Modulation of Wnt signaling is essential for the differentiation of ciliated epithelial cells in human airways

FEBS Letters

Volumn 591, Issue 21, 2017, Pages 3493-3506

  Schmid, Andreas ^a   Sailland, Juliette ^a   Novak, Lisa ^a   Baumlin, Nathalie ^a   Fregien, Nevis ^a   Salathe, Matthias ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

airway epithelium; ciliated cells; Dickkopf; differentiation; Wnt signaling

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; BETA CATENIN; DICKKOPF 1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; SHORT HAIRPIN RNA; DKK1 PROTEIN, HUMAN; GSK3B PROTEIN, HUMAN; INDOLE DERIVATIVE; MALEIMIDE DERIVATIVE; SIGNAL PEPTIDE;

AIRWAY EPITHELIUM CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CILIATED EPITHELIUM CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LETTER; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRACHEA; WESTERN BLOTTING; WNT SIGNALING; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CILIUM; CYTOLOGY; EPITHELIUM CELL; METABOLISM; RESPIRATORY MUCOSA;

CELL DIFFERENTIATION; CELLS, CULTURED; CILIA; EPITHELIAL CELLS; GLYCOGEN SYNTHASE KINASE 3 BETA; HUMANS; INDOLES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALEIMIDES; RESPIRATORY MUCOSA; WNT SIGNALING PATHWAY;

EID: 85033500821     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12851     Document Type: Article

References (75)

