Regulation of contractility by Hsp27 and Hic-5 in rat mesenteric small arteries

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 2, 2008, Pages

  Srinivasan, R ^a   Forman, S ^a   Quinlan, R A ^b   Ohanian, J ^a   Ohanian, V ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

adrenergic; Cell signaling; Cytoskeleton; Smooth muscle; Subcellular localization

Indexed keywords

ACTIN; FOCAL ADHESION KINASE 1; FOCAL ADHESION KINASE 2; HEAT SHOCK PROTEIN 27; HYDROGEN PEROXIDE INDUCIBLE CLONE 5; MITOGEN ACTIVATED PROTEIN KINASE P38; MUSCLE PROTEIN; NORADRENALIN; PAXILLIN; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VASOCONSTRICTOR AGENT;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL FUNCTION; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; ENZYME INHIBITION; HEART MUSCLE CONTRACTILITY; MESENTERIC ARTERY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; BLOTTING, WESTERN; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; ENZYME INHIBITORS; HEAT-SHOCK PROTEINS; HYDROGEN PEROXIDE; IMMUNOPRECIPITATION; MESENTERIC ARTERIES; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; NEOPLASM PROTEINS; NOREPINEPHRINE; OXIDANTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; RATS; RATS, SPRAGUE-DAWLEY; SRC-FAMILY KINASES; SUBCELLULAR FRACTIONS; VASOCONSTRICTOR AGENTS;

EID: 39149088964     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00939.2007     Document Type: Article

References (59)

