Browse > Article
http://dx.doi.org/10.5808/GI.2019.17.1.e8

Insights into the signal transduction pathways of mouse lung type II cells revealed by transcription factor profiling in the transcriptome  

Ramana, Chilakamarti V. (Department of Medicine, Dartmouth-Hitchcock Medical Center, Dartmouth Medical School)
Abstract
Alveolar type II cells constitute a small fraction of the total lung cell mass. However, they play an important role in many cellular processes including trans-differentiation into type I cells as well as repair of lung injury in response to toxic chemicals and respiratory pathogens. Transcription factors are the regulatory proteins dynamically modulating DNA structure and gene expression. Transcription factor profiling in microarray datasets revealed that several members of AP1, ATF, $NF-{\kappa}B$, and C/EBP families involved in diverse responses were expressed in mouse lung type II cells. A transcriptional factor signature consisting of Cebpa, Srebf1, Stat3, Klf5, and Elf3 was identified in lung type II cells, Sox9+ pluripotent lung stem cells as well as in mouse lung development. Identification of the transcription factor profile in mouse lung type II cells will serve as a useful resource and facilitate the integrated analysis of signal transduction pathways and specific gene targets in a variety of physiological conditions.
Keywords
gene signature; lung injury; lung type II cells; microarrays; signal transduction pathways; transcription factor profiling;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Symon A, Harley V. SOX9: A genomic view of tissue specific expression and action. Int J Biochem Cell Biol 2017;87:18-22.   DOI
2 Voronkova MA, Luanpitpong S, Rojanasakul LW, Castranova V, Dinu CZ, Riedel H, et al. SOX9 regulates cancer stem-like properties and metastatic potential of single-walled carbon nanotube-exposed cells. Sci Rep 2017;7:11653.   DOI
3 Wan H, Luo F, Wert SE, Zhang L, Xu Y, Ikegami M, et al. Kruppel-like factor 5 is required for perinatal lung morphogenesis and function. Development 2008;135:2563-2572.   DOI
4 Quinlan T, Spivack S, Mossman BT. Regulation of antioxidant enzymes in lung after oxidant injury. Environ Health Perspect 1994;102 Suppl 2:79-87.
5 Reddy NM, Kleeberger SR, Yamamoto M, Kensler TW, Scollick C, Biswal S, et al. Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiol Genomics 2007;32:74-81.   DOI
6 Nguyen T, Nioi P, Pickett CB. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 2009;284:13291-13295.   DOI
7 Reddy NM, Kleeberger SR, Cho HY, Yamamoto M, Kensler TW, Biswal S, et al. Deficiency in Nrf2-GSH signaling impairs type II cell growth and enhances sensitivity to oxidants. Am J Respir Cell Mol Biol 2007;37:3-8.   DOI
8 Anttila S, Raunio H, Hakkola J. Cytochrome P450-mediated pulmonary metabolism of carcinogens: regulation and cross-talk in lung carcinogenesis. Am J Respir Cell Mol Biol 2011;44:583-590.   DOI
9 Zhang S, Che D, Yang F, Chi C, Meng H, Shen J, et al. Tumor-associated macrophages promote tumor metastasis via the TGF-beta/SOX9 axis in non-small cell lung cancer. Oncotarget 2017;8:99801-99815.   DOI
10 Nichane M, Javed A, Sivakamasundari V, Ganesan M, Ang LT, Kraus P, et al. Isolation and 3D expansion of multipotent Sox9(+) mouse lung progenitors. Nat Methods 2017;14:1205-1212.   DOI
11 Berhane K, Boggaram V. Identification of a novel DNA regulatory element in the rabbit surfactant protein B (SP-B) promoter that is a target for ATF/CREB and AP-1 transcription factors. Gene 2001;268:141-151.   DOI
12 Glasser SW, Burhans MS, Eszterhas SK, Bruno MD, Korfhagen TR. Human SP-C gene sequences that confer lung epithelium-specific expression in transgenic mice. Am J Physiol Lung Cell Mol Physiol 2000;278:L933-L945.   DOI
