Keeping it together: Pulmonary alveoli are maintained by a hierarchy of cellular programs

BioEssays

Volumn 37, Issue 9, 2015, Pages 1028-1037

  Logan, Catriona Y ^a   Desai, Tushar J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alveoli; AT2 cell; Lineage tracing; Lung; Repair; Stem cell; Transdifferentiation

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MAMMAGLOBIN A; NITROGEN DIOXIDE; OXYGEN; SECRETOGLOBIN FAMILY 1A MEMBER 1; SURFACTANT PROTEIN C; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; GAS;

ADULT STEM CELL; AGING; AIR SAC; AMBIENT AIR; ANGIOGENESIS; APPARENT LIFE THREATENING EVENT; ARTICLE; BRONCHIOLE; CELL ACTIVATION; CELL ACTIVITY; CELL COUNT; CELL DAMAGE; CELL DIFFERENTIATION; CELL FUNCTION; CELL HYPERPLASIA; CELL LOSS; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; CELLULAR DISTRIBUTION; CHRONIC OBSTRUCTIVE LUNG DISEASE; DISEASE COURSE; FIBROSING ALVEOLITIS; GENE MUTATION; GENETIC ASSOCIATION; HOMEOSTASIS; HUMAN; HYPEROXIA; INFLUENZA; INJURY SEVERITY; INTERSTITIAL LUNG DISEASE; INTRACELLULAR SIGNALING; LIFESPAN; LUNG ADENOCARCINOMA; LUNG ALVEOLUS; LUNG ALVEOLUS CELL TYPE 1; LUNG ALVEOLUS CELL TYPE 2; LUNG DIFFUSION; LUNG DISEASE; LUNG FIBROSIS; LUNG GAS EXCHANGE; LUNG INJURY; LUNG VENTILATION; NONHUMAN; NUCLEAR REPROGRAMMING; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; SMALL CELL LUNG CANCER; SQUAMOUS CELL LUNG CARCINOMA; STEM CELL NICHE; SURFACE AREA; TISSUE REGENERATION; ANIMAL; BRONCHUS; CYTOLOGY; GAS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; STEM CELL;

ANIMALS; BRONCHI; GASES; HUMANS; NEOPLASMS; PHENOTYPE; PULMONARY ALVEOLI; STEM CELLS;

EID: 84939650518     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201500031     Document Type: Article

References (77)