1. Polosukhin VV, Manouilova LS, Romberger DJ, Matthews KI, Pirruccello SJ, West W, Daughton DM, Millatmal T, Umino T and Rennard SI (2001) Ultrastructural heterogeneity of the alveolar macrophages from tobacco smokers with chronic bronchitis. Ultrastruct Pathol 25, 5–11.
2. Marinas AE, Ciurea P, Pirici D and Ciurea R (2012) Chronic bronchitis: a retrospective clinicopathologic study of 25 cases. Rom J Morphol Embryol 53, 503–513.
3. Puchelle E, Zahm JM, Tournier JM and Coraux C (2006) Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc Am Thorac Soc 3, 726–733.
4. Randell SH (2006) Airway epithelial stem cells and the pathophysiology of chronicobstructive pulmonary disease. Proc Am Thorac Soc 3, 718–725.
5. Lyons JP, Mueller UW, Ji H, Everett C, Fang X, Hsieh JC, Barth AM and McCrea PD (2004) Wnt-4 activates the canonical beta-catenin-mediated Wnt pathway and binds Frizzled-6 CRD: functional implications of Wnt/beta-catenin activity in kidney epithelial cells. Exp Cell Res 298, 369–387.
6. Vladar EK, Bayly RD, Sangoram AM, Scott MP and Axelrod JD (2012) Microtubules enable the planar cell polarity of airway cilia. Curr Biol 22, 2203–2212.
7. Vladar EK, Nayak JV, Milla CE and Axelrod JD (2016) Airway epithelial homeostasis and planar cell polarity signaling depend on multiciliated cell differentiation. JCI Insight 1, 1–18.
8. Pan J, You Y, Huang T and Brody SL (2007) RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1. J Cell Sci 120, 1868–1876.
9. Park TJ, Mitchell BJ, Abitua PB, Kintner C and Wallingford JB (2008) Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat Genet 40, 871–879.
10. Blatt EN, Yan XH, Wuerffel MK, Hamilos DL and Brody SL (1999) Forkhead transcription factor HFH-4 expression is temporally related to ciliogenesis. Am J Respir Cell Mol Biol 21, 168–176.
11. You Y, Huang T, Richer EJ, Schmidt JE, Zabner J, Borok Z and Brody SL (2004) Role of f-box factor foxj1 in differentiation of ciliated airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 286, L650–L657.
12. Choksi SP, Lauter G, Swoboda P and Roy S (2014) Switching on cilia: transcriptional networks regulating ciliogenesis. Development 141, 1427–1441.
13. Pan JH, Adair-Kirk TL, Patel AC, Huang T, Yozamp NS, Xu J, Reddy EP, Byers DE, Pierce RA, Holtzman MJ et al. (2014) Myb permits multilineage airway epithelial cell differentiation. Stem Cells 32, 3245–3256.
14. Ramsay RG and Gonda TJ (2008) MYB function in normal and cancer cells. Nat Rev Cancer 8, 523–534.
15. Ma L, Quigley I, Omran H and Kintner C (2014) Multicilin drives centriole biogenesis via E2f proteins. Genes Dev 28, 1461–1471.
16. Rawlins EL, Ostrowski LE, Randell SH and Hogan BL (2007) Lung development and repair: contribution of the ciliated lineage. Proc Natl Acad Sci U S A 104, 410–417.
17. Volckaert T and De Langhe SP (2015) Wnt and FGF mediated epithelial-mesenchymal crosstalk during lung development. Dev Dyn 244, 342–366.
18. Moon RT, Kohn AD, De Ferrari GV and Kaykas A (2004) WNT and beta-catenin signalling: diseases and therapies. Nat Rev Genet 5, 691–701.
19. Clevers H and Nusse R (2012) Wnt/beta-catenin signaling and disease. Cell 149, 1192–1205.
20. Konigshoff M (2011) Lung cancer in pulmonary fibrosis: tales of epithelial cell plasticity. Respiration 81, 353–358.
21. Van Scoyk M, Randall J, Sergew A, Williams LM, Tennis M and Winn RA (2008) Wnt signaling pathway and lung disease. Transl Res 151, 175–180.
22. Zhao J, Kim KA and Abo A (2009) Tipping the balance: modulating the Wnt pathway for tissue repair. Trends Biotechnol 27, 131–136.
23. Zhang DL, Gu LJ, Liu L, Wang CY, Sun BS, Li Z and Sung CK (2009) Effect of Wnt signaling pathway on wound healing. Biochem Biophys Res Commun 378, 149–151.
24. Beers MF and Morrisey EE (2011) The three R's of lung health and disease: repair, remodeling, and regeneration. J Clin Investig 121, 2065–2073.
25. Caron A, Xu X and Lin X (2012) Wnt/beta-catenin signaling directly regulates Foxj1 expression and ciliogenesis in zebrafish Kupffer's vesicle. Development 139, 514–524.
26. Walentek P, Beyer T, Thumberger T, Schweickert A and Blum M (2012) ATP4a is required for Wnt-dependent Foxj1 expression and leftward flow in Xenopus left-right development. Cell Rep 1, 516–527.
27. McCauley KB, Hawkins F, Serra M, Thomas DC, Jacob A and Kotton DN (2017) Efficient derivation of functional human airway epithelium from pluripotent stem cells via temporal regulation of Wnt signaling. Cell Stem Cell 20, 844–857.e6.
28. Schulte G and Bryja V (2007) The Frizzled family of unconventional G-protein-coupled receptors. Trends Pharmacol Sci 28, 518–525.