13 Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003;4:P3.   DOI
14 Gong X, Sun Z, Cui D, Xu X, Zhu H, Wang L, et al. Isolation and characterization of lung resident mesenchymal stem cells capable of differentiating into alveolar epithelial type II cells. Cell Biol Int 2014;38:405-411.   DOI
15 Lekstrom-Himes J, Xanthopoulos KG. Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J Biol Chem 1998;273:28545-28548.   DOI
16 Reddy NM, Potteti HR, Mariani TJ, Biswal S, Reddy SP. Conditional deletion of Nrf2 in airway epithelium exacerbates acute lung injury and impairs the resolution of inflammation. Am J Respir Cell Mol Biol 2011;45:1161-1168.   DOI
17 Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004;101:6062-6067.   DOI
18 Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998;95:14863-14868.   DOI
19 Rosenfeld MG, Lunyak VV, Glass CK. Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 2006;20:1405-1428.   DOI
20 Inoue K, Takano H, Kaewamatawong T, Shimada A, Suzuki J, Yanagisawa R, et al. Role of metallothionein in lung inflammation induced by ozone exposure in mice. Free Radic Biol Med 2008;45:1714-1722.   DOI
21 Baud V, Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 2001;11:372-377.   DOI
22 Kurakula K, Vos M, Logiantara A, Roelofs JJ, Nieuwenhuis MA, Koppelman GH, et al. Nuclear receptor Nur77 attenuates airway inflammation in mice by suppressing NF-kappaB activity in lung epithelial cells. J Immunol 2015;195:1388-1398.   DOI
23 Suzuki T, Aizawa K, Matsumura T, Nagai R. Vascular implications of the Kruppel-like family of transcription factors. Arterioscler Thromb Vasc Biol 2005;25:1135-1141.   DOI
24 Winkler GS. The mammalian anti-proliferative BTG/Tob protein family. J Cell Physiol 2010;222:66-72.   DOI
25 Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002;109 Suppl:S81-96.   DOI
26 Hai T, Hartman MG. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene 2001;273:1-11.   DOI
27 Ludwig S, Pleschka S, Planz O, Wolff T. Ringing the alarm bells: signalling and apoptosis in influenza virus infected cells. Cell Microbiol 2006;8:375-386.   DOI
28 Chang Y, Edeen K, Lu X, De Leon M, Mason RJ. Keratinocyte growth factor induces lipogenesis in alveolar type II cells through a sterol regulatory element binding protein-1c-dependent pathway. Am J Respir Cell Mol Biol 2006;35:268-274.   DOI
29 Takano H, Inoue K, Yanagisawa R, Sato M, Shimada A, Morita T, et al. Protective role of metallothionein in acute lung injury induced by bacterial endotoxin. Thorax 2004;59:1057-1062.   DOI
30 Murphy EP, Crean D. Molecular interactions between NR4A orphan nuclear receptors and NF-kappaB are required for appropriate inflammatory responses and immune cell homeostasis. Biomolecules 2015;5:1302-1318.   DOI
31 Akella A, Deshpande SB. Pulmonary surfactants and their role in pathophysiology of lung disorders. Indian J Exp Biol 2013;51:5-22.
32 Ware LB, Matthay MA. Keratinocyte and hepatocyte growth factors in the lung: roles in lung development, inflammation, and repair. Am J Physiol Lung Cell Mol Physiol 2002;282:L924-L940.   DOI
33 Adachi J, Kumar C, Zhang Y, Mann M. In-depth analysis of the adipocyte proteome by mass spectrometry and bioinformatics. Mol Cell Proteomics 2007;6:1257-1273.   DOI
34 Flodby P, Barlow C, Kylefjord H, Ahrlund-Richter L, Xanthopoulos KG. Increased hepatic cell proliferation and lung abnormalities in mice deficient in CCAAT/enhancer binding protein alpha. J Biol Chem 1996;271:24753-24760.   DOI
35 Matsuzaki Y, Besnard V, Clark JC, Xu Y, Wert SE, Ikegami M, et al. STAT3 regulates ABCA3 expression and influences lamellar body formation in alveolar type II cells. Am J Respir Cell Mol Biol 2008;38:551-558.   DOI
