Serum-dependent transcriptional networks identify distinct functional roles for H-Ras and N-Ras during initial stages of the cell cycle

Genome Biology

Volumn 10, Issue 11, 2009, Pages

  Castellano, Esther ^a,b   Guerrero, Carmen ^a   Núñez, Alejandro ^a   De Las Rivas, Javier ^a   Santos, Eugenio ^a  

^a CSIC   (Spain)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; H RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN N RAS; STAT1 PROTEIN; UNCLASSIFIED DRUG; RAS PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL GROWTH; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; DNA MICROARRAY; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; FIBROBLAST CULTURE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; IMMUNITY; IMMUNOMODULATION; KNOCKOUT GENE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; CELL CYCLE; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; ONCOGENE RAS; TRANSCRIPTION INITIATION;

ANIMALS; CELL CYCLE; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, RAS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MODELS, GENETIC; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 76249117627     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-11-r123     Document Type: Article

References (85)

1. Abankwa D, Gorfe AA, Hancock JF. Mechanisms of Ras membrane organization and signalling: Ras on a rocker. Cell Cycle 2008, 7:2667-2673. 2782589, 18758236.
2. Colicelli J. Human RAS superfamily proteins and related GTPases. Sci STKE 2004, 2004:RE13. 10.1126/stke.2502004re13, 15367757.
3. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 2008, 9:517-531. 10.1038/nrm2438, 18568040.
4. Rojas JM, Santos E. ras genes and human cancer: different implications and different roles. Curr Genom 2002, 3:295-311. 10.2174/1389202023350381.
5. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 2007, 7:295-308. 10.1038/nrc2109, 17384584.
6. Omerovic J, Hammond DE, Clague MJ, Prior IA. Ras isoform abundance and signalling in human cancer cell lines. Oncogene 2008, 27:2754-2762. 10.1038/sj.onc.1210925, 2557550, 17998936.
7. Maher J, Baker DA, Manning M, Dibb NJ, Roberts IA. Evidence for cell-specific differences in transformation by N-, H- and K-ras. Oncogene 1995, 11:1639-1647.
8. Oliva JL, Zarich N, Martinez N, Jorge R, Castrillo A, Azanedo M, Garcia-Vargas S, Gutierrez-Eisman S, Juarranz A, Bosca L, Gutkind JS, Rojas JM. The P34G mutation reduces the transforming activity of K-Ras and N-Ras in NIH 3T3 cells but not of H-Ras. J Biol Chem 2004, 279:33480-33491. 10.1074/jbc.M404058200, 15181015.
9. Bollag G, McCormick F. Differential regulation of rasGAP and neurofibromatosis gene product activities. Nature 1991, 351:576-579. 10.1038/351576a0, 1904555.
10. Clyde-Smith J, Silins G, Gartside M, Grimmond S, Etheridge M, Apolloni A, Hayward N, Hancock JF. Characterization of RasGRP2, a plasma membrane-targeted, dual specificity Ras/Rap exchange factor. J Biol Chem 2000, 275:32260-32267. 10.1074/jbc.M006087200, 10918068.
11. Jones MK, Jackson JH. Ras-GRF activates Ha-Ras, but not N-Ras or K-Ras 4B, protein in vivo . J Biol Chem 1998, 273:1782-1787. 10.1074/jbc.273.3.1782, 9430727.
12. Hancock JF. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 2003, 4:373-384. 10.1038/nrm1105, 12728271.
13. Plowman SJ, Hancock JF. Ras signaling from plasma membrane and endomembrane microdomains. Biochim Biophys Acta 2005, 1746:274-283. 10.1016/j.bbamcr.2005.06.004, 16039730.
14. Plowman SJ, Muncke C, Parton RG, Hancock JF. H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc Natl Acad Sci USA 2005, 102:15500-15505. 10.1073/pnas.0504114102, 1266090, 16223883.
15. Walsh AB, Bar-Sagi D. Differential activation of the Rac pathway by Ha-Ras and K-Ras. J Biol Chem 2001, 276:15609-15615. 10.1074/jbc.M010573200, 11278702.
