Strain-induced differentiation of fetal type II epithelial cells is mediated via the integrin α6β1-ADAM17/tumor necrosis factor-α-converting enzyme (TACE) signaling pathway

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25646-25657

  Wang, Yulian ^a   Huang, Zheping ^a   Nayak, Pritha S ^a   Matthews, Benjamin D ^b   Warburton, David ^c   Shi, Wei ^c   Sanchez Esteban, Juan ^a  

^a BROWN UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIFFERENTIATION; CONVERTING ENZYME; EPITHELIAL CELLS; FETAL LUNGS; MECHANICAL FORCE; MECHANICAL STRAIN; NECROSIS FACTORS; SIGNALING PATHWAYS;

MECHANICAL ENGINEERING;

BIOLOGICAL ORGANS;

ALPHA6 INTEGRIN ANTIBODY; BETA1 INTEGRIN ANTIBODY; DISINTEGRIN; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME INHIBITOR; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY COMBINING SITE; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; EMBRYO; FETUS EPITHELIUM CELL TYPE II; FETUS LUNG; FETUS LUNG MATURATION; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; LUNG ALVEOLUS EPITHELIUM; MECHANICAL STIMULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADAM ADAMTS; CELL DIFFERENTIATION; CELL SIGNALING; CELL SURFACE RECEPTOR; GROWTH FACTORS; INTEGRINS; LUNG; MECHANOTRANSDUCTION;

ADAM PROTEINS; ANIMALS; CELL DIFFERENTIATION; EPITHELIAL CELLS; INTEGRIN ALPHA6BETA1; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MICE; MICE, KNOCKOUT; PROTEIN BINDING; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSFORMING GROWTH FACTOR ALPHA;

EID: 84883428714     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.473777     Document Type: Article

References (63)

