TF-Cluster: A pipeline for identifying functionally coordinated transcription factors via network decomposition of the shared coexpression connectivity matrix (SCCM)

BMC Systems Biology

Volumn 5, Issue , 2011, Pages

  Nie, Jeff ^a   Stewart, Ron ^a   Zhang, Hang ^d   Thomson, James A ^a,b,e   Ruan, Fang ^c   Cui, Xiaoqi ^c   Wei, Hairong ^c  

^a MORGRIDGE INSTITUTE FOR RESEARCH   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^d Michigan Technological University   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; EUKARYOTA;

ALGORITHM; ANIMAL; ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; BIOLOGY; CELL DIFFERENTIATION; CLUSTER ANALYSIS; COMPUTER PROGRAM; CYTOLOGY; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME; HUMAN; METHODOLOGY; PHYSIOLOGY; PLANT ROOT; SYSTEMS BIOLOGY;

ALGORITHMS; ANIMALS; ARABIDOPSIS; CELL DIFFERENTIATION; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME; HUMANS; MODELS, GENETIC; PLANT ROOTS; SOFTWARE; SYSTEMS BIOLOGY;

EID: 79955091925     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-5-53     Document Type: Article

References (118)

1. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131(5):861-872. 10.1016/j.cell.2007.11.019, 18035408.
2. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318(5858):1917-1920. 10.1126/science.1151526, 18029452.
3. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008, 455(7213):627-632. 10.1038/nature07314, 18754011.
4. Mittler R, Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 2010, 61:443-462. 10.1146/annurev-arplant-042809-112116, 20192746.
5. Cui X, Wang T, Chen HS, Busov V, Wei H. TF-finder: a software package for identifying transcription factors involved in biological processes using microarray data and existing knowledge base. BMC Bioinformatics 2010, 11:425. 10.1186/1471-2105-11-425, 2930629, 20704747.
6. Faith JJ, Hayete B, Thaden JT, Mogno I, Wierzbowski J, Cottarel G, Kasif S, Collins JJ, Gardner TS. Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLoS Biol 2007, 5(1):e8. 10.1371/journal.pbio.0050008, 1764438, 17214507.
7. Gardner TS, di Bernardo D, Lorenz D, Collins JJ. Inferring genetic networks and identifying compound mode of action via expression profiling. Science 2003, 301(5629):102-105. 10.1126/science.1081900, 12843395.
8. Margolin AA, Nemenman I, Basso K, Wiggins C, Stolovitzky G, Dalla Favera R, Califano A. ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics 2006, 7(Suppl 1):S7. 10.1186/1471-2105-7-S1-S7, 1810318, 16723010.
9. Margolin AA, Califano A. Theory and limitations of genetic network inference from microarray data. Ann N Y Acad Sci 2007, 1115:51-72. 10.1196/annals.1407.019, 17925348.
10. Qian J, Lin J, Luscombe NM, Yu H, Gerstein M. Prediction of regulatory networks: genome-wide identification of transcription factor targets from gene expression data. Bioinformatics 2003, 19(15):1917-1926. 10.1093/bioinformatics/btg347, 14555624.
11. Wei H, Kaznessis Y. Inferring gene regulatory relationships by combining target-target pattern recognition and regulator-specific motif examination. Biotechnol Bioeng 2005, 89(1):53-77. 10.1002/bit.20305, 15540196.
12. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 2005, 6(6):451-464. 10.1038/nrg1615, 15883588.
13. Rowicka M, Kudlicki A, Tu BP, Otwinowski Z. High-resolution timing of cell cycle-regulated gene expression. Proc Natl Acad Sci USA 2007, 104(43):16892-16897. 10.1073/pnas.0706022104, 2040468, 17827275.
14. Aulehla A, Pourquie O. Oscillating signaling pathways during embryonic development. Curr Opin Cell Biol 2008, 20(6):632-637. 10.1016/j.ceb.2008.09.002, 18845254.
15. Komili S, Silver PA. Coupling and coordination in gene expression processes: a systems biology view. Nat Rev Genet 2008, 9(1):38-48. 10.1038/nrg2223, 18071322.
16. Raser JM, O'Shea EK. Noise in gene expression: origins, consequences, and control. Science 2005, 309(5743):2010-2013. 10.1126/science.1105891, 1360161, 16179466.
17. Jiang C, Pugh BF. Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 2009, 10(3):161-172. 10.1038/nrg2522, 19204718.
