Epithelial progenitor cells in lung development, maintenance, repair, and disease

Annual Review of Cell and Developmental Biology

Volumn 27, Issue , 2011, Pages 493-512

  Rock, Jason R ^a   Hogan, Brigid L M ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Airway remodeling; Basal cell; Injury and repair; Lung epithelium; Mouse models of lung disease; Stem cell

Indexed keywords

ARTICLE; BASAL CELL; BRONCHUS; CELL FATE; CLARA CELL; EPITHELIUM CELL; EUKARYOTIC FLAGELLUM; GOBLET CELL; HUMAN; LUNG ALVEOLUS; LUNG DEVELOPMENT; LUNG DISEASE; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYSTEM; STEM CELL; TRACHEA;

AIRWAY REMODELING; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; EPITHELIAL CELLS; HOMEOSTASIS; HUMANS; LUNG; LUNG DISEASES; ORGANOGENESIS; RESPIRATORY SYSTEM; STEM CELLS; WOUND HEALING;

VERTEBRATA;

EID: 80054030182     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-100109-104040     Document Type: Article

References (119)

1. Adamson IY, Bowden DH. 1975. Derivation of type 1 epithelium from type 2 cells in the developing rat lung. Lab. Investig. 32:736-45
2. Amy RW, Bowes D, Burri PH, Haines J, ThurlbeckWM. 1977. Postnatal growth of the mouse lung. J. Anat. 124:131-51 (Pubitemid 8187543)
3. Barker N, Van Es JH, Kuipers J, Kujala P, Van Den Born M, et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003-7 (Pubitemid 350014593)
4. Boers JE, Ambergen AW, Thunnissen FB. 1998. Number and proliferation of basal and parabasal cells in normal human airway epithelium. Am. J. Respir. Crit. Care Med. 157:2000-6
5. Bonniaud P, Kolb M, Galt T, Robertson J, Robbins C, et al. 2004. Smad3 null mice develop airspace enlargement and are resistant to TGF-β-mediated pulmonary fibrosis. J. Immunol. 173:2099-108 (Pubitemid 38971648)
6. Borges M, Linnoila RI, Van de Velde HJ, Chen H, Nelkin BD, et al. 1997. An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 386:852-55 (Pubitemid 27181261)
7. Borthwick DW, Shahbazian M, Krantz QT, Dorin JR, Randell SH. 2001. Evidence for stem-cell niches in the tracheal epithelium. Am. J. Respir. Cell Mol. Biol. 24:662-70 (Pubitemid 32550587)
8. Bove PF, Grubb BR, Okada SF, Ribeiro CM, Rogers TD, et al. 2010. Human alveolar type II cells secrete and absorb liquid in response to local nucleotide signaling. J. Biol. Chem. 285:34939-49
9. Breuer R, Zajicek G, Christensen TG, Lucey EC, Snider GL. 1990. Cell kinetics of normal adult hamster bronchial epithelium in the steady state. Am. J. Respir. Cell Mol. Biol. 2:51-58
10. Brody SL, Yan XH, Wuerffel MK, Song SK, Shapiro SD. 2000. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 23:45-51 (Pubitemid 30597094)
11. Burns AR, Smith CW, Walker DC. 2003. Unique structural features that influence neutrophil emigration into the lung. Physiol. Rev. 83:309-36 (Pubitemid 36378675)
12. Cardoso WV, KottonDN. 2008. Specification and patterning of the respiratory system. In StemBook, ed. Stem Cell Res. Community. Cambridge, MA: Harvard Stem Cell Inst. http://www. stembook. org/node/458.
