Dynamic changes in intracellular ROS levels regulate airway basal stem cell homeostasis through Nrf2-dependent notch signaling

Cell Stem Cell

Volumn 15, Issue 2, 2014, Pages 199-214

  Paul, Manash K ^a   Bisht, Bharti ^a   Darmawan, Daphne O ^a   Chiou, Richard ^a   Ha, Vi L ^a   Wallace, William D ^b   Chon, Andrew T ^a   Hegab, Ahmed E ^c   Grogan, Tristan ^b   Elashoff, David A ^b   Alva Ornelas, Jackelyn A ^a   Gomperts, Brigitte N ^a,b,d  

^a MATTEL CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; MACROGOL DERIVATIVE; NFE2L2 PROTEIN, HUMAN; NFE2L2 PROTEIN, MOUSE; NOTCH RECEPTOR; POLIDOCANOL; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; HOMEOSTASIS; HUMAN; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; SIGNAL TRANSDUCTION; STEM CELL; TRACHEA; WOUND HEALING; AIRWAY BASAL STEM CELL; ANIMAL CELL; ARTICLE; CELL RENEWAL; CONTROLLED STUDY; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIOXIDANTS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; HOMEOSTASIS; HUMANS; MICE; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; POLYETHYLENE GLYCOLS; REACTIVE OXYGEN SPECIES; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELLS; TRACHEA; WOUND HEALING;

EID: 84905905334     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.05.009     Document Type: Article

References (49)