1. Joe, P., Wallen, L. D., Chapin, C. J., Lee, C. H., Allen, L., Han, V. K., Dobbs, L. G., Hawgood, S., and Kitterman, J. A. (1997) Effects of mechanical factors on growth and maturation of the lung in fetal sheep. Am. J. Physiol. 272, L95-L105
2. Liu, M., and Post, M. (2000) Invited review: mechanochemical signal transduction in the fetal lung. J. Appl. Physiol. 89, 2078-2084
3. Sanchez-Esteban, J., Cicchiello, L. A., Wang, Y., Tsai, S. W., Williams, L. K., Torday, J. S., and Rubin, L. P. (2001) Mechanical stretch promotes alveolar epithelial type II cell differentiation. J. Appl. Physiol. 91, 589-595
4. Sanchez-Esteban, J., Tsai, S. W., Sang, J., Qin, J., Torday, J. S., and Rubin, L. P. (1998) Effects of mechanical forces on lung-specific gene expression. Am. J. Med. Sci. 316, 200-204
5. Sanchez-Esteban, J., Wang, Y., Cicchiello, L. A., and Rubin, L. P. (2002) Cyclic mechanical stretch inhibits cell proliferation and induces apoptosis in fetal rat lung fibroblasts. Am. J. Physiol. Lung Cell Mol. Physiol. 282, L448-L4566
6. Torday, J. S., Sanchez-Esteban, J., and Rubin, L. P. (1998) Paracrine mediators of mechanotransduction in lung development. Am J. Med. Sci. 316, 205-208
7. Wirtz, H. R., and Dobbs, L. G. (2000) The effects of mechanical forces on lung functions. Respir Physiol. 119, 1-17
8. Scarpelli, E. M., Condorelli, S., and Cosmi, E. V. (1975) Lamb fetal pulmonary fluid. I. Validation and significance of method for determination of volume and volume change. Pediatr Res. 9, 190-195
9. Harding, R. (1997) in The Lung: Scientific Fountations, 2nd Ed. (Crystal, R. G., West, J. B., Banes, P. J., and Weiber, E. R., eds), pp. 2093-2104, Lippincott-Raven, Philadelphia
10. Goldstein, J. D., and Reid, L. M. (1980) Pulmonary hypoplasia resulting from phrenic nerve agenesis and diaphragmatic amyoplasia. J. Pediatr. 97, 282-287
11. Moessinger, A. C., Harding, R., Adamson, T. M., Singh, M., and Kiu, G. T. (1990) Role of lung fluid volume in growth and maturation of the fetal sheep lung. J. Clin. Invest. 86, 1270-1277
12. Wigglesworth, J. S., and Desai, R. (1979) Effect on lung growth of cervical cord section in the rabbit fetus. Early Hum. Dev. 3, 51-65
13. Rama, K. M., Acarregui, M. J., and Snyder, J. M. (1997) in Lung Growth and Development (McDonald, J. A., ed), pp. 119-162, Marcel Dekker, Inc., New Yorkk
14. Singh, A. B., and Harris, R. C. (2005) Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal. 17, 1183-1193
15. Massagué, J., and Pandiella, A. (1993) Membrane-anchored growth factors. Annu. Rev. Biochem. 62, 515-541
16. Miettinen, P. J., Berger, J. E., Meneses, J., Phung, Y., Pedersen, R. A., Werb, Z., and Derynck, R. (1995) Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376, 337-341
17. Miettinen, P. J., Warburton, D., Bu, D., Zhao, J. S., Berger, J. E., Minoo, P., Koivisto, T., Allen, L., Dobbs, L., Werb, Z., and Derynck, R. (1997) Impaired lung branching morphogenesis in the absence of functional EGF receptor. Dev. Biol. 186, 224-236
18. Sibilia, M., Kroismayr, R., Lichtenberger, B. M., Natarajan, A., Hecking, M., and Holcmann, M. (2007) The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75, 770-787
19. Sibilia, M., and Wagner, E. F. (1995) Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234-238
20. Patel, N. V., Acarregui, M. J., Snyder, J. M., Klein, J. M., Sliwkowski, M. X., and Kern, J. A. (2000) Neuregulin-1 and human epidermal growth factor receptors 2 and 3 play a role in human lung development in vitro. Am. J. Respir. Cell Mol. Biol. 22, 432-440
21. Liu, W., Purevdorj, E., Zscheppang, K., von Mayersbach, D., Behrens, J., Brinkhaus, M. J., Nielsen, H. C., Schmiedl, A., and Dammann, C. E. (2010) ErbB4 regulates the timely progression of late fetal lung development. Biochim. Biophys. Acta 1803, 832-839
22. Zscheppang, K., Liu, W., Volpe, M. V., Nielsen, H. C., and Dammann, C. E. (2007) ErbB4 regulates fetal surfactant phospholipid synthesis in primary fetal rat type II cells. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L429-L435
23. Sanchez-Esteban, J., Wang, Y., Gruppuso, P. A., and Rubin, L. P. (2004) Mechanical stretch induces fetal type II cell differentiation via an epidermal growth factor receptor-extracellular-regulated protein kinase signaling pathway. Am. J. Respir. Cell Mol. Biol. 30, 76-83
