Regulation of actin dynamics by WNT-5A: Implications for human airway smooth muscle contraction

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Koopmans, Tim ^a   Kumawat, Kuldeep ^a   Halayko, Andrew J ^b   Gosens, Reinoud ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; WNT5A PROTEIN; WNT5A PROTEIN, HUMAN;

ANIMAL; BOVINE; HUMAN; METABOLISM; MONOCYTE; MUSCLE ISOMETRIC CONTRACTION; PHYSIOLOGY; PROTEIN MULTIMERIZATION; SMOOTH MUSCLE; TRACHEA;

ACTINS; ANIMALS; CATTLE; HUMANS; ISOMETRIC CONTRACTION; MONOCYTES; MUSCLE, SMOOTH; PROTEIN MULTIMERIZATION; TRACHEA; WNT-5A PROTEIN;

EID: 84979895481     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep30676     Document Type: Article

References (54)

1. WHO. Asthma. Available at: http://www.who.int/respiratory/asthma/en/(2013).
2. Bai, T. R. Abnormalities in airway smooth muscle in fatal asthma. A comparison between trachea and bronchus. Am. Rev. Respir. Dis. 143, 441-443 (1991).
3. Cerrina, J. et al. Human isolated bronchial muscle preparations from asthmatic patients: effects of indomethacin and contractile agonists. Prostaglandins 37, 457-469 (1989).
4. Chin, L. Y. M. et al. Mechanical properties of asthmatic airway smooth muscle. Eur. Respir. J. 40, 45-54 (2012).
5. Ma, X. et al. Changes in biophysical and biochemical properties of single bronchial smooth muscle cells from asthmatic subjects. Am. J. Physiol. Lung Cell. Mol. Physiol. 283, L1181-1189 (2002).
6. Matsumoto, H. et al. Comparison of gel contraction mediated by airway smooth muscle cells from patients with and without asthma. Thorax 62, 848-854 (2007).
7. Sutcliffe, A. et al. Increased nicotinamide adenine dinucleotide phosphate oxidase 4 expression mediates intrinsic airway smooth muscle hypercontractility in asthma. Am. J. Respir. Crit. Care Med. 185, 267-274 (2012).
8. Ijpma, G. et al. Human trachealis and main bronchi smooth muscle are normoresponsive in asthma. Am. J. Respir. Crit. Care Med. 191, 884-893 (2015).
9. Fish, J. E., Peterman, V. I., Cugell, D. W. Effect of deep inspiration on airway conductance in subjects with allergic rhinitis and allergic asthma. J. Allergy Clin. Immunol. 60, 41-46 (1977).
10. Fish, J. E., Ankin, M. G., Kelly, J. F., Peterman, V. I. Regulation of bronchomotor tone by lung inflation in asthmatic and nonasthmatic subjects. J. Appl. Physiol. 50, 1079-1086 (1981).
11. Lim, T. K., Pride, N. B., Ingram, R. H. Effects of volume history during spontaneous and acutely induced air-flow obstruction in asthma. Am. Rev. Respir. Dis. 135, 591-596 (1987).
12. Lim, T. K., Ang, S. M., Rossing, T. H., Ingenito, E. P., Ingram, R. H. The effects of deep inhalation on maximal expiratory flow during intensive treatment of spontaneous asthmatic episodes. Am. Rev. Respir. Dis. 140, 340-343 (1989).
13. Skloot, G., Permutt, S., Togias, A. Airway hyperresponsiveness in asthma: a problem of limited smooth muscle relaxation with inspiration. J. Clin. Invest. 96, 2393-2403 (1995).
14. Benayoun, L., Druilhe, A., Dombret, M.-C., Aubier, M., Pretolani, M. Airway structural alterations selectively associated with severe asthma. Am. J. Respir. Crit. Care Med. 167, 1360-1368 (2003).
15. Luillette, R. et al. Myosin, transgelin, and myosin light chain kinase: expression and function in asthma. Am. J. Respir. Crit. Care Med. 179, 194-204 (2009).
16. Woodruff, P. et al. Hyperplasia of smooth muscle in mild to moderate asthma without changes in cell size or gene expression. Am. J. Respir. Crit. Care Med. 169, 1001-1006 (2004).
17. Kuo, K. H., Wang, L., Par P. D., Ford, L. E., Seow, C. Y. Myosin thick filament lability induced by mechanical strain in airway smooth muscle. J. Appl. Physiol. Bethesda Md 1985 90, 1811-1816 (2001).
18. Solway, J. et al. Actin dynamics: a potential integrator of smooth muscle (Dys-)function and contractile apparatus gene expression in asthma. Parker B. Francis lecture. Chest 123, 392S-8S (2003).
19. Lavoie, T. L. et al. Disrupting actin-myosin-actin connectivity in airway smooth muscle as a treatment for asthma Proc. Am. Thorac. Soc. 6, 295-300 (2009).
20. Smolich, B., McMahon, J., McMahon, A., Papkoff, J. Wnt family proteins are secreted and associated with the cell surface. Mol. Biol. Cell 4, 1267-1275 (1993).
21. Willert, K. et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452 (2003).
22. Nusse, R. Wnt signaling in disease and in development. Cell Res. 15, 28-32 (2005).
23. Kumawat, K. et al. Noncanonical WNT-5A signaling regulates TGF-induced extracellular matrix production by airway smooth muscle cells. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 27, 1631-1643 (2013).
24. Choy, D. et al. Gene expression patterns of Th2 inflammation and intercellular communication in asthmatic airways. J. Immunol. Baltim. Md 1950 186, 1861-1869 (2011).
25. Ault, K., Durmowicz, G., Galione, A., Harger, P., Busa, W. Modulation of Xenopus embryo mesoderm-specific gene expression and dorsoanterior patterning by receptors that activate the phosphatidylinositol cycle signal transduction pathway. Dev. Camb. Engl. 122, 2033-2041 (1996).
