Regenerative activity of the lung after epithelial injury

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 7, 2013, Pages 922-930

  Vaughan, Andrew E ^a   Chapman, Harold A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epithelial mesenchymal transition; Signaling; Stem progenitor cell

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 3; FIBROBLAST GROWTH FACTOR; INTERLEUKIN 6; PLATELET DERIVED GROWTH FACTOR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA1; TRANSCRIPTION FACTOR;

APOPTOSIS; BREAST CELL; CANCER CELL; CELL ACTIVATION; CELL EXPANSION; CELL MOTILITY; CELL RENEWAL; CELL SHAPE; CELL SURVIVAL; CLARA CELL; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL EXPOSURE; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; HUMAN; HYPOXIA; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; LUNG GAS EXCHANGE; LUNG INJURY; MESENCHYME CELL; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; TISSUE REGENERATION; VIRUS INFECTION; ANIMAL; CELL DIFFERENTIATION; LUNG; METABOLISM; STEM CELL;

GASTROPODA;

ANIMALS; CELL DIFFERENTIATION; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; LUNG; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84877012655     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.11.020     Document Type: Review

References (104)

1. Finigan J.H., Downey G.P., Kern J.A. HER receptor signaling in acute lung injury. Am. J. Respir. Cell Mol. Biol. 2012, 47(4):395-404.
2. Konigshoff M., Eickelberg O. WNT signaling in lung disease: a failure or a regeneration signal?. Am. J. Respir. Cell Mol. Biol. 2010, 42:21-31.
3. Xu K., Moghal N., Egan S.E. Notch signaling in lung development and disease. Adv. Exp. Med. Biol. 2012, 727:89-98.
4. Morrisey E.E. Wnt signaling and pulmonary fibrosis. Am. J. Pathol. 2003, 162:1393-1397.
5. Gribar S.C., Richardson W.M., Sodhi C.P., Hackam D.J. No longer an innocent bystander: epithelial toll-like receptor signaling in the development of mucosal inflammation. Mol. Med. 2008, 14:645-659.
6. Chambers R.C. Procoagulant signalling mechanisms in lung inflammation and fibrosis: novel opportunities for pharmacological intervention?. Br. J. Pharmacol. 2008, 153(Suppl. 1):S367-S378.
7. 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.
8. Selman M., Pardo A. Role of epithelial cells in idiopathic pulmonary fibrosis: from innocent targets to serial killers. Proc. Am. Thorac. Soc. 2006, 3:364-372.
9. Tam A., Wadsworth S., Dorscheid D., Man S.F., Sin D.D. The airway epithelium: more than just a structural barrier. Ther. Adv. Respir. Dis. 2011, 5(4):255-273.
10. Islam S.A., Luster A.D. T cell homing to epithelial barriers in allergic disease. Nat. Med. 2012, 18:705-715.
11. Parker D., Prince A. Innate immunity in the respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 2011, 45:189-201.
12. Locksley R.M. Asthma and allergic inflammation. Cell 2010, 140:777-783.
13. Shetty S., Padijnayayveetil J., Tucker T., Stankowska D., Idell S. The fibrinolytic system and the regulation of lung epithelial cell proteolysis, signaling, and cellular viability. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295:L967-L975.
14. Beers M.F., Morrisey E.E. The three R's of lung health and disease: repair, remodeling, and regeneration. J. Clin. Invest. 2011, 121:2065-2073.
15. Crosby L.M., Waters C.M. Epithelial repair mechanisms in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 298:L715-L731.
16. Borok Z., Whitsett J.A., Bitterman P.B., Thannickal V.J., Kotton D.N., Reynolds S.D., Krasnow M.A., Bianchi D.W., Morrisey E.E., Hogan B.L., Kurie J.M., Walker D.C., Radisky D.C., Nishimura S.L., Violette S.M., Noble P.W., Shapiro S.D., Blaisdell C.J., Chapman H.A., Kiley J., Gail D., Hoshizaki D. Cell plasticity in lung injury and repair: report from an NHLBI workshop, April 19-20. Proc. Am. Thorac. Soc. 2010, 8:215-222.
17. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
18. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
19. Greenburg G., Hay E.D. Epithelia suspended in collagen gels can lose polarity and express characteristics of migrating mesenchymal cells. J. Cell Biol. 1982, 95:333-339.
20. Ip Y.T., Gridley T. Cell movements during gastrulation: snail dependent and independent pathways. Curr. Opin. Genet. Dev. 2002, 12:423-429.
