Non-genetic heterogeneity of cells in development: More than just noise

Development

Volumn 136, Issue 23, 2009, Pages 3853-3862

  Huang, Sui ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOLOGICAL ACTIVITY; CELL FATE; CELL HETEROGENEITY; CELL MATURATION; CELL POPULATION; CONCEPTUAL FRAMEWORK; DEVELOPMENTAL BIOLOGY; EPIGENETICS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC HETEROGENEITY; HUMAN; MAMMAL CELL; MULTIPOTENT STEM CELL; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; POPULATION DISTRIBUTION; POPULATION DYNAMICS; PRIORITY JOURNAL; SIGNAL NOISE RATIO;

ANIMALS; CELLS; EPIGENESIS, GENETIC; GENETIC HETEROGENEITY; MODELS, GENETIC;

MAMMALIA;

EID: 70450162700     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.035139     Document Type: Article

References (90)

1. Aird, W. C. (2004). Endothelial cell heterogeneity: a case for nature and nurture. Blood 103, 3994.
2. Aurell, E. and Sneppen, K. (2002). Epigenetics as a first exit problem. Phys. Rev. Lett. 88, 048101.
3. Austin, D. W., Allen, M. S., McCollum, J. M., Dar, R. D., Wilgus, J. R., Sayler, G. S., Samatova, N. F., Cox, C. D. and Simpson, M. L. (2006). Gene network shaping of inherent noise spectra. Nature 439, 608-611.
4. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L. and Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science 305, 1622-1625.
5. Baldinger, K. (1980). Semantic Theory. Oxford: Blackwell.
6. Bar-Yam, Y., Harmon, D. and de Bivort, B. (2009). Systems biology. Attractors and democratic dynamics. Science 323, 1016-1017.
7. Bonifer, C., Hoogenkamp, M., Krysinska, H. and Tagoh, H. (2008). How transcription factors program chromatin-lessons from studies of the regulation of myeloid-specific genes. Semin. Immunol. 20, 257-263.
8. Brock, A., Chang, H. and Huang, S. (2009). Non-genetic heterogeneity-a mutation-independent driving force for the somatic evolution of tumours. Nat. Rev. Genet. 10, 336-342.
9. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrana, J., Jones, K., Grotewold, L. and Smith, A. (2007). Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234.
10. Chang, H. H., Oh, P. Y., Ingber, D. E. and Huang, S. (2006). Multistable and multistep dynamics in neutrophil differentiation. BMC Cell Biol. 7, 11.
11. Chang, H. H., Hemberg, M., Barahona, M., Ingber, D. E. and Huang, S. (2008). Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544-547.
12. Cohen, A. A., Geva-Zatorsky, N., Eden, E., Frenkel-Morgenstern, M., Issaeva, I., Sigal, A., Milo, R., Cohen-Saidon, C., Liron, Y., Kam, Z. et al. (2008). Dynamic proteomics of individual cancer cells in response to a drug. Science 322, 1511-1516.
13. Diercks, A., Kostner, H. and Ozinsky, A. (2009). Resolving cell population heterogeneity: real-time PCR for simultaneous multiplexed gene detection in multiple single-cell samples. PLoS One 27, e6326.
14. Dietrich, J. E. and Hiiragi, T. (2007). Stochastic patterning in the mouse pre-implantation embryo. Development 134, 4219-4231.
15. Elowitz, M. B., Levine, A. J., Siggia, E. D. and Swain, P. S. (2002). Stochastic gene expression in a single cell. Science 297, 1183-1186.
16. Enver, T., Pera, M., Peterson, C. and Andrews, P. W. (2009). Stem cell states, fates, and the rules of attraction. Cell Stem Cell 4, 387-397.
17. Frauenfelder, H., Sligar, S. G. and Wolynes, P. G. (1991). The energy landscapes and motions of proteins. Science 254, 1598-1603.
