Quantitative proteome analysis of alveolar type-II cells reveals a connection of integrin receptor subunits beta 2/6 and WNT signaling

Journal of Proteome Research

Volumn 12, Issue 12, 2013, Pages 5598-5608

  Mukhametshina, Regina T ^a,d   Ruhs, Aaron ^a   Singh, Indrabahadur ^a   Hasan, Diya ^a   Contreras, Adriana ^a   Mehta, Aditi ^a   Nikam, Vandana S ^a   Ahlbrecht, Katrin ^a   Carraro, Gianni ^b   Cabrera Fuentes, Hector A ^b,d   Jiang, Dongsheng ^c   Voswinckel, Robert ^a   Seeger, Werner ^a   Bellusci, Saverio ^b   Scharffetter Kochanek, Karin ^c   Bagaeva, Tatyana V ^d   Preissner, Klaus T ^b   Boettger, Thomas ^a   Braun, Thomas ^a   Krüger, Marcus ^a   Barreto, Guillermo ^a   more..

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF ULM   (Germany)

^d KAZAN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

ATII cells; integrin; lung; SILAC mice; WNT signaling

Indexed keywords

BETA2 INTEGRIN RECEPTOR; BETA6 INTEGRIN RECEPTOR; INTEGRIN RECEPTOR; MEMBRANE PROTEIN; SURFACTANT PROTEIN C; TRANSCRIPTOME; UNCLASSIFIED DRUG; WNT PROTEIN; BETA INTEGRIN; BETA6 INTEGRIN; CD18 ANTIGEN; PROTEIN BINDING; PROTEIN C; PROTEOME;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL SUBPOPULATION; CELL TYPE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; LABORATORY DEVICE; LUNG ALVEOLUS CELL TYPE 2; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MICROARRAY; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERSED PHASE LIQUID CHROMATOGRAPHY; SIGNAL TRANSDUCTION; STABLE ISOTOPE LABELING WITH AMINO ACIDS IN CELL CULTURE; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; LUNG ALVEOLUS; METABOLISM; MOLECULAR GENETICS; RESPIRATORY TRACT MUCOSA; STEM CELL; TISSUE MICROARRAY; WNT SIGNALING PATHWAY;

ANIMALS; ANTIGENS, CD18; CELL MEMBRANE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; INTEGRIN BETA CHAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE ANNOTATION; PROTEIN BINDING; PROTEIN C; PROTEOME; PULMONARY ALVEOLI; RESPIRATORY MUCOSA; STEM CELLS; TISSUE ARRAY ANALYSIS; WNT SIGNALING PATHWAY;

EID: 84890085133     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400573k     Document Type: Article

References (52)

