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Outline

Noise-driven stem cell and progenitor population dynamics

2008, PloS one

https://doi.org/10.1371/JOURNAL.PONE.0002922

Abstract

The balance between maintenance of the stem cell state and terminal differentiation is influenced by the cellular environment. The switching between these states has long been understood as a transition between attractor states of a molecular network. Herein, stochastic fluctuations are either suppressed or can trigger the transition, but they do not actually determine the attractor states. We present a novel mathematical concept in which stem cell and progenitor population dynamics are described as a probabilistic process that arises from cell proliferation and small fluctuations in the state of differentiation. These state fluctuations reflect random transitions between different activation patterns of the underlying regulatory network. Importantly, the associated noise amplitudes are state-dependent and set by the environment. Their variability determines the attractor states, and thus actually governs population dynamics. This model quantitatively reproduces the observed dynamic...

References (65)

  1. Korobkova E, Emonet T, Vilar JM, Shimizu TS, Cluzel P (2004) From molecular noise to behavioural variability in a single bacterium. Nature 428: 574-578.
  2. Thattai M, van Oudenaarden A (2004) Stochastic gene expression in fluctuating environments. Genetics 167: 523-530.
  3. Samoilov M, Plyasunov S, Arkin AP (2005) Stochastic amplification and signaling in enzymatic futile cycles through noise-induced bistability with oscillations. Proc Natl Acad Sci U S A 102: 2310-2315.
  4. Fange D, Elf J (2006) Noise-induced Min phenotypes in E. coli. PLoS Comput Biol 2: e80.
  5. Maamar H, Raj A, Dubnau D (2007) Noise in gene expression determines cell fate in Bacillus subtilis. Science 317: 526-529.
  6. Samoilov MS, Price G, Arkin AP (2006) From fluctuations to phenotypes: the physiology of noise. Sci STKE 2006: re17.
  7. Thattai M, van Oudenaarden A (2002) Attenuation of noise in ultrasensitive signaling cascades. Biophys J 82: 2943-2950.
  8. Stelling J, Sauer U, Szallasi Z, Doyler FJ, Doyle J (2004) Robustness of cellular functions. Cell 118: 675-685.
  9. Acar M, Becskei A, van Oudenaarden A (2005) Enhancement of cellular memory by reducing stochastic transitions. Nature 435: 228-232.
  10. Hooshangi S, Thiberge S, Weiss R (2005) Ultrasensitivity and noise propagation in a synthetic transcriptional cascade. Proc Natl Acad Sci U S A 102: 3581-3586.
  11. Arias AM, Hayward P (2006) Filtering transcriptional noise during development: concepts and mechanisms. Nat Rev Genet 7: 34-44.
  12. El-Samad H, Khammash M (2006) Regulated degradation is a mechanism for suppressing stochastic fluctuations in gene regulatory networks. Biophys J 90: 3749-3761.
  13. Freeman M (2000) Feedback control of intercellular signalling in development. Nature 408: 313-319.
  14. Szutorisz H, Georgiou A, Tora L, Dillon N (2006) The proteasome restricts permissive transcription at tissue-specific gene loci in embryonic stem cells. Cell 127: 1375-1388.
  15. Zwaka TP (2006) Keeping the noise down in ES cells. Cell 127: 1301-1302.
  16. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, et al. (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450: 1230-1234.
  17. Potten CS, Loeffler M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001-1020.
  18. Loeffler M, Roeder I (2002) Tissue stem cells: definition, plasticity, heteroge- neity, self-organization and models-a conceptual approach. Cells Tissues Organs 171: 8-26.
  19. Wilson A, Trumpp A (2006) Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 6: 93-106.
  20. Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T (2006) Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol 207: 331-339.
  21. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
  22. Ingber DE (2006) Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 50: 255-266.
  23. Gosh K, Ingber DE (2007) Micromechanical control of cell and tissue development: Implications for tissue engineering. Adv Drug Deliv Rev.
  24. Drayson MT, Michell RH, Durham J, Brown G (2001) Cell proliferation and CD11b expression are controlled independently during HL60 cell differentiation initiated by 1,25 alpha-dihydroxyvitamin D(3) or all-trans-retinoic acid. Exp Cell Res 266: 126-134.
  25. Kitajima K, Haque M, Nakamura H, Hirano T, Utiyama H (2001) Loss of irreversibility of granulocytic differentiation induced by dimethyl sulfoxide in HL-60 sublines with a homogeneously staining region. Biochem Biophys Res Commun 288: 1182-1187.
  26. Brown G, Drayson MT, Durham J, Toellner KM, Hughes PJ, et al. (2002) HL60 cells halted in G1 or S phase differentiate normally. Exp Cell Res 281: 28-38.
  27. Chang HH, Oh PY, Ingber DE, Huang S (2006) Multistable and multistep dynamics in neutrophil differentiation. BMC Cell Biol 7: 11.
  28. Gibbs JD, Liebermann DA, Hoffman B (2007) Terminal myeloid differentiation is uncoupled from cell cycle arrest. Cell Cycle 6: 1205-1209.
  29. Isaacs FJ, Hasty J, Cantor CR, Collins JJ (2003) Prediction and measurement of an autoregulatory genetic module. Proc Natl Acad Sci U S A 100: 7714-7719.