16. Ehrhardt A, David MD, Ehrhardt GR, Schrader JW. Distinct mechanisms determine the patterns of differential activation of H-Ras, N-Ras, K-Ras 4B, and M-Ras by receptors for growth factors or antigen. Mol Cell Biol 2004, 24:6311-6323. 10.1128/MCB.24.14.6311-6323.2004, 434254, 15226433.
17. Hamilton M, Wolfman A. Oncogenic Ha-Ras-dependent mitogen-activated protein kinase activity requires signaling through the epidermal growth factor receptor. J Biol Chem 1998, 273:28155-28162. 10.1074/jbc.273.43.28155, 9774435.
18. Matallanas D, Sanz-Moreno V, Arozarena I, Calvo F, Agudo-Ibanez L, Santos E, Berciano MT, Crespo P. Distinct utilization of effectors and biological outcomes resulting from site-specific Ras activation: Ras functions in lipid rafts and Golgi complex are dispensable for proliferation and transformation. Mol Cell Biol 2006, 26:100-116. 10.1128/MCB.26.1.100-116.2006, 1317613, 16354683.
19. Prior IA, Muncke C, Parton RG, Hancock JF. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 2003, 160:165-170. 10.1083/jcb.200209091, 2172642, 12527752.
20. Rocks O, Peyker A, Bastiaens PI. Spatio-temporal segregation of Ras signals: one ship, three anchors, many harbors. Curr Opin Cell Biol 2006, 18:351-357. 10.1016/j.ceb.2006.06.007, 16781855.
21. Voice JK, Klemke RL, Le A, Jackson JH. Four human ras homologs differ in their abilities to activate Raf-1, induce transformation, and stimulate cell motility. J Biol Chem 1999, 274:17164-17170. 10.1074/jbc.274.24.17164, 10358073.
22. Johnson L, Greenbaum D, Cichowski K, Mercer K, Murphy E, Schmitt E, Bronson RT, Umanoff H, Edelmann W, Kucherlapati R, Jacks T. K-ras is an essential gene in the mouse with partial functional overlap with N-ras. Genes Dev 1997, 11:2468-2481. 10.1101/gad.11.19.2468, 316567, 9334313.
23. Koera K, Nakamura K, Nakao K, Miyoshi J, Toyoshima K, Hatta T, Otani H, Aiba A, Katsuki M. K-ras is essential for the development of the mouse embryo. Oncogene 1997, 15:1151-1159. 10.1038/sj.onc.1201284, 9294608.
24. Esteban LM, Vicario-Abejon C, Fernandez-Salguero P, Fernandez-Medarde A, Swaminathan N, Yienger K, Lopez E, Malumbres M, McKay R, Ward JM, Pellicer A, Santos E. Targeted genomic disruption of H-ras and N-ras, individually or in combination, reveals the dispensability of both loci for mouse growth and development. Mol Cell Biol 2001, 21:1444-1452. 10.1128/MCB.21.5.1444-1452.2001, 86690, 11238881.
25. Plowman SJ, Williamson DJ, O'Sullivan MJ, Doig J, Ritchie AM, Harrison DJ, Melton DW, Arends MJ, Hooper ML, Patek CE. While K-ras is essential for mouse development, expression of the K-ras 4A splice variant is dispensable. Mol Cell Biol 2003, 23:9245-9250. 10.1128/MCB.23.24.9245-9250.2003, 309700, 14645534.
26. Umanoff H, Edelmann W, Pellicer A, Kucherlapati R. The murine N-ras gene is not essential for growth and development. Proc Natl Acad Sci USA 1995, 92:1709-1713. 10.1073/pnas.92.5.1709, 42589, 7878045.
27. Potenza N, Vecchione C, Notte A, De Rienzo A, Rosica A, Bauer L, Affuso A, De Felice M, Russo T, Poulet R, Cifelli G, De Vita G, Lembo G, Di Lauro R. Replacement of K-Ras with H-Ras supports normal embryonic development despite inducing cardiovascular pathology in adult mice. EMBO Rep 2005, 6:432-437. 10.1038/sj.embor.7400397, 1299307, 15864294.
28. Brem R, Certa U, Neeb M, Nair AP, Moroni C. Global analysis of differential gene expression after transformation with the v-H-ras oncogene in a murine tumor model. Oncogene 2001, 20:2854-2858. 10.1038/sj.onc.1204403, 11420697.
