Adenovirus type 5 exerts genome-wide control over cellular programs governing proliferation, quiescence, and survival

Genome Biology

Volumn 8, Issue 4, 2007, Pages

  Miller, Daniel L ^a,b   Myers, Chad L ^a,c   Rickards, Brenden ^a   Coller, Hilary A ^a   Flint, S Jane ^a  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c Princeton University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; E1A PROTEIN; E1B PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR E2F; VIRUS PROTEIN; RNA;

ADENOVIRUS 5; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL HYBRIDIZATION; CELL PROLIFERATION; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION PROFILING; GENE FUNCTION; HOST CELL; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; NONHUMAN; RNA SYNTHESIS; RNA TRANSLATION; VIRAL GENETICS; VIRUS INFECTION; ADENOVIRUS; CELL CULTURE; CELL CYCLE; CLASSIFICATION; CLUSTER ANALYSIS; CYTOLOGY; DNA MICROARRAY; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; GENOME; HELA CELL; KINETICS; METABOLISM; NUCLEIC ACID HYBRIDIZATION; PATHOGENICITY; PHYSIOLOGY; VIROLOGY;

ADENOVIRIDAE; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS TYPE 5;

ADENOVIRIDAE; APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CLUSTER ANALYSIS; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME; HELA CELLS; HUMANS; KINETICS; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA; VIRAL PROTEINS;

EID: 35748973572     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2007-8-4-r58     Document Type: Article

References (107)

1. Trentin JJ Yabe Y Taylor G The quest for human cancer viruses. Science 1962, 137:835-841. 10.1126/science.137.3533.835 13922417
2. Shenk T Adenoviridae and their replication Virology New York, NY: Raven Press Fields B, Howley P, Knipe D 4 2001, 2265-2300.
3. Berk AJ Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 2005, 24:7673-7685. 10.1038/ sj.onc.1209040 16299528
4. Moran E DNA tumor virus transforming proteins and the cell cycle. Curr Opin Genet Dev 1993, 3:63-70. 10.1016/S0959-437X(05)80342-9 8453277
5. Nevins JR E2F: A link between the Rb tumor suppressor protein and viral oncoproteins. Science 1992, 258:424-429. 10.1126/science.1411535 1411535
6. Frisch SM Mymryk JS Adenovirus-5 E1A: Paradox and paradigm. Nat Rev Mol Cell Biol 2002, 3:441-452. 10.1038/nrm827 12042766
7. Levine AJ The p53 protein and its interactions with the oncogene products of the small DNA tumor viruses. Virology 1990, 177:419-426. 10.1016/0042-6822(90)90505-L 2142553
8. Berget SM Moore C Sharp PA Spliced segments at the 5′ terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci USA 1977, 74:3171-3175. 431482 269380 10.1073/pnas.74.8.3171
9. Chow LT Gelinas RE Broker TR Roberts RJ An amazing sequence arrangement at the 5′ ends of adenovirus 2 messenger RNA. Cell 1977, 12:1-8. 10.1016/0092-8674(77)90180-5 902310
10. Moran E Mathews MB Multiple functional domains in the adenovirus E1A gene. Cell 1987, 48:177-178. 10.1016/0092-8674(87)90418-1 2948653
11. Schaeper U Subramanian T Lim L Boyd JM Chinnadurai G Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J Biol Chem 1998, 273:8549-8552. 10.1074/ jbc.273.15.8549 9535825
12. Avvakumov N Kajon AE Hoeben RC Mymryk JS Comprehensive sequence analysis of the E1A proteins of human and simian adenoviruses. Virology 2004, 329:477-492. 15518825
13. Flint J Shenk T Viral transactivating proteins. Annu Rev Genet 1997, 31:177-212. 10.1146/annurev.genet.31.1.177 9442894
