Cell type-specific expression of adenomatous polyposis coli in lung development, injury, and repair

Developmental Dynamics

Volumn 239, Issue 8, 2010, Pages 2288-2297

  Li, Aimin ^a   Xing, Yiming ^a   Chan, Belinda ^a   Heisterkamp, Nora ^b   Groffen, John ^b   Borok, Zea ^a   Minoo, Parviz ^a   Li, Changgong ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

Author keywords

Adenomatous polyposis coli; Airway epithelium; Injury; Lung development; Repair

Indexed keywords

NAPHTHALENE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL CELL; CELL FUNCTION; CELL MIGRATION; CELL SHAPE; CELL TYPE; CELLULAR DISTRIBUTION; CILIATED EPITHELIUM; CLARA CELL; COLON POLYPOSIS; CONTROLLED STUDY; DIFFERENTIAL DISPLAY; IMMUNOREACTIVITY; LUNG DEVELOPMENT; LUNG INJURY; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE; SQUAMOUS CELL METAPLASIA; STEM CELL; TISSUE REPAIR;

ADENOMATOUS POLYPOSIS COLI PROTEIN; GENE EXPRESSION REGULATION; LUNG; LUNG INJURY; NAPHTHALENES; REGENERATION; STEM CELLS; TISSUE DISTRIBUTION; WOUND HEALING;

EID: 77955010878     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22364     Document Type: Article

References (52)