1. Rock, J. R.; Hogan, B. L. Epithelial progenitor cells in lung development, maintenance, repair, and disease Annu. Rev. Cell Dev. Biol. 2011, 27, 493-512
2. Eramo, A.; Haas, T. L.; De Maria, R. Lung cancer stem cells: tools and targets to fight lung cancer Oncogene 2010, 29 (33) 4625-35
3. Rawlins, E. L.; Hogan, B. L. Epithelial stem cells of the lung: privileged few or opportunities for many? Development 2006, 133 (13) 2455-65
4. Adamson, I. Y.; Bowden, D. H. The type 2 cell as progenitor of alveolar epithelial regeneration. A cytodynamic study in mice after exposure to oxygen Lab. Invest. 1974, 30 (1) 35-42
5. Evans, M. J.; Cabral, L. J.; Stephens, R. J.; Freeman, G. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO2 Exp. Mol. Pathol. 1975, 22 (1) 142-50
6. Reddy, R.; Buckley, S.; Doerken, M.; Barsky, L.; Weinberg, K.; Anderson, K. D.; Warburton, D.; Driscoll, B. Isolation of a putative progenitor subpopulation of alveolar epithelial type 2 cells Am. J. Physiol.: Lung Cell. Mol. Physiol. 2004, 286 (4) L658-67
7. Fujino, N.; Kubo, H.; Suzuki, T.; Ota, C.; Hegab, A. E.; He, M.; Suzuki, S.; Yamada, M.; Kondo, T.; Kato, H.; Yamaya, M. Isolation of alveolar epithelial type II progenitor cells from adult human lungs Lab. Invest. 2011, 91 (3) 363-78
8. Ong, S. E.; Blagoev, B.; Kratchmarova, I.; Kristensen, D. B.; Steen, H.; Pandey, A.; Mann, M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 2002, 1 (5) 376-86
9. Kruger, M.; Moser, M.; Ussar, S.; Thievessen, I.; Luber, C. A.; Forner, F.; Schmidt, S.; Zanivan, S.; Fassler, R.; Mann, M. SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function Cell 2008, 134 (2) 353-64
10. Wehrle-Haller, B. Assembly and disassembly of cell matrix adhesions Curr. Opin. Cell Biol. 2012, 24 (5) 569-81
11. Campbell, I. D.; Humphries, M. J. Integrin structure, activation, and interactions Cold Spring Harbor Perspect. Biol. 2011, 3, 3
12. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines Cell 2002, 110 (6) 673-87
13. Tan, S. M. The leucocyte beta2 (CD18) integrins: the structure, functional regulation and signalling properties Biosci. Rep. 2012, 32 (3) 241-69
14. Munger, J. S.; Sheppard, D. Cross talk among TGF-beta signaling pathways, integrins, and the extracellular matrix Cold Spring Harbor Perspect. Biol. 2011, 3 (11) a005017
15. Mori, S.; Wu, C. Y.; Yamaji, S.; Saegusa, J.; Shi, B.; Ma, Z.; Kuwabara, Y.; Lam, K. S.; Isseroff, R. R.; Takada, Y. K.; Takada, Y. Direct binding of integrin alphavbeta3 to FGF1 plays a role in FGF1 signaling J. Biol. Chem. 2008, 283 (26) 18066-75
16. Presta, M.; Dell'Era, P.; Mitola, S.; Moroni, E.; Ronca, R.; Rusnati, M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis Cytokine Growth Factor Rev. 2005, 16 (2) 159-78
17. Schambony, A.; Kunz, M.; Gradl, D. Cross-regulation of Wnt signaling and cell adhesion Differentiation 2004, 72 (7) 307-18
18. Oloumi, A.; McPhee, T.; Dedhar, S. Regulation of E-cadherin expression and beta-catenin/Tcf transcriptional activity by the integrin-linked kinase Biochim. Biophys. Acta 2004, 1691 (1) 1-15
19. Peters, T.; Sindrilaru, A.; Hinz, B.; Hinrichs, R.; Menke, A.; Al-Azzeh, E. A.; Holzwarth, K.; Oreshkova, T.; Wang, H.; Kess, D.; Walzog, B.; Sulyok, S.; Sunderkotter, C.; Friedrich, W.; Wlaschek, M.; Krieg, T.; Scharffetter- Kochanek, K. Wound-healing defect of CD18(-/-) mice due to a decrease in TGF-beta1 and myofibroblast differentiation EMBO J. 2005, 24 (19) 3400-10
20. Cabrera Fuentes, H. A.; Kalacheva, N. V.; Mukhametshina, R. T.; Zelenichin, P. V.; Kolpakov, A. I.; Barreto, G.; Praissner, K. T.; Il'inskaia, O. N. [Binase penetration into alveolar epithelial cells does not induce cell death] Biomeditsinskaia khimiia 2012, 58 (3) 272-80
21. Xiang, X.; Benson, K. F.; Chada, K. Mini-mouse: disruption of the pygmy locus in a transgenic insertional mutant Science 1990, 247 (4945) 967-9
22. Wisniewski, J. R.; Zougman, A.; Mann, M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome J. Proteome Res. 2009, 8 (12) 5674-8
23. Wisniewski, R. J. Protocol to enrich and analyze plasma membrane proteins Methods Mol. Biol. 2009, 528, 127-34
24. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6 (5) 359-62
25. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26 (12) 1367-72
26. Cox, J.; Matic, I.; Hilger, M.; Nagaraj, N.; Selbach, M.; Olsen, J. V.; Mann, M. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics Nat. Protoc. 2009, 4 (5) 698-705
27. Xu, Y.; Ikegami, M.; Wang, Y.; Matsuzaki, Y.; Whitsett, J. A. Gene expression and biological processes influenced by deletion of Stat3 in pulmonary type II epithelial cells BMC Genom. 2007, 8, 455
28. Maier, H. J.; Schips, T. G.; Wietelmann, A.; Kruger, M.; Brunner, C.; Sauter, M.; Klingel, K.; Bottger, T.; Braun, T.; Wirth, T. Cardiomyocyte- specific IkappaB kinase (IKK)/NF-kappaB activation induces reversible inflammatory cardiomyopathy and heart failure Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (29) 11794-9
