Genome-wide analyses of Nkx2-1 binding to transcriptional target genes uncover novel regulatory patterns conserved in lung development and tumors

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Tagne, Jean Bosco ^a   Gupta, Sumeet ^b   Gower, Adam C ^c   Shen, Steven S ^a   Varma, Saaket ^a   Lakshminarayanan, Meenakshi ^a   Cao, Yuxia ^a   Spira, Avrum ^a,c   Volkert, Thomas L ^b   Ramirez, Maria I ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN B1; CYCLIN B2; SCATTER FACTOR RECEPTOR; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR NKX2 1; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; THYROID NUCLEAR FACTOR 1;

ANIMAL CELL; ANIMAL TISSUE; ANLN GENE; ARTICLE; ASNS GENE; BCL2 GENE; CCNB1 GENE; CCNB2 GENE; CDCA71 GENE; CDKN2C GENE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CNBP GENE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DEVELOPMENTAL STAGE; E2F3 GENE; EMBRYO; ERBB3 GENE; ERH GENE; FGFR3 GENE; FKBP1A GENE; FURIN GENE; GENE EXPRESSION; GENE TARGETING; HMOX1 GENE; HRAS1 GENE; HUMAN; IGF2 GENE; LUNG ADENOCARCINOMA; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; MAP3K11 GENE; MFGE8 GENE; MMP14 GENE; MOUSE; MSH2 GENE; NCAPH GENE; NEK6 GENE; NONHUMAN; NOTCH1 GENE; NUCLEOTIDE SEQUENCE; ODC1 GENE; PARD3 GENE; PAWR GENE; PIK3CA GENE; PRDX1 GENE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PTPRF GENE; RACGAP1 GENE; RHOB GENE; SOX4 GENE; SQUAMOUS CELL CARCINOMA; TFF1 GENE; UBE2C GENE; ANIMAL; CELL CYCLE; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENETICS; LUNG; LUNG NON SMALL CELL CANCER; LUNG TUMOR; METABOLISM; PATHOLOGY; POLYMERASE CHAIN REACTION; PRENATAL DEVELOPMENT; REPRODUCIBILITY; SIGNAL TRANSDUCTION;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONSERVED SEQUENCE; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LUNG; LUNG NEOPLASMS; MICE; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84855369392     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029907     Document Type: Article

References (71)

1. Vias M, Massie CE, East P, Scott H, Warren A, et al. (2008) Pro-neural transcription factors as cancer markers. BMC Med Genomics 1: 17.
2. Boggaram V, (2009) Thyroid transcription factor-1 (TTF-1/Nkx2.1/TITF1) gene regulation in the lung. Clin Sci (Lond) 116: 27-35.
3. Kwei KA, Kim YH, Girard L, Kao J, Pacyna-Gengelbach M, et al. (2008) Genomic profiling identifies TITF1 as a lineage-specific oncogene amplified in lung cancer. Oncogene 27: 3635-3640.
4. Stenhouse G, Fyfe N, King G, Chapman A, Kerr KM, (2004) Thyroid transcription factor 1 in pulmonary adenocarcinoma. J Clin Pathol 57: 383-387.
5. Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, et al. (1996) The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10: 60-69.
6. DeFelice M, Silberschmidt D, DiLauro R, Xu Y, Wert SE, et al. (2003) TTF-1 phosphorylation is required for peripheral lung morphogenesis, perinatal survival, and tissue-specific gene expression. J Biol Chem 278: 35574-35583.
7. Wert SE, Dey CR, Blair PA, Kimura S, Whitsett JA, (2002) Increased expression of thyroid transcription factor-1 (TTF-1) in respiratory epithelial cells inhibits alveolarization and causes pulmonary inflammation. Dev Biol 242: 75-87.
8. Galambos C, Levy H, Cannon CL, Vargas SO, Reid LM, et al. (2010) Pulmonary Pathology in Thyroid Transcription Factor-1 Deficiency Syndrome. Am J Respir Crit Care Med.
9. Kendall J, Liu Q, Bakleh A, Krasnitz A, Nguyen KC, et al. (2007) Oncogenic cooperation and coamplification of developmental transcription factor genes in lung cancer. Proc Natl Acad Sci U S A 104: 16663-16668.
