Nonmuscle myosin IIA regulates intestinal epithelial barrier in vivo and plays a protective role during experimental colitis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Naydenov, Nayden G ^a   Feygin, Alex ^a   Wang, Dongdong ^a   Kuemmerle, John F ^b   Harris, Gianni ^c   Conti, Mary Anne ^d   Adelstein, Robert S ^d   Ivanov, Andrei I ^a,b,e  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN; CLDN7 PROTEIN, MOUSE; CYTOKINE; DEXTRAN SULFATE; IMMUNOGLOBULIN A; ISOPROTEIN; MYOSIN IIA;

ACTIN FILAMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MOUSE; NEUTROPHIL; PATHOLOGY; PERMEABILITY; TIGHT JUNCTION; TISSUE INJURY;

ACTIN CYTOSKELETON; ANIMALS; CLAUDINS; COLITIS; CYTOKINES; DEXTRAN SULFATE; IMMUNOGLOBULIN A; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; NEUTROPHILS; NONMUSCLE MYOSIN TYPE IIA; PERMEABILITY; PROLAPSE; PROTEIN ISOFORMS; TIGHT JUNCTIONS;

EID: 84964319706     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24161     Document Type: Article

References (53)

1. Marchiando, A. M., Graham, W. V. and Turner, J. R. Epithelial barriers in homeostasis and disease. Ann Rev Pathol 5, 119-144 (2010).
2. Suzuki, T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mole Life Sci 70, 631-659 (2013).
3. Ivanov, A. I. and Naydenov, N. G. Dynamics and regulation of epithelial adherens junctions: recent discoveries and controversies. Int Rev Cell Mol Biol 303, 27-99 (2013).
4. Takeichi, M. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nature reviews Mol Cell Biol 15, 397-410 (2014).
5. Troyanovsky, S. Adherens junction assembly. Subcell Biochem 60, 89-108 (2012).
6. Anderson, J. M. and Van Itallie, C. M. Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1, a002584 (2009).
7. Koval, M. Differential pathways of claudin oligomerization and integration into tight junctions. Tissue Barriers 1, e24518 (2013).
8. Lu, Z., Ding, L., Lu, Q. and Chen, Y.-H. Claudins in intestines: Distribution and functional significance in health and diseases. Tissue Barriers 1, e24978 (2013).
9. McCole, D. F. Phosphatase regulation of intercellular junctions. Tissue Barriers 1, e26713 (2013).
10. Quiros, M. and Nusrat, A. RhoGTPases, actomyosin signaling and regulation of the epithelial Apical Junctional Complex. Sem Cell Dev Biol 36, 194-203 (2014).
11. Ivanov, A. I. Actin motors that drive formation and disassembly of epithelial apical junctions. Front Biosci 13, 6662-6681 (2008).
12. Rodgers, L. S. and Fanning, A. S. Regulation of epithelial permeability by the actin cytoskeleton. Cytoskeleton 68, 653-660 (2011).
13. Ivanov, A. I., Parkos, C. A. and Nusrat, A. Cytoskeletal regulation of epithelial barrier function during inflammation. Am J. Pathol 177, 512-524 (2010).
14. Heissler, S. M. and Manstein, D. J. Nonmuscle myosin-2: mix and match. Cell Mol Life Sci 70, 1-21 (2013).
15. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. and Horwitz, A. R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nature reviews Mol Cell Biol 10, 778-790 (2009).
16. Al-Sadi, R., Ye, D., Dokladny, K. and Ma, T. Y. Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 180, 5653-5661 (2008).
17. Clayburgh, D. R. et al. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J Clin Invest 115, 2702-2715 (2005).
18. Ivanov, A. I. et al. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. Plos one 2, e658 (2007).
19. Ivanov, A. I., Hunt, D., Utech, M., Nusrat, A. and Parkos, C. A. Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol Biol Cell 16, 2636-2650 (2005).
20. Ivanov, A. I., McCall, I. C., Parkos, C. A. and Nusrat, A. Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol Biol Cell 15, 2639-2651 (2004).
21. Shen, L. et al. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci 119, 2095-2106 (2006).
22. Utech, M. et al. Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 16, 5040-5052 (2005).
23. Zolotarevsky, Y. et al. A membrane-permeant peptide that inhibits MLC kinase restores barrier function in in vitro models of intestinal disease. Gastroenterology 123, 163-172 (2002).
24. Shen, L., Weber, C. R., Raleigh, D. R., Yu, D. and Turner, J. R. Tight junction pore and leak pathways: a dynamic duo. Ann Rev Physiol 73, 283-309 (2011).
25. Su, L. et al. TNFR2 activates MLCK-dependent tight junction dysregulation to cause apoptosis-mediated barrier loss and experimental colitis. Gastroenterology 145, 407-415 (2013).