14. Nevins JR Mechanism of activation of early viral transcription by the adenovirus E1A gene product. Cell 1981, 26:213-220. 10.1016/ 0092-8674(81)90304-4 7332929
15. Jones N Shenk T An adenovirus type 5 early gene function regulates expression of other early viral genes. Proc Natl Acad Sci USA 1979, 76:3665-3669. 383893 291030 10.1073/pnas.76.8.3665
16. Ricciardi RP Jones RL Cepko CL Sharp PA Roberts BE Expression of early adenovirus genes requires a viral encoded acidic polypeptide. Proc Natl Acad Sci USA 1981, 78:6121-6125. 348989 6947217 10.1073/pnas.78.10.6121
17. Berk AJ Adenovirus promoters and E1A transactivation. Ann Rev Genet 1986, 20:45-79. 10.1146/annurev.ge.20.120186.000401 3028247
18. Boyer TG Martin ME Lees E Ricciardi RP Berk AJ Mammalian Srb/Mediator complex is targeted by adenovirus E1A protein. Nature 1999, 399:276-279. 10.1038/20466 10353252
19. Wang G Cantin GT Stevens JL Berk AJ Characterization of mediator complexes from HeLa cell nuclear extract. Mol Cell Biol 2001, 21:4604-4613. 87123 11416138 10.1128/MCB.21.14.4604-4613.2001
20. Stevens JL Cantin GT Wang G Shevchenko A Shevchenko A Berk AJ Transcription control by E1A and MAP kinase pathway via Sur2 mediator subunit. Science 2002, 296:755-758. 10.1126/science.1068943 11934987
21. Cantin GT Stevens JL Berk AJ Activation domain-mediator interactions promote transcription preinitiation complex assembly on promoter DNA. Proc Natl Acad Sci USA 2003, 100:12003-12008. 218703 14506297 10.1073/ pnas.2035253100
22. Malik S Roeder RG Dynamic regulation of pol II transcription by the mammalian Mediator complex. Trends Biochem Sci 2005, 30:256-263. 10.1016/ j.tibs.2005.03.009 15896744
23. Conaway RC Sato S Tomomori-Sato C Yao T Conaway JW The mammalian Mediator complex and its role in transcriptional regulation. Trends Biochem Sci 2005, 30:250-255. 10.1016/j.tibs.2005.03.002 15896743
24. Kovesdi I Reichel R Nevins JR Identification of a cellular transcription factor involved in E1A trans-activation. Cell 1986, 45:219-228. 10.1016/ 0092-8674(86)90386-7 2938741
25. Dyson N The regulation of E2F by pRB-family proteins. Genes Dev 1998, 12:2245-2262. 9694791
26. Howe JA Mymryk JS Egan C Branton PE Bayley ST Retinoblastoma growth suppressor and a 300-kDa protein appear to regulate cellular DNA synthesis. Proc Natl Acad Sci USA 1990, 87:5883-5887. 54433 2143024 10.1073/pnas.87.15.5883
27. Stein RW Corrigan M Yaciuk P Whelan J Moran E Analysis of E1A-mediated growth regulation functions: Binding of the 300-kilodalton cellular product correlates with E1A enhancer repression function and DNA synthesis-inducing activity. J Virol 1990, 64:4421-4427. 247911 2143544
28. Wang HG Rikitake Y Carter MC Yaciuk P Abraham SE Zerler B Moran E Identification of specific adenovirus E1A N-terminal residues critical to the binding of cellular proteins and to the control of cell growth. J Virol 1993, 67:476-488. 237385 8416379
29. Braithwaite AW Cheetham BF Li P Parish CR Waldron-Stevens LK Bellett A Adenovirus-induced alterations of the cell growth cycle: A requirement for expression of E1A but not of E1B. J Virol 1983, 45:192-199. 256401 6823012
30. Spindler KR Eng CY Berk AJ An adenovirus early region 1A protein is required for maximal viral DNA replication in growth-arrested human cells. J Virol 1985, 53:742-750. 254702 3973965