29. Veeman MT, Axelrod JD and Moon RT (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5, 367–377.
30. Kohn AD and Moon RT (2005) Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38, 439–446.
31. Sugimura R and Li L (2010) Noncanonical Wnt signaling in vertebrate development, stem cells, and diseases. Birth Defects Res C Embryo Today 90, 243–256.
32. Glinka A, Wu W, Delius H, Monaghan AP, Blumenstock C and Niehrs C (1998) Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357–362.
33. Mao B, Wu W, Li Y, Hoppe D, Stannek P, Glinka A and Niehrs C (2001) LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411, 321–325.
34. Qin X, Zhang H, Zhou X, Wang C, Zhang H, Zhang X and Ye L (2007) Proliferation and migration mediated by Dkk-1/Wnt/beta-catenin cascade in a model of hepatocellular carcinoma cells. Transl Res 150, 281–294.
35. Bernacki SH, Nelson AL, Abdullah L, Sheehan JK, Harris A, Davis CW and Randell SH (1999) Mucin gene expression during differentiation of human airway epithelia in vitro. Muc4 and muc5b are strongly induced. Am J Respir Cell Mol Biol 20, 595–604.
36. Schmid A, Bai G, Schmid N, Zaccolo M, Ostrowski LE, Conner GE, Fregien N and Salathe M (2006) Real-time analysis of cAMP-mediated regulation of ciliary motility in singleprimary human airway epithelial cells. J Cell Sci 119, 4176–4186.
37. Nlend MC, Bookman RJ, Conner GE and Salathe M (2002) Regulator of G-protein signaling protein 2 modulates purinergic calcium and ciliary beat frequency responses in airway epithelia. Am J Respir Cell Mol Biol 27, 436–445.
38. Sutto Z, Conner GE and Salathe M (2004) Regulation of human airway ciliary beat frequency by intracellular pH. J Physiol 560, 519–532.
39. Schmid A, Sutto Z, Schmid N, Novak L, Ivonnet P, Horvath G, Conner G, Fregien N and Salathe M (2010) Decreased soluble adenylyl cyclase activity in cystic fibrosis is related to defective apical bicarbonate exchange and affects ciliary beat frequency regulation. J Biol Chem 285, 29998–30007.
40. Pfaff EM, Becker S, Gunther A and Konigshoff M (2011) Dickkopf proteins influence lung epithelial cell proliferation in idiopathic pulmonary fibrosis. Eur Respir J 37, 79–87.
41. Casalino-Matsuda SM, Monzon ME, Day AJ and Forteza RM (2009) Hyaluronan fragments/CD44 mediate oxidative stress-induced MUC5B up-regulation in airway epithelium. Am J Respir Cell Mol Biol 40, 277–285.
42. Baumlin-Schmid N, Salathe M and Fregien NL (2016) Optimal lentivirus production and cell culture conditions necessary to successfully transduce primary human bronchial epithelial cells. J Vis Exp 113, e54176.
43. Ross AJ, Dailey LA, Brighton LE and Devlin RB (2007) Transcriptional profiling of mucociliary differentiation in human airway epithelial cells. Am J Respir Cell Mol Biol 37, 169–185.
44. Handeli S and Simon JA (2008) A small-molecule inhibitor of Tcf/beta-catenin signaling down-regulates PPARgamma and PPARdelta activities. Mol Cancer Ther 7, 521–529.
45. Baarsma HA, Meurs H, Halayko AJ, Menzen MH, Schmidt M, Kerstjens HA and Gosens R (2011) Glycogen synthase kinase-3 regulates cigarette smoke extract- and IL-1beta-induced cytokine secretion by airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 300, L910–L919.
46. Ostrowski LE and Nettesheim P (1995) Inhibition of ciliated cell differentiation by fluid submersion. Exp Lung Res 21, 957–970.
47. Gerovac BJ, Valencia M, Baumlin N, Salathe M, Conner GE and Fregien NL (2014) Submersion and hypoxia inhibit ciliated cell differentiation in a notch-dependent manner. Am J Respir Cell Mol Biol 51, 516–525.
48. 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.
49. Brechbuhl HM, Ghosh M, Smith MK, Smith RW, Li B, Hicks DA, Cole BB, Reynolds PR and Reynolds SD (2011) Beta-catenin dosage is a critical determinant of tracheal basal cell fate determination. Am J Pathol 179, 367–379.
50. Li C, Li A, Li M, Xing Y, Chen H, Hu L, Tiozzo C, Anderson S, Taketo MM and 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.
51. Giangreco A, Lu L, Vickers C, Teixeira VH, Groot KR, Butler CR, Ilieva EV, George PJ, Nicholson AG, Sage EK et al. (2012) beta-Catenindetermines upper airway progenitor cell fate and preinvasive squamous lung cancer progressionby modulating epithelial-mesenchymal transition. J Pathol 226, 575–587.
52. Smith MK, Koch PJ and Reynolds SD (2012) Direct and indirect roles for beta-catenin in facultative basal progenitor cell differentiation. Am J Physiol Lung Cell Mol Physiol 302, L580–L594.
53. Sun Z, Gong X, Zhu H, Wang C, Xu X, Cui D, Qian W and Han X (2014) Inhibition of Wnt/beta-catenin signaling promotes engraftment of mesenchymal stem cells to repair lung injury. J Cell Physiol 229, 213–224.