29. Croonquist PA, Linden MA, Zhao F, Van Ness BG. Gene profiling of a myeloma cell line reveals similarities and unique signatures among IL-6 response, N-ras-activating mutations, and coculture with bone marrow stromal cells. Blood 2003, 102:2581-2592. 10.1182/blood-2003-04-1227, 12791645.
30. Kim S, Lee YZ, Kim YS, Bahk YY. A proteomic approach for protein-profiling the oncogenic ras induced transformation (H-, K-, and N-Ras) in NIH/3T3 mouse embryonic fibroblasts. Proteomics 2008, 8:3082-3093. 10.1002/pmic.200800106, 18601226.
31. Ohnami S, Aoki K, Yoshida K, Hatanaka K, Suzuki K, Sasaki H, Yoshida T. Expression profiles of pancreatic cancer cell lines infected with antisense K-ras-expressing adenoviral vector. Biochem Biophys Res Commun 2003, 309:798-803. 10.1016/j.bbrc.2003.08.073, 13679043.
32. Sweet-Cordero A, Mukherjee S, Subramanian A, You H, Roix JJ, Ladd-Acosta C, Mesirov J, Golub TR, Jacks T. An oncogenic KRAS2 expression signature identified by cross-species gene-expression analysis. Nat Genet 2005, 37:48-55.
33. Vasseur S, Malicet C, Calvo EL, Labrie C, Berthezene P, Dagorn JC, Iovanna JL. Gene expression profiling by DNA microarray analysis in mouse embryonic fibroblasts transformed by rasV12 mutated protein and the E1A oncogene. Mol Cancer 2003, 2:19. 10.1186/1476-4598-2-19, 153489, 12685932.
34. Zuber J, Tchernitsa OI, Hinzmann B, Schmitz AC, Grips M, Hellriegel M, Sers C, Rosenthal A, Schafer R. A genome-wide survey of RAS transformation targets. Nat Genet 2000, 24:144-152. 10.1038/72799, 10655059.
35. Castellano E, De Las Rivas J, Guerrero C, Santos E. Transcriptional networks of knockout cell lines identify functional specificities of H-Ras and N-Ras: significant involvement of N-Ras in biotic and defense responses. Oncogene 2007, 26:917-933. 10.1038/sj.onc.1209845, 16909116.
36. Pruitt K, Der CJ. Ras and Rho regulation of the cell cycle and oncogenesis. Cancer Lett 2001, 171:1-10. 10.1016/S0304-3835(01)00528-6, 11485822.
37. Gille H, Downward J. Multiple ras effector pathways contribute to G(1) cell cycle progression. J Biol Chem 1999, 274:22033-22040. 10.1074/jbc.274.31.22033, 10419529.
38. Marshall C. How do small GTPase signal transduction pathways regulate cell cycle entry?. Curr Opin Cell Biol 1999, 11:732-736. 10.1016/S0955-0674(99)00044-7, 10600705.
39. Stacey D, Kazlauskas A. Regulation of Ras signaling by the cell cycle. Curr Opin Genet Dev 2002, 12:44-46. 10.1016/S0959-437X(01)00262-3, 11790553.
40. Takuwa N, Takuwa Y. Regulation of cell cycle molecules by the Ras effector system. Mol Cell Endocrinol 2001, 177:25-33. 10.1016/S0303-7207(01)00439-7, 11377817.
41. Taylor SJ, Shalloway D. Cell cycle-dependent activation of Ras. Curr Biol 1996, 6:1621-1627. 10.1016/S0960-9822(02)70785-9, 8994826.
42. Bar-Sagi D, Feramisco JR. Microinjection of the ras oncogene protein into PC12 cells induces morphological differentiation. Cell 1985, 42:841-848. 10.1016/0092-8674(85)90280-6, 2996779.
43. Greenberg ME, Hermanowski AL, Ziff EB. Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol 1986, 6:1050-1057. 367614, 2431274.
44. Jones SM, Kazlauskas A. Growth-factor-dependent mitogenesis requires two distinct phases of signalling. Nat Cell Biol 2001, 3:165-172. 10.1038/35055073, 11175749.
