Novel insights into embryonic stem cell self-renewal revealed through comparative human and mouse systems biology networks

Stem Cells

Volumn 32, Issue 5, 2014, Pages 1161-1172

  Dowell, Karen G ^a,b   Simons, Allen K ^a   Bai, Hao ^c   Kell, Braden ^a   Wang, Zack Z ^b,c   Yun, Kyuson ^a,d   Hibbs, Matthew A ^a,b,d  

^a Jackson Laboratory   (United States)

^b UNIVERSITY OF MAINE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TRINITY UNIVERSITY   (United States)

Author keywords

Biomathematical modeling; Cell signaling, Genomics; Computational biology; Embryonic stem cells; Pluripotent stem cells

Indexed keywords

ACTIVIN A; FIBROBLAST GROWTH FACTOR; LEUKEMIA INHIBITORY FACTOR; OCTAMER TRANSCRIPTION FACTOR 4; THREONINE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; BAYESIAN LEARNING; CELL RENEWAL; EMBRYONIC STEM CELL; GENE FUNCTION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; MOUSE; NONHUMAN; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SYSTEMS BIOLOGY; ALGORITHM; ANIMAL; BAYES THEOREM; BIOLOGY; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; COMPARATIVE STUDY; CYTOLOGY; GENE REGULATORY NETWORK; METABOLISM; PROCEDURES; REPRODUCIBILITY;

ALGORITHMS; ANIMALS; BAYES THEOREM; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; EMBRYONIC STEM CELLS; GENE REGULATORY NETWORKS; HUMANS; MICE; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY;

EID: 84898932788     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1612     Document Type: Article