54. Chen BY, Wang X, Wang ZY, Wang YZ, Chen LW and Luo ZJ (2013) Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/beta-catenin signaling pathway. J Neurosci Res 91, 30–41.
55. Sakurai R, Cerny LM, Torday JS and Rehan VK (2011) Mechanism for nicotine-induced up-regulation of Wnt signaling in human alveolar interstitial fibroblasts. Exp Lung Res 37, 144–154.
56. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday JS and Rehan VK (2009) Hyperoxia-induced neonatal rat lung injury involves activation of TGF-β and Wnt signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 296, L1031–L1041.
57. Simon DM, Arikan MC, Srisuma S, Bhattacharya S, Tsai LW, Ingenito EP, Gonzalez F, Shapiro SD and Mariani TJ (2006) Epithelial cell PPAR[gamma] contributes to normal lung maturation. FASEB J 20, 1507–1509.
58. Morales E, Sakurai R, Husain S, Paek D, Gong M, Ibe B, Li Y, Husain M, Torday JS and Rehan VK (2014) Nebulized PPARgamma agonists: a novel approach to augment neonatal lung maturation and injury repair in rats. Pediatr Res 75, 631–640.
59. Yoshioka S, King ML, Ran S, Okuda H, MacLean JA 2nd, McAsey ME, Sugino N, Brard L, Watabe K and Hayashi K (2012) WNT7A regulates tumor growth and progression in ovarian cancer through the WNT/beta-catenin pathway. Mol Cancer Res 10, 469–482.
60. Le Grand F, Jones AE, Seale V, Scime A and Rudnicki MA (2009) Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4, 535–547.
61. Kandyba E, Leung Y, Chen YB, Widelitz R, Chuong CM and Kobielak K (2013) Competitive balance of intrabulge BMP/Wnt signaling reveals a robust gene network ruling stem cell homeostasis and cyclic activation. Proc Natl Acad Sci U S A 110, 1351–1356.
62. Hackett NR, Shaykhiev R, Walters MS, Wang R, Zwick RK, Ferris B, Witover B, Salit J and Crystal RG (2011) The human airway epithelial basal cell transcriptome. PLoS One 6, e18378.
63. Cai Y, Lechner MS, Nihalani D, Prindle MJ, Holzman LB and Dressler GR (2002) Phosphorylation of Pax2 by the c-Jun N-terminal kinase and enhanced Pax2-dependent transcription activation. J Biol Chem 277, 1217–1222.
64. Liu G, Bafico A and Aaronson SA (2005) The mechanism of endogenous receptor activation functionally distinguishes prototype canonical and noncanonical Wnts. Mol Cell Biol 25, 3475–3482.
65. Bernard P, Fleming A, Lacombe A, Harley VR and Vilain E (2008) Wnt4 inhibits beta-catenin/TCF signalling by redirecting beta-catenin to the cell membrane. Biol Cell 100, 167–177.
66. Endo Y, Wolf V, Muraiso K, Kamijo K, Soon L, Uren A, Barshishat-Kupper M and Rubin JS (2005) Wnt-3a-dependent cell motility involves RhoA activation and is specifically regulated by dishevelled-2. J Biol Chem 280, 777–786.
67. Tu X, Joeng KS, Nakayama KI, Nakayama K, Rajagopal J, Carroll TJ, McMahon AP and Long F (2007) Noncanonical Wnt signaling through G protein-linked PKCdelta activation promotes bone formation. Dev Cell 12, 113–127.
68. Samarzija I, Sini P, Schlange T, Macdonald G and Hynes NE (2009) Wnt3a regulates proliferation and migration of HUVEC via canonical and non-canonical Wnt signaling pathways. Biochem Biophys Res Commun 386, 449–454.
69. Wang Y, Sun Z, Qiu X, Li Y, Qin J and Han X (2009) Roles of Wnt/beta-catenin signaling in epithelial differrentiation of mesenchymal stem cells. Biochem Biophys Res Commun 390, 1309–1314.
70. Brezillon S, Dupuit F, Hinnrasky J, Marchand V, Kalin N, Tummler B and Puchelle E (1995) Decreased expression of the CFTR protein in remodeled human nasal epithelium from non-cystic fibrosis patients. Lab Invest 72, 191–200.
71. Kreda SM, Mall M, Mengos A, Rochelle L, Yankaskas J, Riordan JR and Boucher RC (2005) Characterization of wild-type and deltaF508 cystic fibrosis transmembrane regulator in human respiratory epithelia. Mol Biol Cell 16, 2154–2167.
72. Mucenski ML, Nation JM, Thitoff AR, Besnard V, Xu Y, Wert SE, Harada N, Taketo MM, Stahlman MT and Whitsett JA (2005) Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Am J Physiol Lung Cell Mol Physiol 289, L971–L979.
73. Boscke R, Vladar EK, Konnecke M, Husing B, Linke R, Pries R, Reiling N, Axelrod JD, Nayak JV and Wollenberg B (2017) Wnt signaling in chronic rhinosinusitis with nasal polyps. Am J Respir Cell Mol Biol 56, 575–584.
74. Kalinin AE, Kajava AV and Steinert PM (2002) Epithelial barrier function: assembly and structural features of the cornified cell envelope. BioEssays 24, 789–800.
75. Milara J, Peiro T, Serrano A and Cortijo J (2013) Epithelial to mesenchymal transition is increased in patients with COPD and induced by cigarette smoke. Thorax 68, 410–420.