Toward a Rosetta stone for the stem cell genome: Stochastic gene expression, network architecture, and external influences

Stem Cell Research

Volumn 1, Issue 3, 2008, Pages 157-168

  Halley, Julianne D ^a   Winkler, David A ^a,b   Burden, Frank R ^a,b,c  

^a CSIRO   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c SciMetrics   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL POPULATION; CELL TYPE; CONCEPTUAL FRAMEWORK; CYTOLOGY; GENE CONTROL; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETIC CODE; GENOME; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC SYSTEM; HUMAN; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; STEM CELL; STOCHASTIC MODEL; TRANSCRIPTION REGULATION;

EID: 49149115509     PISSN: 18735061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scr.2008.03.001     Document Type: Review

References (139)

1. Adams G.B., and Scadden D.T. The hematopoietic stem cell in its place. Nat. Immunol. 7 (2006) 333
2. Akashi K. Lineage promiscuity and plasticity in hematopoietic development. Ann. N. Y. Acad. Sci. 1044 (2005) 125-131
3. Akashi K., He X., Chen J., Iwasaki H., Niu C., Steenhard B., Zhang J., Haug J., and Li L. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 101 (2003) 383-390
4. Albert R., and Barabási A.L. Statistical mechanics of complex networks. Rev. Mod. Phys. 74 (2002) 47-97
5. Anderson C. Self-organization in relation to several similar concepts: are the boundaries to self-organization indistinct?. Biol. Bull. 202 (2002) 247-255
6. Arkin A., Ross J., and McAdams H.H. Stochastic kinetic analysis of developmental pathway bifurcation in phage λ-infected Escherichia coli cells. Genetics 149 (1998) 1633-1648
7. Barkai N., and Leibler S. Robustness in simple biochemical networks. Nature 387 (1997) 913
8. Bird A., and Tweedie S. Transcriptional noise and the evolution of gene number. Philos. Trans. Biol. Sci. 349 (1995) 249-253
9. Blazis D.E.J. Introduction: the limits to self-organization in biological systems. Biol. Bull. 202 (2002) 245-246
10. Bonabeau E. Social insect colonies as complex adaptive systems. Ecosystems 1 (1998) 437-443
11. Bonabeau E., Theraulaz G., Deneubourg J.-L., Aron S., and Camazine S. Self-organization in social insects. TREE 12 (1997) 188-193
12. Bonabeau E., Dorigo M., and Theraulaz G. Swarm Intelligence: from Natural to Artificial Systems (1999), Oxford Univ. Press, New York
13. Bornholdt S. Less is more in modeling large genetic networks. Science 310 (2005) 449-451
14. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., Gifford D.K., Melton D.A., Jaenisch R., and Young R.A. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122 (2005) 947-956
15. Brown G., Bunce C.M., Lord J.M., and McConnell F.M. The development of cell lineages: a sequential model. Differentiation 39 (1988) 83-89
16. Bruno L., Hoffmann R., McBlane F., Brown J., Gupta R., Joshi C., Pearson S., Seidl T., Heyworth C., and Enver T. Molecular signatures of self-renewal, differentiation, and lineage choice in multipotential hemopoietic progenitor cells in vitro. Mol. Cell. Biol. 24 (2004) 741-756
17. Cai J., Weiss M.L., and Rao M.S. In search of "stemness.". Exp. Hematol. 32 (2004) 585-598
18. Camazine S., Deneubourg J.-L., Franks N., Theraulaz G., and Bonabeau E. Self-Organization in Biological Systems (2001), Princeton Univ. Press, Princeton, NJ
19. Cantor A.B., and Orkin S.H. Hematopoietic development: a balancing act. Curr. Opin. Genet. Dev. 11 (2001) 513-519
20. Cantor A.B., and Orkin S.H. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 21 (2002) 3368-3376
21. Chelly J., Concordet J.-P., Kaplan J.-C., and Kahn A. Illegitimate transcription: transcription of any gene in any cell type. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 2617-2621
22. Ciliberti S., Martin O.C., and Wagner A. Robustness can evolve gradually in complex regulatory gene networks with varying topology. PLoS Comput. Biol. 3 (2007) 164-173
23. Cinquin O., and Demongeot J. Positive and negative feedback: striking a balance between necessary antagonists. J. Theor. Biol. 216 (2002) 229-241