18. Becskei A, Kaufmann BB, van Oudenaarden A. Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat Genet 2005, 37(9):937-944. 10.1038/ng1616, 16086016.
19. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol 2006, 4(10):e309. 10.1371/journal.pbio.0040309, 1563489, 17048983.
20. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30(7):1575-1584. 10.1093/nar/30.7.1575, 101833, 11917018.
21. Frey BJ, Dueck D. Clustering by passing messages between data points. Science 2007, 315(5814):972-976. 10.1126/science.1136800, 17218491.
22. Giuliano CJ, Kerley-Hamilton JS, Bee T, Freemantle SJ, Manickaratnam R, Dmitrovsky E, Spinella MJ. Retinoic acid represses a cassette of candidate pluripotency chromosome 12p genes during induced loss of human embryonal carcinoma tumorigenicity. Biochim Biophys Acta 2005, 1731(1):48-56.
23. Wang ZX, Kueh JL, Teh CH, Rossbach M, Lim L, Li P, Wong KY, Lufkin T, Robson P, Stanton LW. Zfp206 is a transcription factor that controls pluripotency of embryonic stem cells. Stem Cells 2007, 25(9):2173-2182. 10.1634/stemcells.2007-0085, 17628018.
24. Yu HB, Kunarso G, Hong FH, Stanton LW. Zfp206, Oct4, and Sox2 are integrated components of a transcriptional regulatory network in embryonic stem cells. J Biol Chem 2009, 284(45):31327-31335. 10.1074/jbc.M109.016162, 2781530, 19740739.
25. Giorgetti A, Montserrat N, Aasen T, Gonzalez F, Rodriguez-Piza I, Vassena R, Raya A, Boue S, Barrero MJ, Corbella BA, et al. Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell 2009, 5(4):353-357. 10.1016/j.stem.2009.09.008, 2779776, 19796614.
26. Gopalakrishnan S, Van Emburgh BO, Shan J, Su Z, Fields CR, Vieweg J, Hamazaki T, Schwartz PH, Terada N, Robertson KD. A novel DNMT3B splice variant expressed in tumor and pluripotent cells modulates genomic DNA methylation patterns and displays altered DNA binding. Mol Cancer Res 2009, 7(10):1622-1634. 10.1158/1541-7786.MCR-09-0018, 2783805, 19825994.
27. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 2006, 10(1):105-116. 10.1016/j.devcel.2005.10.017, 1868458, 16399082.
28. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006, 38(4):431-440. 10.1038/ng1760, 16518401.
29. Fouse SD, Shen Y, Pellegrini M, Cole S, Meissner A, Van Neste L, Jaenisch R, Fan G. Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2008, 2(2):160-169. 10.1016/j.stem.2007.12.011, 3070208, 18371437.
30. Kranc KR, Bamforth SD, Braganca J, Norbury C, van Lohuizen M, Bhattacharya S. Transcriptional coactivator Cited2 induces Bmi1 and Mel18 and controls fibroblast proliferation via Ink4a/ARF. Mol Cell Biol 2003, 23(21):7658-7666. 10.1128/MCB.23.21.7658-7666.2003, 207593, 14560011.
31. Kranc KR, Schepers H, Rodrigues NP, Bamforth S, Villadsen E, Ferry H, Bouriez-Jones T, Sigvardsson M, Bhattacharya S, Jacobsen SE, et al. Cited2 is an essential regulator of adult hematopoietic stem cells. Cell Stem Cell 2009, 5(6):659-665. 10.1016/j.stem.2009.11.001, 2828538, 19951693.
32. Greber B, Lehrach H, Adjaye J. Silencing of core transcription factors in human EC cells highlights the importance of autocrine FGF signaling for self-renewal. BMC Dev Biol 2007, 7:46. 10.1186/1471-213X-7-46, 1885259, 17506876.
33. Stein MI, Zhu J, Emerson SG. Molecular pathways regulating the self-renewal of hematopoietic stem cells. Exp Hematol 2004, 32(12):1129-1136. 10.1016/j.exphem.2004.08.012, 15588937.
34. Miyake N, Brun AC, Magnusson M, Miyake K, Scadden DT, Karlsson S. HOXB4-induced self-renewal of hematopoietic stem cells is significantly enhanced by p21 deficiency. Stem Cells 2006, 24(3):653-661. 10.1634/stemcells.2005-0328, 16210402.