1. Bertalanffy FD, Leblond CP. 1955. Structure of respiratory tissue. Lancet 269: 1365-8.
2. Kauffman SL. 1980. Cell proliferation in the mammalian lung. Int Rev Exp Pathol 22: 131-91.
3. Uhal BD. 1997. Cell cycle kinetics in the alveolar epithelium. Am J Physiol 272: L1031-45.
4. Leblond CP. 1964. Classification of cell populations on the basis of their proliferative behavior. Natl Cancer I Monogr 14: 119-50.
5. Buckingham ME, Meilhac SM. 2011. Tracing cells for tracking cell lineage and clonal behavior. Dev Cell 21: 394-409.
6. Meban C. 1980. Thickness of the air-blood barriers in vertebrate lungs. J Anat 131: 299-307.
7. Low FN. 1953. The pulmonary alveolar epithelium of laboratory mammals and man. Anat Rec 117: 241-63.
8. Dobbs LG, Johnson MD, Vanderbilt J, Allen L, et al. 2010. The great big alveolar TI cell: evolving concepts and paradigms. Cell Physiol Biochem 25: 55-62.
9. Weibel ER. 1971. The mystery of "non-nucleated plates" in the alveolar epithelium of the lung explained. Acta Anat (Basel) 78: 425-43.
10. Whitsett JA, Wert SE, Weaver TE. 2015. Diseases of pulmonary surfactant homeostasis. Annu Rev Pathol 10: 371-93.
11. Meyrick B, Reid L. 1968. The alveolar brush cell in rat lung-a third pneumonocyte. J Ultrastruct Res 23: 71-80.
12. Reid L, Meyrick B, Antony VB, Chang LY, et al. 2005. The mysterious pulmonary brush cell: a cell in search of a function. Am J Respir Crit Care Med 172: 136-9.
13. Chapman HA, Li X, Alexander JP, Brumwell A, et al. 2011. Integrin alpha6beta4 identifies an adult distal lung epithelial population with regenerative potential in mice. J Clin Invest 121: 2855-62.
14. Vaughan AE, Brumwell AN, Xi Y, Gotts JE, et al. 2015. Lineage-negative progenitors mobilize to regenerate lung epithelium after major injury. Nature 517: 621-5.
15. Kumar PA, Hu Y, Yamamoto Y, Hoe NB, et al. 2011. Distal airway stem cells yield alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell 147: 525-38.
16. Hong KU, Reynolds SD, Watkins S, Fuchs E, et al. 2004. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 164: 577-88.
17. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, et al. 2005. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121: 823-35.
18. McQualter JL, Yuen K, Williams B, Bertoncello I. 2010. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc Natl Acad Sci USA 107: 1414-9.
19. Treutlein B, Brownfield DG, Wu AR, Neff NF, et al. 2014. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509: 371-5.
20. Leblond CP, Walker BE. 1956. Renewal of cell populations. Physiol Rev 36: 255-76.
21. Kapanci Y, Weibel ER, Kaplan HP, Robinson FR. 1969. Pathogenesis and reversibility of the pulmonary lesions of oxygen toxicity in monkeys. II. Ultrastructural and morphometric studies. Lab Invest 20: 101-18.
22. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, et al. 2011. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci USA 108: E1475-83.
23. Desai TJ, Brownfield DG, Krasnow MA. 2014. Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature 507: 190-4.
24. Lajtha LG. 1979. Stem cell concepts. Differentiation 14: 23-34.
25. Smith LJ. 1983. The effect of type 2 cell mitosis on the surfactant system of injured mouse lungs. J Lab Clin Med 102: 434-43.
26. Ramalho-Santos M, Willenbring H. 2007. On the origin of the term "stem cell". Cell Stem Cell 1: 35-8.
27. Becker AJ, McCulloch EA, Till JE. 1963. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197: 452-4.
28. Fuchs E. 2009. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137: 811-9.
29. Barker N. 2014. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol 15: 19-33.
30. Barkauskas CE, Cronce MJ, Rackley CR, Bowie EJ, et al. 2013. Type 2 alveolar cells are stem cells in adult lung. J Clin Invest 123: 3025-36.
31. Adamson IY, Bowden DH. 1974. The type 2 cell as progenitor of alveolar epithelial regeneration. A cytodynamic study in mice after exposure to oxygen. Lab Invest 30: 35-42.
32. Lin C, Song H, Huang C, Yao E, et al. 2012. Alveolar type II cells possess the capability of initiating lung tumor development. PLoS ONE 7: e53817.
33. Adamson IY, Bowden DH, Wyatt JP. 1970. Oxygen poisoning in mice. Ultrastructural and surfactant studies during exposure and recovery. Arch Pathol 90: 463-72.
34. Evans MJ, Cabral LJ, Stephens RJ, Freeman G. 1975. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO2. Exp Mol Pathol 22: 142-50.
35. Zuo W, Zhang T, Wu DZ, Guan SP, et al. 2015. p63(+) Krt5(+) distal airway stem cells are essential for lung regeneration. Nature 517: 616-20.
36. Dor Y, Melton DA. 2008. Facultative endocrine progenitor cells in the adult pancreas. Cell 132: 183-4.
37. Dor Y, Brown J, Martinez OI, Melton DA. 2004. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-6.
38. Grompe M. 2014. Liver stem cells, where art thou? Cell Stem Cell 15: 257-8.
39. Adamson IY, Bowden DH. 1977. Origin of ciliated alveolar epithelial cells in bleomycin-induced lung injury. Am J Pathol 87: 569-80.
40. Adamson IY, Bowden DH. 1979. Bleomycin-induced injury and metaplasia of alveolar type 2 cells. Relationship of cellular responses to drug presence in the lung. Am J Pathol 96: 531-44.
41. Loosli CG, Stinson SF, Ryan DP, Hertweck MS, et al. 1975. The destruction of type 2 pneumocytes by airborne influenza PR8-A virus; its effect on surfactant and lecithin content of the pneumonic lesions of mice. Chest 67: 7S-14S.
42. Stinson SF, Ryan DP, Hertweck S, Hardy JD, et al. 1976. Epithelial and surfactant changes in influenzal pulmonary lesions. Arch Pathol Lab Med 100: 147-53.
43. Kretzschmar K, Watt FM. 2012. Lineage tracing. Cell 148: 33-45.