24. Cinquin O., and Demongeot J. High-dimensional switches and the modelling of cellular differentiation. J. Theor. Biol. 233 (2005) 391-411
25. Collins J.J. Fishing for function in noise. Nature 402 (1999) 241-242
26. Collins J.J., Chow C.C., and Imhoff T.T. Stochastic resonance without tuning. Nature 376 (1995) 236-238
27. Collins J.J., Imhoff T.T., and Grigg P. Noise-enhanced tactile sensation. Nature 383 (1996) 770
28. Colvin G.A., Lambert J.-F., Abedi M., Dooner M.S., Demers D., Moore B.E., Greer D., Aliotta J.M., Pimentel J., Cerny J., Lum L.G., and Quesenberry P.J. Differentiation hotspots: the deterioration of hierarchy and stochasm. Blood Cells Mol. Dis. 32 (2004) 34-41
29. Cory S. Wavering on commitment. Nature 401 (1999) 538-539
30. Cross M.A., and Enver T. The lineage commitment of haemopoietic progenitor cells. Curr. Opin. Genet. Dev. 7 (1997) 609-613
31. Cross M.A., Heyworth C.M., Murrell A.M., Bockamp E.O., Dexter T.M., and Green A.R. Expression of lineage restricted transcription factors precedes lineage specific differentiation in a multipotent haemopoietic progenitor cell line. Oncogene 9 (1994) 3013-3016
32. Cross M.A., Heyworth C.M., and Dexter T.M. How do stem cells decide what to do?. The Molecular Basis of Cellular Defence Mechanisms (1997), Wiley, Chichester 3-18
33. Davey R.E., and Zandstra P.W. Signal processing underlying extrinsic control of stem cell fate. Curr. Opin. Hematol. 11 (2004) 95-101
34. Davidson E.H. The Regulatory Genome (2006), Academic Press, San Diego
35. Davidson E.H., McClay D.R., and Hood L. Regulatory gene networks and the properties of the developmental process. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 1475-1480
36. Elowitz M.B., Levine A.J., Siggia E.D., and Swain P.S. Stochastic gene expression in a single cell. Science 297 (2002) 1183-1186
37. Enver T., and Greaves M. Loops, lineage, and leukemia. Cell 94 (1998) 9-12
38. Ferretti C., Bruni L., Dangles-Marie V., Pecking A.P., and Bellet D. Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts. Hum. Reprod. Update 13 (2007) 121-141
39. Ferster D. Is neural noise just a nuisance?. Science 273 (1996) 1812
40. Fortunel N.O., Otu H.H., Ng H.-H., Chen J., Mu X., Chevassut T., Li X., Joseph M., Bailey C., Hatzfeld J.A., Hatzfeld A., Usta F., Vega V.B., Long P.M., Libermann T.A., and Lim B. Comment on "'Stemness': transcriptional profiling of embryonic and adult stem cells" and "A stem cell molecular signature" I. Science 302 (2003) 393 author reply p. 393
41. Fuchs E., Tumbar T., and Guasch G. Socializing with the neighbors. Cell 116 (2004) 769-778
42. Gangenahalli G.U., Gupta P., Saluja D., Verma Y.K., Kishore V., Chandra R., Sharma R.K., and Ravindranath T. Stem cell fate specification: role of master regulatory switch transcription factor PU.1 in differential hematopoiesis. Stem Cells Dev. 14 (2005) 140-152
43. Ghaemmaghami S., Huh W.-K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., and Weissman J.S. Global analysis of protein expression in yeast. Nature 425 (2003) 737
44. Gilden D.L., Thornton T., and Mallon M.W. 1/f noise in human cognition. Science 267 (1995) 1837
45. Goldfarb A.N. Transcriptional control of megakaryocyte development. Oncogene 26 (2007) 6795-6802
46. Graf T. Differentiation plasticity of hematopoietic cells. Blood 99 (2002) 3089-3101
47. Guptasarma P. Does replication-induced transcription regulate synthesis of the myriad low copy number proteins of Escherichia coli?. BioEssays 17 (1995) 987-997
48. Haken H. Synergetics (1977), Springer-Verlag, Berlin
49. Haken H. Synergetics (1983), Springer-Verlag, Berlin
50. Haken H. Synergetics as a strategy to cope with complex systems. In: Haken H., and Mikhailov A. (Eds). Interdisciplinary Approaches to Nonlinear Complex Systems (1992), Springer-Verlag, Berlin
51. Halley J.D., and Winkler D.A. Critical-like self-organization and natural selection: two facets of a single evolutionary process?. BioSystems 92 (2008) 148-158
52. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
53. Hartwell L.H., Hopfield J.J., Leibler S., and Murray A.W. From molecular to modular cell biology. Nature 402 (1999) C47-C52