35. Kelz MB, Nestler EJ. deltaFosB: a molecular switch underlying long-term neural plasticity. Curr Opin Neurol 2000, 13(6):715-720. 10.1097/00019052-200012000-00017, 11148675.
36. Joosten PH, van Zoelen EJ, Murre C. Pax1/E2a double-mutant mice develop non-lethal neural tube defects that resemble human malformations. Transgenic Res 2005, 14(6):983-987. 10.1007/s11248-005-2540-9, 16315099.
37. Vahava O, Morell R, Lynch ED, Weiss S, Kagan ME, Ahituv N, Morrow JE, Lee MK, Skvorak AB, Morton CC, et al. Mutation in transcription factor POU4F3 associated with inherited progressive hearing loss in humans. Science 1998, 279(5358):1950-1954. 10.1126/science.279.5358.1950, 9506947.
38. Bosnakovski D, Daughters RS, Xu Z, Slack JM, Kyba M. Biphasic myopathic phenotype of mouse DUX, an ORF within conserved FSHD-related repeats. PLoS One 2009, 4(9):e7003. 10.1371/journal.pone.0007003, 2737622, 19756142.
39. Garcia-Barcelo MM, Lau DK, Ngan ES, Leon TY, Liu TT, So MT, Miao XP, Lui VC, Wong KK, Ganster RW, et al. Evaluation of the thyroid transcription factor-1 gene (TITF1) as a Hirschsprung's disease locus. Ann Hum Genet 2007, 71(Pt 6):746-754. 10.1111/j.1469-1809.2007.00384.x, 17640327.
40. Bajard L, Relaix F, Lagha M, Rocancourt D, Daubas P, Buckingham ME. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev 2006, 20(17):2450-2464. 10.1101/gad.382806, 1560418, 16951257.
41. Teboul L, Hadchouel J, Daubas P, Summerbell D, Buckingham M, Rigby PW. The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis. Development 2002, 129(19):4571-4580.
42. Hadchouel J, Tajbakhsh S, Primig M, Chang TH, Daubas P, Rocancourt D, Buckingham M. Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo. Development 2000, 127(20):4455-4467.
43. Daubas P, Crist CG, Bajard L, Relaix F, Pecnard E, Rocancourt D, Buckingham M. The regulatory mechanisms that underlie inappropriate transcription of the myogenic determination gene Myf5 in the central nervous system. Dev Biol 2009, 327(1):71-82. 10.1016/j.ydbio.2008.11.031, 19100730.
44. Daubas P, Tajbakhsh S, Hadchouel J, Primig M, Buckingham M. Myf5 is a novel early axonal marker in the mouse brain and is subjected to post-transcriptional regulation in neurons. Development 2000, 127(2):319-331.
45. Home P, Ray S, Dutta D, Bronshteyn I, Larson M, Paul S. GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J Biol Chem 2009, 284(42):28729-28737. 10.1074/jbc.M109.016840, 2781418, 19700764.
46. Xu RH. In vitro induction of trophoblast from human embryonic stem cells. Methods Mol Med 2006, 121:189-202.
47. Ma GT, Roth ME, Groskopf JC, Tsai FY, Orkin SH, Grosveld F, Engel JD, Linzer DI. GATA-2 and GATA-3 regulate trophoblast-specific gene expression in vivo. Development 1997, 124(4):907-914.
48. Buttitta L, Mo R, Hui CC, Fan CM. Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 2003, 130(25):6233-6243. 10.1242/dev.00851, 14602680.
49. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 2003, 5(6):877-889. 10.1016/S1534-5807(03)00363-0, 14667410.
50. Brunelli S, Cossu G. A role for MSX2 and necdin in smooth muscle differentiation of mesoangioblasts and other mesoderm progenitor cells. Trends Cardiovasc Med 2005, 15(3):96-100. 10.1016/j.tcm.2005.04.004, 16039969.
51. Godwin AR, Capecchi MR. Hair defects in Hoxc13 mutant mice. J Investig Dermatol Symp Proc 1999, 4(3):244-247. 10.1038/sj.jidsp.5640221, 10674376.
52. Futaki S, Hayashi Y, Emoto T, Weber CN, Sekiguchi K. Sox7 plays crucial roles in parietal endoderm differentiation in F9 embryonal carcinoma cells through regulating Gata-4 and Gata-6 expression. Mol Cell Biol 2004, 24(23):10492-10503. 10.1128/MCB.24.23.10492-10503.2004, 529033, 15542856.