18. Furusawa, C. and Kaneko, K. (2001). Theory of robustness of irreversible differentiation in a stem cell system: chaos hypothesis. J. Theor. Biol. 209, 395-416.
19. Goldberg, A. D., Allis, C. D. and Bernstein, E. (2007). Epigenetics: a landscape takes shape. Cell 128, 635-638.
20. Goodwin, B. (1993). How the Leopard Changed Its Spots: The Evolution of Complexity. Princeton: Princeton University Press.
21. Graf, T. (2002). Differentiation plasticity of hematopoietic cells. Blood 99, 3089-3101.
22. Graf, T. and Stadtfeld, M. (2008). Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 3, 480-483.
23. Grundel, R. and Rubin, H. (1988). Maintenance of multiplication rate stability by cell populations in the face of heterogeneity among individual cells. J. Cell Sci. 91, 571-576.
24. Hayashi, K., Lopes, S. M., Tang, F. and Surani, M. A. (2008). Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3, 391-401.
25. Hirata, H., Yoshiura, S., Ohtsuka, T., Bessho, Y., Harada, T., Yoshikawa, K. and Kageyama, R. (2002). Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298, 840-843.
26. Huang, A. C., Hu, L., Kauffman, S. A., Zhang, W. and Shmulevich, I. (2009). Using cell fate attractors to uncover transcriptional regulation of HL60 neutrophil differentiation. BMC Syst. Biol. 3, 20.
27. Huang, S. (2009). Reprogramming cell fates: reconciling rarity with robustness. BioEssays 31, 546-560.
28. Huang, S. and Kauffman, S. (2009). Complex gene regulatory networks-from structure to biological observables: cell fate determination. In Encyclopedia of Complexity and Systems Science (ed. R. A. Meyers). Berlin: Springer.
29. Huang, S., Eichler, G., Bar-Yam, Y. and Ingber, D. E. (2005). Cell fates as high-dimensional attractor states of a complex gene regulatory network. Phys. Rev. Lett. 94, 128701.
30. Huang, S., Guo, Y. P., May, G. and Enver, T. (2007). Bifurcation dynamics of cell fate decision in bipotent progenitor cells. Dev. Biol. 305, 695-713.
31. Jablonka, E. (1994). Inheritance systems and the evolution of new levels of individuality. J. Theor. Biol. 170, 301-309.
32. Jablonka, E. and Lamb, M. J. (2002). The changing concept of epigenetics. Ann. New York Acad. Sci. 981, 82-96.
33. Joshi, C. V. and Enver, T. (2002). Plasticity revisited. Curr. Opin. Cell Biol. 14, 749-755.
34. Kaern, M., Elston, T. C., Blake, W. J. and Collins, J. J. (2005). Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6, 451-464.
35. Kalmar, T., Lim, C., Hayward, P., Munoz-Descalzo, S., Nichols, J., Garcia-Ojalvo, J. and Martinez Arias, A. (2009). Regulated fluctuations in nano g expression mediate cell fate decisions in embryonic stem cells. PLoS Biol. 7, e1000149.
36. Kaneko, K. (2006). Life: An Introduction to Complex Systems Biology. Berlin: Springer.
37. Kaneko, K. (2007). Evolution of robustness to noise and mutation in gene expression dynamics. PLoS One 2, e434.
38. Kashiwagi, A., Urabe, I., Kaneko, K. and Yomo, T. (2006). Adaptive response of a gene network to environmental changes by fitness-induced attractor selection. PLoS ONE 1, e49.
39. Kaufmann, B. B. and van Oudenaarden, A. (2007). Stochastic gene expression: from single molecules to the proteome. Curr. Opin. Genet. Dev. 17, 107-112.
40. Kaufmann, B. B., Yang, Q., Mettetal, J. T. and van Oudenaarden, A. (2007). Heritable stochastic switching revealed by single-cell genealogy. PLoS Biol. 5, e239.