13. Cardoso WV, Lu J. 2006. Regulation of early lung morphogenesis: questions, facts and controversies. Development 133:1611-24 (Pubitemid 43810969)
14. Chen G, Korfhagen TR, Xu Y, Kitzmiller J, Wert SE, et al. 2009. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J. Clin. Investig. 119:2914-24
15. Chen J, Knowles HJ, Hebert JL, Hackett BP. 1998. Mutation of themouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J. Clin. Investig. 102:1077-82 (Pubitemid 28436267)
16. Chiba S. 2006. Notch signaling in stem cell systems. Stem Cells 24:2437-47 (Pubitemid 44674304)
17. Chilosi M, Poletti V, Murer B, Lestani M, Cancellieri A, et al. 2002. Abnormal re-epithelialization and lung remodeling in idiopathic pulmonary fibrosis: the role of N-p63. Lab. Investig. 82:1335-45 (Pubitemid 35191537)
18. Christie JD, Edwards LB, Aurora P, Dobbels F, Kirk R, et al. 2008. Registry of the International Society for Heart and Lung Transplantation: twenty-fifth official adult lung and heart/lung transplantation report-2008. J. Heart Lung Transplant. 27:957-69
19. Coalson JJ. 2006. Pathology of bronchopulmonary dysplasia. Semin. Perinatol. 30:179-84 (Pubitemid 44062675)
20. Cole BB, Smith RW, Jenkins KM, Graham BB, Reynolds PR, Reynolds SD. 2010. Tracheal basal cells: a facultative progenitor cell pool. Am. J. Pathol. 177:362-76
21. Crum CP, McKeon FD. 2010. p63 in epithelial survival, germ cell surveillance, and neoplasia. Annu. Rev. Pathol. 5:349-71
22. Dang TP, Eichenberger S, Gonzalez A, Olson S, CarboneDP. 2003. Constitutive activation ofNotch3 inhibits terminal epithelial differentiation in lungs of transgenic mice. Oncogene 22:1988-97 (Pubitemid 36523636)
23. Daniely Y, Liao G, Dixon D, Linnoila RI, Lori A, et al. 2004. Critical role of p63 in the development of a normal esophageal and tracheobronchial epithelium. Am. J. Physiol. Cell Physiol. 287:C171-81
24. Das RM. 1984. The effects of intermittent starvation on lung development in suckling rats. Am. J. Pathol. 117:326-32 (Pubitemid 15209046)
25. Engelhardt JF, Schlossberg H, Yankaskas JR, Dudus L. 1995. Progenitor cells of the adult human airway involved in submucosal gland development. Development 121:2031-46
26. Evans CM, Williams OW, Tuvim MJ, Nigam R, Mixides GP, et al. 2004. Mucin is produced by Clara cells in the proximal airways of antigen-challenged mice. Am. J. Respir. Cell Mol. Biol. 31:382-94 (Pubitemid 39330948)
27. Evans MJ, Cabral LJ, Stephens RJ, Freeman G. 1973. Renewal of alveolar epithelium in the rat following exposure to NO2. Am. J. Pathol. 70:175-98
28. 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
29. Evans MJ, Shami SG, Cabral-Anderson LJ, Dekker NP. 1986. Role of nonciliated cells in renewal of the bronchial epithelium of rats exposed to NO2. Am. J. Pathol. 123:126-33 (Pubitemid 16038141)
30. Evans MJ, Van Winkle LS, Fanucchi MV, Plopper CG. 2001. Cellular and molecular characteristics of basal cells in airway epithelium. Exp. Lung Res. 27:401-15 (Pubitemid 32641827)
31. Gharaee-Kermani M, Ullenbruch M, Phan SH. 2005. Animal models of pulmonary fibrosis. Methods Mol. Med. 117:251-59
32. Guseh JS, Bores SA, Stanger BZ, Zhou Q, Anderson WJ, et al. 2009. Notch signaling promotes airwaymucous metaplasia and inhibits alveolar development. Development 136:1751-59