31. Zerler B Roberts RJ Mathews MB Moran E Different functional domains of the adenovirus E1A genes are involved in the regulation of host cell cycle products. Mol Cell Biol 1987, 7:821-829. 365140 2881197
32. Wold WS Doronin K Toth K Kuppuswamy M Lichtenstein DL Tollefson AE Immune responses to adenoviruses: Viral evasion mechanisms and their implications for the clinic. Curr Opin Immunol 1999, 11:380-386. 10.1016/ S0952-7915(99)80064-8 10448144
33. Horwitz MS Adenovirus immunoregulatory genes and their cellular targets. Virology 2001, 279:1-8. 10.1006/viro.2000.0738 11145883
34. Cuconati A White E Viral homologs of BCL-2: Role of apoptosis in the regulation of virus infection. Genes Dev 2002, 16:2465-2478. 10.1101/ gad.1012702 12368257
35. Teodoro JG Branton PE Regulation of p53-dependent apoptosis, transcriptional repression, and cell transformation by phosphorylation of the 55-kilodalton E1B protein of human adenovirus type 5. J Virol 1997, 71:3620-3627. 191510 9094635
36. Yew PR Berk AJ Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 1992, 357:82-85. 10.1038/357082a0 1533443
37. Roth J Dobbelstein M Freedman DA Shenk T Levine AJ Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J 1998, 17:554-564. 1170405 9430646 10.1093/emboj/17.2.554
38. Steegenga WT Riteco N Jochemsen AG Fallaux FJ Bos JL The large E1B protein together with the E4orf6 protein target p53 for active degradation in adenovirus infected cells. Oncogene 1998, 16:349-357. 10.1038/sj.onc.1201540 9467960
39. Querido E Marcellus RC Lai A Charbonneau R Teodoro JG Ketner G Branton PE Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J Virol 1997, 71:3788-3798. 191529 9094654
40. Iftode C Flint SJ Viral synthesis-dependent titration of a cellular repressor activates transcription of the human adenovirus type 2 IVa2 gene. Proc Natl Acad Sci USA 2004, 101:17831-17836. 539761 15591107 10.1073/pnas.0407786101
41. Lin HJ Flint SJ Identification of a cellular repressor of transcription of the adenoviral late IVa2 gene that is unaltered in activity in infected cells. Virology 2000, 277:397-410. 10.1006/viro.2000.0598 11080487
42. Tribouley C Lutz P Staub A Kedinger C The product of the adenovirus intermediate gene IVa2 is a transcription activator of the major late promoter. J Virol 1994, 68:4450-4457. 236370 8207818
43. Pardo-Mateos A Young CS Adenovirus IVa2 protein plays an important role in transcription from the major late promoter in vivo. Virology 2004, 327:50-59. 10.1016/j.virol.2004.06.011 15327897
44. Benihoud K Yeh P Perricaudet M Adenovirus vectors for gene delivery. Curr Opin Biotechnol 1999, 10:440-447. 10.1016/S0958-1669(99)00007-5 10508634
45. Basak SK Kiertscher SM Harui A Roth MD Modifying adenoviral vectors for use as gene-based cancer vaccines. Viral Immunol 2004, 17:182-196. 10.1089/0882824041310603 15279698
46. Ghosh SS Gopinath P Ramesh A Adenoviral vectors: A promising tool for gene therapy. Appl Biochem Biotechnol 2006, 133:9-29. 10.1385/ ABAB:133:1:9 16622281
47. Verma IM Weitzman MD Gene therapy: Twenty-first century medicine. Annu Rev Biochem 2005, 74:711-738. 10.1146/annurev.biochem.74.050304.091637 15952901
48. Lichtenstein DL Wold WS Experimental infections of humans with wild-type adenoviruses and with replication-competent adenovirus vectors: replication, safety, and transmission. Cancer Gene Ther 2004, 11:819-829. 10.1038/sj.cgt.7700765 15359291