26. Slusarski, D., Corces, V., Moon, R. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390, 410-413 (1997).
27. Sheldahl, L., Park, M., Malbon, C., Moon, R. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. CB 9, 695-698 (1999).
28. Kl, M., Sheldahl, L., Malbon, C., Moon, R. Ca(2+ )/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275, 12701-12711 (2000).
29. Kikuchi, A., Yamamoto, H., Sato, A., Matsumoto, S. Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. Oxf. Engl. 204, 17-33 (2012).
30. Gosens, R. et al. Caveolin-1 is required for contractile phenotype expression by airway smooth muscle cells. J. Cell. Mol. Med. 15, 2430-2442 (2011).
31. Smith, P. G., Roy, C., Zhang, Y. N., Chauduri, S. Mechanical stress increases RhoA activation in airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 28, 436-442 (2003).
32. Sit, S.-T., Manser, E. Rho GTPases and their role in organizing the actin cytoskeleton. J. Cell Sci. 124, 679-683 (2011).
33. Kumawat, K. et al. TGF-activated kinase 1 (TAK1) signaling regulates TGF-induced WNT-5A expression in airway smooth muscle cells via Sp1 and -catenin. Plos One 9, e94801 (2014).
34. Mack, C. P., Somlyo, A. V., Hautmann, M., Somlyo, A. P., Owens, G. K. Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization. J. Biol. Chem. 276, 341-347 (2001).
35. Cervantes, S., Yamaguchi, T. P., Hebrok, M. Wnt5a is essential for intestinal elongation in mice. Dev. Biol. 326, 285-294 (2009).
36. Mericskay, M., Kitajewski, J., Sassoon, D. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Dev. Camb. Engl. 131, 2061-2072 (2004).
37. Cohen, E. D., Miller, M. F., Wang, Z., Moon, R. T., Morrisey, E. E. Wnt5a and Wnt11 are essential for second heart field progenitor development. Dev. Camb. Engl. 139, 1931-1940 (2012).
38. Verkaar, F., Zaman, G. J. R. A model for signaling specificity of Wnt/Frizzled combinations through co-receptor recruitment. FEBS Lett. 584, 3850-3854 (2010).
39. Baarsma, H. A. et al. Activation of WNT/-catenin signaling in pulmonary fibroblasts by TGF- is increased in chronic obstructive pulmonary disease. PloS One 6, e25450 (2011).
40. Kumawat, K. et al. Noncanonical WNT-5A signaling regulates TGF-induced extracellular matrix production by airway smooth muscle cells. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 27, 1631-1643 (2013).
41. Shimizu, R. T., Blank, R. S., Jervis, R., Lawrenz-Smith, S. C., Owens, G. K. The smooth muscle alpha-actin gene promoter is differentially regulated in smooth muscle versus non-smooth muscle cells. J. Biol. Chem. 270, 7631-7643 (1995).
42. Madsen, C. S., Hershey, J. C., Hautmann, M. B., White, S. L., Owens, G. K. Expression of the smooth muscle myosin heavy chain gene is regulated by a negative-acting GC-rich element located between two positive-acting serum response factor-binding elements. J. Biol. Chem. 272, 6332-6340 (1997).
43. Li, L., Liu, Z., Mercer, B., Overbeek, P., Olson, E. N. Evidence for serum response factor-mediated regulatory networks governing SM22alpha transcription in smooth, skeletal, and cardiac muscle cells. Dev. Biol. 187, 311-321 (1997).
44. Sotiropoulos, A., Gineitis, D., Copeland, J., Treisman, R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98, 159-169 (1999).
45. Mack, C. P. Signaling mechanisms that regulate smooth muscle cell differentiation. Arterioscler. Thromb. Vasc. Biol. 31, 1495-1505 (2011).
46. Morita, T., Mayanagi, T., Sobue, K. Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J. Cell Biol. 179, 1027-1042 (2007).
47. O'Connor, J. W., Gomez, E. W. Cell adhesion and shape regulate TGF-beta1-induced epithelial-myofibroblast transition via MRTF-A signaling. PloS One 8, e83188 (2013).
48. Hautmann, M. B., Adam, P. J., Owens, G. K. Similarities and differences in smooth muscle alpha-actin induction by TGF-beta in smooth muscle versus non-smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 19, 2049-2058 (1999).
49. Hu, B., Wu, Z., Phan, S. H. Smad3 mediates transforming growth factor-beta-induced alpha-smooth muscle actin expression. Am. J. Respir. Cell Mol. Biol. 29, 397-404 (2003).
50. Valcourt, U., Kowanetz, M., Niimi, H., Heldin, C.-H., Moustakas, A. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol. Biol. Cell 16, 1987-2002 (2005).
51. Sebe, A. et al. Transforming growth factor-beta-induced alpha-smooth muscle cell actin expression in renal proximal tubular cells is regulated by p38beta mitogen-activated protein kinase, extracellular signal-regulated protein kinase1,2 and the Smad signalling during epithelial-myofibroblast transdifferentiation. Nephrol. Dial. Transplant. Off. Publ. Eur. Dial. Transpl. Assoc.-Eur. Ren. Assoc. 23, 1537-1545 (2008).
52. Gosens, R. et al. Role of caveolin-1 in p42/p44 MAP kinase activation and proliferation of human airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L523-534 (2006).
53. Ruijter, J. M. et al. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37, e45 (2009).
54. Ruijter, J. M. et al. Evaluation of qPCR curve analysis methods for reliable biomarker discovery: bias, resolution, precision, and implications. Methods San Diego Calif 59, 32-46 (2013).