33. Hackett TL, Shaheen F, Johnson A, Wadsworth S, Pechkovsky DV, et al. 2008. Characterization of side population cells from human airway epithelium. Stem Cells 26:2576-85
34. Homer RJ, Zhu Z, Cohn L, Lee CG, White WI, et al. 2006. Differential expression of chitinases identify subsets of murine airway epithelial cells in allergic inflammation. Am. J. Physiol. Lung Cell Mol. Physiol. 291:L502-11. (Pubitemid 44343728)
35. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. 2004a. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am. J. Pathol. 164:577-88 (Pubitemid 38364673)
36. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. 2004b. In vivo differentiation potential of tracheal basal cells: evidence for multipotent and unipotent subpopulations. Am. J. Physiol. Lung Cell Mol. Physiol. 286:L643-49. (Pubitemid 38365046)
37. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, et al. 2010. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 176:85-97
38. Ito T, Udaka N, Okudela K, Yazawa T, Kitamura H. 2003. Mechanisms of neuroendocrine differentiation in pulmonary neuroendocrine cells and small cell carcinoma. Endocr. Pathol. 14:133-39 (Pubitemid 38147005)
39. Ito T, Udaka N, Yazawa T, Okudela K, Hayashi H, et al. 2000. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127:3913-21
40. Jones PH. 2010. Stem cell fate in proliferating tissues: equal odds in a game of chance. Dev. Cell 19:489-90
41. Kajstura J, Rota M, Hall SR, Hosoda T, D'Amario D, et al. 2011. Evidence for human lung stem cells. New Engl. J. Med. 364:1795-806
42. Kapanci Y, Ribaux C, Chaponnier C, Gabbiani G. 1992. Cytoskeletal features of alveolar myofibroblasts and pericytes in normal human and rat lung. J. Histochem. Cytochem. 40:1955-63
43. Kauffman SL. 1980. Cell proliferation in the mammalian lung. Int. Rev. Exp. Pathol. 22:131-91 (Pubitemid 12152687)
44. Kauffman SL, Burri PH, Weibel ER. 1974. The postnatal growth of the rat lung. II. Autoradiography. Anat. Rec. 180:63-76
45. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, et al. 2005. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121:823-35 (Pubitemid 40806415)
46. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, et al. 2006. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc. Natl. Acad. Sci. USA 103:13180-85 (Pubitemid 44338936)
47. Knox SM, Lombaert IM, Reed X, Vitale-Cross L, Gutkind JS, Hoffman MP. 2010. Parasympathetic innervation maintains epithelial progenitor cells during salivary organogenesis. Science 329:1645-47
48. Kwinta P, Pietrzyk JJ. 2010. Preterm birth and respiratory disease in later life. Expert Rev. Respir. Med. 4:593-604
49. Langston C, Kida K, Reed M, ThurlbeckWM. 1984. Human lung growth in late gestation and in the neonate. Am. Rev. Respir. Dis. 129:607-13 (Pubitemid 14126782)
50. Lindahl P, Karlsson L, Hellstrom M, Gebre-Medhin S, Willetts K, et al. 1997. Alveogenesis failure in PDGFA-deficient mice is coupled to lack of distal spreading of alveolar smooth muscle cell progenitors during lung development. Development 124:3943-53 (Pubitemid 27483322)
51. Liu JY, Nettesheim P, Randell SH. 1994. Growth and differentiation of tracheal epithelial progenitor cells. Am. J. Physiol. 266:L296-307.