44. Rawlins EL, Okubo T, Xue Y, Brass DM, et al. 2009. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 4: 525-34.
45. Zemke AC, Snyder JC, Brockway BL, Drake JA, et al. 2009. Molecular staging of epithelial maturation using secretory cell-specific genes as markers. Am J Resp Cell Mol 40: 340-8.
46. Reinert RB, Kantz J, Misfeldt AA, Poffenberger G, et al. 2012. Tamoxifen-induced Cre-loxP recombination is prolonged in pancreatic islets of adult mice. PLoS ONE 7: e33529.
47. Li H, Cho SN, Evans CM, Dickey BF, et al. 2008. Cre-mediated recombination in mouse Clara cells. Genesis 46: 300-7.
48. Morinaga R, Okamoto I, Furuta K, Kawano Y, et al. 2007. Sequential occurrence of non-small cell and small cell lung cancer with the same EGFR mutation. Lung Cancer 58: 411-3.
49. Niederst MJ, Sequist LV, Poirier JT, Mermel CH, et al. 2015. RB loss in resistant EGFR mutant lung adenocarcinomas that transform to small-cell lung cancer. Nat Commun 6: 6377.
50. Kang SM, Kang HJ, Shin JH, Kim H, et al. 2007. Identical epidermal growth factor receptor mutations in adenocarcinomatous and squamous cell carcinomatous components of adenosquamous carcinoma of the lung. Cancer 109: 581-7.
51. Han X, Li F, Fang Z, Gao Y, et al. 2014. Transdifferentiation of lung adenocarcinoma in mice with Lkb1 deficiency to squamous cell carcinoma. Nat Commun 5: 3261.
52. Maeda Y, Tsuchiya T, Hao H, Tompkins DH, et al. 2012. Kras(G12D) and Nkx2-1 haploinsufficiency induce mucinous adenocarcinoma of the lung. J Clin Invest 122: 4388-400.
53. Snyder EL, Watanabe H, Magendantz M, Hoersch S, et al. 2013. Nkx2-1 represses a latent gastric differentiation program in lung adenocarcinoma. Mol Cell 50: 185-99.
54. Kapere Ochieng J, Schilders K, Kool H, Buscop-van Kempen M, et al. 2014. Differentiated type II pneumocytes can be reprogrammed by ectopic Sox2 expression. PLoS ONE 9: e107248.
55. Konerding MA, Gibney BC, Houdek JP, Chamoto K, et al. 2012. Spatial dependence of alveolar angiogenesis in post-pneumonectomy lung growth. Angiogenesis 15: 23-32.
56. Brody JS, Burki R, Kaplan N. 1978. Deoxyribonucleic acid synthesis in lung cells during compensatory lung growth after pneumonectomy. Am Rev Respir Dis 117: 307-16.
57. Hodnett PA, Naidich DP. 2013. Fibrosing interstitial lung disease. A practical high-resolution computed tomography-based approach to diagnosis and management and a review of the literature. Am J Respir Crit Care Med 188: 141-9.
58. Uhal BD, Joshi I, Hughes WF, Ramos C, et al. 1998. Alveolar epithelial cell death adjacent to underlying myofibroblasts in advanced fibrotic human lung. Am J Physiol 275: L1192-9.
59. Armanios MY, Chen JJ, Cogan JD, Alder JK, et al. 2007. Telomerase mutations in families with idiopathic pulmonary fibrosis. New Engl J Med 356: 1317-26.
60. Kuo CS, Desai TJ. 2015. Cellular mechanisms of alveolar pathology in childhood interstitial lung diseases: current insights from mouse genetics. Curr Opin Pediatr 27: 341-7.
61. Witschi H. 1990. Responses of the lung to toxic injury. Environ Health Perspect 85: 5-13.
62. Collard HR, Moore BB, Flaherty KR, Brown KK, et al. 2007. Acute exacerbations of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 176: 636-43.
63. Rennard SI. 1998. COPD: overview of definitions, epidemiology, and factors influencing its development. Chest 113: 235S-41S.
64. Lin H, Jiang S. 2015. Combined pulmonary fibrosis and emphysema (CPFE): an entity different from emphysema or pulmonary fibrosis alone. J Thorac Dis 7: 767-79.
65. Alder JK, Guo N, Kembou F, Parry EM, et al. 2011. Telomere length is a determinant of emphysema susceptibility. Am J Resp Crit Care 184: 904-12.
66. Jain R, Barkauskas CE, Takeda N, Bowie EJ, et al. 2015. Plasticity of Hopx+ type I alveolar cells to regenerate type II cells in the lung. Nat Commun 6: 6727.
67. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, et al. 2011. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci USA 108: E1475-83.
68. Zheng D, Limmon GV, Yin L, Leung NHN, et al. 2012. Regeneration of alveolar type I and II cells from Scgb1a1-expressing cells following severe pulmonary damage induced by bleomycin and influenza. PLoS ONE 7: e48451.
69. Giangreco A, Reynolds SD, Stripp BR. 2002. Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am J Pathol 161: 173-82.
70. Randell SH, Comment CE, Ramaekers FC, Nettesheim P. 1991. Properties of rat tracheal epithelial cells separated based on expression of cell surface alpha-galactosyl end groups. Am J Respir Cell Mol Biol 4: 544-54.
71. Tata PR, Mou H, Pardo-Saganta A, Zhao R, et al. 2013. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503: 218-23.
72. Song H, Yao E, Lin C, Gacayan R, et al. 2012. Functional characterization of pulmonary neuroendocrine cells in lung development, injury, and tumorigenesis. Proc Natl Acad Sci USA 109: 17531-6.
73. Rock JR, Onaitis MW, Rawlins EL, Lu Y, et al. 2009. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA 106: 12771-5.
74. Xu X, Rock JR, Lu Y, Futtner C, et al. 2012. Evidence for type II cells as cells of origin of K-Ras-induced distal lung adenocarcinoma. Proc Natl Acad Sci USA 109: 4910-5.
75. Lin C, Song H, Huang C, Yao E, et al. 2012. Alveolar type II cells possess the capability of initiating lung tumor development. PLoS ONE 7: e53817.
76. Sutherland KD, Proost N, Brouns I, Adriaensen D, et al. 2011. Cell of origin of small cell lung cancer: inactivation of Trp53 and Rb1 in distinct cell types of adult mouse lung. Cancer Cell 19: 754-64.
77. Park KS, Liang MC, Raiser DM, Zamponi R, et al. 2011. Characterization of the cell of origin for small cell lung cancer. Cell Cycle 10: 2806-15.