24. Huang, Z., Wang, Y., Nayak, P. S., Dammann, C. E., and Sanchez-Esteban, J. (2012) Stretch-induced fetal type II cell differentiation is mediated via ErbB1-ErbB4 interactions. J. Biol. Chem. 287, 18091-18102
25. Wang, Y., Maciejewski, B. S., Soto-Reyes, D., Lee, H. S., Warburton, D., and Sanchez-Esteban, J. (2009) Mechanical stretch promotes fetal type II epithelial cell differentiation via shedding of HB-EGF and TGF-α. J. Physiol. 587, 1739-1753
26. Blobel, C. P. (2005) ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 6, 32-43
27. Seals, D. F., and Courtneidge, S. A. (2003) The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17, 7-30
28. Kheradmand, F., and Werb, Z. (2002) Shedding light on sheddases: role in growth and development. Bioessays 24, 8-12
29. Zhao, J., Chen, H., Peschon, J. J., Shi, W., Zhang, Y., Frank, S. J., and Warburton, D. (2001) Pulmonary hypoplasia in mice lacking tumor necrosis factor-α converting enzyme indicates an indispensable role for cell surface protein shedding during embryonic lung branching morphogenesis. Dev. Biol. 232, 204-218
30. Zhao, J., Chen, H., Wang, Y. L., and Warburton, D. (2001) Abrogation of tumor necrosis factor-alpha converting enzyme inhibits embryonic lung morphogenesis in culture. Int. J. Dev. Biol. 45, 623-631
31. Peschon, J. J., Slack, J. L., Reddy, P., Stocking, K. L., Sunnarborg, S. W., Lee, D. C., Russell, W. E., Castner, B. J., Johnson, R. S., Fitzner, J. N., Boyce, R. W., Nelson, N., Kozlosky, C. J., Wolfson, M. F., Rauch, C. T., Cerretti, D. P., Paxton, R. J., March, C. J., and Black, R. A. (1998) An essential role for ectodomain shedding in mammalian development. Science 282, 1281-1284
32. Lee, D. C., Sunnarborg, S. W., Hinkle, C. L., Myers, T. J., Stevenson, M. Y., Russell, W. E., Castner, B. J., Gerhart, M. J., Paxton, R. J., Black, R. A., Chang, A., and Jackson, L. F. (2003) TACE/ADAM17 processing of EGFR ligands indicates a role as a physiological convertase. Ann. N.Y. Acad. Sci. 995, 22-38
33. Sahin, U., Weskamp, G., Kelly, K., Zhou, H. M., Higashiyama, S., Peschon, J., Hartmann, D., Saftig, P., and Blobel, C. P. (2004) Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J. Cell Biol. 164, 769-779
34. Wang, N., Butler, J. P., and Ingber, D. E. (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127
35. Bershadsky, A. D., Balaban, N. Q., and Geiger, B. (2003) Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19, 677-695
36. Clark, E. A., and Brugge, J. S. (1995) Integrins and signal transduction pathways: the road taken. Science 268, 233-239
37. Ingber, D. (1991) Integrins as mechanochemical transducers. Curr. Opin. Cell Biol. 3, 841-848
38. Meyer, C. J., Alenghat, F. J., Rim, P., Fong, J. H., Fabry, B., and Ingber, D. E. (2000) Mechanical control of cyclic AMP signalling and gene transcription through integrins. Nat. Cell Biol. 2, 666-668
39. Alenghat, F. J., and Ingber, D. E. (2002) Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci. STKE 2002, pe6
40. Katsumi, A., Orr, A. W., Tzima, E., and Schwartz, M. A. (2004) Integrins in mechanotransduction. J. Biol. Chem. 279, 12001-12004
41. Shyy, J. Y., and Chien, S. (2002) Role of integrins in endothelial mechanosensing of shear stress. Circ. Res. 91, 769-775
42. Sanchez-Esteban, J., Wang, Y., Filardo, E. J., Rubin, L. P., and Ingber, D. E. (2006) Integrins β1, α6, and α3 contribute to mechanical strain-induced differentiation of fetal lung type II epithelial cells via distinct mechanisms. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L343-L350
43. White, J. M. (2003) ADAMs: modulators of cell-cell and cell-matrix interactions. Curr. Opin. Cell Biol. 15, 598-606
44. Wang, Y., Maciejewski, B. S., Lee, N., Silbert, O., McKnight, N. L., Frangos, J. A., and Sanchez-Esteban, J. (2006) Strain-induced fetal type II epithelial cell differentiation is mediated via cAMP-PKA-dependent signaling pathway. Am. J. Physiol. Lung Cell Mol. Physiol. 291, L820-L827
45. Glogauer, M., and Ferrier, J. (1998) A new method for application of force to cells via ferric oxide beads. Pflugers Arch 435, 320-327