45. Pardee AB. G1 events and regulation of cell proliferation. Science 1989, 246:603-608. 10.1126/science.2683075, 2683075.
46. Riabowol KT, Vosatka RJ, Ziff EB, Lamb NJ, Feramisco JR. Microinjection of fos-specific antibodies blocks DNA synthesis in fibroblast cells. Mol Cell Biol 1988, 8:1670-1676. 363327, 2454395.
47. Siegfried Z, Ziff EB. Transcription activation by serum, PDGF, and TPA through the c-fos DSE: cell type specific requirements for induction. Oncogene 1989, 4:3-11.
48. Sun A, Bagella L, Tutton S, Romano G, Giordano A. From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J Cell Biochem 2007, 102:1400-1404. 10.1002/jcb.21609, 17979151.
49. 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, 4:249-264. 10.1093/biostatistics/4.2.249, 12925520.
50. 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. 10.1073/pnas.091062498, 33173, 11309499.
51. Collins CA, Watt FM. Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for beta-catenin and Notch signalling. Dev Biol 2008, 324:55-67. 10.1016/j.ydbio.2008.08.034, 18805411.
52. Lane MA, Xu J, Wilen EW, Sylvester R, Derguini F, Gudas LJ. LIF removal increases CRABPI and CRABPII transcripts in embryonic stem cells cultured in retinol or 4-oxoretinol. Mol Cell Endocrinol 2008, 280:63-74. 10.1016/j.mce.2007.09.010, 2225994, 18006143.
53. Fambrough D, McClure K, Kazlauskas A, Lander ES. Diverse signaling pathways activated by growth factor receptors induce broadly overlapping, rather than independent, sets of genes. Cell 1999, 97:727-741. 10.1016/S0092-8674(00)80785-0, 10380925.
54. Herschman HR. Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem 1991, 60:281-319. 10.1146/annurev.bi.60.070191.001433, 1883198.
55. Rollins BJ, Stiles CD. Serum-inducible genes. Adv Cancer Res 1989, 53:1-32. full_text, 2678945.
56. Hopewell R, Li L, MacGregor D, Nerlov C, Ziff EB. Regulation of cell proliferation and differentiation by Myc. J Cell Sci Suppl 1995, 19:85-89.
57. Leonard DG, Ziff EB, Greene LA. Identification and characterization of mRNAs regulated by nerve growth factor in PC12 cells. Mol Cell Biol 1987, 7:3156-3167. 367950, 3670309.
58. Siegfried Z, Ziff EB. Altered transcriptional activity of c-fos promoter plasmids in v-raf-transformed NIH 3T3 cells. Mol Cell Biol 1990, 10:6073-6078. 361409, 2122238.
59. Blais A, Dynlacht BD. Hitting their targets: an emerging picture of E2F and cell cycle control. Curr Opin Genet Dev 2004, 14:527-532. 10.1016/j.gde.2004.07.003, 15380244.
60. Ma Y, Croxton R, Moorer RL, Cress WD. Identification of novel E2F1-regulated genes by microarray. Arch Biochem Biophys 2002, 399:212-224. 10.1006/abbi.2002.2761, 11888208.
61. Polager S, Kalma Y, Berkovich E, Ginsberg D. E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis. Oncogene 2002, 21:437-446. 10.1038/sj.onc.1205102, 11821956.
62. Wells J, Graveel CR, Bartley SM, Madore SJ, Farnham PJ. The identification of E2F1-specific target genes. Proc Natl Acad Sci USA 2002, 99:3890-3895. 10.1073/pnas.062047499, 122619, 11904439.
63. Dobrowolski S, Harter M, Stacey DW. Cellular ras activity is required for passage through multiple points of the G0/G1 phase in BALB/c 3T3 cells. Mol Cell Biol 1994, 14:5441-5449. 359063, 8035821.
64. Feig LA, Cooper GM. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol 1988, 8:3235-3243. 363555, 3145408.
65. Mulcahy LS, Smith MR, Stacey DW. Requirement for ras proto-oncogene function during serum-stimulated growth of NIH 3T3 cells. Nature 1985, 313:241-243. 10.1038/313241a0, 3918269.