41. Kauffman, S. (1969a). Homeostasis and differentiation in random genetic control networks. Nature 224, 177-178.
42. Kauffman, S. A. (1969b). Metabolic stability and epigenesis in randomly constructed genetic nets. J. Theor. Biol. 22, 437-467.
43. Kauffman, S. A. (1993). The Origins of Order. New York: Oxford University Press.
44. Klevecz, R. R., Bolen, J., Forrest, G. and Murray, D. B. (2004). A genomewide oscillation in transcription gates DNA replication and cell cycle. Proc. Natl. Acad. Sci. USA 101, 1200-1205.
45. Kobayashi, T., Mizuno, H., Imayoshi, I., Furusawa, C., Shirahige, K. and Kageyama, R. (2009). The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev. 23, 1870-1875.
46. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705.
47. Krutzik, P. O., Irish, J. M., Nolan, G. P. and Perez, O. D. (2004). Analysis of protein phosphorylation and cellular signaling events by flow cytometry: techniques and clinical applications. Clin. Immunol. 110, 206-221.
48. Lahav, G., Rosenfeld, N., Sigal, A., Geva-Zatorsky, N., Levine, A. J., Elowitz, M. B. and Alon, U. (2004). Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat. Genet. 36, 147-150.
49. Lei, J. (2009). Stochasticity in single gene expression with both intrinsic noise and fluctuation in kinetic parameters. J. Theor. Biol. 256, 485-492.
50. Lengauer, C., Kinzler, K. W. and Vogelstein, B. (1998). Genetic instabilities in human cancers. Nature 396, 643-649.
51. Levsky, J. M., Shenoy, S. M., Pezo, R. C. and Singer, R. H. (2002). Single-cell gene expression profiling. Science 297, 836-840.
52. Lewontin, R. (2000). The Triple Helix: Gene, Organism, and Environment. Cambridge: Harvard University Press.
53. Loeb, L. A. (2001). A mutator phenotype in cancer. Cancer Res. 61, 3230-3239.
54. Losick, R. and Desplan, C. (2008). Stochasticity and cell fate. Science 320, 65-68.
55. Mantzaris, N. V. (2006). Stochastic and deterministic simulations of heterogeneous cell population dynamics. J. Theor. Biol. 241, 690-706.
56. Mantzaris, N. V. (2007). From single-cell genetic architecture to cell population dynamics: quantitatively decomposing the effects of different population heterogeneity sources for a genetic network with positive feedback architecture. Biophys. J. 92, 4271-4288.
57. Morange, M. (2001). The Misunderstood Gene. Cambridge: Harvard University Press.
58. Nicolis, G. (1986). Dissipative systems. Rep. Prog. Phys. 49, 873-949.
59. Nicolis, G. and Prigogine, I. (1989). Exploring Complexity: An Introduction. New York: W.H. Freeman & Company.
60. Novick, A. and Weiner, M. (1957). Enzyme induction as an all-or-none phenomenon. Proc. Natl. Acad. Sci. USA 43, 553-566.
61. Oates, A. C., Gorfinkiel, N., Gonzalez-Gaitan, M. and Heisenberg, C. P. (2009). Quantitative approaches in developmental biology. Nat. Rev. Genet. 10, 517-530.
62. Orkin, S. H. and Zon, L. I. (2002). Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat. Immunol. 3, 323-328.
63. Patrascioiu, A. (1987). The Ergodic-hypothesis, a complicated problem in mathematics and physics. Los Alamos Science 15, 263-279.
64. Paulsson, J. (2004). Summing up the noise in gene networks. Nature 427, 415-418.
65. Petrosky, T. and Prigogine, I. (1993). Poincare resonances and the limits of trajectory dynamics. Proc. Natl. Acad. Sci. USA 90, 9393-9397.
66. Prigogine, I. (1997). The End of Certainty. New York: Free Press.
67. Ptashne, M. (2007). On the use of the word 'epigenetic'. Curr. Biol. 17, R233-R236.