21. Boulay J.L., Dennefeld C., Alberga A. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 1987, 330:395-398.
22. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
23. Chen Z.F., Behringer R.R. Twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev. 1995, 9:686-699.
24. Nieto M.A. Epithelial-mesenchymal transitions in development and disease: old views and new perspectives. Int. J. Dev. Biol. 2009, 53:1541-1547.
25. 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, 121:4409-4419.
26. Yamaguchi T.P., Harpal K., Henkemeyer M., Rossant J. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 1994, 8:3032-3044.
27. Zhou L., Dey C.R., Wert S.E., Whitsett J.A. Arrested lung morphogenesis in transgenic mice bearing an SP-C-TGF-beta 1 chimeric gene. Dev. Biol. 1996, 175:227-238.
28. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000, 2:84-89.
29. Blanco M.J., Moreno-Bueno G., Sarrio D., Locascio A., Cano A., Palacios J., Nieto M.A. Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 2002, 21:3241-3246.
30. Cheng C.W., Wu P.E., Yu J.C., Huang C.S., Yue C.T., Wu C.W., Shen C.Y. Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 2001, 20:3814-3823.
31. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat. Rev. Cancer 2007, 7:415-428.
32. Blechschmidt K., Sassen S., Schmalfeldt B., Schuster T., Hofler H., Becker K.F. The E-cadherin repressor Snail is associated with lower overall survival of ovarian cancer patients. Br. J. Cancer 2008, 98:489-495.
33. Shih J.Y., Tsai M.F., Chang T.H., Chang Y.L., Yuan A., Yu C.J., Lin S.B., Liou G.Y., Lee M.L., Chen J.J., Hong T.M., Yang S.C., Su J.L., Lee Y.C., Yang P.C. Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin. Cancer Res. 2005, 11:8070-8078.
34. Shih J.Y., Yang P.C. The EMT regulator slug and lung carcinogenesis. Carcinogenesis 2011, 32:1299-1304.
35. Martin T.A., Goyal A., Watkins G., Jiang W.G. Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann. Surg. Oncol. 2005, 12:488-496.
36. Guarino M., Rubino B., Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007, 39:305-318.
37. M.H. Chui, Insights into cancer metastasis from a clinicopathologic perspective: epithelial mesenchymal transition is not a necessary step, Int. J. Cancer (in press).
38. Tarin D., Thompson E.W., Newgreen D.F. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res. 2005, 65:5996-6000. (discussion 6000-5991).
39. Biddle A., Mackenzie I.C. Cancer stem cells and EMT in carcinoma. Cancer Metastasis Rev. 2012.
40. de Herreros A.G., Peiro S., Nassour M., Savagner P. Snail family regulation and epithelial mesenchymal transitions in breast cancer progression. J. Mammary Gland Biol. Neoplasia 2010, 15:135-147.
41. Egeblad M., Nakasone E.S., Werb Z. Tumors as organs: complex tissues that interface with the entire organism. Dev. Cell 2010, 18:884-901.
42. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., Yamauchi M., Gasser D.L., Weaver V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
43. Eckert M.A., Lwin T.M., Chang A.T., Kim J., Danis E., Ohno-Machado L., Yang J. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 2011, 19:372-386.
44. Ansieau S., Bastid J., Doreau A., Morel A.P., Bouchet B.P., Thomas C., Fauvet F., Puisieux I., Doglioni C., Piccinin S., Maestro R., Voeltzel T., Selmi A., Valsesia-Wittmann S., Caron de Fromentel C., Puisieux A. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008, 14:79-89.
45. Franco D.L., Mainez J., Vega S., Sancho P., Murillo M.M., de Frutos C.A., Del Castillo G., Lopez-Blau C., Fabregat I., Nieto M.A. Snail1 suppresses TGF-beta-induced apoptosis and is sufficient to trigger EMT in hepatocytes. J. Cell Sci. 2010, 123:3467-3477.
46. Gal A., Sjoblom T., Fedorova L., Imreh S., Beug H., Moustakas A. Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 2008, 27:1218-1230.
47. Tanjore H., Blackwell T.S., Lawson W.E. Emerging evidence for endoplasmic reticulum stress in the pathogenesis of idiopathic pulmonary fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 302:L721-L729.