References (80)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282: 1145-1147.
2. Gokhale PJ, Andrews PW,. The development of pluripotent stem cells. Curr Opin Genet Dev 2012; 22: 403-408.
3. Ginis I, Luo Y, Miura T, et al. Differences between human and mouse embryonic stem cells. Dev Biol 2004; 269: 360-380.
4. Brown S, Teo A, Pauklin S, et al. Activin/nodal signaling controls divergent transcriptional networks in human embryonic stem cells and in endoderm progenitors. Stem Cells 2011; 29: 1176-1185.
5. Welling M, Geijsen N,. Uncovering the true identity of naive pluripotent stem cells. Trends Cell Biol 2013; 23: 442-448.
6. Martin GR,. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78: 7634-7638.
7. Evans MJ, Kaufman MH,. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292: 154-156.
8. Greber B, Wu G, Bernemann C, et al. Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 2010; 6: 215-226.
9. Saunders A, Faiola F, Wang J,. Pursuing self-renewal and pluripotency with the stem cell factor nanog. Stem Cells 2013; 31: 1227-1236.
10. Nichols J, Smith A,. The origin and identity of embryonic stem cells. Development 2011; 138: 3-8.
11. Nichols J, Smith A,. Naive and primed pluripotent states. Cell Stem Cell 2009; 4: 487-492.
12. Lanza RP,. Essent Stem Cell Biol 2006; xxxi: 548.
13. De Los Angeles A, Loh YH, Tesar PJ, et al. Accessing naive human pluripotency. Curr Opin Genet Dev 2012; 22: 272-282.
14. Tesar PJ, Chenoweth JG, Brook FA, et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007; 448: 196-199.
15. Tomoda K, Takahashi K, Leung K, et al. Derivation conditions impact X-inactivation status in female human induced pluripotent stem cells. Cell Stem Cell 2012; 11: 91-99.
16. Nazor KL, Altun G, Lynch C, et al. Recurrent variations in DNA methylation in human pluripotent stem cells and their differentiated derivatives. Cell Stem Cell 2012; 10: 620-634.
17. Chenoweth JG, McKay RD, Tesar PJ,. Epiblast stem cells contribute new insight into pluripotency and gastrulation. Dev Growth Different 2010; 52: 293-301.
18. Tachibana M, Sparman M, Ramsey C, et al. Generation of chimeric rhesus monkeys. Cell 2012; 148: 285-295.
19. Takahashi K, Yamanaka S,. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-676.
20. Ema M, Mori D, Niwa H, et al. Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell 2008; 3: 555-567.
21. Buganim Y, Faddah DA, Jaenisch R,. Mechanisms and models of somatic cell reprogramming. Nat Rev Genet 2013; 14: 427-439.
22. Meissner A,. Epigenetic modifications in pluripotent and differentiated cells. Nat Biotechnol 2010; 28: 1079-1088.
23. Jaenisch R, Young R,. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 2008; 132: 567-582.
24. Chambers I, Tomlinson SR,. The transcriptional foundation of pluripotency. Development 2009; 136: 2311-2322.
25. Dowell KG, Simons AK, Wang ZZ, et al. Cell-type-specific predictive network yields novel insights into mouse embryonic stem cell self-renewal and cell fate. PLoS One 2013; 8: e56810.
26. Huttenhower C, Hibbs MA, Myers CL, et al. The impact of incomplete knowledge on evaluation: An experimental benchmark for protein function prediction. Bioinformatics 2009; 25: 2404-2410.
27. Hibbs MA,. Advanced Bioinformatics Tools and Strategies. In: Principles and Practices of Plant Genomics. Vol. 3, Enfield, NH: Science Publishers 2010.
28. Russell S, Norvig P,. Artifical Intelligence: A Modern Approach, III ed. Fort Collins, CO: Prentice Hall, 2009.
29. Charniak E,. Bayesian networks without tears. AI Magazine 1991; 91: 50-63.
30. Darwiche A,. Modeling and Reasoning with Bayesian Networks. Cambridge; New York: Cambridge University Press, 2009.
31. Hibbs MA, Myers CL, Huttenhower C, et al. Directing experimental biology: A case study in mitochondrial biogenesis. PLoS Comput Biol 2009; 5: e1000322.
32. Bult CJ, Kadin JA, Richardson JE, et al. The Mouse Genome Database: Enhancements and updates. Nucleic Acids Res 2010; 38: D586-D592.
33. Dolan ME, Ni L, Camon E, Blake JA,. A procedure for assessing GO annotation consistency. Bioinformatics 2005; 21: i136-i143.
34. Kanehisa M,. The KEGG database. Novartis Found Symp 2002; 247: 91-101;discussion 101-103, 119-128, 244-152.
35. Kelder T, van Iersel MP, Hanspers K, et al. WikiPathways: Building research communities on biological pathways. Nucl Acids Res 2012; 40: D1301-D1307.
36. Huttenhower C, Schroeder M, Chikina MD, et al. The Sleipnir library for computational functional genomics. Bioinformatics 2008; 24: 1559-1561.
37. Guan Y, Myers CL, Lu R, et al. A genomewide functional network for the laboratory mouse. PLoS Comput Biol 2008; 4: e1000165.
38. Myers CL, Barrett DR, Hibbs MA, et al. Finding function: Evaluation methods for functional genomic data. BMC Genom 2006; 7: 187.
39. Huttenhower C, Haley EM, Hibbs MA, et al. Exploring the human genome with functional maps. Genome Res 2009; 19: 1093-1106.
40. Dennis G Jr, Sherman BT, Hosack DA, et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery Genome Biology 2003; 4: P3.
41. Blake JA, Dolan M, Drabkin H, et al. The gene ontology in 2010: Extensions and refinements. Nucl Acids Res 2010; 38: D331-D335.
42. Horvath S, Dong J,. Geometric interpretation of gene coexpression network analysis. PLoS Comput Biol 2008; 4: e1000117.
43. Bai H, Chen K, Gao YX, et al. Bcl-xL enhances single-cell survival and expansion of human embryonic stem cells without affecting self-renewal. Stem Cell Res 2012; 8: 26-37.
44. Bai H, Gao Y, Arzigian M, et al. BMP4 regulates vascular progenitor development in human embryonic stem cells through a Smad-dependent pathway. J Cell Biochem 2010; 109: 363-374.