1. Aoki K, Taketo MM. 2007. Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J Cell Sci 120: 3327-3335.
2. Bienz M. 2002. The subcellular destinations of APC proteins. Nat Rev Mol Cell Biol 3:328-338.
3. Buckpitt A, Boland B, Isbell M, Morin D, Shultz M, Baldwin R, Chan K, Karlsson A, Lin C, Taff A, West J, Fanucchi M, Van Winkle L, Plopper C. 2002. Naphthalene-induced respiratory tract toxicity: metabolic mechanisms of toxicity. Drug Metab Rev 34:791-820.
4. Chilosi M, Doglioni C. 2001. Constitutive p63 expression in airway basal cells. A molecular target in diffuse lung diseases. Sarcoidosis Vasc Diffuse Lung Dis 18:23-26.
5. Dikovskaya D, Schiffmann D, Newton IP, Oakley A, Kroboth K, Sansom O, Jamieson TJ, Meniel V, Clarke A, Nathke IS. 2007. Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J Cell Biol 176:183-195.
6. Etienne-Manneville S, Hall A. 2003. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421:753-756.
7. Fanucchi MV, Murphy ME, Buckpitt AR, Philpot RM, Plopper CG. 1997. Pulmonary cytochrome P450 monooxygenase and Clara cell differentiation in mice. Am J Respir Cell Mol Biol 17:302-314.
8. Giangreco A, Arwert EN, Rosewell IR, Snyder J, Watt FM, Stripp BR. 2009. Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci U S A 106: 9286-9291.
9. Groden J, Thliveris A, Samowitz W, Carlson M, Gelbert L, Albertsen H, Joslyn G, Stevens J, Spirio L, Robertson M, et al. 1991. Identification and characterization of the familial adenomatous polyposis coli gene. Cell 66:589-600.
10. Ha NC, Tonozuka T, Stamos JL, Choi HJ, Weis WI. 2004. Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol Cell 15:511-521.
11. Hanson CA, Miller JR. 2005. Non-traditional roles for the Adenomatous Polyposis Coli (APC) tumor suppressor protein. Gene 361:1-12. (Pubitemid 41506930)
12. Harwood AJ. 2001. Regulation of GSK-3: a cellular multiprocessor. Cell 105: 821-824.
13. Hong KU, Reynolds SD, Giangreco A, Hurley CM, Stripp BR. 2001. Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 24:671-681.
14. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. 2004. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 164:577-588.
15. Kida H, Mucenski ML, Thitoff AR, Le Cras TD, Park KS, Ikegami M, Muller W, Whitsett JA. 2008. GP130-STAT3 regulates epithelial cell migration and is required for repair of the bronchiolar epithelium. Am J Pathol 172: 1542-1554.
16. Kroboth K, Newton IP, Kita K, Dikovskaya D, Zumbrunn J, Waterman-Storer CM, Nathke IS. 2007. Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol Biol Cell 18:910-918.
17. Langford KJ, Askham JM, Lee T, Adams M, Morrison EE. 2006a. Examination of actin and microtubule dependent APC localisations in living mammalian cells. BMC Cell Biol 7:3.
18. Langford KJ, Lee T, Askham JM, Morrison EE. 2006b. Adenomatous polyposis coli localization is both cell type and cell context dependent. Cell Motil Cytoskeleton 63:483-492. (Pubitemid 44162637)
19. Lawson GW, Van Winkle LS, Toskala E, Senior RM, Parks WC, Plopper CG. 2002. Mouse strain modulates the role of the ciliated cell in acute tracheobronchial airway injury-distal airways. Am J Pathol 160:315-327. (Pubitemid 34052292)
20. Levesque BM, Zhou S, Shan L, Johnston P, Kong Y, Degan S, Sunday ME. 2007. NPAS1 regulates branching morphogenesis in embryonic lung. Am J Respir Cell Mol Biol 36:427-434.
21. Li M, Li C, Liu YH, Xing Y, Hu L, Borok Z, Kwong KY, Minoo P. 2008. Mesodermal deletion of transforming growth factor-beta receptor II disrupts lung epithelial morphogenesis: cross-talk between TGF-beta and Sonic hedgehog pathways. J Biol Chem 283: 36257-36264.
22. Li C, Li A, Li M, Xing Y, Chen H, Hu L, Tiozzo C, Anderson S, Taketo MM, Minoo P. 2009. Stabilized beta-catenin in lung epithelial cells changes cell fate and leads to tracheal and bronchial polyposis. Dev Biol 334:97-108.
23. Liu MG, Li NP, Wu RL, Ma Y, Hong YZ, Tian D, Zhu M. 2006. [Dynamic changes of adenomatous polyposis coli protein and glycogen synthase kinase 3beta in the repair of the injured air-way epithelial cells in smoking mice.]. Sheng Li Xue Bao 58:255-261.
24. McCartney BM, Dierick HA, Kirkpatrick C, Moline MM, Baas A, Peifer M, Bejsovec A. 1999. Drosophila APC2 is a cytoskeletally-associated protein that regulates wingless signaling in the embryonic epidermis. J Cell Biol 146: 1303-1318.
25. Mimori-Kiyosue Y, Shiina N, Tsukita S. 2000. Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J Cell Biol 148:505-518.
26. Miyashiro I, Senda T, Matsumine A, Baeg GH, Kuroda T, Shimano T, Miura S, Noda T, Kobayashi S, Monden M, et al. 1995. Subcellular localization of the APC protein: immunoelectron microscopic study of the association of the APC protein with catenin. Oncogene 11: 89-96.
27. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. 1997. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275:1787-1790.
28. Munemitsu S, Souza B, Muller O, Albert I, Rubinfeld B, Polakis P. 1994. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res 54: 3676-3681.
29. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P. 1995. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A 92:3046-3050.
30. Nathke IS. 2004. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 20:337-366.
31. Nathke IS, Adams CL, Polakis P, Sellin JH, Nelson WJ. 1996. The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J Cell Biol 134:165-179.
32. Oshima M, Oshima H, Kitagawa K, Kobayashi M, Itakura C, Taketo M. 1995. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc Natl Acad Sci U S A 92:4482-4486.
33. Park KS, Wells JM, Zorn AM, Wert SE, Laubach VE, Fernandez LG, Whitsett JA. 2006. Transdifferentiation of ciliated cells during repair of the respiratory epithelium. Am J Respir Cell Mol Biol 34:151-157.
34. Polakis P. 1997. The adenomatous polyposis coli (APC) tumor suppressor. Biochim Biophys Acta 1332:F127-F147.
35. Poulsen TT, Biologist XN, Poulsen HS, Linnoila RI. 2008. Acute damage by naphthalene triggers expression of the neuroendocrine marker PGP9.5 in airway epithelial cells. Toxicol Lett 181:67-74
36. Rawlins EL, Hogan BL. 2006. Epithelial stem cells of the lung: privileged few or opportunities for many? Development 133:2455-2465.
37. Rawlins EL, Ostrowski LE, Randell SH, Hogan BL. 2007. Lung development and repair: contribution of the ciliated lineage. Proc Natl Acad Sci U S A 104: 410-417.
38. Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, Hasegawa H, Wang F, Hogan BL. 2009. The role of Scgb1a1+ Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 4:525-534.
39. Reinacher-Schick A, Gumbiner BM. 2001. Apical membrane localization of the adenomatous polyposis coli tumor suppressor protein and subcellular distribution of the beta-catenin destruction complex in polarized epithelial cells. J Cell Biol 152:491-502.
40. Reynolds SD, Hong KU, Giangreco A, Mango GW, Guron C, Morimoto Y, Stripp BR. 2000. Conditional Clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells. Am J Physiol Lung Cell Mol Physiol 278:L1256-L1263.
41. Rosin-Arbesfeld R, Ihrke G, Bienz M. 2001. Actin-dependent membrane association of the APC tumour suppressor in polarized mammalian epithelial cells. EMBO J 20:5929-5939.
42. Senda T, Miyashiro I, Matsumine A, Baeg GH, Monden T, Kobayashil S, Monden M, Toyoshima K, Akiyama T. 1996. The tumor suppressor protein APC colocalizes with beta-catenin in the colon epithelial cells. Biochem Biophys Res Commun 223:329-334.
43. Senda T, Iizuka-Kogo A, Onouchi T, Shimomura A. 2007. Adenomatous polyposis coli (APC) plays multiple roles in the intestinal and colorectal epithelia. Med Mol Morphol 40:68-81.
44. Singh G, Singh J, Katyal SL, Brown WE, Kramps JA, Paradis IL, Dauber JH, Macpherson TA, Squeglia N. 1988. Identification, cellular localization, isolation, and characterization of human Clara cell-specific 10 KD protein. J Histochem Cytochem 36:73-80.
45. Smith KJ, Johnson KA, Bryan TM, Hill DE, Markowitz S, Willson JK, Paraskeva C, Petersen GM, Hamilton SR, Vogelstein B, et al. 1993. The APC gene product in normal and tumor cells. Proc Natl Acad Sci U S A 90:2846-2850.
46. Strayer M, Savani RC, Gonzales LW, Zaman A, Cui Z, Veszelovszky E, Wood E, Ho YS, Ballard PL. 2002. Human surfactant protein B promoter in transgenic mice: temporal, spatial, and stimulus-responsive regulation. Am J Physiol Lung Cell Mol Physiol 282:L394-L404.
47. Van Winkle LS, Buckpitt AR, Nishio SJ, Isaac JM, Plopper CG. 1995. Cellular response in naphthalene-induced Clara cell injury and bronchiolar epithelial repair in mice. Am J Physiol 269: L800-L818.
48. Wen Y, Eng CH, Schmoranzer J, Cabrera- Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG. 2004. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 6: 820-830.
49. Wong MH, Hermiston ML, Syder AJ, Gordon JI. 1996. Forced expression of the tumor suppressor adenomatosis polyposis coli protein induces disordered cell migration in the intestinal epithelium. Proc Natl Acad Sci U S A 93:9588-9593.
50. Xing Y, Li C, Li A, Sridurongrit S, Tiozzo C, Bellusci S, Borok Z, Kaartinen V, Minoo P. 2010. Signaling via Alk5 controls the ontogeny of lung Clara cells. Development 137:825-833.
51. Yu X, Bienz M. 1999. Ubiquitous expression of a Drosophila adenomatous polyposis coli homolog and its localization in cortical actin caps. Mech Dev 84: 69-73. (Pubitemid 29331654)
52. Zumbrunn J, Kinoshita K, Hyman AA, Nathke IS. 2001. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr Biol 11: 44-49.