54. Hasty J., Pradines J., Dolnik M., and Collins J.J. Noise-based switches and amplifiers for gene expression. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 2075-2080
55. Haylock D.N., and Nilsson S.K. Stem cell regulation by the hematopoietic stem cell niche. Cell Cycle 4 (2005) 1353-1355
56. Haylock D.N., Williams B., Johnston H., Liu M., Rutherford K., Whitty G., Simmons P., Bertoncello I., and Nilsson S. HSC with higher hemopoietic potential reside at the bone marrow endosteum. Stem Cells 25 (2007) 1062-1069
57. Heissig B., Ohki Y., Sato Y., Rafii S., Werb Z., and Hattori K. A role for niches in hematopoietic cell development. Hematology 10 (2005) 247-253
58. Hermsen R., Tans S., and ten Wolde P.R. Transcriptional regulation by competing transcription factor modules. PLoS Comput. Biol. 2 (2006) e164
59. Hiden U., Bilban M., Knofler M., and Desoye G. Kisspeptins and the placenta: regulation of trophoblast invasion. Rev. Endocr. Metab. Disord. 8 (2007) 31-39
60. Howard-Ashby M., Materna S.C., Brown C.T., Tu Q., Oliveri P., Cameron R.A., and Davidson E.H. High regulatory gene use in sea urchin embryogenesis: implications for bilaterian development and evolution. Dev. Biol. 300 (2006) 27-34
61. Hu M., Krause D., Greaves M., et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 11 (1997) 774-785
62. Hu Z., Mellor J., Wu J., Kanehisa M., Stuart J.M., and DeLisi C. Towards zoomable multidimensional maps of the cell. Nat. Biotechnol. 25 (2007) 547-554
63. Huang S., Eichler G., Bar-Yam Y., and Ingber D.E. Cell fates as high dimensional attractor states of a complex gene regulatory network. Phys. Rev. Lett. 94 (2005) 128701
64. Huang S., Guo Y.P., May G., and Enver T. Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol. 305 (2007) 695-713
65. Istrail S., and Davidson E.H. Gene regulatory networks special feature: logic functions of the genomic cis-regulatory code. Proc. Natl. Acad. Sci. 102 (2005) 4954-4959
66. Ivanova N.B., et al. A stem cell molecular signature. Science 298 (2002) 601-604
67. Joung J.-G., Shin D., Seong R.H., and Zhang B.-T. Identification of regulatory modules by co-clustering latent variable models: stem cell differentiation. Bioinformatics 22 (2006) 2005-2011
68. Kærn M., Elston T.C., Blake W.J., and Collins J.J. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6 (2005) 451
69. Kaletta T., Schnabel H., and Schnabel R. Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 390 (1997) 294
70. Karsten S.L., Kudo L.C., Jackson R., Sabatti C., Kornblum H.I., and Geschwind D.H. Global analysis of gene expression in neural progenitors reveals specific cell-cycle, signaling, and metabolic networks. Dev. Biol. 261 (2003) 165-182
71. Knofler M., Sooranna S.R., Daoud G., Whitley G.S., Markert U.R., Xia Y., Cantiello H., and Hauguel-de Mouzon S. Trophoblast signalling: knowns and unknowns-a workshop report. Placenta 26 (2005) S49
72. Ko M.S.H. Induction mechanism of a single gene molecule: stochastic or deterministic. BioEssays 14 (1992) 341-346
73. Laforge B., Guez D., Martinez M., and Kupiec J.J. Modeling embryogenesis and cancer: an approach based on an equilibrium between the autostabilization of stochastic gene expression and the interdependence of cells for proliferation. Prog. Biophys. Mol. Biol. 89 (2005) 93-120
74. Lauffenburger D.A. Cell signaling pathways as control modules: complexity for simplicity?. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 5031-5033
75. Lee J.T., and Herlyn M. Microenvironmental influences in melanoma progression. J. Cell. Biochem. 101 (2007) 862-872
76. Li L.H., and Neaves W.B. Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 66 (2006) 4553-4557
77. Li F., Tiede B., Massague J., and Kang Y.B. Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res. 17 (2007) 3-14
78. Li H.C., Fan X.L., and Houghton J. Tumor microenvironment: the role of the tumor stroma in cancer. J. Cell. Biochem. 101 (2007) 805-815
79. Lin H. The stem-cell niche theory: lessons from flies. Nat. Rev. Genet. 3 (2002) 931-940
80. Loose M., and Patient R. Global genetic regulatory networks controlling hematopoietic cell fates. Curr. Opin. Hematol. 13 (2006) 229-236