29. Volckaert, T.; Dill, E.; Campbell, A.; Tiozzo, C.; Majka, S.; Bellusci, S.; De Langhe, S. P. Parabronchial smooth muscle constitutes an airway epithelial stem cell niche in the mouse lung after injury J. Clin. Invest. 2011, 121 (11) 4409-19
30. Luo, B. H.; Carman, C. V.; Springer, T. A. Structural basis of integrin regulation and signaling Annu. Rev. Immunol. 2007, 25, 619-47
31. Jeyaseelan, S.; Hsuan, S. L.; Kannan, M. S.; Walcheck, B.; Wang, J. F.; Kehrli, M. E.; Lally, E. T.; Sieck, G. C.; Maheswaran, S. K. Lymphocyte function-associated antigen 1 is a receptor for Pasteurella haemolytica leukotoxin in bovine leukocytes Infect. Immun. 2000, 68 (1) 72-9
32. Antal-Szalmas, P.; Strijp, J. A.; Weersink, A. J.; Verhoef, J.; Van Kessel, K. P. Quantitation of surface CD14 on human monocytes and neutrophils J. Leukocyte Biol. 1997, 61 (6) 721-8
33. Leong, J.; Zhou, M.; Jacob, A.; Wang, P. Aging-related hyperinflammation in endotoxemia is mediated by the alpha2A-adrenoceptor and CD14/TLR4 pathways Life Sci. 2010, 86 (19-20) 740-6
34. Autero, M.; Gahmberg, C. G. Phorbol diesters increase the phosphorylation of the leukocyte common antigen CD45 in human T cells Eur. J. Immunol. 1987, 17 (10) 1503-6
35. Coraux, C.; Meneguzzi, G.; Rousselle, P.; Puchelle, E.; Gaillard, D. Distribution of laminin 5, integrin receptors, and branching morphogenesis during human fetal lung development Dev. Dyn. 2002, 225 (2) 176-85
36. O'Reilly, A. M.; Lee, H. H.; Simon, M. A. Integrins control the positioning and proliferation of follicle stem cells in the Drosophila ovary J. Cell Biol. 2008, 182 (4) 801-15
37. Sheppard, D. Functions of pulmonary epithelial integrins: from development to disease Physiol. Rev. 2003, 83 (3) 673-86
38. Sanchez-Esteban, J.; Wang, Y.; Filardo, E. J.; Rubin, L. P.; Ingber, D. E. Integrins beta1, alpha6, and alpha3 contribute to mechanical strain-induced differentiation of fetal lung type II epithelial cells via distinct mechanisms Am. J. Physiol.: Lung Cell. Mol. Physiol. 2006, 290 (2) L343-50
39. Crosby, L. M.; Waters, C. M. Epithelial repair mechanisms in the lung Am. J. Physiol.: Lung Cell. Mol. Physiol. 2010, 298 (6) L715-31
40. Henderson, N. C.; Sheppard, D. Integrin-mediated regulation of TGFbeta in fibrosis Biochim. Biophys. Acta 2013, 1832 (7) 891-6
41. Brafman, D. A.; Phung, C.; Kumar, N.; Willert, K. Regulation of endodermal differentiation of human embryonic stem cells through integrin-ECM interactions Cell Death Differ. 2013, 20 (3) 369-81
42. Chapman, H. A.; Li, X.; Alexander, J. P.; Brumwell, A.; Lorizio, W.; Tan, K.; Sonnenberg, A.; Wei, Y.; Vu, T. H. Integrin alpha6beta4 identifies an adult distal lung epithelial population with regenerative potential in mice J. Clin. Invest. 2011, 121 (7) 2855-62
43. Whitsett, J. A.; Kalinichenko, V. V. Integrin alpha6beta4 defines a novel lung epithelial progenitor cell: a step forward for cell-based therapies for pulmonary disease J. Clin. Invest. 2011, 121 (7) 2543-5
44. Gazdhar, A.; Temuri, A.; Knudsen, L.; Gugger, M.; Schmid, R. A.; Ochs, M.; Geiser, T. Targeted gene transfer of hepatocyte growth factor to alveolar type II epithelial cells reduces lung fibrosis in rats Hum. Gene Ther. 2013, 24 (1) 105-16
45. Aoshiba, K.; Nagai, A. Senescence hypothesis for the pathogenetic mechanism of chronic obstructive pulmonary disease Proc. Am. Thoracic Society 2009, 6 (7) 596-601
46. Tsuji, T.; Aoshiba, K.; Nagai, A. Alveolar cell senescence in patients with pulmonary emphysema Am. J. Respir. Crit. Care Med. 2006, 174 (8) 886-93
47. Gad, A.; Callender, D. L.; Killeen, E.; Hudak, J.; Dlugosz, M. A.; Larson, J. E.; Cohen, J. C.; Chander, A. Transient in utero disruption of cystic fibrosis transmembrane conductance regulator causes phenotypic changes in alveolar type II cells in adult rats BMC Cell Biol. 2009, 10, 24
48. Song, Y.; Pittet, J. F.; Huang, X.; He, H.; Lynch, S. V.; Violette, S. M.; Weinreb, P. H.; Horan, G. S.; Carmago, A.; Sawa, Y.; Bernstein, X. L.; Wiener-Kronish, J. P. Role of integrin alphav beta6 in acute lung injury induced by Pseudomonas aeruginosa Infect. Immun. 2008, 76 (6) 2325-32
49. Hu, B.; Jennings, J. H.; Sonstein, J.; Floros, J.; Todt, J. C.; Polak, T.; Curtis, J. L. Resident murine alveolar and peritoneal macrophages differ in adhesion of apoptotic thymocytes Am. J. Respir. Cell Mol. Biol. 2004, 30 (5) 687-93
50. Sheppard, D. Modulation of acute lung injury by integrins Proc. Am. Thorac. Soc. 2012, 9 (3) 126-9
51. Arosio, D.; Casagrande, C.; Manzoni, L. Integrin-mediated drug delivery in cancer and cardiovascular diseases with peptide-functionalized nanoparticles Curr. Med. Chem. 2012, 19 (19) 3128-51
52. Li, C.; Li, A.; Xing, Y.; Li, M.; Chan, B.; Ouyang, R.; Taketo, M. M.; Kucherlapati, R.; Borok, Z.; Minoo, P. Apc deficiency alters pulmonary epithelial cell fate and inhibits Nkx2.1 via triggering TGF-beta signaling Dev. Biol. 2013, 378 (1) 13-24