68. Raj, A. and van Oudenaarden, A. (2008). Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226.
69. Ravin, R., Hoeppner, D. J., Munno, D. M., Carmel, L., Sullivan, J., Levitt, D. L., Miller, J. L., Athaide, C., Panchision, D. M. and McKay, R. D. (2008). Potency and fate specification in CNS stem cell populations in vitro. Cell Stem Cell 3, 670-680.
70. Rubin, H. (1992). Mechanisms for enduring biological change. Am. J. Physiol. 262, L111-L113.
71. Schroeder, T. (2008). Imaging stem-cell-driven regeneration in mammals. Nature 453, 345-351.
72. Sigal, A., Milo, R., Cohen, A., Geva-Zatorsky, N., Klein, Y., Liron, Y., Rosenfeld, N., Danon, T., Perzov, N. and Alon, U. (2006). Variability and memory of protein levels in human cells. Nature 444, 643-646.
73. Silva, J. and Smith, A. (2008). Capturing pluripotency. Cell 132, 532-536.
74. Singh, A. M., Hamazaki, T., Hankowski, K. E. and Terada, N. (2007). A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25, 2534-2542.
75. Skupin, A., Kettenmann, H., Winkler, U., Wartenberg, M., Sauer, H., Tovey, S. C., Taylor, C. W. and Falcke, M. (2008). How does intracellular Ca2+ oscillate: by chance or by the clock? Biophys. J. 94, 2404-2411.
76. Slack, J. M. W. (2002). Timeline-Conrad Hal Waddington: the last renaissance biologist? Nat. Rev. Genet. 3, 889-895.
77. Spencer, S. L., Gaudet, S., Albeck, J. G., Burke, J. M. and Sorger, P. K. (2009). Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459, 428-432.
78. Spudich, J. L. and Koshland, D. E., Jr (1976). Non-genetic individuality: chance in the single cell. Nature 262, 467-471.
79. Stockholm, D., Benchaouir, R., Picot, J., Rameau, P., Neildez, T. M., Landini, G., Laplace-Builhe, C. and Paldi, A. (2007). The origin of phenotypic heterogeneity in a clonal cell population in vitro. PLoS ONE 2, e394.
80. Strohman, R. (1994). Epigenesis: the missing beat in biotechnology? Biotechnology (NY) 12, 156-164.
81. Strohman, R. C. (1997). The coming Kuhnian revolution in biology. Nat. Biotechnol. 15, 194-200.
82. Takasuka, N., White, M. R., Wood, C. D., Robertson, W. R. and Davis, J. R. (1998). Dynamic changes in prolactin promoter activation in individual living lactotrophic cells. Endocrinology 139, 1361-1368.
83. Tomlinson, I., Sasieni, P. and Bodmer, W. (2002). How many mutations in a cancer? Am. J. Pathol. 160, 755-758.
84. Volfson, D., Marciniak, J., Blake, W. J., Ostroff, N., Tsimring, L. S. and Hasty, J. (2006). Origins of extrinsic variability in eukaryotic gene expression. Nature 439, 861-864.
85. Waddington, C. H. (1942). The epigenotype. Endeavour 1, 18-20.
86. Waddington, C. H. (1957). The Strategy of the Genes. London: Allen and Unwin.
87. Walczak, A. M., Onuchic, J. N. and Wolynes, P. G. (2005). Absolute rate theories of epigenetic stability. Proc. Natl. Acad. Sci. USA 102, 18926-18931.
88. Wang, J., Xu, L. and Wang, E. (2008). Potential landscape and flux framework of nonequilibrium networks: robustness, dissipation, and coherence of biochemical oscillations. Proc. Natl. Acad. Sci. USA 105, 12271-12276.
89. Warren, L., Bryder, D., Weissman, I. L. and Quake, S. R. (2006). Transcription factor profiling in individual hematopoietic progenitors by digital RT-PCR. Proc. Natl. Acad. Sci. USA 103, 17807-17812.
90. Zernicka-Goetz, M., Morris, S. A. and Bruce, A. W. (2009). Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat. Rev. Genet. 10, 467-477.