53. Sturgeon K, Kaneko T, Biemann M, Gauthier A, Chawengsaksophak K, Cordes SP. Cdx1 refines positional identity of the vertebrate hindbrain by directly repressing Mafb expression. Development 138(1):65-74. 10.1242/dev.058727, 21098558.
54. Filippi A, Tiso N, Deflorian G, Zecchin E, Bortolussi M, Argenton F. The basic helix-loop-helix olig3 establishes the neural plate boundary of the trunk and is necessary for development of the dorsal spinal cord. Proc Natl Acad Sci USA 2005, 102(12):4377-4382. 10.1073/pnas.0407284102, 549604, 15731351.
55. Onishi A, Peng GH, Hsu C, Alexis U, Chen S, Blackshaw S. Pias3-dependent SUMOylation directs rod photoreceptor development. Neuron 2009, 61(2):234-246. 10.1016/j.neuron.2008.12.006, 2701228, 19186166.
56. Lee J, Sayegh J, Daniel J, Clarke S, Bedford MT. PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J Biol Chem 2005, 280(38):32890-32896. 10.1074/jbc.M506944200, 16051612.
57. Stegmann K, Boecker J, Kosan C, Ermert A, Kunz J, Koch MC. Human transcription factor SLUG: mutation analysis in patients with neural tube defects and identification of a missense mutation (D119E) in the Slug subfamily-defining region. Mutat Res 1999, 406(2-4):63-69.
58. Karas B, Amyot L, Johansen C, Sato S, Tabata S, Kawaguchi M, Szczyglowski K. Conservation of lotus and Arabidopsis basic helix-loop-helix proteins reveals new players in root hair development. Plant Physiol 2009, 151(3):1175-1185. 10.1104/pp.109.143867, 2773103, 19675148.
59. Yi K, Menand B, Bell E, Dolan L. A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nat Genet 2010, 42(3):264-267. 10.1038/ng.529, 20139979.
60. Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 2007, 316(5830):1477-1480. 10.1126/science.1142618, 17556585.
61. Singh SK, Fischer U, Singh M, Grebe M, Marchant A. Insight into the early steps of root hair formation revealed by the procuste1 cellulose synthase mutant of Arabidopsis thaliana. BMC Plant Biol 2008, 8:57. 10.1186/1471-2229-8-57, 2396171, 18485206.
62. Jung J, Won SY, Suh SC, Kim H, Wing R, Jeong Y, Hwang I, Kim M. The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta 2007, 225(3):575-588. 10.1007/s00425-006-0373-2, 16937017.
63. Wilson K, Long D, Swinburne J, Coupland G. A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 1996, 8(4):659-671. 10.1105/tpc.8.4.659, 161127, 8624440.
64. Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P. FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 2004, 577(3):528-534. 10.1016/j.febslet.2004.10.062, 15556641.
65. Yuan YX, Zhang J, Wang DW, Ling HQ. AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 2005, 15(8):613-621. 10.1038/sj.cr.7290331, 16117851.
66. Bennett T, van den Toorn A, Sanchez-Perez GF, Campilho A, Willemsen V, Snel B, Scheres B. SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 2010, 22(3):640-654. 10.1105/tpc.109.072272, 2861445, 20197506.
67. Willemsen V, Bauch M, Bennett T, Campilho A, Wolkenfelt H, Xu J, Haseloff J, Scheres B. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 2008, 15(6):913-922. 10.1016/j.devcel.2008.09.019, 19081078.
68. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010, 464(7290):913-916. 10.1038/nature08836, 20220754.
69. Zhou W, Wei L, Xu J, Zhai Q, Jiang H, Chen R, Chen Q, Sun J, Chu J, Zhu L, et al. Arabidopsis Tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 2010, 22(11):3692-3709. 10.1105/tpc.110.075721, 3015123, 21045165.
70. Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P. Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 2005, 102(36):12978-12983. 10.1073/pnas.0504039102, 1200278, 16123132.
71. Fu X, Harberd NP. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 2003, 421(6924):740-743. 10.1038/nature01387, 12610625.
72. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T. Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 2005, 19(16):1855-1860. 10.1101/gad.1331305, 1186185, 16103214.
73. Grant EH, Fujino T, Beers EP, Brunner AM. Characterization of NAC domain transcription factors implicated in control of vascular cell differentiation in Arabidopsis and Populus. Planta 2010, 232(2):337-352. 10.1007/s00425-010-1181-2, 20458494.