1. E. Barreiro, V.I. Peinado, J.B. Galdiz, E. Ferrer, J. Marin-Corral, F. Sánchez, J. Gea, J.A. Barberà ENIGMA in COPD Project Cigarette smoke-induced oxidative stress: A role in chronic obstructive pulmonary disease skeletal muscle dysfunction Am. J. Respir. Crit. Care Med. 182 2010 477 488
2. C. Blanpain, W.E. Lowry, H.A. Pasolli, and E. Fuchs Canonical notch signaling functions as a commitment switch in the epidermal lineage Genes Dev. 20 2006 3022 3035
3. D.W. Borthwick, M. Shahbazian, Q.T. Krantz, J.R. Dorin, and S.H. Randell Evidence for stem-cell niches in the tracheal epithelium Am. J. Respir. Cell Mol. Biol. 24 2001 662 670
4. Cancer Genome Atlas Research Network Comprehensive genomic characterization of squamous cell lung cancers Nature 489 2012 519 525
5. S. Chuikov, B.P. Levi, M.L. Smith, and S.J. Morrison Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress Nat. Cell Biol. 12 2010 999 1006
6. G.M. DeNicola, F.A. Karreth, T.J. Humpton, A. Gopinathan, C. Wei, K. Frese, D. Mangal, K.H. Yu, C.J. Yeo, and E.S. Calhoun et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis Nature 475 2011 106 109
7. X. Gao, C.M. Vockley, F. Pauli, K.M. Newberry, Y. Xue, S.H. Randell, T.E. Reddy, and B.L. Hogan Evidence for multiple roles for grainyheadlike 2 in the establishment and maintenance of human mucociliary airway epithelium Proc. Natl. Acad. Sci. USA 110 2013 9356 9361
8. M. Ghosh, S. Ahmad, A. Jian, B. Li, R.W. Smith, K.M. Helm, M.A. Seibold, S.D. Groshong, C.W. White, and S.D. Reynolds Human tracheobronchial basal cells. Normal versus remodeling/repairing phenotypes in vivo and in vitro Am. J. Respir. Cell Mol. Biol. 49 2013 1127 1134
9. J.S. Guseh, S.A. Bores, B.Z. Stanger, Q. Zhou, W.J. Anderson, D.A. Melton, and J. Rajagopal Notch signaling promotes airway mucous metaplasia and inhibits alveolar development Development 136 2009 1751 1759
10. S. He, D. Nakada, and S.J. Morrison Mechanisms of stem cell self-renewal Annu. Rev. Cell Dev. Biol. 25 2009 377 406
11. A.E. Hegab, V.L. Ha, J.L. Gilbert, K.X. Zhang, S.P. Malkoski, A.T. Chon, D.O. Darmawan, B. Bisht, A.T. Ooi, and M. Pellegrini et al. Novel stem/progenitor cell population from murine tracheal submucosal gland ducts with multipotent regenerative potential Stem Cells 29 2011 1283 1293
12. A.E. Hegab, V.L. Ha, Y.S. Attiga, D.W. Nickerson, and B.N. Gomperts Isolation of basal cells and submucosal gland duct cells from mouse trachea J. Vis. Exp. Sep 14 2012 e3731
13. A.E. Hegab, V.L. Ha, D.O. Darmawan, J.L. Gilbert, A.T. Ooi, Y.S. Attiga, B. Bisht, D.W. Nickerson, and B.N. Gomperts Isolation and in vitro characterization of basal and submucosal gland duct stem/progenitor cells from human proximal airways Stem Cells Transl. Med. 1 2012 719 724
14. R.S. Herbst, J.V. Heymach, and S.M. Lippman Lung cancer N. Engl. J. Med. 359 2008 1367 1380
15. C. Hicks, S.H. Johnston, G. diSibio, A. Collazo, T.F. Vogt, and G. Weinmaster Fringe differentially modulates Jagged1 and Delta1 signalling through Notch1 and Notch2 Nat. Cell Biol. 2 2000 515 520
16. C.E. Hochmuth, B. Biteau, D. Bohmann, and H. Jasper Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila Cell Stem Cell 8 2011 188 199
17. K.U. Hong, S.D. Reynolds, S. Watkins, E. Fuchs, and B.R. Stripp Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium Am. J. Pathol. 164 2004 577 588
18. Y.Y. Jang, and S.J. Sharkis A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche Blood 110 2007 3056 3063
19. E. Kansanen, S.M. Kuosmanen, H. Leinonen, and A.L. Levonen The Keap1-Nrf2 pathway: Mechanisms of activation and dysregulation in cancer Redox Biol. 1 2013 45 49
20. J.H. Kim, R.K. Thimmulappa, V. Kumar, W. Cui, S. Kumar, P. Kombairaju, H. Zhang, J. Margolick, W. Matsui, and T. Macvittie et al. NRF2-mediated Notch pathway activation enhances hematopoietic reconstitution following myelosuppressive radiation J. Clin. Invest. 124 2014 730 741
21. J.E. Le Belle, N.M. Orozco, A.A. Paucar, J.P. Saxe, J. Mottahedeh, A.D. Pyle, H. Wu, and H.I. Kornblum Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner Cell Stem Cell 8 2011 59 71
22. J.M. Lee, J. Li, D.A. Johnson, T.D. Stein, A.D. Kraft, M.J. Calkins, R.J. Jakel, and J.A. Johnson Nrf2, a multi-organ protector? FASEB J. 19 2005 1061 1066
23. C. Luxenburg, H.A. Pasolli, S.E. Williams, and E. Fuchs Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation Nat. Cell Biol. 13 2011 203 214
24. D. Malhotra, R. Thimmulappa, A. Navas-Acien, A. Sandford, M. Elliott, A. Singh, L. Chen, X. Zhuang, J. Hogg, and P. Pare et al. Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1 Am. J. Respir. Crit. Care Med. 178 2008 592 604
25. S.P. Malkoski, T.G. Cleaver, S.L. Lu, J.G. Lighthall, and X.J. Wang Keratin promoter based gene manipulation in the murine conducting airway Int. J. Biol. Sci. 6 2010 68 79