49. Everts B van der Poel HG Replication-selective oncolytic viruses in the treatment of cancer. Cancer Gene Ther 2005, 12:141-161. 10.1038/ sj.cgt.7700771 15472714
50. Dobbelstein M Replicating adenoviruses in cancer therapy. Curr Top Microbiol Immunol 2004, 273:291-334. 14674605
51. Gonzalez R Huang W Finnen R Bragg C Flint SJ Adenovirus E1B 55-kilodalton protein is required for both regulation of mRNA export and efficient entry into the late phase of infection in normal human fibroblasts. J Virol 2006, 80:964-974. 1346875 16378998 10.1128/ JVI.80.2.964-974.2006
52. Princeton University PUMA database http://puma.princeton.edu
53. Tusher VG Tibshirani R Chu G Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121. 33173 11309499 10.1073/pnas.091062498
54. Zhao LY Colosimo AL Liu Y Wan Y Liao D Adenovirus E1B 55-kilodalton oncoprotein binds to Daxx and eliminates enhancement of p53-dependent transcription by Daxx. J Virol 2003, 77:11809-11821. 229361 14557665 10.1128/JVI.77.21.11809-11821.2003
55. Granberg F Svensson C Pettersson U Zhao H Modulation of host cell gene expression during onset of the late phase of an adenovirus infection is focused on growth inhibition and cell architecture. Virology 2005, 343:236-245. 10.1016/j.virol.2005.08.023 16169035
56. Schwarz E Freese UK Gissmann L Mayer W Roggenbuck B Stremlau A zur Hausen H Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985, 314:111-114. 10.1038/314111a0 2983228
57. Helt AM Galloway DA Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 2003, 24:159-169. 10.1093/carcin/24.2.159 12584163
58. Uhnoo I Svensson L Wadell G Enteric adenoviruses. Baillieres Clin Gastroenterol 1990, 4:627-642. 10.1016/0950-3528(90)90053-J 1962727
59. Vousden KH Regulation of the cell cycle by viral oncoproteins. Semin Cancer Biol 1995, 6:109-116. 10.1006/scbi.1995.0014 7647307
60. Yeung KY Haynor DR Ruzzo WL Validating clustering for gene expression data. Bioinformatics 2001, 17:309-318. 10.1093/bioinformatics/17.4.309 11301299
61. Gene Ontology Consortium http://www.geneontology.org
62. Coller HA Sang L Roberts JM A new description of cellular quiescence. PLoS Biol 2006, 4:e83. 1393757 16509772 10.1371/journal.pbio.0040083
63. Goodbourn S Didcock L Randall RE Interferons: Cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 2000, 81:2341-2364. 10993923
64. Hatada EN Krappmann D Scheidereit C NF-kappaB and the innate immune response. Curr Opin Immunol 2000, 12:52-58. 10.1016/ S0952-7915(99)00050-3 10679399
65. Iyer VR Eisen MB Ross DT Schuler G Moore T Lee JC Trent JM Staudt LM Hudson J Jr Boguski MS The transcriptional program in the response of human fibroblasts to serum. Science 1999, 283:83-87. 10.1126/ science.283.5398.83 9872747
66. Chang HY Chi JT Dudoit S Bondre C van de Rijn M Botstein D Brown PO Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 2002, 99:12877-12882. 130553 12297622 10.1073/pnas.162488599
67. Chang HY Sneddon JB Alizadeh AA Sood R West RB Montgomery K Chi JT van de Rijn M Botstein D Brown PO Gene expression signature of fibroblast serum response predicts human cancer progression: Similarities between tumors and wounds. PLoS Biol 2004, 2:E7. 314300 14737219 10.1371/ journal.pbio.0020007
68. Whitfield ML Sherlock G Saldanha AJ Murray JI Ball CA Alexander KE Matese JC Perou CM Hurt MM Brown PO Botstein D Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell 2002, 13:1977-2000. 117619 12058064 10.1091/ mbc.02-02-0030.