74. Gardiner J, Sherr I, Scarpella E. Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol 2010, 54(8-9):1389-1396. 10.1387/ijdb.093006jg, 20563990.
75. Lee HW, Kim NY, Lee DJ, Kim J. LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol 2009, 151(3):1377-1389. 10.1104/pp.109.143685, 2773067, 19717544.
76. Zhong R, Richardson EA, Ye ZH. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 2007, 19(9):2776-2792. 10.1105/tpc.107.053678, 2048704, 17890373.
77. Raynaud C, Sozzani R, Glab N, Domenichini S, Perennes C, Cella R, Kondorosi E, Bergounioux C. Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J 2006, 47(3):395-407. 10.1111/j.1365-313X.2006.02799.x, 16771839.
78. Sozzani R, Maggio C, Giordo R, Umana E, Ascencio-Ibañez JT, Hanley-Bowdoin L, Bergounioux C, Cella R, Albani D. The E2FD/DEL2 factor is a component of a regulatory network controlling cell proliferation and development in Arabidopsis. Plant Molecular Biology 2009, 72(4-5):381-395. 10.1007/s11103-009-9577-8, 19937368.
79. Menges M, Hennig L, Gruissem W, Murray JA. Cell cycle-regulated gene expression in Arabidopsis. J Biol Chem 2002, 277(44):41987-42002. 10.1074/jbc.M207570200, 12169696.
80. Kim JH, Kende H. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci USA 2004, 101(36):13374-13379. 10.1073/pnas.0405450101, 516574, 15326298.
81. Kim JH, Choi D, Kende H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 2003, 36(1):94-104. 10.1046/j.1365-313X.2003.01862.x, 12974814.
82. Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM. HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell 2004, 16(10):2586-2600. 10.1105/tpc.104.024869, 520957, 15367721.
83. d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, Jenczewski E, Mercier R. Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLoS Genet 2008, 4(11):e1000274. 10.1371/journal.pgen.1000274, 2581889, 19043546.
84. Sehnke PC, Laughner BJ, Lyerly Linebarger CR, Gurley WB, Ferl RJ. Identification and characterization of GIP1, an Arabidopsis thaliana protein that enhances the DNA binding affinity and reduces the oligomeric state of G-box binding factors. Cell Res 2005, 15(8):567-575. 10.1038/sj.cr.7290326, 16117846.
85. Jiang H, Li H, Bu Q, Li C. The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response. Plant Signal Behav 2009, 4(5):464-466. 10.4161/psb.4.5.8543, 2676768, 19816098.
86. Olsson AS, Engstrom P, Soderman E. The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Mol Biol 2004, 55(5):663-677. 10.1007/s11103-004-1581-4, 15604708.
87. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 2004, 16(9):2481-2498. 10.1105/tpc.104.022699, 520947, 15319476.
88. Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 2004, 16(3):596-615. 10.1105/tpc.019000, 385275, 14973164.
89. Oda Y, Yoshimura Y, Ohnishi H, Tadokoro M, Katsube Y, Sasao M, Kubo Y, Hattori K, Saito S, Horimoto K, et al. Induction of pluripotent stem cells from human third molar mesenchymal stromal cells. J Biol Chem 2010, 285(38):29270-29278. 10.1074/jbc.M109.055889, 20595386.
90. Masip M, Veiga A, Izpisua Belmonte JC, Simon C. Reprogramming with defined factors: from induced pluripotency to induced transdifferentiation. Mol Hum Reprod 2010, 16(11):856-868. 10.1093/molehr/gaq059, 20616150.
91. Kotlyar M, Fuhrman S, Ableson A, Somogyi R. Spearman correlation identifies statistically significant gene expression clusters in spinal cord development and injury. Neurochem Res 2002, 27(10):1133-1140. 10.1023/A:1020969208033, 12462411.
92. Spearman C. The proof and measurement of association between two things. American Journal of Psychology 1904, 15:72-101.
93. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4(2):249-264. 10.1093/biostatistics/4.2.249, 12925520.
94. Redman JC, Haas BJ, Tanimoto G, Town CD. Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. Plant J 2004, 38(3):545-561. 10.1111/j.1365-313X.2004.02061.x, 15086809.
95. Persson S, Wei H, Milne J, Page GP, Somerville CR. Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 2005, 102(24):8633-8638. 10.1073/pnas.0503392102, 1142401, 15932943.
96. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122(6):947-956. 10.1016/j.cell.2005.08.020, 3006442, 16153702.
97. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, Vassena R, Bilic J, Pekarik V, Tiscornia G, et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008, 26(11):1276-1284. 10.1038/nbt.1503, 18931654.
98. Monk M, Hitchins M, Hawes S. Differential expression of the embryo/cancer gene ECSA(DPPA2), the cancer/testis gene BORIS and the pluripotency structural gene OCT4, in human preimplantation development. Mol Hum Reprod 2008, 14(6):347-355. 10.1093/molehr/gan025, 18467432.
99. Isono K, Fujimura Y, Shinga J, Yamaki M, J OW, Takihara Y, Murahashi Y, Takada Y, Mizutani-Koseki Y, Koseki H. Mammalian polyhomeotic homologues Phc2 and Phc1 act in synergy to mediate polycomb repression of Hox genes. Mol Cell Biol 2005, 25(15):6694-6706. 10.1128/MCB.25.15.6694-6706.2005, 1190356, 16024804.
100. Zwaka TP. Breathing chromatin in pluripotent stem cells. Dev Cell 2006, 10(1):1-2. 10.1016/j.devcel.2005.12.007, 16399069.
101. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N, Gotoh Y. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004, 131(12):2791-2801. 10.1242/dev.01165, 15142975.
102. Murata Y, Doi T, Taniguchi H, Fujiyoshi Y. Proteomic analysis revealed a novel synaptic proline-rich membrane protein (PRR7) associated with PSD-95 and NMDA receptor. Biochem Biophys Res Commun 2005, 327(1):183-191. 10.1016/j.bbrc.2004.11.154, 15629447.
103. Elms P, Siggers P, Napper D, Greenfield A, Arkell R. Zic2 is required for neural crest formation and hindbrain patterning during mouse development. Dev Biol 2003, 264(2):391-406. 10.1016/j.ydbio.2003.09.005, 14651926.
104. Shuai B, Reynaga-Pena CG, Springer PS. The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol 2002, 129(2):747-761. 10.1104/pp.010926, 161698, 12068116.
105. Gan Y, Yu H, Peng J, Broun P. Genetic and molecular regulation by DELLA proteins of trichome development in Arabidopsis. Plant Physiol 2007, 145(3):1031-1042. 10.1104/pp.107.104794, 2048772, 17704233.
106. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, et al. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 2007, 19(8):2531-2543. 10.1105/tpc.107.052274, 2002633, 17766401.
107. Kares C, Prinsen E, Van Onckelen H, Otten L. IAA synthesis and root induction with iaa genes under heat shock promoter control. Plant Mol Biol 1990, 15(2):225-236. 10.1007/BF00036909, 2129423.
108. Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 2009, 21(6):1659-1668. 10.1105/tpc.109.066480, 2714926, 19491238.
109. Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 2008, 20(10):2763-2782. 10.1105/tpc.108.061325, 2590737, 18952777.
110. Ohashi-Ito K, Bergmann DC. Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. Development 2007, 134(16):2959-2968. 10.1242/dev.006296, 17626058.
111. Li Y, Zheng L, Corke F, Smith C, Bevan MW. Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 2008, 22(10):1331-1336. 10.1101/gad.463608, 2377187, 18483219.
112. Bureau M, Rast MI, Illmer J, Simon R. JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root. Plant Mol Biol 2010, 74(4-5):479-491. 10.1007/s11103-010-9688-2, 20852917.
113. Ohashi K. [HANABA TARANU, a GATA transcription factor which affects shoot apical meristem development]. Seikagaku 2006, 78(9):888-891.
114. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 2010, 61(4):672-685. 10.1111/j.1365-313X.2009.04092.x, 19947981.
115. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 2004, 134(4):1683-1696. 10.1104/pp.103.033431, 419842, 15047901.
116. Binder BM, Walker JM, Gagne JM, Emborg TJ, Hemmann G, Bleecker AB, Vierstra RD. The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 2007, 19(2):509-523. 10.1105/tpc.106.048140, 1867343, 17307926.
117. Thomas PQ, Johnson BV, Rathjen J, Rathjen PD. Sequence, genomic organization, and expression of the novel homeobox gene Hesx1. J Biol Chem 1995, 270(8):3869-3875. 10.1074/jbc.270.8.3869, 7876132.
118. Ezashi T, Ghosh D, Roberts RM. Repression of Ets-2-induced transactivation of the tau interferon promoter by Oct-4. Mol Cell Biol 2001, 21(23):7883-7891. 10.1128/MCB.21.23.7883-7891.2001, 99954, 11689681.