  30. Huang S, Eichler G, Bar-Yam Y, Ingber DE (2005) Cell fates as high- dimensional attractor states of a complex gene regulatory network. Phys Rev Lett 94: 128701.
  31. Kaern M, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-464.
  32. Quesenberry PJ, Dooner G, Dooner M, Colvin G (2005) The stem cell continuum: considerations on the heterogeneity and plasticity of marrow stem cells. Stem Cell Rev 1: 29-36.
  33. Viswanathan S, Davey RE, Cheng D, Raghu RC, Lauffenburger DA, et al. (2005) Clonal evolution of stem and differentiated cells can be predicted by integrating cell-intrinsic and -extrinsic parameters. Biotechnol Appl Biochem 42: 119-131.
  34. Kashiwagi A, Urabe I, Kaneko K, Yomo T (2006) Adaptive response of a gene network to environmental changes by fitness-induced attractor selection. PLoS ONE 1: e49.
  35. Roeder I, Horn M, Glauche I, Hochhaus A, Mueller MC, et al. (2006) Dynamic modeling of imatinib-treated chronic myeloid leukemia: functional insights and clinical implications. Nat Med 12: 1181-1184.
  36. Roeder I, Lorenz R (2006) Asymmetry of stem cell fate and the potential impact of the niche: observations, simulations, and interpretations. Stem Cell Rev 2: 171-180.
  37. Loeffler M, Roeder I (2004) Conceptual models to understand tissue stem cell organization. Curr Opin Hematol 11: 81-87.
  38. Roeder I, Braesel K, Lorenz R, Loeffler M (2007) Stem cell fate analysis revisited: interpretation of individual clone dynamics in the light of a new paradigm of stem cell organization. J Biomed Biotechnol 2007: 84656.
  39. Glauche I, Cross M, Loeffler M, Roeder I (2007) Lineage specification of hematopoietic stem cells: mathematical modeling and biological implications. Stem Cells 25: 1791-1799.
  40. Rando OJ, Paulsson J (2006) Noisy silencing of chromatin. Dev Cell 11: 134-136.
  41. Xu EY, Zawadzki KA, Broach JR (2006) Single-cell observations reveal intermediate transcriptional silencing states. Mol Cell 23: 219-229.
  42. Waddington CH (1956) Principles of Embryology. Allan and Unwin Ltd: London.
  43. Wang J, Huang B, Xia X, Sun Z (2006) Funneled landscape leads to robustness of cell networks: yeast cell cycle. PLoS Comput Biol 2: e147.
  44. Ao P, Kwon C, Qian H (2007) On the existence of potential landscape in the evolution of complex systems. Complexity 12: 19-27.
  45. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, et al. (2007) Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
  46. Kepler TB, Elston TC (2001) Stochasticity in transcriptional regulation: origins, consequences, and mathematical representations. Biophys J 81: 3116-3136.
  47. van Kampen NG (2004) Stochastic processes in physics and chemistry. Elsevier: Amsterdam.
  48. Beckmann J, Scheitza S, Wernet P, Fischer JC, Giebel B (2007) Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins. Blood 109: 5494-5501.
  49. Holtz MS, Slovak ML, Zhang F, Sawyers CL, Forman SJ, et al. (2002) Imatinib mesylate (STI571) inhibits growth of primitive malignant progenitors in chronic myelogenous leukemia through reversal of abnormally increased proliferation. Blood 99: 3792-3800.
  50. Leon K, Faro J, Carneiro J (2004) A general mathematical framework to model generation structure in a population of asynchronously dividing cells. J Theor Biol 229: 455-476.
  51. Becskei A, Kaufmann BB, van Oudenaarden A (2005) Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat Genet 37: 937-944.
  52. Pedraza JM, van Oudenaarden A (2005) Noise propagation in gene networks. Science 307: 1965-1969.
  53. Raser JM, O'Shea EK (2005) Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013.
  54. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, et al. (2006) Noise in protein expression scales with natural protein abundance. Nat Genet 38: 636-643.
  55. Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, et al. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846.
  56. Kerszberg M (2004) Noise, delays, robustness, canalization and all that. Curr Opin Genet Dev 14: 440-445.
  57. Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8: 9-22.
  58. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, et al. (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130: 1083-1094.
  59. Chang HH, Hemberg M, Barahona M, Ingber DE, Huang S (2008) Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453: 544-547.
  60. Ozbudak EM, Thattai M, Lim HN, Shraiman BI, Van Oudenaarden A (2004) Multistability in the lactose utilization network of Escherichia coli. Nature 427: 737-740.
  61. Tabaka M, Cybulski O, Holyst R (2008) Accurate genetic switch in Escherichia coli: novel mechanism of regulation by co-repressor. J Mol Biol 377: 1002-1014.
  62. Merino E, Jensen RA, Yanofsky C (2008) Evolution of bacterial trp operons and their regulation. Curr Opin Microbiol 11: 78-86.
  63. Gosh K, Ingber DE (2007) Micromechanical control of cell and tissue development: Implications for tissue engineering.
  64. Ingber DE, Levin M (2007) What lies at the interface of regenerative medicine and developmental biology? Development 134: 2541-2547.
  65. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1992) Numerical Recipes in C. Cambridge University Press: Cambridge, UK.