52. Liu Y, Hogan BL. 2002. Differential gene expression in the distal tip endoderm of the embryonic mouse lung. Gene Expr. Patterns 2:229-33 (Pubitemid 36356056)
53. Livraghi A, Grubb BR, Hudson EJ, Wilkinson KJ, Sheehan JK, et al. 2009. Airway and lung pathology due to mucosal surface dehydration in β-epithelial Na+ channel-overexpressing mice: role of TNF-α and IL-4Rα signaling, influence of neonatal development, and limited efficacy of glucocorticoid treatment. J. Immunol. 182:4357-67
54. Lloyd C, Yu QC, Cheng J, Turksen K, Degenstein L, et al. 1995. The basal keratin network of stratified squamous epithelia: defining K15 function in the absence of K14. J. Cell Biol. 129:1329-44
55. Lum S, Kirkby J, Welsh L, Marlow N, Hennessy E, Stocks J. 2011. Nature and severity of lung function abnormalities in extremely pre-term children at 11 years of age. Eur. Respir. J. 37:1199-207
56. Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE, et al. 2008. Clinical transplantation of a tissueengineered airway. Lancet 372:2023-30
57. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC. 2004. Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat. Med. 10:487-93 (Pubitemid 38667907)
58. Massaro GD, McCoy L, Massaro D. 1988. Postnatal undernutrition slows development of bronchiolar epithelium in rats. Am. J. Physiol. 255:R521-26
59. McDowell EM, Newkirk C, Coleman B. 1985. Development of hamster tracheal epithelium: II. Cell proliferation in the fetus. Anat. Rec. 213:448-56 (Pubitemid 16224228)
60. 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 107:1414-19
61. Meltzer EB, Noble PW. 2008. Idiopathic pulmonary fibrosis. Orphanet. J. Rare Dis. 3:8.
62. Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, et al. 1994. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120:2749-71
63. Metzger RJ, Klein OD, Martin GR, Krasnow MA. 2008. The branching programme of mouse lung development. Nature 453:745-50 (Pubitemid 351793786)
64. Minoo P, Su G, Drum H, Bringas P, Kimura S. 1999. Defects in tracheoesophageal and lung morphogenesis in Nkx2. 1(-/-) mouse embryos. Dev. Biol. 209:60-71 (Pubitemid 29194313)
65. Monaghan AP, Kaestner KH, Grau E, Schutz G. 1993. Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 α, β and γ genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm. Development 119:567-78 (Pubitemid 23337404)
66. Montgomery RK, Shivdasani RA. 2009. Prominin1 (CD133) as an intestinal stem cell marker: promise and nuance. Gastroenterology 136:2051-54
67. Morimoto M, Liu Z, Cheng HT, Winters N, Bader D, Kopan R. 2010. Canonical Notch signaling in the developing lung is required for determination of arterial smoothmuscle cells and selection of Clara versus ciliated cell fate. J. Cell Sci. 123:213-24
68. Morrisey EE, Hogan BL. 2010. Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev. Cell 18:8-23
69. Ng CY, Madsen JC, Rosengard BR, Allan JS. 2009. Immunosuppression for lung transplantation. Front. Biosci. 14:1627-41
70. Ott HC, Clippinger B, Conrad C, Schuetz C, Pomerantseva I, et al. 2010. Regeneration and orthotopic transplantation of a bioartificial lung. Nat. Med. 16:927-33
71. Pardo A, SelmanM. 2002. Idiopathic pulmonary fibrosis: new insights in its pathogenesis. Int. J. Biochem. Cell Biol. 34:1534-38
72. Park SW, Verhaeghe C, Nguyenvu LT, Barbeau R, Eisley CJ, et al. 2009. Distinct roles of FOXA2 and FOXA3 in allergic airway disease and asthma. Am. J. Respir. Crit. CareMed. 180:603-10
73. Perl AK, Kist R, Shan Z, Scherer G, Whitsett JA. 2005. Normal lung development and function after Sox9 inactivation in the respiratory epithelium. Genesis 41:23-32 (Pubitemid 40269719)