69. Li E Stupack D Klemke R Cheresh DA Nemerow GR Adenovirus endocytosis via alpha(v) integrins requires phosphoinositide-3-OH kinase. J Virol 1998, 72:2055-2061. 109499 9499060
70. Bader AG Kang S Zhao L Vogt PK Oncogenic PI3K deregulates transcription and translation. Nat Rev Cancer 2005, 5:921-929. 10.1038/nrc1753 16341083
71. Martinez-Gac L Alvarez B Garcia Z Marques M Arrizabalaga M Carrera AC Phosphoinositide 3-kinase and Forkhead, a switch for cell division. Biochem Soc Trans 2004, 32:360-361. 10.1042/BST0320360 15046609
72. Burgering BM Kops GJ Cell cycle and death control: Long live Forkheads. Trends Biochem Sci 2002, 27:352-360. 10.1016/S0968-0004(02)02113-8 12114024
73. Brunet A Datta SR Greenberg ME Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 2001, 11:297-305. 10.1016/S0959-4388(00)00211-7 11399427
74. Stevaux O Dyson NJ A revised picture of the E2F transcriptional network and RB function. Curr Opin Cell Biol 2002, 14:684-691. 10.1016/ S0955-0674(02)00388-5 12473340
75. Giangrande PH Zhu W Schlisio S Sun X Mori S Gaubatz S Nevins JR A role for E2F6 in distinguishing G1/S- and G2/M-specific transcription. Genes Dev 2004, 18:2941-2951. 534654 15574595 10.1101/gad.1239304
76. Attwooll C Oddi S Cartwright P Prosperini E Agger K Steensgaard P Wagener C Sardet C Moroni MC Helin K A novel repressive E2F6 complex containing the polycomb group protein, EPC1, that interacts with EZH2 in a proliferation-specific manner. J Biol Chem 2005, 280:1199-1208. 10.1074/jbc.M412509200 15536069
77. Di Stefano L Jensen MR Helin K E2F7, a novel E2F featuring DP-independent repression of a subset of E2F-regulated genes. EMBO J 2003, 22:6289-6298. 291854 14633988 10.1093/emboj/cdg613
78. Guerra S Lopez-Fernandez LA Conde R Pascual-Montano A Harshman K Esteban M Microarray analysis reveals characteristic changes of host cell gene expression in response to attenuated modified vaccinia virus Ankara infection of human HeLa cells. J Virol 2004, 78:5820-5834. 415835 15140980 10.1128/JVI.78.11.5820-5834.2004
79. Wu L Timmers C Maiti B Saavedra HI Sang L Chong GT Nuckolls F Giangrande P Wright FA Field SJ The E2F1-3 transcription factors are essential for cellular proliferation. Nature 2001, 414:457-462. 10.1038/35106593 11719808
80. Hatakeyama M Weinberg RA The role of RB in cell cycle control. Prog Cell Cycle Res 1995, 1:9-19. 9552350
81. Nevins JR Adenovirus E1A: Transcription regulation and alteration of cell growth control. Curr Top Microbiol Immunol 1995, 199:25-32. 7555080
82. Adams PD Kaelin WG Jr Transcriptional control by E2F. Semin Cancer Biol 1995, 6:99-108. 10.1006/scbi.1995.0013 7647312
83. Tao Y Kassatly RF Cress WD Horowitz JM Subunit composition determines E2F DNA-binding site specificity. Mol Cell Biol 1997, 17:6994-7007. 232556 9372931
84. Kel AE Kel-Margoulis OV Farnham PJ Bartley SM Wingender E Zhang MQ Computer-assisted identification of cell cycle-related genes: New targets for E2F transcription factors. J Mol Biol 2001, 309:99-120. 10.1006/jmbi.2001.4650 11491305
85. Bieda M Xu X Singer MA Green R Farnham PJ Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res 2006, 16:595-605. 1457046 16606705 10.1101/gr.4887606
86. Ren B Cam H Takahashi Y Volkert T Terragni J Young RA Dynlacht BD E2F integrates cell cycle progression with DNA repair, replication, and G2/M checkpoints. Genes Dev 2002, 16:245-256. 155321 11799067 10.1101/ gad.949802