10. Perner S, Wagner PL, Soltermann A, LaFargue C, Tischler V, et al. (2009) TTF1 expression in non-small cell lung carcinoma: association with TTF1 gene amplification and improved survival. J Pathol 217: 65-72.
11. Maeda Y, Dave V, Whitsett JA, (2007) Transcriptional control of lung morphogenesis. Physiol Rev 87: 219-244.
12. Kolla V, Gonzales LW, Gonzales J, Wang P, Angampalli S, et al. (2007) Thyroid transcription factor in differentiating type II cells: regulation, isoforms, and target genes. Am J Respir Cell Mol Biol 36: 213-225.
13. Zhou L, Lim L, Costa RH, Whitsett JA, (1996) Thyroid transcription factor-1, hepatocyte nuclear factor-3beta, surfactant protein B, C, and Clara cell secretory protein in developing mouse lung. J Histochem Cytochem 44: 1183-1193.
14. Scholzen T, Gerdes J, (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182: 311-322.
15. Kumar AS, Venkatesh VC, Planer BC, Feinstein SI, Ballard PL, (1997) Phorbol ester down-regulation of lung surfactant protein B gene expression by cytoplasmic trapping of thyroid transcription factor-1 and hepatocyte nuclear factor 3. J Biol Chem 272: 20764-20773.
16. Peca D, Petrini S, Tzialla C, Boldrini R, Morini F, et al. (2011) Altered surfactant homeostasis and recurrent respiratory failure secondary to TTF-1 nuclear targeting defect. Respir Res 12: 115.
17. Silberschmidt D, Rodriguez-Mallon A, Mithboakar P, Cali G, Amendola E, et al. (2011) In vivo role of different domains and of phosphorylation in the transcription factor Nkx2-1. BMC Dev Biol 11: 9.
18. Butt SJ, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G, et al. (2008) The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59: 722-732.
19. Elias LA, Potter GB, Kriegstein AR, (2008) A time and a place for nkx2-1 in interneuron specification and migration. Neuron 59: 679-682.
20. Nobrega-Pereira S, Kessaris N, Du T, Kimura S, Anderson SA, et al. (2008) Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59: 733-745.
21. Li C, Cai J, Pan Q, Minoo P, (2000) Two functionally distinct forms of NKX2.1 protein are expressed in the pulmonary epithelium. Biochem Biophys Res Commun 270: 462-468.
22. Zannini M, Acebron A, De Felice M, Arnone MI, Martin-Perez J, et al. (1996) Mapping and functional role of phosphorylation sites in the thyroid transcription factor-1 (TTF-1). J Biol Chem 271: 2249-2254.
23. Lee TI, Johnstone SE, Young RA, (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748.
24. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, et al. (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804.
25. Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, et al. (2000) Genome-wide location and function of DNA binding proteins. Science 290: 2306-2309.
26. Lu J, Izvolsky KI, Qian J, Cardoso WV, (2005) Identification of FGF10 targets in the embryonic lung epithelium during bud morphogenesis. J Biol Chem 280: 4834-4841.
27. Mariani TJ, Reed JJ, Shapiro SD, (2002) Expression profiling of the developing mouse lung: insights into the establishment of the extracellular matrix. Am J Respir Cell Mol Biol 26: 541-548.
28. Liu D, Yi M, Smith M, Mendelson CR, (2008) TTF-1 response element is critical for temporal and spatial regulation and necessary for hormonal regulation of human surfactant protein-A2 promoter activity. Am J Physiol Lung Cell Mol Physiol 295: L264-271.
29. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA, (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4: R70.
30. Morrisey EE, Hogan BL, (2010) Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 18: 8-23.
31. Arrieta O, Gonzalez-De la Rosa CH, Arechaga-Ocampo E, Villanueva-Rodriguez G, Ceron-Lizarraga TL, et al. (2010) Randomized phase II trial of All-trans-retinoic acid with chemotherapy based on paclitaxel and cisplatin as first-line treatment in patients with advanced non-small-cell lung cancer. J Clin Oncol 28: 3463-3471.