46. Glogauer, M., Ferrier, J., and McCulloch, C. A. (1995) Magnetic fields applied to collagen-coated ferric oxide beads induce stretch-activated Ca2+ flux in fibroblasts. Am. J. Physiol. 269, C1093-C1104
47. Chan, M. W., Chaudary, F., Lee, W., Copeland, J. W., and McCulloch, C. A. (2010) Force-induced myofibroblast differentiation through collagen receptors is dependent on mammalian diaphanous (mDia). J. Biol. Chem. 285, 9273-9281
48. Matthews, B. D., Overby, D. R., Alenghat, F. J., Karavitis, J., Numaguchi, Y., Allen, P. G., and Ingber, D. E. (2004) Mechanical properties of individual focal adhesions probed with a magnetic microneedle. Biochem. Biophys. Res. Commun. 313, 758-764
49. Gooz, P., Dang, Y., Higashiyama, S., Twal, W. O., Haycraft, C. J., and Gooz, M. (2012) A disintegrin and metalloenzyme (ADAM) 17 activation is regulated by α5β1 integrin in kidney mesangial cells. PLoS One 7, e33350
50. Papadakis, K., Luks, F. I., De Paepe, M. E., Piasecki, G. J., and Wesselhoeft, C. W., Jr. (1997) Fetal lung growth after tracheal ligation is not solely a pressure phenomenon. J. Pediatr Surg. 32, 347-351
51. Luks, F. I., Roggin, K. K., Wild, Y. K., Piasecki, G. J., Rubin, L. P., Lesieur-Brooks, A. M., and De Paepe, M. E. (2001) Effect of lung fluid composition on type II cellular activity after tracheal occlusion in the fetal lamb. J. Pediatr. Surg. 36, 196-201
52. Zhan, M., Jin, B., Chen, S. E., Reecy, J. M., and Li, Y. P. (2007) TACE release of TNF-α mediates mechanotransduction-induced activation of p38 MAPK and myogenesis. J. Cell Sci. 120, 692-701
53. Shiomi, T., Tschumperlin, D. J., Park, J. A., Sunnarborg, S. W., Horiuchi, K., Blobel, C. P., and Drazen, J. M. (2011) TNF-α-converting enzyme/a disintegrin and metalloprotease-17 mediates mechanotransduction in murine tracheal epithelial cells. Am. J. Respir. Cell Mol. Biol. 45, 376-385
54. Khoor, A., Stahlman, M. T., Gray, M. E., and Whitsett, J. A. (1994) Temporal- spatial distribution of SP-B and SP-C proteins and mRNAs in developing respiratory epithelium of human lung. J. Histochem. Cytochem 42, 1187-1199
55. Lu, X., Lu, D., Scully, M. F., and Kakkar, V. V. (2007) Structure-activity relationship studies on ADAM protein-integrin interactions. Cardiovasc Hematol Agents Med Chem 5, 29-42
56. Bridges, L. C., and Bowditch, R. D. (2005) ADAM-Integrin Interactions: potential integrin regulated ectodomain shedding activity. Curr. Pharm. Des. 11, 837-847
57. Huang, J., Bridges, L. C., and White, J. M. (2005) Selective modulation of integrin-mediated cell migration by distinctADAMfamily members. Mol. Biol. Cell 16, 4982-4991
58. Dideberg, V., Théâtre, E., Farnir, F., Vermeire, S., Rutgeerts, P., De Vos, M., Belaiche, J., Franchimont, D., Van Gossum, A., Louis, E., and Bours, V. (2006) The TNF/ADAM 17 system: implication of an ADAM 17 haplotype in the clinical response to infliximab in Crohn's disease. Pharmacogenet Genomics 16, 727-734
59. Bax, D. V., Messent, A. J., Tart, J., van Hoang, M., Kott, J., Maciewicz, R. A., and Humphries, M. J. (2004) Integrin α5β1 and ADAM-17 interact in vitro and co-localize in migrating HeLa cells. J. Biol. Chem. 279, 22377-22386
60. Heidemann, J., Maaser, C., Lügering, A., Spahn, T. W., Zimmer, K. P., Herbst, H., Rafiee, P., Domschke, W., Krieglstein, C. F., Binion, D. G., and Kucharzik, T. F. (2006) Expression of vascular cell adhesion molecule-1 (CD 106) in normal and neoplastic human esophageal squamous epithelium. Int. J. Oncol. 28, 77-85
61. Nath, D., Slocombe, P. M., Webster, A., Stephens, P. E., Docherty, A. J., and Murphy, G. (2000) Meltrin gamma(ADAM-9) mediates cellular adhesion through α(6)β(1 )integrin, leading to a marked induction of fibroblast cell motility. J. Cell Sci. 113, 2319-2328
62. Chen, J., Fabry, B., Schiffrin, E. L., and Wang, N. (2001) Twisting integrin receptors increases endothelin-1 gene expression in endothelial cells. Am. J. Physiol. Cell Physiol 280, C1475-C1484
63. Smith, K. M., Gaultier, A., Cousin, H., Alfandari, D., White, J. M., and DeSimone, D. W. (2002) The cysteine-rich domain regulates ADAM protease function in vivo. J. Cell Biol. 159, 893-902