Biphasic regulation of myosin light chain phosphorylation by p21-activated kinase modulates intestinal smooth muscle contractility

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 1200-1213

  Chu, Ji ^a   Pham, Ngoc T ^a   Olate, Nicole ^a   Kislitsyna, Karina ^a   Day, Mary Clare ^a   LeTourneau, Phillip A ^a   Kotss, Alexander ^b   Stewart, Randolph H ^c   Laine, Glen A ^c   Cox, Charles S ^a,c   Uray, Karen ^a,c  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; ENZYMES; MUSCLE; STRESSES;

IDEAL MODEL; IN-VIVO; INTESTINAL MOTILITIES; INTESTINAL SMOOTH MUSCLE; KINASE ACTIVITY; MECHANICAL STRETCHING; MYOSIN LIGHT CHAINS; P-21 ACTIVATED KINASE; SMOOTH MUSCLE CELLS; SMOOTH MUSCLES;

PHOSPHORYLATION;

MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; P21 ACTIVATED KINASE; SMALL INTERFERING RNA; THREONINE;

ARTICLE; BIOPHYSICS; CONTROL CYCLICAL CELL STRETCHING; CONTROLLED STUDY; DISEASE ASSOCIATION; EDEMA CYCLICAL CELL STRETCHING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME SUBUNIT; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINAL DYSMOTILITY; INTESTINE CONTRACTION; INTESTINE MUSCLE; MUSCLE STRESS; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SMOOTH MUSCLE CONTRACTILITY; SMOOTH MUSCLE FIBER;

EID: 84872355795     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.370718     Document Type: Article

References (56)