26. Su, L. et al. Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136, 551-563 (2009).
27. Feighery, L. M. et al. Myosin light chain kinase inhibition: correction of increased intestinal epithelial permeability in vitro. Pharm Res 25, 1377-1386 (2008).
28. Heissler, S. M. and Sellers, J. R. Four things to know about myosin light chains as reporters for non-muscle myosin-2 dynamics in live cells. Cytoskeleton 72, 65-70, (2015).
29. Chan, W. et al. Myosin II regulatory light chain is required for trafficking of bile salt export protein to the apical membrane in Madin-Darby canine kidney cells. J Biol Chem 280, 23741-23747, (2005).
30. Szymanski, P. T. and Goyal, R. K. Calponin binds to the 20-kilodalton regulatory light chain of myosin. Biochemistry 38, 3778-3784, (1999).
31. Xu, J. et al. Nonmuscle myosin light-chain kinase mediates neutrophil transmigration in sepsis-induced lung inflammation by activating beta2 integrins. Nature immunol 9, 880-886, (2008).
32. Beach, J. R. and Hammer, J. A., 3rd. Myosin II isoform co-assembly and differential regulation in mammalian systems. Experimental cell research 334, 2-9 (2015).
33. Babbin, B. A. et al. Non-muscle myosin IIA differentially regulates intestinal epithelial cell restitution and matrix invasion. Am J Pathol 174, 436-448 (2009).
34. Ivanov, A. I., Samarin, S. N., Bachar, M., Parkos, C. A. and Nusrat, A. Protein kinase C activation disrupts epithelial apical junctions via ROCK-II dependent stimulation of actomyosin contractility. BMC Cell Biol 10, 36-43, (2009).
35. Wald, F. A. et al. Aberrant expression of the polarity complex atypical PKC and non-muscle myosin IIA in active and inactive inflammatory bowel disease. Virchows Archiv 459, 331-338 (2011).
36. Conti, M. A., Even-Ram, S., Liu, C., Yamada, K. M. and Adelstein, R. S. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J Biol Chem 279, 41263-41266 (2004).
37. de Valliere, C. et al. G Protein-coupled pH-sensing Receptor OGR1 Is a Regulator of Intestinal Inflammation. Inflamm Bowel Dis 21, 1269-1281, (2015).
38. Matharu, K. S. et al. Toll-like receptor 4-mediated regulation of spontaneous Helicobacter-dependent colitis in IL-10-deficient mice. Gastroenterology 137, 1380-1390 (2009).
39. Neurath, M. F., Fuss, I., Kelsall, B. L., Stuber, E. and Strober, W. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J Exp Med 182, 1281-1290 (1995).
40. Schumann, M. et al. CCR7 deficiency causes diarrhea associated with altered ion transport in colonocytes in the absence of overt colitis. Mucosal Immunol 5, 377-387 (2012).
41. Laukoetter, M. G. et al. JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 204, 3067-3076 (2007).
42. Khounlotham, M. et al. Compromised intestinal epithelial barrier induces adaptive immune compensation that protects from colitis. Immunity 37, 563-573 (2012).
43. Naydenov, N. G. et al. A membrane fusion protein alphaSNAP is a novel regulator of epithelial apical junctions. PloS one 7, e34320 (2012).
44. Smalley-Freed, W. G. et al. p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J Clin Invest 120, 1824-1835 (2010).
45. Walker, A. et al. Non-muscle myosin II regulates survival threshold of pluripotent stem cells. Nature Commun 1, 71 (2010).
46. Zhao, B. et al. The non-muscle-myosin-II heavy chain Myh9 mediates colitis-induced epithelium injury by restricting Lgr5+ stem cells. Nature Commun 6, 7166 (2015).
47. Barreau, F. and Hugot, J. P. Intestinal barrier dysfunction triggered by invasive bacteria. Curr Opin Microbiol 17, 91-98 (2014).
48. Cunningham, K. E. and Turner, J. R. Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann N Y Acad Sci 1258, 34-42 (2012).
49. Jacobelli, J. et al. Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions. Nature immunol 11, 953-961 (2010).
50. Madison, B. B. et al. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277, 33275-33283 (2002).
51. Rhee, L. et al. Expression of TNFAIP3 in intestinal epithelial cells protects from DSS- but not TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 303, G220-227 (2012).
52. Kennedy, R. J. et al. Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease. Br J Surg 87, 1346-1351 (2000).
53. Ivanov, A. I., Pero, R. S., Scheck, A. C. and Romanovsky, A. A. Prostaglandin E(2)-synthesizing enzymes in fever: differential transcriptional regulation. Am J Physiol Regul, Integr Comp Physiol 283, R1104-1117 (2002).