32. Feng Y, Wan H, Liu J, Zhang R, Ma Q, et al. (2010) The angiotensin-converting enzyme 2 in tumor growth and tumor-associated angiogenesis in non-small cell lung cancer. Oncol Rep 23: 941-948.
33. Rigas JR, Dragnev KH, (2005) Emerging role of rexinoids in non-small cell lung cancer: focus on bexarotene. Oncologist 10: 22-33.
34. Kho AT, Zhao Q, Cai Z, Butte AJ, Kim JY, et al. (2004) Conserved mechanisms across development and tumorigenesis revealed by a mouse development perspective of human cancers. Genes Dev 18: 629-640.
35. Liu H, Kho AT, Kohane IS, Sun Y, (2006) Predicting survival within the lung cancer histopathological hierarchy using a multi-scale genomic model of development. PLoS Med 3: e232.
36. Powers S, Mu D, (2008) Genetic similarities between organogenesis and tumorigenesis of the lung. Cell Cycle 7: 200-204.
37. Chong JL, Tsai SY, Sharma N, Opavsky R, Price R, et al. (2009) E2f3a and E2f3b contribute to the control of cell proliferation and mouse development. Mol Cell Biol 29: 414-424.
38. Humbert PO, Verona R, Trimarchi JM, Rogers C, Dandapani S, et al. (2000) E2f3 is critical for normal cellular proliferation. Genes Dev 14: 690-703.
39. Parisi T, Yuan TL, Faust AM, Caron AM, Bronson R, et al. (2007) Selective requirements for E2f3 in the development and tumorigenicity of Rb-deficient chimeric tissues. Mol Cell Biol 27: 2283-2293.
40. Visel A, Thaller C, Eichele G, (2004) GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32: D552-556.
41. Sonnenberg E, Meyer D, Weidner KM, Birchmeier C, (1993) Scatter factor/hepatocyte growth factor and its receptor, the c-met tyrosine kinase, can mediate a signal exchange between mesenchyme and epithelia during mouse development. J Cell Biol 123: 223-235.
42. Kimura S, Ward JM, Minoo P, (1999) Thyroid-specific enhancer-binding protein/thyroid transcription factor 1 is not required for the initial specification of the thyroid and lung primordia. Biochimie 81: 321-327.
43. Yuan B, Li C, Kimura S, Engelhardt RT, Smith BR, et al. (2000) Inhibition of distal lung morphogenesis in Nkx2.1(-/-)embryos. Dev Dyn 217: 180-190.
44. Bardou O, Trinh NT, Brochiero E, (2009) Molecular diversity and function of K+ channels in airway and alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 296: L145-155.
45. Olver RE, Walters DV, S MW, (2004) Developmental regulation of lung liquid transport. Annu Rev Physiol 66: 77-101.
46. Tanaka H, Yanagisawa K, Shinjo K, Taguchi A, Maeno K, et al. (2007) Lineage-specific dependency of lung adenocarcinomas on the lung development regulator TTF-1. Cancer Res 67: 6007-6011.
47. Weir BA, Woo MS, Getz G, Perner S, Ding L, et al. (2007) Characterizing the cancer genome in lung adenocarcinoma. Nature 450: 893-898.
48. Myong NH, (2003) Thyroid transcription factor-1 (TTF-1) expression in human lung carcinomas: its prognostic implication and relationship with wxpressions of p53 and Ki-67 proteins. J Korean Med Sci 18: 494-500.
49. Winslow MM, Dayton TL, Verhaak RG, Kim-Kiselak C, Snyder EL, et al. (2011) Suppression of lung adenocarcinoma progression by Nkx2-1. Nature 473: 101-104.
50. Cooper CS, Nicholson AG, Foster C, Dodson A, Edwards S, et al. (2006) Nuclear overexpression of the E2F3 transcription factor in human lung cancer. Lung Cancer 54: 155-162.
51. Oeggerli M, Tomovska S, Schraml P, Calvano-Forte D, Schafroth S, et al. (2004) E2F3 amplification and overexpression is associated with invasive tumor growth and rapid tumor cell proliferation in urinary bladder cancer. Oncogene 23: 5616-5623.