1. Kasai, Y., Tsutsumi, O., Taketani, Y., Endo, M., and Iino, M. (1995) Stretch-induced enhancement of contractions in uterine smooth muscle of rats. J. Physiol. 486, 373-384
2. Sanders, K. M., and Koh, S. D. (2006) Two-pore-domain potassium channels in smooth muscles. New components of myogenic regulation. J. Physiol. 570, 37-43
3. Farrugia, G., Holm, A. N., Rich, A., Sarr, M. G., Szurszewski, J. H., and Rae, J. L. (1999) A mechanosensitive calcium channel in human intestinal smooth muscle cells. Gastroenterology 117, 900-905 (Pubitemid 29468233)
4. Burnstock, G., and Prosser, C. L. (1960) Responses of smooth muscles to quick stretch. Relation of stretch to conduction. Am. J. Physiol. 198, 921-925
5. Mann, J. M., Lam, R. H., Weng, S., Sun, Y., and Fu, J. (2012) A silicone-based stretchable micropost array membrane for monitoring live-cell subcellular cytoskeletal response. Lab Chip 12, 731-740
6. Shi, X. Z., Lin, Y. M., Powell, D. W., and Sarna, S. K. (2011) Pathophysiology of motility dysfunction in bowel obstruction. Role of stretch-induced COX-2. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G99-G108
7. Chu, J., Miller, C. T., Kislitsyna, K., Laine, G. A., Stewart, R. H., Cox, C. S., and Uray, K. S. (2012) Decreased myosin phosphatase target subunit 1 (MYPT1) phosphorylation via attenuated rho kinase and zipper-interacting kinase activities in edematous intestinal smooth muscle. Neurogastroenterol. Motil. 24, 257-2566, e109
8. Kehlet, H., and Holte, K. (2001) Review of postoperative ileus. Am. J. Surg. 182, 3S-10S (Pubitemid 34072941)
9. Balogh, Z., McKinley, B. A., Cocanour, C. S., Kozar, R. A., Valdivia, A., Sailors, R. M., and Moore, F. A. (2003) Supranormal trauma resuscitation causes more cases of abdominal compartment syndrome. Arch. Surg. 138, 637-642; discussion 642-633
10. Norton, J. A., Ott, L. G., McClain, C., Adams, L., Dempsey, R. J., Haack, D., Tibbs, P. A., and Young, A. B. (1988) Intolerance to enteral feeding in the brain-injured patient. J. Neurosurg. 68, 62-66 (Pubitemid 18019134)
11. Cox, C. S., Jr., Radhakrishnan, R., Villarrubia, L., Xue, H., Uray, K., Gill, B. S., Stewart, R. H., and Laine, G. A. (2008) Hypertonic saline modulation of intestinal tissue stress and fluid balance. Shock 29, 598-602 (Pubitemid 351544080)
12. Uray, K. S., Laine, G. A., Xue, H., Allen, S. J., and Cox, C. S., Jr. (2007) Edema-induced intestinal dysfunction is mediated by STAT3 activation. Shock 28, 239-244 (Pubitemid 47220837)
13. Uray, K. S., Wright, Z., Kislitsyna, K., Xue, H., and Cox, C. S., Jr. (2010) Nuclear factor-κB activation by edema inhibits intestinal contractile activity. Crit. Care Med. 38, 861-870
14. Uray, K. S., Laine, G. A., Xue, H., Allen, S. J., and Cox, C. S., Jr. (2006) Intestinal edema decreases intestinal contractile activity via decreased myosin light chain phosphorylation. Crit. Care Med. 34, 2630-2637 (Pubitemid 44413064)
15. Shah, S. K., Fogle, L. N., Aroom, K. R., Gill, B. S., Moore-Olufemi, S. D., Jimenez, F., Uray, K. S., Walker, P. A., Stewart, R. H., Laine, G. A., and Cox, C. S., Jr. (2010) Hydrostatic intestinal edema induced signaling pathways. Potential role of mechanical forces. Surgery 147, 772-779
16. Kamm, K. E., and Stull, J. T. (1985) The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu. Rev. Pharmacol. Toxicol. 25, 593-620 (Pubitemid 15090995)
17. Somlyo, A. P., and Somlyo, A. V. (1994) Signal transduction and regulation in smooth muscle. Nature 372, 231-236 (Pubitemid 24352442)
18. Somlyo, A. P., and Somlyo, A. V. (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II. Modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325-1358 (Pubitemid 37222274)
19. Hirano, K., Derkach, D. N., Hirano, M., Nishimura, J., and Kanaide, H. (2003) Protein kinase network in the regulation of phosphorylation and dephosphorylation of smooth muscle myosin light chain. Mol. Cell Biochem. 248, 105-114 (Pubitemid 36833647)
20. Takuwa, Y. (1996) Regulation of vascular smooth muscle contraction. The roles of Ca2+, protein kinase C and myosin light chain phosphatase. Jpn. Heart J. 37, 793-813
21. Ito, M., Nakano, T., Erdodi, F., and Hartshorne, D. J. (2004) Myosin phosphatase. Structure, regulation and function. Mol. Cell Biochem. 259, 197-209 (Pubitemid 38519232)
22. Takizawa, N., Koga, Y., and Ikebe, M. (2002) Phosphorylation of CPI17 and myosin binding subunit of type 1 protein phosphatase by p21-activated kinase. Biochem. Biophys. Res. Commun. 297, 773-778 (Pubitemid 35230317)
23. Kiss, E., Murányi, A., Csortos, C., Gergely, P., Ito, M., Hartshorne, D. J., and Erdodi, F. (2002) Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochem. J. 365, 79-87
24. MacDonald, J. A., Borman, M. A., Murányi, A., Somlyo, A. V., Hartshorne, D. J., and Haystead, T. A. (2001) Identification of the endogenous smooth muscle myosin phosphatase-associated kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 2419-2424 (Pubitemid 32209497)
25. Katsumi, A., Milanini, J., Kiosses, W. B., del Pozo, M. A., Kaunas, R., Chien, S., Hahn, K. M., and Schwartz, M. A. (2002) Effects of cell tension on the small GTPase Rac. J. Cell Biol. 158, 153-164
26. Dharmawardhane, S., Sanders, L. C., Martin, S. S., Daniels, R. H., and Bokoch, G. M. (1997) Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138, 1265-1278 (Pubitemid 27415053)
27. Zhang, H., Landmann, F., Zahreddine, H., Rodriguez, D., Koch, M., and Labouesse, M. (2011) A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 471, 99-103
28. Sanders, L. C., Matsumura, F., Bokoch, G. M., and de Lanerolle, P. (1999) Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085