48. Zhong Q., Zhou B., Ann D.K., Minoo P., Liu Y., Banfalvi A., Krishnaveni M.S., Dubourd M., Demaio L., Willis B.C., Kim K.J., Dubois R.M., Crandall E.D., Beers M.F., Borok Z. Role of endoplasmic reticulum stress in epithelial-mesenchymal transition of alveolar epithelial cells: effects of misfolded surfactant protein. Am. J. Respir. Cell Mol. Biol. 2011, 45:498-509.
49. Lawson W.E., Cheng D.S., Degryse A.L., Tanjore H., Polosukhin V.V., Xu X.C., Newcomb D.C., Jones B.R., Roldan J., Lane K.B., Morrisey E.E., Beers M.F., Yull F.E., Blackwell T.S. Endoplasmic reticulum stress enhances fibrotic remodeling in the lungs. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10562-10567.
50. Bridges R.S., Kass D., Loh K., Glackin C., Borczuk A.C., Greenberg S. Gene expression profiling of pulmonary fibrosis identifies Twist1 as an antiapoptotic molecular "rectifier" of growth factor signaling. Am. J. Pathol. 2009, 175:2351-2361.
51. Pozharskaya V., Torres-Gonzalez E., Rojas M., Gal A., Amin M., Dollard S., Roman J., Stecenko A.A., Mora A.L. Twist: a regulator of epithelial-mesenchymal transition in lung fibrosis. PLoS One 2009, 4:e7559.
52. Jayachandran A., Konigshoff M., Yu H., Rupniewska E., Hecker M., Klepetko W., Seeger W., Eickelberg O. SNAI transcription factors mediate epithelial-mesenchymal transition in lung fibrosis. Thorax 2009, 64:1053-1061.
53. Puchelle E., Zahm J.M., Tournier J.M., Coraux C. Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 2006, 3:726-733.
54. Giangreco A., Lu L., Vickers C., Teixeira V.H., Groot K.R., Butler C.R., Ilieva E.V., George P.J., Nicholson A.G., Sage E.K., Watt F.M., Janes S.M. beta-Catenin determines upper airway progenitor cell fate and preinvasive squamous lung cancer progression by modulating epithelial-mesenchymal transition. J. Pathol. 2012, 226:575-587.
55. Hudson L.G., Choi C., Newkirk K.M., Parkhani J., Cooper K.L., Lu P., Kusewitt D.F. Ultraviolet radiation stimulates expression of Snail family transcription factors in keratinocytes. Mol. Carcinog. 2007, 46:257-268.
56. Savagner P., Kusewitt D.F., Carver E.A., Magnino F., Choi C., Gridley T., Hudson L.G. Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes. J. Cell. Physiol. 2005, 202:858-866.
57. Kim K.K., Kugler M.C., Wolters P.J., Robillard L., Galvez M.G., Brumwell A.N., Sheppard D., Chapman H.A. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13180-13185.
58. Zeisberg M., Yang C., Martino M., Duncan M.B., Rieder F., Tanjore H., Kalluri R. Fibroblasts derive from hepatocytes in liver fibrosis via epithelial to mesenchymal transition. J. Biol. Chem. 2007, 282:23337-23347.
59. Tanjore H., Xu X.C., Polosukhin V.V., Degryse A.L., Li B., Han W., Sherrill T.P., Plieth D., Neilson E.G., Blackwell T.S., Lawson W.E. Contribution of epithelial-derived fibroblasts to bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 2009, 180:657-665.
60. Kalluri R., Neilson E.G. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 2003, 112:1776-1784.
61. Iwaisako K., Brenner D.A., Kisseleva T. What's new in liver fibrosis? The origin of myofibroblasts in liver fibrosis. J. Gastroenterol. Hepatol. 2012, 27(Suppl. 2):65-68.
62. Humphreys B.D., Lin S.L., Kobayashi A., Hudson T.E., Nowlin B.T., Bonventre J.V., Valerius M.T., McMahon A.P., Duffield J.S. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 2010, 176:85-97.
63. Hardie W.D., Hagood J.S., Dave V., Perl A.K., Whitsett J.A., Korfhagen T.R., Glasser S. Signaling pathways in the epithelial origins of pulmonary fibrosis. Cell Cycle 2010, 9:2769-2776.
64. Rock J.R., Barkauskas C.E., Cronce M.J., Xue Y., Harris J.R., Liang J., Noble P.W., Hogan B.L. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:E1475-E1483.