81. Madan Babu M., Luscombe N.M., Aravind L., Gerstein M., and Teichmann S.A. Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol. 14 (2004) 283-291
82. Mangan S., Zaslaver A., and Alon U. The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J. Mol. Biol. 334 (2003) 197-204
83. Marx J. Mutant stem cells may seed cancer. Science 301 (2003) 1308-1310
84. Materna S.C., and Davidson E.H. Logic of gene regulatory networks. Curr. Opin. Biotechnol. 18 (2007) 351-354
85. McAdams H.H., and Arkin A. Stochastic mechanisms in gene expression. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 814-819
86. McAdams H.H., and Arkin A. It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet. 15 (1999) 65-69
87. Metallo C.M., Mohr J.C., Detzel C.J., de Pablo J.J., Van Wie B.J., and Palecek S.P. Engineering the stem cell microenvironment. Biotechnol. Prog. 23 (2007) 18-23
88. Miyamoto T., Iwasaki H., Reizis B., Ye M., Graf T., Weissman I.L., and Akashi K. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev. Cell 3 (2002) 137-147
89. Moore K.A., and Lemischka I.R. Stem cells and their niches. Science 311 (2006) 1880-1885
90. Nicolis G., and Prigogine I. Self-Organization in Nonequilibrium Systems (1977), Wiley, New York
91. Nilsson S.K., and Simmons P.J. Transplantable stem cells: home to specific niches. Curr. Opin. Hematol. 11 (2004) 102-106
92. Nilsson S.K., Johnston H.M., and Coverdale J.A. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 97 (2001) 2293-2299
93. Nutt S.L., Heavey B., Rolink A.G., and Busslinger M. Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 401 (1999) 556
94. Orkin S.H. Diversification of haematopoietic stem cells to specific lineages. Nat. Rev. Genet. 1 (2000) 57-64
95. Patel K.J., Pambuccian S.E., Ondrey F.G., Adams G.L., and Gaffney P.M. Genes associated with early development, apoptosis and cell cycle regulation define a gene expression profile of adenoid cystic carcinoma. Oral Oncol. 42 (2006) 994-1004
96. Pedraza J.M., and van Oudenaarden A. Noise propagation in gene networks. Science 307 (2005) 1965
97. Phillips R.L., Ernst R.E., Brunk B., Ivanova N., Mahan M.A., Deanehan J.K., Moore K.A., Overton G.C., and Lemischka I.R. The genetic program of hematopoietic stem cells. Science 288 (2000) 1635-1640
98. Ptashne M., and Gann A. Genes and Signals (2002), Cold Spring Harbor Laboratory Press, New York
99. Qu K., Haidar A.A., Fan J., Ensman L., Tuncay K., Jolly M., and Ortoleva P. Cancer onset and progression: a genome-wide, nonlinear dynamical systems perspective on onconetworks. J. Theor. Biol. 246 (2007) 234-244
100. Raj A., Peskin C.S., Tranchina D., Vargas D.Y., and Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 4 (2006) 1707-1719
101. Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., and Melton D.A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298 (2002) 596-600
102. Rao C.V., and Arkin A.P. Control motifs for intracellular regulatory networks. Annu. Rev. Biomed. Eng. 3 (2001) 391-419
103. Rao C.V., Wolf D.M., and Arkin A.P. Control, exploitation and tolerance of intracellular noise. Nature 420 (2002) 231-237
104. Raser J.M., and O'Shea E.K. Control of stochasticity in eukaryotic gene expression. Science 304 (2004) 1811
105. Raser J.M., and O'Shea E.K. Noise in gene expression: origins, consequences, and control. Science 309 (2005) 2010
106. Raubenheimer E.J., and Noffke C.E.E. Pathogenesis of bone metastasis: a review. J. Oral Pathol. Med. 35 (2006) 129-135
107. Ravasz E., Somera A.L., Mongru D.A., Oltvai Z.N., and Barabási A.L. Hierarchical organization of modularity in metabolic networks. Science 297 (2002) 1551-1555
108. Rizo A., Vellenga E., de Haan G., and Schuringa J.J. Signaling pathways in self-renewing hematopoietic and leukemic stem cells: do all stem cells need a niche?. Hum. Mol. Genet. 15 (2006) R210-R219
109. Roeder I., and Glauche I. Towards an understanding of lineage specification in hematopoietic stem cells: a mathematical model for the interaction of transcription factors GATA-1 and PU.1. J. Theor. Biol. 241 (2006) 852-865