45. Bai H, Xie YL, Gao YX, et al. The balance of positive and negative effects of TGF-beta signaling regulates the development of hematopoietic and endothelial progenitors in human pluripotent stem cells. Stem Cells Dev 2013; 22: 2765-2776.
46. Myers CL, Robson D, Wible A, et al. Discovery of biological networks from diverse functional genomic data. Genome Biol 2005; 6: R114.
47. Troyanskaya OG, Dolinski K, Owen AB, et al. A Bayesian framework for combining heterogeneous data sources for gene function prediction (in Saccharomyces cerevisiae). Proc Natl Acad Sci USA 2003; 100: 8348-8353.
48. Tsuneyoshi N, Sumi T, Onda H, et al. PRDM14 suppresses expression of differentiation marker genes in human embryonic stem cells. Biochem Biophys Res Commun 2008; 367: 899-905.
49. Chan YS, Goke J, Lu X, et al. A PRC2-dependent repressive role of PRDM14 in human embryonic stem cells and induced pluripotent stem cell reprogramming. Stem Cells 2012; 31: 682-692.
50. Cheng Q, Chang JT, Geradts J, et al. Amplification and high-level expression of heat shock protein 90 marks aggressive phenotypes of human epidermal growth factor receptor 2 negative breast cancer. Breast Cancer Res 2012; 14: R62.
51. Ren J, Wang R, Huang G, et al. sFRP1 inhibits epithelial-mesenchymal transition in A549 human lung adenocarcinoma cell line. Cancer Biother Radiopharm 2013; 28: 565-571.
52. Katoh M,. Comparative integromics on non-canonical WNT or planar cell polarity signaling molecules: Transcriptional mechanism of PTK7 in colorectal cancer and that of SEMA6A in undifferentiated ES cells. Int J Mol Med 2007; 20: 405-409.
53. Zhang T, Meng L, Dong W, et al. High expression of PRDM14 correlates with cell differentiation and is a novel prognostic marker in resected non-small cell lung cancer. Med Oncol 2013; 30: 605.
54. Lodish HF, Berk A, Kaiser C, et al. Molecular Cell Biology, 6th ed. New York, NY: WH Freeman and Co., 2008.
55. Gundersen GG, Worman HJ,. Nuclear positioning. Cell 2013; 152: 1376-1389.
56. Kele J, Andersson ER, Villaescusa JC, et al. SFRP1 and SFRP2 dose-dependently regulate midbrain dopamine neuron development in vivo and in embryonic stem cells. Stem Cells 2012; 30: 865-875.
57. Shahi MH, Rey JA, Castresana JS,. The sonic hedgehog-GLI1 signaling pathway in brain tumor development. Expert Opin Ther Targets 2012; 16: 1227-1238.
58. Wu Q, Sun CC, Lin HY, et al. Repulsive guidance molecule (RGM) family proteins exhibit differential binding kinetics for bone morphogenetic proteins (BMPs). PLoS One 2012; 7: e46307.
59. Doege CA, Inoue K, Yamashita T, et al. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 2012; 488: 652-655.
60. Krishnakumar R, Kraus WL,. The PARP side of the nucleus: Molecular actions, physiological outcomes, and clinical targets. Mol Cell 2010; 39: 8-24.
61. Lickert H, Cox B, Wehrle C, et al. Dissecting Wnt/beta-catenin signaling during gastrulation using RNA interference in mouse embryos. Development 2005; 132: 2599-2609.
62. He S, Nakada D, Morrison SJ,. Mechanisms of stem cell self-renewal. Ann Rev Cell Dev Biol 2009; 25: 377-406.
63. Vallier L, Touboul T, Brown S, et al. Signaling pathways controlling pluripotency and early cell fate decisions of human induced pluripotent stem cells. Stem Cells 2009; 27: 2655-2666.
64. Minkovsky A, Barakat TS, Sellami N, et al. The pluripotency factor-bound intron 1 of Xist is dispensable for X chromosome inactivation and reactivation in vitro and in vivo. Cell Rep 2013; 3: 905-918.
65. Lanner F, Rossant J,. The role of FGF/Erk signaling in pluripotent cells. Development 2010; 137: 3351-3360.
66. Nishimura T, Utsunomiya Y, Hoshikawa M, et al. Structure and expression of a novel human FGF, FGF-19, expressed in the fetal brain. Biochim Biophys Acta 1999; 1444: 148-151.
67. Borello U, Cobos I, Long JE, et al. FGF15 promotes neurogenesis and opposes FGF8 function during neocortical development. Neural Dev 2008; 3: 17.
68. Kristensen DM, Kalisz M, Nielsen JH,. Cytokine signalling in embryonic stem cells. Apmis 2005; 113: 756-772.
69. Okita K, Yamanaka S,. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr Stem Cell Res Ther 2006; 1: 103-111.
70. Ying QL, Wray J, Nichols J, et al. The ground state of embryonic stem cell self-renewal. Nature 2008; 453: 519-523.
71. Niwa H, Burdon T, Chambers I, et al. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1998; 12: 2048-2060.
72. Liu N, Lu M, Tian X, et al. Molecular mechanisms involved in self-renewal and pluripotency of embryonic stem cells. J Cell Physiol 2007; 211: 279-286.
73. Matoba R, Niwa H, Masui S, et al. Dissecting Oct3/4-regulated gene networks in embryonic stem cells by expression profiling. PLoS One 2006; 1: e26.
74. Wang J, Alexander P, Wu L, et al. Dependence of mouse embryonic stem cells on threonine catabolism. Science 2009; 325: 435-439.
75. Shyh-Chang N, Locasale JW, Lyssiotis CA, et al. Influence of threonine metabolism on S-adenosylmethionine and histone methylation. Science 2013; 339: 222-226.
76. Wang J, Alexander P, McKnight SL,. Metabolic specialization of mouse embryonic stem cells. Cold Spring Harbor Symp Quant Biol 2011, 76: 183-193.
77. Hindley C, Philpott A,. The cell cycle and pluripotency. Biochem J 2013; 451: 135-143.
78. Shyh-Chang N, Daley GQ,. Lin28: Primal regulator of growth and metabolism in stem cells. Cell Stem Cell 2013; 12: 395-406.
79. Peng S, Chen LL, Lei XX, et al. Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem Cells 2011; 29: 496-504.
80. Cho J, Chang H, Kwon SC, et al. LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 2012; 151: 765-777.