29. Wirth, A., Schroeter, M., Kock-Hauser, C., Manser, E., Chalovich, J. M., De Lanerolle, P., and Pfitzer, G. (2003) Inhibition of contraction and myosin light chain phosphorylation in guinea-pig smooth muscle by p21-activated kinase 1. J. Physiol. 549, 489-500 (Pubitemid 36701760)
30. Chew, T. L., Masaracchia, R. A., Goeckeler, Z. M., and Wysolmerski, R. B. (1998) Phosphorylation of non-muscle myosin II regulatory light chain by p21-activated kinase (γ-PAK). J. Muscle Res. Cell Motil. 19, 839-854 (Pubitemid 29054480)
31. Ramos, E., Wysolmerski, R. B., and Masaracchia, R. A. (1997) Myosin phosphorylation by human cdc42-dependent S6/H4 kinase/γPAK from placenta and lymphoid cells. Recept. Signal Transduct. 7, 99-110
32. Sells, M. A., Boyd, J. T., and Chernoff, J. (1999) p21-activated kinase 1 (Pak1) regulates cell motility in mammalian fibroblasts. J. Cell Biol. 145, 837-849 (Pubitemid 29240859)
33. Hidetaka, K. (2009) Phos-tag Western blotting for detecting stoichiometric protein phosphorylation in cells. Nat. Protoc. 2009, doi: 10.1038/nprot.2009.170
34. Girish, V., and Vijayalakshmi, A. (2004) Affordable image analysis using NIH Image/ImageJ. Indian J. Cancer 41, 47 (Pubitemid 38623932)
35. Sutherland, C., and Walsh, M. P. (2012) Myosin regulatory light chain diphosphorylation slows relaxation of arterial smooth muscle. J. Biol. Chem. 287, 24064-24076
36. Sells, M. A., Knaus, U. G., Bagrodia, S., Ambrose, D. M., Bokoch, G. M., and Chernoff, J. (1997) Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7, 202-210 (Pubitemid 27164726)
37. Ikebe, M., and Hartshorne, D. J. (1985) Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase. J. Biol. Chem. 260, 10027-10031 (Pubitemid 16244088)
38. Ikebe, M., Hartshorne, D. J., and Elzinga, M. (1986) Identification, phosphorylation, and dephosphorylation of a second site for myosin light chain kinase on the 20,000-dalton light chain of smooth muscle myosin. J. Biol. Chem. 261, 36-39 (Pubitemid 16144806)
39. Mori, S., Iwaoka, R., Eto, M., and Ohki, S. Y. (2009) Solution structure of the inhibitory phosphorylation domain of myosin phosphatase targeting subunit 1. Proteins 77, 732-735
40. Funk, S. D., Yurdagul, A., Jr., Green, J. M., Jhaveri, K. A., Schwartz, M. A., and Orr, A. W. (2010) Matrix-specific protein kinase A signaling regulates p21-activated kinase activation by flow in endothelial cells. Circ. Res. 106, 1394-1403
41. Deacon, S. W., Beeser, A., Fukui, J. A., Rennefahrt, U. E., Myers, C., Chernoff, J., and Peterson, J. R. (2008) An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase. Chem. Biol. 15, 322-331 (Pubitemid 351508427)
42. Li, C., and Xu, Q. (2000) Mechanical stress-initiated signal transductions in vascular smooth muscle cells. Cell. Signal. 12, 435-445
43. Ding, H. L., Ryder, J. W., Stull, J. T., and Kamm, K. E. (2009) Signaling processes for initiating smooth muscle contraction upon neural stimulation. J. Biol. Chem. 284, 15541-15548
44. Murthy, K. S. (2006) Signaling for contraction and relaxation in smooth muscle of the gut. Annu. Rev. Physiol. 68, 345-374
45. Niiro, N., and Ikebe, M. (2001) Zipper-interacting protein kinase induces Ca2+-free smooth muscle contraction via myosin light chain phosphorylation. J. Biol. Chem. 276, 29567-29574
46. Deng, J. T., Van Lierop, J. E., Sutherland, C., and Walsh, M. P. (2001) Ca2+-independent smooth muscle contraction. A novel function for in-tegrin- linked kinase. J. Biol. Chem. 276, 16365-16373
47. Grassie, M. E., Moffat, L. D., Walsh, M. P., and MacDonald, J. A. (2011) The myosin phosphatase targeting protein (MYPT) family. A regulated mechanism for achieving substrate specificity of the catalytic subunit of protein phosphatase type 1δ. Arch. Biochem. Biophys. 510, 147-159
48. Sheehan, K. A., Ke, Y., and Solaro, R. J. (2007) p21-activated kinase-1 and its role in integrated regulation of cardiac contractility. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R963-R973 (Pubitemid 47358913)
49. Seasholtz, T. M., Radeff-Huang, J., Sagi, S. A., Matteo, R., Weems, J. M., Cohen, A. S., Feramisco, J. R., and Brown, J. H. (2004) Rho-mediated cytoskeletal rearrangement in response to LPA is functionally antagonized by Rac1 and PIP2. J. Neurochem. 91, 501-512 (Pubitemid 39363449)
50. Nimnual, A. S., Taylor, L. J., and Bar-Sagi, D. (2003) Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5, 236-241 (Pubitemid 36322251)
51. Kaneko-Kawano, T., Takasu, F., Naoki, H., Sakumura, Y., Ishii, S., Ueba, T., Eiyama, A., Okada, A., Kawano, Y., and Suzuki, K. (2012) Dynamic regulation of myosin light chain phosphorylation by Rho-kinase. PLoS One 7, e39269
52. Murthy, K. S., Zhou, H., Grider, J. R., Brautigan, D. L., Eto, M., and Makhlouf, G. M. (2003) Differential signalling by muscarinic receptors in smooth muscle. m2-mediated inactivation of myosin light chain kinase via Gi3, Cdc42/Rac1, and p21-activated kinase 1 pathway, and m3-mediated MLC20 (20 kDa regulatory light chain of myosin II) phosphorylation via Rho-associated kinase/myosin phosphatase targeting subunit 1 and protein kinase C/CPI-17 pathway. Biochem. J. 374, 145-155
53. Bokoch, G. M. (2003) Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781
54. Zeng, Q., Lagunoff, D., Masaracchia, R., Goeckeler, Z., Côté, G., and Wysolmerski, R. (2000) Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II. J. Cell Sci. 113, 471-482 (Pubitemid 30116653)
55. Rudrabhatla, R. S., Sukumaran, S. K., Bokoch, G. M., and Prasadarao, N. V. (2003) Modulation of myosin light-chain phosphorylation by p21-activated kinase 1 in Escherichia coli invasion of human brain microvascular endothelial cells. Infect. Immun. 71, 2787-2797 (Pubitemid 36519893)
56. Coniglio, S. J., Zavarella, S., and Symons, M. H. (2008) Pak1 and Pak2 mediate tumor cell invasion through distinct signaling mechanisms. Mol. Cell Biol. 28, 4162-4172 (Pubitemid 351812999)