66. Carmona-Saez P, Chagoyen M, Tirado F, Carazo JM, Pascual-Montano A. GENECODIS: a web-based tool for finding significant concurrent annotations in gene lists. Genome Biol 2007, 8:R3. 10.1186/gb-2007-8-1-r3, 1839127, 17204154.
67. Boggs DF, Miller JH. Absence of an hypoxic depression of metabolism in preproenkephalin knockout mice. Respir Physiol Neurobiol 2006, 152:92-99. 10.1016/j.resp.2005.06.004, 16095981.
68. Nitsche JF, Schuller AG, King MA, Zengh M, Pasternak GW, Pintar JE. Genetic dissociation of opiate tolerance and physical dependence in delta-opioid receptor-1 and preproenkephalin knock-out mice. J Neurosci 2002, 22:10906-10913.
69. Dimberg A, Karlberg I, Nilsson K, Oberg F. Ser727/Tyr701-phosphorylated Stat1 is required for the regulation of c-Myc, cyclins, and p27Kip1 associated with ATRA-induced G0/G1 arrest of U-937 cells. Blood 2003, 102:254-261. 10.1182/blood-2002-10-3149, 12637327.
70. Pilz A, Ramsauer K, Heidari H, Leitges M, Kovarik P, Decker T. Phosphorylation of the Stat1 transactivating domain is required for the response to type I interferons. EMBO Rep 2003, 4:368-373. 10.1038/sj.embor.embor802, 1319158, 12671680.
71. Shuai K, Schindler C, Prezioso VR, Darnell JE. Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science 1992, 258:1808-1812. 10.1126/science.1281555, 1281555.
72. Hengartner MO. The biochemistry of apoptosis. Nature 2000, 407:770-776. 10.1038/35037710, 11048727.
73. Wajant H. Death receptors. Essays Biochem 2003, 39:53-71.
74. Parone PA, James D, Martinou JC. Mitochondria: regulating the inevitable. Biochimie 2002, 84:105-111. 10.1016/S0300-9084(02)01380-9, 12022941.
75. Critchley-Thorne RJ, Simons DL, Yan N, Miyahira AK, Dirbas FM, Johnson DL, Swetter SM, Carlson RW, Fisher GA, Koong A, Holmes S, Lee PP. Impaired interferon signaling is a common immune defect in human cancer. Proc Natl Acad Sci USA 2009, 106:9010-9015. 10.1073/pnas.0901329106, 19451644.
76. Wang S, Koromilas AE. Stat1 is an inhibitor of Ras-MAPK signaling and Rho small GTPase expression with implications in the transcriptional signature of Ras transformed cells. Cell Cycle 2009, 8:2070-2079.
77. Gough DJ, Corlett A, Schlessinger K, Wegrzyn J, Larner AC, Levy DE. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009, 324:1713-1716. 10.1126/science.1171721, 19556508.
78. Affymetrix. , http://affymetrix.com/index.affx
79. NCBI Gene Expresión Omnibus (GEO) Accesion Display. , http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE14829
80. Murtagh F. Multidimensional clustering algorithms. COMPSTAT Lectures 4 1985, 131. Wuerzburg: Physica-Verlag.
81. Genecodis 2.0, UCM access, Madrid. , http://genecodis.dacya.ucm.es/
82. The Gene Ontology Database. , http://www.geneontology.org/
83. KEGG Pathway Database. , http://www.genome.ad.jp/kegg/pathway.html
84. Herrmann PC, Gillespie JW, Charboneau L, Bichsel VE, Paweletz CP, Calvert VS, Kohn EC, Emmert-Buck MR, Liotta LA, Petricoin EF. Mitochondrial proteome: altered cytochrome c oxidase subunit levels in prostate cancer. Proteomics 2003, 3:1801-1810. 10.1002/pmic.200300461, 12973739.
85. Wulfkuhle JD, Aquino JA, Calvert VS, Fishman DA, Coukos G, Liotta LA, Petricoin EF. Signal pathway profiling of ovarian cancer from human tissue specimens using reverse-phase protein microarrays. Proteomics 2003, 3:2085-2090. 10.1002/pmic.200300591, 14595806.