87. Boyd JM Subramanian T Schaeper U La Regina M Bayley S Chinnadurai G A region in the C-terminus of adenovirus 2/5 E1a protein is required for association with a cellular phosphoprotein and important for the negative modulation of T24-ras mediated transformation, tumorigenesis and metastasis. EMBO J 1993, 12:469-478. 413230 8440238
88. Chinnadurai G CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol Cell 2002, 9:213-224. 10.1016/ S1097-2765(02)00443-4 11864595
89. Yew PR Liu X Berk AJ Adenovirus E1B oncoprotein tethers a transcriptional repression domain to p53. Genes Dev 1994, 8:190-202. 8299938
90. Martin ME Berk AJ Adenovirus E1B 55K represses p53 activation in vitro. J Virol 1998, 72:3146-3154. 109770 9525640
91. Martin ME Berk AJ Corepressor required for adenovirus E1B 55,000-molecular-weight protein repression of basal transcription. Mol Cell Biol 1999, 19:3403-3414. 84133 10207064
92. Liu Y Colosimo AL Yang XJ Liao D Adenovirus E1B 55-kilodalton oncoprotein inhibits p53 acetylation by PCAF. Mol Cell Biol 2000, 20:5540-5553. 86007 10891493 10.1128/MCB.20.15.5540-5553.2000
93. Prives C Signaling to p53: Breaking the MDM2-p53 circuit. Cell 1998, 95:5-8. 10.1016/S0092-8674(00)81774-2 9778240
94. Kannan K Amariglio N Rechavi G Jakob-Hirsch J Kela I Kaminski N Getz G Domany E Givol D DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene 2001, 20:2225-2234. 10.1038/ sj.onc.1204319 11402317
95. Flint SJ Gallimore PH Sharp PA Comparison of viral RNA sequences in adenovirus 2-transformed and lytically infected cells. J Mol Biol 1975, 96:47-68. 10.1016/0022-2836(75)90181-3 1099215
96. Williams JF Oncogenic transformation of hamster embryo cells in vitro by adenovirus type 5. Nature 1973, 243:162-163. 10.1038/243162a0 4706286
97. Gonzalez RA Flint SJ Effects of mutations in the adenoviral E1B 55 kDa protein coding sequence on viral late mRNA metabolism. J Virol 2002, 76:4507-4519. 155063 11932416 10.1128/JVI.76.9.4507-4519.2002
98. Reich NC Sarnow P Duprey E Levine AJ Monoclonal antibodies which recognise native and denatured forms of the adenovirus DNA-binding protein. Virology 1983, 128:480-484. 10.1016/0042-6822(83)90274-X 6310869
99. Lunt R Vayda ME Young M Flint SJ Isolation and characterization of monoclonal antibodies against the adenovirus core proteins. Virology 1988, 164:275-279. 10.1016/0042-6822(88)90645-9 3363867
100. SOURCE http://smd.stanford.edu/cgi-bin/source/sourceBatchSearch
101. Protein Information Resource http://pir.georgetown.edu/pirwww/search/ batch.shtml
102. Monti S Tamayo P Mesirov J Golub T Consensus clustering: A resampling-based method for visualization of gene expression microarray data. Machine Learning 2003, 52:91-118. 10.1023/A:1023949509487
103. Saeed AI Sharov V White J Li J Liang W Bhagabati N Braisted J Klapa M Currier T Thiagarajan M TM4: A free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378. 12613259
104. Princeton University PUMA database for Ad5 http://genomics-pubs.princeton.edu/Ad5_HFF
105. Java Treeview http://jtreeview.sourceforge.net
106. Boyle EI Weng S Gollub J Jin H Botstein D Cherry JM Sherlock G GO:TErmFinder - open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004, 20:3710-3715. 10.1093/bioinformatics/bth456 15297299
107. Sealfon RS Hibbs MA Huttenhower C Myers CL Troyanskaya OG GOLEM: An interactive graph-based gene-ontology navigation and analysis tool. BMC Bioinformatics 2006, 7:443. 1618863 17032457 10.1186/1471-2105-7-443