65. Kim K.K., Wei Y., Szekeres C., Kugler M.C., Wolters P.J., Hill M.L., Frank J.A., Brumwell A.N., Wheeler S.E., Kreidberg J.A., Chapman H.A. Epithelial cell alpha3beta1 integrin links beta-catenin and Smad signaling to promote myofibroblast formation and pulmonary fibrosis. J. Clin. Invest. 2009, 119:213-224.
66. Willis B.C., Liebler J.M., Luby-Phelps K., Nicholson A.G., Crandall E.D., du Bois R.M., Borok Z. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am. J. Pathol. 2005, 166:1321-1332.
67. Marmai C., Sutherland R.E., Kim K.K., Dolganov G.M., Fang X., Kim S.S., Jiang S., Golden J.A., Hoopes C.W., Matthay M.A., Chapman H.A., Wolters P.J. Alveolar epithelial cells express mesenchymal proteins in patients with idiopathic pulmonary fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 301:L71-L78.
68. Morbini P., Inghilleri S., Campo I., Oggionni T., Zorzetto M., Luisetti M. Incomplete expression of epithelial-mesenchymal transition markers in idiopathic pulmonary fibrosis. Pathol. Res. Pract. 2011, 207:559-567.
69. Rowe R.G., Lin Y., Shimizu-Hirota R., Hanada S., Neilson E.G., Greenson J.K., Weiss S.J. Hepatocyte-derived Snail1 propagates liver fibrosis progression. Mol. Cell. Biol. 2011, 31:2392-2403.
70. Kim Y., Kugler M.C., Wei Y., Kim K.K., Li X., Brumwell A.N., Chapman H.A. Integrin alpha3beta1-dependent beta-catenin phosphorylation links epithelial Smad signaling to cell contacts. J. Cell Biol. 2009, 184:309-322.
71. Sugimoto H., LeBleu V.S., Bosukonda D., Keck P., Taduri G., Bechtel W., Okada H., Carlson W., Bey P., Rusckowski M., Tampe B., Tampe D., Kanasaki K., Zeisberg M., Kalluri R. Activin-like kinase 3 is important for kidney regeneration and reversal of fibrosis. Nat. Med. 2012, 18:396-404.
72. Miettinen P.J., Ebner R., Lopez A.R., Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 1994, 127:2021-2036.
73. Feng X.H., Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21:659-693.
74. Chapman H.A. Epithelial-mesenchymal interactions in pulmonary fibrosis. Annu. Rev. Physiol. 2010, 73:413-435.
75. Radisky D.C., Levy D.D., Littlepage L.E., Liu H., Nelson C.M., Fata J.E., Leake D., Godden E.L., Albertson D.G., Nieto M.A., Werb Z., Bissell M.J. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005, 436:123-127.
76. Yang M.H., Wu M.Z., Chiou S.H., Chen P.M., Chang S.Y., Liu C.J., Teng S.C., Wu K.J. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 2008, 10:295-305.
77. Lu X., Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin. Cancer Res. 2010, 16:5928-5935.
78. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008, 10:593-601.
79. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008, 22:894-907.
80. Vettori S., Gay S., Distler O. Role of MicroRNAs in fibrosis. Open Rheumatol. J. 2012, 6:130-139.
81. Xiao J., Meng X.M., Huang X.R., Chung A.C., Feng Y.L., Hui D.S., Yu C.M., Sung J.J., Lan H.Y. miR-29 inhibits bleomycin-induced pulmonary fibrosis in mice. Mol. Ther. 2012, 20:1251-1260.
82. Tanjore H., Cheng D.S., Degryse A.L., Zoz D.F., Abdolrasulnia R., Lawson W.E., Blackwell T.S. Alveolar epithelial cells undergo epithelial-to-mesenchymal transition in response to endoplasmic reticulum stress. J. Biol. Chem. 2011, 286:30972-30980.
83. Lawson W.E., Polosukhin V.V., Stathopoulos G.T., Zoia O., Han W., Lane K.B., Li B., Donnelly E.F., Holburn G.E., Lewis K.G., Collins R.D., Hull W.M., Glasser S.W., Whitsett J.A., Blackwell T.S. Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin. Am. J. Pathol. 2005, 167:1267-1277.
84. Guo W., Keckesova Z., Donaher J.L., Shibue T., Tischler V., Reinhardt F., Itzkovitz S., Noske A., Zurrer-Hardi U., Bell G., Tam W.L., Mani S.A., van Oudenaarden A., Weinberg R.A. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012, 148:1015-1028.
85. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., Campbell L.L., Polyak K., Brisken C., Yang J., Weinberg R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
86. Biddle A., Liang X., Gammon L., Fazil B., Harper L.J., Emich H., Costea D.E., Mackenzie I.C. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res. 2011, 71:5317-5326.
87. Newkirk K.M., Duncan F.J., Brannick E.M., Chandler H.L., Parent A.E., Kusewitt D.F. The acute cutaneous inflammatory response is attenuated in Slug-knockout mice. Lab. Invest. 2008, 88:831-841.
88. Hotz B., Visekruna A., Buhr H.J., Hotz H.G. Beyond epithelial to mesenchymal transition: a novel role for the transcription factor Snail in inflammation and wound healing. J. Gastrointest. Surg. 2010, 14:388-397.
89. Shi M., Zhu J., Wang R., Chen X., Mi L., Walz T., Springer T.A. Latent TGF-beta structure and activation. Nature 2011, 474:343-349.
90. Homma S., Nagaoka I., Abe H., Takahashi K., Seyama K., Nukiwa T., Kira S. Localization of platelet-derived growth factor and insulin-like growth factor I in the fibrotic lung. Am. J. Respir. Crit. Care Med. 1995, 152:2084-2089.
91. Rock J.R., Randell S.H., Hogan B.L. Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling. Dis. Model. Mech. 2010, 3:545-556.
92. 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.
93. Kotton D.N. Next-generation regeneration: the hope and hype of lung stem cell research. Am. J. Respir. Crit. Care Med. 2012, 185:1255-1260.
94. Kajstura J., Rota M., Hall S.R., Hosoda T., D'Amario D., Sanada F., Zheng H., Ogórek B., Rondon-Clavo C., Ferreira-Martins J., Matsuda A., Arranto C., Goichberg P., Giordano G., Haley K.J., Bardelli S., Rayatzadeh H., Liu X., Quaini F., Liao R., Leri A., Perrella M.A., Loscalzo J., Anversa P. Evidence for human lung stem cells. N. Engl. J. Med. 2011, 364:1795-1806.
95. 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, 22:142-150.
96. Evans M.J., Johnson L., Stephens R.J., Freeman G. Renewal of the terminal bronchiolar epithelium in the rat following exposure to NO2 or O3. Lab. Invest. 1976, 246-257.
97. Reynolds S.D., Giangreco A., Power J.H.T., Stripp B.R. Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am. J. Pathol. 2000, 156:269-278.
98. Kim C.F.B., Jackson E.L., Woolfenden A.E., Lawrence S., Babar I., Vogel S., Crowley D., Bronson R.T., Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005, 121:823-835.
99. Rawlins E.L., Okubo T., Xue Y., Brass D.M., Auten R.L., Hasegawa H., Wang F., Hogan B.L.M. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 2009, 4:525-534.
100. Chapman H.A., Li X., Alexander J.P., Brumwell A., Lorizio W., Tan K., Sonnenberg A., Wei Y., Vu T.H. Integrin α6β4 identifies an adult distal lung epithelial population with regenerative potential in mice. J. Clin. Invest. 2011, 121:2855-2862.
101. Kumar P.A., Hu Y., Yamamoto Y., Hoe N.B., Wei T.S., Mu D., Sun Y., Joo L.S., Dagher R., Zielonka E.M., Wang de Y., Lim B., Chow V.T., Crum C.P., Xian W., McKeon F. Distal airway stem cells yield alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell 2011, 147:525-538.
102. Ding B.S., Nolan D.J., Guo P., Babazadeh A.O., Cao Z., Rosenwaks Z., Crystal R.G., Simons M., Sato T.N., Worgall S., Shido K., Rabbany S.Y., Rafii S. Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell 2011, 147:539-553.
103. Butler J.P., Loring S.H., Patz S., Tsuda A., Yablonskiy D.A., Mentzer S.J. Evidence for adult lung growth in humans. N. Engl. J. Med. 2012, 367:244-247.
104. Seimetz M., Parajuli N., Pichl A., Veit F., Kwapiszewska G., Weisel F.C., Milger K., Egemnazarov B., Turowska A., Fuchs B., Nikam S., Roth M., Sydykov A., Medebach T., Klepetko W., Jaksch P., Dumitrascu R., Garn H., Voswinckel R., Kostin S., Seeger W., Schermuly R.T., Grimminger F., Ghofrani H.A., Weissmann N. Inducible NOS inhibition reverses tobacco-smoke-induced emphysema and pulmonary hypertension in mice. Cell 2011, 147:293-305.