110. Rosenbauer F., and Tenen D.G. Transcription factors in myeloid development: balancing differentiation with transformation. Nat. Rev. Immunol. 7 (2007) 105
111. Ross I.L., Browne C.M., and Hume D.A. Transcription of individual genes in eukaryotic cells occurs randomly and infrequently. Immunol. Cell Biol. 72 (1994) 177-185
112. Roth F.P., Hughes J.D., Estep P.W., and Church G.M. Finding DNA regulatory motifs within unaligned noncoding sequences clustered by whole-genome mRNA quantitation. Nat. Biotechnol. 16 (1998) 939-945
113. Rothenberg E.V., and Anderson M.K. Elements of transcription factor network design for T-lineage specification. Dev. Biol. 246 (2002) 29-44
114. Rothenberg E.V., Telfer J.C., and Anderson M.K. Transcriptional regulation of lymphocyte lineage commitment. BioEssays 21 (1999) 726-742
115. Ruiz i Altaba A., Sánchez P., and Dahmane N. Gli and Hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. 2 (2002) 361-372
116. Russell D.F., Wilkens L.A., and Moss F. Use of behavioural stochastic resonance by paddle fish for feeding. Nature 402 (1999) 291-294
117. Segal E., Shapira M., Pe'er A.R.D., Botstein D., Koller D., and Friedman N. Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data. Nat. Genet. 34 (2003) 166-176
118. Shivdasani R.A., and Orkin S.H. The transcriptional control of hematopoiesis. Blood 87 (1996) 4025-4039
119. Sinha S. Complexity vs. stability in small-world networks. Phys. A Stat. Mech. Appl. 346 (2005) 147-153
120. Sternberg P.W., and Félix M.A. Evolution of cell lineage. Curr. Opin. Genet. Dev. 7 (1997) 543-550
121. Sulston J.E., and Horvitz H.R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56 (1977) 110
122. Swain P.S., Elowitz M.B., and Siggia E.D. Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 12795-12800
123. Swiers G., Patient R., and Loose M. Genetic regulatory networks programming hematopoietic stem cells and erythroid lineage specification. Dev. Biol. 294 (2006) 525-540
124. Taichman R.S. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105 (2005) 2631-2639
125. Tavazoie S., Hughes J.D., Campbell M.J., Cho R.J., and Church G.M. Systematic determination of genetic network architecture. Nat. Genet. 22 (1999) 281-285
126. Tomlin C.J., and Axelrod J.D. Biology by numbers: mathematical modelling in developmental biology. Nat. Rev. Genet. 8 (2007) 331
127. Traynelis S.F., and Jaramillo F. Getting the most out of noise in the central nervous system. Trends Neurosci. 21 (1998) 137
128. Tsai R.Y.L. A molecular view of stem cell and cancer cell self-renewal. Int. J. Biochem. Cell Biol. 36 (2004) 684-694
129. Tyagi S. RT-PCR enters the realm of stochastic gene expression. Genetic Eng. Biotechnol. News (2007) 27
130. Vogel G. 'Stemness' genes still elusive. Science 302 (2003) 371
131. von Dassow G., Meir E., Munro E.M., and Odell G.M. The segment polarity network is a robust developmental module. Nature 406 (2000) 188-192
132. Weatherall D.J. Phenotype-genotype relationship in monogenic disease: lessons from the thalassemias. Nat. Rev. Genet. 2 (2001) 245-255
133. Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T., Turner D., Rupp R., Hollenberg S., et al. The myoD gene family: nodal point during specification of the muscle cell lineage. Science (1991) 761-766
134. Wiesenfeld K., and Moss F. Stochastic resonance and the benefits of noise: from ice ages to crayfish and SQUIDs. Nature 373 (1995) 33-36
135. Wilczynski J.R. Cancer and pregnancy share similar mechanisms of immunological escape. Chemotherapy 52 (2006) 107-110
136. Wilmers C.C., Sinha S., and Brede M. Examining the effects of species richness on community stability: an assembly model approach. Oikos 99 (2002) 363-367
137. Wilson A., and Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat. Rev. Immunol. 6 (2006) 93-106
138. Yin T., and Li L.H. The stem cell niches in bone. J. Clin. Invest. 116 (2006) 1195-1201
139. Zlokarnik G., Negulescu P.A., Knapp T.E., Mere L., Burres N., Feng L., Whitney M., Roemer K., and Tsien R.Y. Quantitation of transcription and clonal selection of single living cells with β-lactamase as reporter. Science 279 (1998) 84-88