74. Perl AK, Riethmacher D, Whitsett JA. 2011. Conditional depletion of airway progenitor cells induces peribronchiolar fibrosis. Am. J. Respir. Crit. CareMed. 183:511-21
75. Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L, et al. 2010. Tissue-engineered lungs for in vivo implantation. Science 329:538-41
76. Post LC, Ternet M, Hogan BL. 2000. Notch/Delta expression in the developing mouse lung. Mech. Dev. 98:95-98
77. Que J, Choi M, Ziel JW, Klingensmith J, Hogan BL. 2006. Morphogenesis of the trachea and esophagus: current players and new roles for noggin and Bmps. Differentiation 74:422-37 (Pubitemid 44215412)
78. Que J, Luo X, Schwartz RJ, Hogan BL. 2009. Multiple roles for Sox2 in the developing and adult mouse trachea. Development 136:1899-907
79. Que J, Okubo T, Goldenring JR, Nam KT, Kurotani R, et al. 2007. Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development 134:2521-31 (Pubitemid 47074146)
80. Randell SH. 2006. Airway epithelial stem cells and the pathophysiology of chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 3:718-25 (Pubitemid 44788231)
81. Randell SH, Comment CE, Ramaekers FC, Nettesheim P. 1991. Properties of rat tracheal epithelial cells separated based on expression of cell surface α-galactosyl end groups. Am. J. Respir. Cell Mol. Biol. 4:544-54
82. Rawlins EL. 2008. Lung epithelial progenitor cells: lessons from development. Proc. Am. Thorac. Soc. 5:675-81
83. Rawlins EL, Clark CP, Xue Y, Hogan BL. 2009a. The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 136:3741-45
84. Rawlins EL, Hogan BL. 2006, Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133:2455-65 (Pubitemid 44123396)
85. Rawlins EL, Hogan BL. 2008. Ciliated epithelial cell lifespan in the mouse trachea and lung. Am. J. Physiol. Lung Cell Mol. Physiol. 295:L231-34.
86. Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, et al. 2009b. 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
87. Rawlins EL, Ostrowski LE, Randell SH, Hogan BL. 2007. Lung development and repair: contribution of the ciliated lineage. Proc. Natl. Acad. Sci. USA 104:410-17 (Pubitemid 46123040)
88. Reynolds SD, Giangreco A, Power JH, Stripp BR. 2000. Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am. J. Pathol. 156:269-78 (Pubitemid 30644460)
89. Reynolds SD, Reynolds PR, Pryhuber GS, Finder JD, Stripp BR. 2002. Secretoglobins SCGB3A1 and SCGB3A2 define secretory cell subsets in mouse and human airways. Am. J. Respir. Crit. Care Med. 166:1498-509 (Pubitemid 35387301)
90. Rock JR, Gao X, Xue Y, Randell SH, Kong Y-Y, Hogan BL. 2011. Notch-dependent differentiation of adult airway basal stem cells. Cell Stem Cell 8:639-48
91. Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, et al. 2009. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc. Natl. Acad. Sci. USA 106:12771-75
92. Rock JR, Randell SH, Hogan BL. 2010. Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis. Model. Mech. 3:545-56
93. Roy MG, Rahmani M, Hernandez JR, Alexander SN, Ehre C, et al. 2011. Mucin production during prenatal and postnatal murine lung development. Am. J. Respir. Cell Mol. Biol. 44:755-60
94. Sangiorgi E, Capecchi MR. 2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40:915-20 (Pubitemid 351913652)
95. Schoch KG, Lori A, Burns KA, Eldred T, Olsen JC, Randell SH. 2004. A subset of mouse tracheal epithelial basal cells generates large colonies in vitro. Am. J. Physiol. Lung Cell Mol. Physiol. 286:L631-42. (Pubitemid 38365045)
96. Shan L, Aster JC, Sklar J, Sunday ME. 2007. Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice. Am. J. Physiol. Lung Cell Mol. Physiol. 292:L500-9.