36 Lee CM, Wu J, Xia Y, Hu J. ESE-1 in early development: approaches for the future. Front Cell Dev Biol 2016;4:73.
37 Wang H, Yu Z, Huo S, Chen Z, Ou Z, Mai J, et al. Overexpression of ELF3 facilitates cell growth and metastasis through PI3K/Akt and ERK signaling pathways in non-small cell lung cancer. Int J Biochem Cell Biol 2018;94:98-106.   DOI
38 Murray CJ, Lopez AD. Global mortality, disability, and the contribution of risk factors: Global Burden of Disease Study. Lancet 1997;349:1436-1442.   DOI
39 Hippenstiel S, Opitz B, Schmeck B, Suttorp N. Lung epithelium as a sentinel and effector system in pneumonia: molecular mechanisms of pathogen recognition and signal transduction. Respir Res 2006;7:97.   DOI
40 Castell JV, Donato MT, Gomez-Lechon MJ. Metabolism and bioactivation of toxicants in the lung. The in vitro cellular approach. Exp Toxicol Pathol 2005;57 Suppl 1:189-204.   DOI
41 Maeda Y, Dave V, Whitsett JA. Transcriptional control of lungmorphogenesis. Physiol Rev 2007;87:219-244.   DOI
42 Perl AK, Wert SE, Loudy DE, Shan Z, Blair PA, Whitsett JA. Conditional recombination reveals distinct subsets of epithelial cells in trachea, bronchi, and alveoli. Am J Respir Cell Mol Biol 2005;33:455-462.   DOI
43 Fehrenbach H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2001;2:33-46.   DOI
44 Wright JR, Dobbs LG. Regulation of pulmonary surfactant secretion and clearance. Annu Rev Physiol 1991;53:395-414.   DOI
45 Corti M, Brody AR, Harrison JH. Isolation and primary culture of murine alveolar type II cells. Am J Respir Cell Mol Biol 1996;14:309-315.   DOI
46 Michael P, Brabant D, Bleiblo F, Ramana CV, Rutherford M, Khurana S, et al. Influenza A induced cellular signal transduction pathways. J Thorac Dis 2013;5 Suppl 2:S132-141.
47 Xu L, Yoon H, Zhao MQ, Liu J, Ramana CV, Enelow RI. Cutting edge: pulmonary immunopathology mediated by antigen-specific expression of TNF-alpha by antiviral CD8+ T-cells. J Immunol 2004;173:721-725.   DOI
48 Morales Johansson H, Newman DR, Sannes PL. Whole-genome analysis of temporal gene expression during early transdifferentiation of human lung alveolar epithelial type 2 cells in vitro. PLoS One 2014;9:e93413.   DOI
49 Newman V, Gonzalez RF, Matthay MA, Dobbs LG. A novel alveolar type I cell-specific biochemical marker of human acute lung injury. Am J Respir Crit Care Med 2000;161:990-995.   DOI
50 Boylan GM, Pryde JG, Dobbs LG, McElroy MC. Identification of a novel antigen on the apical surface of rat alveolar epithelial type II and Clara cells. Am J Physiol Lung Cell Mol Physiol 2001;280:L1318-L1326.   DOI
51 Roper JM, Staversky RJ, Finkelstein JN, Keng PC, O'Reilly MA. Identification and isolation of mouse type II cells on the basis of intrinsic expression of enhanced green fluorescent protein. Am J Physiol Lung Cell Mol Physiol 2003;285:L691-700.   DOI
52 Shyamsundar R, Kim YH, Higgins JP, Montgomery K, Jorden M, Sethuraman A, et al. A DNA microarray survey of gene expression in normal human tissues. Genome Biol 2005;6:R22.   DOI
53 Ballard PL, Lee JW, Fang X, Chapin C, Allen L, Segal MR, et al. Regulated gene expression in cultured type II cells of adult human lung. Am J Physiol Lung Cell Mol Physiol 2010;299:L36-L50.   DOI
54 Mariani TJ, Reed JJ, Shapiro SD. Expression profiling of the developing mouse lung: insights into the establishment of the extracellular matrix. Am J Respir Cell Mol Biol 2002;26:541-548.   DOI
55 Martinez JM, Afshari CA, Bushel PR, Masuda A, Takahashi T, Walker NJ. Differential toxicogenomic responses to 2,3,7,8-tetrachlorodibenzo-p-dioxin in malignant and nonmalignant human airway epithelial cells. Toxicol Sci 2002;69:409-423.   DOI
56 Dave NB, Kaminski N. Analysis of microarray experiments for pulmonary fibrosis. Methods Mol Med 2005;117:333-358.
57 Xu Y, Ikegami M, Wang Y, Matsuzaki Y, Whitsett JA. Gene expression and biological processes influenced by deletion of Stat3 in pulmonary type II epithelial cells. BMC Genomics 2007;8:455.   DOI
58 Ramana CV, Chintapalli J, Xu L, Alia C, Zhou J, Bruder D, et al. Lung epithelial NF-kappaB and Stat1 signaling in response to CD8+ T-cell antigen recognition. J Interferon Cytokine Res 2006;26:318-327.   DOI
59 Lizio M, Harshbarger J, Abugessaisa I, Noguchi S, Kondo A, Severin J, et al. Update of the FANTOM web resource: high resolution transcriptome of diverse cell types in mammals. Nucleic Acids Res 2017;45:D737-D743.   DOI