CAS  Google Scholar 

  116. Mitchell PO, Mills T, O’Connor RS, Graubert T, Dzierzak E, Pavlath GK. Sca-1 negatively regulates proliferation and differentiation of muscle cells. Dev Biol. 2005;283(1):240–52.

    PubMed  CAS  Google Scholar 

  117. Molnar G, Ho ML, Schroedl NA. Evidence for multiple satellite cell populations and a non-myogenic cell type that is regulated differently in regenerating and growing skeletal muscle. Tissue Cell. 1996;28(5):547–56.

    PubMed  CAS  Google Scholar 

  118. Schultz E. Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol. 1996;175(1):84–94.

    PubMed  CAS  Google Scholar 

  119. Deasy BM, Li Y, Huard J. Tissue engineering with muscle-derived stem cells. Curr Opin Biotechnol. 2004;15(5):419–23.

    PubMed  CAS  Google Scholar 

  120. Zammit P, Beauchamp J. The skeletal muscle satellite cell: stem cell or son of stem cell? Differentiation. 2001;68(4–5): 193–204.

    PubMed  CAS  Google Scholar 

  121. Wagers AJ, Conboy IM. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell. 2005;122(5):659–67.

    PubMed  CAS  Google Scholar 

  122. Cairns J. Mutation selection and the natural history of cancer. Nature. 1975;255(5505):197–200.

    PubMed  CAS  Google Scholar 

  123. Cairns J. Somatic stem cells and the kinetics of mutagenesis and carcinogenesis. Proc Natl Acad Sci U S A. 2002;99(16): 10567–70.

    PubMed  CAS  Google Scholar 

  124. Rando TA. The immortal strand hypothesis: segregation and reconstruction. Cell. 2007;129(7):1239–43.

    PubMed  CAS  Google Scholar 

  125. Lansdorp PM. Immortal strands? Give me a break. Cell. 2007;129(7):1244–7.

    PubMed  CAS  Google Scholar 

  126. Lark KG, Consigli RA, Minocha HC. Segregation of sister chromatids in mammalian cells. Science. 1966;154(753):1202–5.

    PubMed  CAS  Google Scholar 

  127. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci. 2002;115(Pt 11):2381–8.

    PubMed  CAS  Google Scholar 

  128. Karpowicz P, Morshead C, Kam A, et al. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro. J Cell Biol. 2005;170(5): 721–32.

    PubMed  CAS  Google Scholar 

  129. Conboy MJ, Karasov AO, Rando TA. High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol. 2007;5(5):e102.

    PubMed  Google Scholar 

  130. Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol. 2006;8(7):677–87.

    PubMed  CAS  Google Scholar 

  131. Kiel MJ, He S, Ashkenazi R, et al. Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature. 2007;449(7159):238–42.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Orthopaedic Surgery and Bioengineering, University of Pittsburgh, Stem Cell Research Center, Children’s Hospital of Pittsburgh of UPMC, McGowan Institute of Regenerative Medicine, University of Pittsburgh Medical Center; 5113 Rangos Research Center, 3705 Fifth Avenue, Pittsburgh, PA, 15213

    Bridget M. Deasy

Authors
  1. Bridget M. Deasy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bridget M. Deasy .

Editor information

Editors and Affiliations

  1. Memorial Sloan-Kettering Cancer Center, New York, NY, USA

    Vinagolu K. Rajasekhar MSc, MPhil, PhD

  2. Invitrogen Corporation, Frederick, MD, USA

    Mohan C. Vemuri Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC, a part of Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Deasy, B.M. (2009). Asymmetric Behavior in Stem Cells. In: Rajasekhar, V.K., Vemuri, M.C. (eds) Regulatory Networks in Stem Cells. Stem Cell Biology and Regenerative Medicine. Humana Press. https://doi.org/10.1007/978-1-60327-227-8_2

Download citation

Publish with us

Policies and ethics

Search

Navigation