97. Shen MM, Wang X, Economides KD, Walker D, Abate-Shen C. 2008. Progenitor cells for the prostate epithelium: roles in development, regeneration, and cancer. Cold Spring Harb. Symp. Quant. Biol. 73:529-38
98. Sirianni FE, Chu FS, Walker DC. 2003. Human alveolar wall fibroblasts directly link epithelial type 2 cells to capillary endothelium. Am. J. Respir. Crit. Care Med. 168:1532-37 (Pubitemid 38037341)
99. Tesei A, Zoli W, Arienti C, Storci G, Granato AM, et al. 2009. Isolation of stem/progenitor cells from normal lung tissue of adult humans. Cell Prolif. 42:298-308
100. Tilley AE, Harvey BG, Heguy A, Hackett NR, Wang R, et al. 2009. 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. 179:457-66
101. Tompkins DH, Besnard V, Lange AW, Wert SE, Keiser AR, et al. 2009. Sox2 is required for maintenance and differentiation of bronchiolar Clara, ciliated, and goblet cells. PLoS ONE 4:e8248
102. Tsao PN, Chen F, Izvolsky KI, Walker J, Kukuruzinska MA, et al. 2008. γ-secretase activation of Notch signaling regulates the balance of proximal and distal fates in progenitor cells of the developing lung. J. Biol. Chem. 283:29532-44
103. Tsao PN, Vasconcelos M, Izvolsky KI, Qian J, Lu J, CardosoWV. 2009. Notch signaling controls the balance of ciliated and secretory cell fates in developing airways. Development 136:2297-307
104. Uhal BD. 1997. Cell cycle kinetics in the alveolar epithelium. Am. J. Physiol. 272:L1031-45.
105. Van Der Flier LG, Clevers H. 2009. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 71:241-60
106. Van Lommel A. 2001. Pulmonary neuroendocrine cells (PNEC) and neuroepithelial bodies (NEB): chemoreceptors and regulators of lung development. Paediatr. Respir. Rev. 2:171-76 (Pubitemid 32694565)
107. Van Lommel A, Lauweryns JM, Berthoud HR. 1998. Pulmonary neuroepithelial bodies are innervated by vagal afferent nerves: an investigation with in vivo anterograde DiI tracing and confocal microscopy. Anat. Embryol. 197:325-30 (Pubitemid 28156110)
108. Visvader JE, Smith GH. 2011. Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harb. Perspect. Biol. doi:10. 1101/cshperspect. a004879
109. Voynow JA, Fischer BM, Roberts BC, Proia AD. 2005. Basal-like cells constitute the proliferating cell population in cystic fibrosis airways. Am. J. Respir. Crit. CareMed. 172:1013-18
110. Wan H, Kaestner KH, Ang SL, Ikegami M, Finkelman FD, et al. 2004. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development 131:953-64 (Pubitemid 38263209)
111. Watt FM, Jensen KB. 2009. Epidermal stem cell diversity and quiescence. EMBO Mol. Med. 1:260-67
112. Wendel DP, Taylor DG, Albertine KH, Keating MT, Li DY. 2000. Impaired distal airway development in mice lacking elastin. Am. J. Respir. Cell Mol. Biol. 23:320-26
113. Whitsett JA, Wert SE, Weaver TE. 2010. Alveolar surfactant homeostasis and the pathogenesis of pulmonary disease. Annu. Rev. Med. 61:105-19
114. WilliamsMC. 2003. Alveolar type I cells:molecular phenotype and development. Annu. Rev. Physiol. 65:669-95 (Pubitemid 38249172)
115. Williams OW, Sharafkhaneh A, Kim V, Dickey BF, Evans CM. 2006. Airway mucus: from production to secretion. Am. J. Respir. Cell Mol. Biol. 34:527-36
116. Willis BC, duBois RM, Borok Z. 2006. Epithelial origin of myofibroblasts during fibrosis in the lung. Proc. Am. Thorac. Soc. 3:377-82 (Pubitemid 43845416)
117. Wongtrakool C, Malpel S, Gorenstein J, Sedita J, Ramirez MI, et al. 2003. Down-regulation of retinoic acid receptor αsignaling is required for sacculation and type I cell formation in the developing lung. J. Biol. Chem. 278:46911-18 (Pubitemid 37452273)
118. Wright JR. 2005. Immunoregulatory functions of surfactant proteins. Nat. Rev. Immunol. 5:58-68 (Pubitemid 40070331)
119. Yamamoto H, Yun EJ, Gerber HP, Ferrara N, Whitsett JA, Vu TH. 2007. Epithelial-vascular cross talk mediated by VEGF-A andHGF signaling directs primary septae formation during distal lung morphogenesis. Dev. Biol. 308:44-53 (Pubitemid 47087777)