26. J.T. McDonald, K. Kim, A.J. Norris, E. Vlashi, T.M. Phillips, C. Lagadec, L. Della Donna, J. Ratikan, H. Szelag, L. Hlatky, and W.H. McBride Ionizing radiation activates the Nrf2 antioxidant response Cancer Res. 70 2010 8886 8895
27. H. Morimoto, K. Iwata, N. Ogonuki, K. Inoue, O. Atsuo, M. Kanatsu-Shinohara, T. Morimoto, C. Yabe-Nishimura, and T. Shinohara ROS are required for mouse spermatogonial stem cell self-renewal Cell Stem Cell 12 2013 774 786
28. K.B. Myant, P. Cammareri, E.J. McGhee, R.A. Ridgway, D.J. Huels, J.B. Cordero, S. Schwitalla, G. Kalna, E.L. Ogg, and D. Athineos et al. ROS production and NF-κB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation Cell Stem Cell 12 2013 761 773
29. K. Naka, T. Muraguchi, T. Hoshii, and A. Hirao Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells Antioxid. Redox Signal. 10 2008 1883 1894
30. S. Nakamura, M. Oshima, J. Yuan, A. Saraya, S. Miyagi, T. Konuma, S. Yamazaki, M. Osawa, H. Nakauchi, H. Koseki, and A. Iwama Bmi1 confers resistance to oxidative stress on hematopoietic stem cells PLoS ONE 7 2012 e36209
31. T. Nguyen, P. Nioi, and C.B. Pickett The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress J. Biol. Chem. 284 2009 13291 13295
32. H. Okawa, H. Motohashi, A. Kobayashi, H. Aburatani, T.W. Kensler, and M. Yamamoto Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity Biochem. Biophys. Res. Commun. 339 2006 79 88
33. A. Ooi, K. Dykema, A. Ansari, D. Petillo, J. Snider, R. Kahnoski, J. Anema, D. Craig, J. Carpten, B.T. Teh, and K.A. Furge CUL3 and NRF2 mutations confer an NRF2 activation phenotype in a sporadic form of papillary renal cell carcinoma Cancer Res. 73 2013 2044 2051
34. L. Raj, T. Ide, A.U. Gurkar, M. Foley, M. Schenone, X. Li, N.J. Tolliday, T.R. Golub, S.A. Carr, and A.F. Shamji et al. Selective killing of cancer cells by a small molecule targeting the stress response to ROS Nature 475 2011 231 234
35. J.R. Rock, and B.L. Hogan Epithelial progenitor cells in lung development, maintenance, repair, and disease Annu. Rev. Cell Dev. Biol. 27 2011 493 512
36. J.R. Rock, M.W. Onaitis, E.L. Rawlins, Y. Lu, C.P. Clark, Y. Xue, S.H. Randell, and B.L. Hogan Basal cells as stem cells of the mouse trachea and human airway epithelium Proc. Natl. Acad. Sci. USA 106 2009 12771 12775
37. J.R. Rock, S.H. Randell, and B.L. Hogan Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling Dis. Model. Mech. 3 2010 545 556
38. J.R. Rock, X. Gao, Y. Xue, S.H. Randell, Y.Y. Kong, and B.L. Hogan Notch-dependent differentiation of adult airway basal stem cells Cell Stem Cell 8 2011 639 648
39. A. Sakaue-Sawano, H. Kurokawa, T. Morimura, A. Hanyu, H. Hama, H. Osawa, S. Kashiwagi, K. Fukami, T. Miyata, and H. Miyoshi et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression Cell 132 2008 487 498
40. H. Satoh, T. Moriguchi, K. Taguchi, J. Takai, J.M. Maher, T. Suzuki, P.T. Winnard Jr., V. Raman, M. Ebina, T. Nukiwa, and M. Yamamoto Nrf2-deficiency creates a responsive microenvironment for metastasis to the lung Carcinogenesis 31 2010 1833 1843
41. J.C. Snyder, R.M. Teisanu, and B.R. Stripp Endogenous lung stem cells and contribution to disease J. Pathol. 217 2009 254 264
42. M.B. Sporn, and K.T. Liby NRF2 and cancer: the good, the bad and the importance of context Nat. Rev. Cancer 12 2012 564 571
43. T. Suzuki, H. Motohashi, and M. Yamamoto Toward clinical application of the Keap1-Nrf2 pathway Trends Pharmacol. Sci. 34 2013 340 346
44. R.K. Thimmulappa, K.H. Mai, S. Srisuma, T.W. Kensler, M. Yamamoto, and S. Biswal Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray Cancer Res. 62 2002 5196 5203
45. A.E. Tilley, B.G. Harvey, A. Heguy, N.R. Hackett, R. Wang, T.P. O'Connor, and R.G. Crystal Down-regulation of the notch pathway in human airway epithelium in association with smoking and chronic obstructive pulmonary disease Am. J. Respir. Crit. Care Med. 179 2009 457 466
46. P.N. Tsao, M. Vasconcelos, K.I. Izvolsky, J. Qian, J. Lu, and W.V. Cardoso Notch signaling controls the balance of ciliated and secretory cell fates in developing airways Development 136 2009 2297 2307
47. N. Wakabayashi, S. Shin, S.L. Slocum, E.S. Agoston, J. Wakabayashi, M.K. Kwak, V. Misra, S. Biswal, M. Yamamoto, and T.W. Kensler Regulation of notch1 signaling by nrf2: implications for tissue regeneration Sci. Signal. 3 2010 ra52
48. K. Wang, T. Zhang, Q. Dong, E.C. Nice, C. Huang, and Y. Wei Redox homeostasis: the linchpin in stem cell self-renewal and differentiation Cell Death Dis. 4 2013 e537
49. B. Westhoff, I.N. Colaluca, G. D'Ario, M. Donzelli, D. Tosoni, S. Volorio, G. Pelosi, L. Spaggiari, G. Mazzarol, and G. Viale et al. Alterations of the Notch pathway in lung cancer Proc. Natl. Acad. Sci. USA 106 2009 22293 22298