52. Arinaga M, Noguchi T, Takeno S, Chujo M, Miura T, et al. (2003) Clinical implication of cyclin B1 in non-small cell lung cancer. Oncol Rep 10: 1381-1386.
53. Singhal S, Vachani A, Antin-Ozerkis D, Kaiser LR, Albelda SM, (2005) Prognostic implications of cell cycle, apoptosis, and angiogenesis biomarkers in non-small cell lung cancer: a review. Clin Cancer Res 11: 3974-3986.
54. Yoshida T, Tanaka S, Mogi A, Shitara Y, Kuwano H, (2004) The clinical significance of Cyclin B1 and Wee1 expression in non-small-cell lung cancer. Ann Oncol 15: 252-256.
55. Hofmann HS, Hansen G, Burdach S, Bartling B, Silber RE, et al. (2004) Discrimination of human lung neoplasm from normal lung by two target genes. Am J Respir Crit Care Med 170: 516-519.
56. Nakamura Y, Matsubara D, Goto A, Ota S, Sachiko O, et al. (2008) Constitutive activation of c-Met is correlated with c-Met overexpression and dependent on cell-matrix adhesion in lung adenocarcinoma cell lines. Cancer Sci 99: 14-22.
57. Nakamura Y, Niki T, Goto A, Morikawa T, Miyazawa K, et al. (2007) c-Met activation in lung adenocarcinoma tissues: an immunohistochemical analysis. Cancer Sci 98: 1006-1013.
58. Stav D, Bar I, Sandbank J, (2007) Usefulness of CDK5RAP3, CCNB2, and RAGE genes for the diagnosis of lung adenocarcinoma. Int J Biol Markers 22: 108-113.
59. Naxerova K, Bult CJ, Peaston A, Fancher K, Knowles BB, et al. (2008) Analysis of gene expression in a developmental context emphasizes distinct biological leitmotifs in human cancers. Genome Biol 9: R108.
60. Reynolds PR, Kasteler SD, Cosio MG, Sturrock A, Huecksteadt T, et al. (2008) RAGE: developmental expression and positive feedback regulation by Egr-1 during cigarette smoke exposure in pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 294: L1094-1101.
61. Arnone MI, Zannini M, Di Lauro R, (1995) The DNA binding activity and the dimerization ability of the thyroid transcription factor I are redox regulated. J Biol Chem 270: 12048-12055.
62. De Felice M, Damante G, Zannini M, Francis-Lang H, Di Lauro R, (1995) Redundant domains contribute to the transcriptional activity of the thyroid transcription factor 1. J Biol Chem 270: 26649-26656.
63. Cao Y, Vo T, Millien G, Tagne JB, Kotton D, et al. (2010) Epigenetic mechanisms modulate thyroid transcription factor 1-mediated transcription of the surfactant protein B gene. J Biol Chem 285: 2152-2164.
64. Berghmans T, Paesmans M, Mascaux C, Martin B, Meert AP, et al. (2006) Thyroid transcription factor 1-a new prognostic factor in lung cancer: a meta-analysis. Ann Oncol 17: 1673-1676.
65. Haring M, Offermann S, Danker T, Horst I, Peterhansel C, et al. (2007) Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods 3: 11.
66. Reimer JJ, Turck F, (2010) Genome-wide mapping of protein-DNA interaction by chromatin immunoprecipitation and DNA microarray hybridization (ChIP-chip). Part A: ChIP-chip molecular methods. Methods Mol Biol 631: 139-160.
67. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
68. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
69. Dai M, Wang P, Boyd AD, Kostov G, Athey B, et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33: e175.
70. Chang JT, Nevins JR, (2006) GATHER: a systems approach to interpreting genomic signatures. Bioinformatics 22: 2926-2933.
71. Ramirez MI, Rishi AK, Cao YX, Williams MC, (1997) TGT3, thyroid transcription factor I, and Sp1 elements regulate transcriptional activity of the 1.3-kilobase pair promoter of T1alpha, a lung alveolar type I cell gene. J Biol Chem 272: 26285-26294.