1. Akamatsu S, Nakajima K, Ishisaki A, Matsuno H, Tanabe K, Takei M, Takenaka M, Hirade K, Yoshimi N, Suga H, Oiso Y, Kato K, Kozawa O. Vasopressin phosphorylates HSP27 in aortic smooth muscle cells. J Cell Biochem 92: 1203-1211, 2004.
2. An SS, Fabry B, Mellema M, Bursac P, Gerthoffer WT, Kayyali US, Gaestel M, Shore SA, Fredberg JJ. Role of heat shock protein 27 in cytoskeletal remodeling of the airway smooth muscle cell. J Appl Physiol 96: 1701-1713, 2004.
3. Bain J, McLauchlan H, Elliott M, Cohen P. The specificities of protein kinase inhibitors: an update. Biochem J 371: 199-204, 2003.
4. Barany M, Barron JT, Gu L, Barany K. Exchange of the actin-bound nucleotide in intact arterial smooth muscle. J Biol Chem 276: 48398-48403, 2001.
5. Bitar KN. HSP27 phosphorylation and interaction with actin-myosin in smooth muscle contraction. Am J Physiol Gastrointest Liver Physiol 282: G894-G903, 2002.
6. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein dye binding. Anal Biochem 72: 248-254, 1976.
7. Brinson AE, Harding T, Diliberto PA, He Y, Li X, Hunter D, Herman B, Earp HS, Graves LM. Regulation of calcium-dependent tyrosine kinase in vascular smooth muscle cells by angiotensin II and platelet derived growth factor. J Biol Chem 273: 1711-1718, 1998.
8. Brown MC, Turner CE. Paxillin: adapting to change. Physiol Rev 84: 1315-1339, 2004.
9. Burridge K, Chrzanowska-Wodnicka M. Focal adhesions, contractility and signaling. Annu Rev Cell Dev Biol 12: 463-519, 1996.
10. Cao W, Sohn UD, Bitar KN, Behar J, Biancani P, Harnett KM. MAPK mediates PKC-dependent contraction of cat esophageal and lower esophageal sphincter circular smooth muscle. Am J Physiol Gastrointest Liver Physiol 285: G86-G95, 2003.
11. Cipolla M, Osol G. Vascular smooth muscle actin cytoskeleton in cerebral artery forced dilation. Stroke 29: 1223-1228, 1998.
12. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105, 2000.
13. Eyers PA, van den IJ, Quinlan RA, Goedert M, Cohen P. Use of a drug-resistant mutant of stress-activated protein kinase 2a/p38 to validate the in vivo specificity of SB 203580. FEBS Lett 451: 191-196, 1999.
14. Ferns G, Shams S, Shafi S. Heat shock protein 27: its potential role in vascular disease. Int J Exp Pathol 87: 253-274, 2006.
15. Frame MC. Newest findings on the oldest oncogene; how activated src does it. J Cell Sci 117: 989-998, 2004.
16. Fujita H, Kamiguchi K, Cho D, Shibanuma M, Morimoto C, Tachibana K. Interaction of Hic-5, a senescence-related protein, with focal adhesion kinase. J Biol Chem 273: 26516-26521, 1998.
17. Gerthoffer WT, Gunst SJ. Signal transduction in smooth muscle (invited review): focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol 91: 963-972, 2001.
18. Hagel M, George EL, Kim A, Tamimi R, Opitz SL, Turner CE, Imamoto A, Thomas SM. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol Cell Biol 22: 901-915, 2002.
19. Hanke JH, Gardner DG, Ghangelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA. Discovery of a novel, potent, and Src family - selective tyrosine kinase inhibitor. J Biol Chem 271: 695-701, 1996.
20. Hetey SE, Lalonde DP, Turner CE. Tyrosine-phosphorylated Hic-5 inhibits epidermal growth factor-induced lamellipodia formation. Exp Cell Res 311: 147-156, 2005.
21. Hirade K, Kozawa O, Tanabe K, Niwa M, Matsuno H, Oiso Y, Akamatsu S, Ito H, Kato K, Katagiri Y, Uematsu T. Thrombin stimulates dissociation and induction of HSP27 via p38 MAPK in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 283: H941-H948, 2002.
22. Hirade K, Tanabe K, Niwa M, Ishisaki A, Nakajima K, Nakamura M, Sugiyama T, Katagiri Y, Kato K, Kozawa O. Adenylyl cyclase-cAMP system inhibits thrombin-induced HSP27 in vascular smooth muscle cells. J Cell Biochem 94: 573-584, 2005.
23. Ishino M, Aoto H, Sasaski H, Suzuki R, Sasaki T. Phosphorylation of Hic-5 at tyrosine 60 by CAKbeta and Fyn. FEBS Lett 474: 179-183, 2000.
24. Jia Y, Ransom RF, Shibanuma M, Liu C, Welsh MJ, Smoyer WE. Identification and characterization of hic-5/ARA55 as an hsp27 binding protein. J Biol Chem 276: 39911-39918, 2001.
25. Kim-Kaneyama JR, Suzuki W, Ichikawa K, Ohki T, Kohno Y, Sata M, Nose K, Shibanuma M. Uni-axial stretching regulates intracellular localization of Hic-5 expressed in smooth-muscle cells in vivo. J Cell Sci 118: 937-949, 2005.
26. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
27. Landry J, Lambert H, Zhou M, Lavoie JN, Hickey E, Weber LA, Anderson CW. Human HSP27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J Biol Chem 267: 794-803, 1992.
28. Lavoie JN, Lambert H, Hickey E, Weber LA, Landry J. Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27. Mol Cell Biol 15: 505-516, 1995.
29. Lee HM, Won KJ, Kim J, Park HJ, Kim HJ, Roh HY, Lee SH, Lee CK, Kim B. Endothelin-1 induces contraction via a Syk-mediated p38 mitogen-activated protein kinase pathway in rat aortic smooth muscle. J Pharm Sci 103: 427-433, 2007.
30. Lindquist S, Craig EA. The heat shock proteins. Annu Rev Genet 22: 631-677, 1988.
31. Matsuya M, Sasaki H, Aoto H, Mitaka T, Nagura K, Ohba T, Ishino M, Takahashi S, Suzuki R, Sasaki T. Cell adhesion kinase beta forms a complex with a new member, Hic-5, of proteins localized at focal adhesions. J Biol Chem 273: 1003-1014, 1998.
32. McLemore EC, Tessier DJ, Thresher J, Komalavilas P, Brophy CM. Role of the small heat shock proteins in regulating vascular smooth muscle tone. J Am Coll Surg 201: 30-36, 2005.
33. Mehta D, Gunst SJ. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol 519: 829-840, 1999.
34. Meloche S, Landry J, Huot J, Houle F, Marceau F, Giasson E. p38 MAP kinase pathway regulates angiotensin II-induced contraction of rat vascular smooth muscle. Am J Physiol Heart Circ Physiol 279: H741-H751, 2000.
35. Nishiya N, Tachibana K, Shibanuma M, Mashimo JI, Nose K. Hic-5-reduced cell spreading on fibronectin: competitive effects between paxillin and Hic-5 through interaction with focal adhesion kinase. Mol Cell Biol 21: 5332-5345, 2001.
36. Ohanian J, Cunliffe P, Ceppi E, Alder A, Heerkens E, Ohanian V. Activation of p38 mitogen-activated protein kinases by endothelin and noradrenaline in small arteries, regulation by calcium influx and tyrosine kinases, and their role in contraction. Arterioscler Thromb Vasc Biol 21: 1921-1927, 2001.
37. Ohanian J, Ohanian V, Shaw L, Bruce C, Heagerty AM. Involvement of tyrosine phosphorylation in endothelin-1-induced calcium-sensitization in rat small mesenteric arteries. Br J Pharmacol 120: 653-661, 1997.
38. Ohanian V, Gatfield K, Ohanian J. Role of the actin cytoskeleton in G-protein-coupled receptor activation of PYK2 and paxillin in vascular smooth muscle. Hypertension 46: 93-99, 2005.
39. Opazo Saez A, Zhang W, Wu Y, Turner CE, Tang DD, Gunst SJ. Tension development during contractile stimulation of smooth muscle requires recruitment of paxillin and vinculin to the membrane. Am J Physiol Cell Physiol 286: C433-C447, 2004.
40. Patil SB, Pawar MD, Bitar KN. Phosphorylated HSP27 essential for acetylcholine-induced association of RhoA with PKC-α. Am J Physiol Gastrointest Liver Physiol 286: G635-G644, 2004.
41. Pavalko FM, Adam LP, Wu MF, Walker TL, Gunst SJ. Phosphorylation of dense-plaque proteins talin and paxillin during tracheal smooth muscle contraction. Am J Physiol Cell Physiol 268: C563-C571, 1995.
42. Pichon S, Bryckaert M, Berrou E. Control of actin dynamics by p38 MAP kinase - Hsp27 distribution in the lamellipodium of smooth muscle cells. J Cell Sci 117: 2569-2577, 2004.
43. Rao KM, Betschart JM, Virji MA. Hormone-induced actin polymerization in rat hepatoma cells and human leucocytes. Biochem J 230: 709-714, 1985.
44. Richardson A, Malik RK, Hildebrand JD, Parsons JT. Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol Cell Biol 17: 6906-6914, 1997.
45. Rogalla T, Ehrnsperger M, Preville X, Kotlyarov A, Lutsch G, Ducasse C, Paul C, Wieske M, Arrigo AP, Buchner J, Gaestel M. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J Biol Chem 274: 18947-18956, 1999.
46. Shibanuma M, Mashimo J, Kuroki T, Nose K. Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J Biol Chem 269: 26767-26774, 1994.
47. Somara S, Bitar KN. Phosphorylated HSP27 modulates the association of phosphorylated caldesmon with tropomyosin in colonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 291: G630-G639, 2006.
48. 2+ sensitivity of smooth muscle and non-muscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
49. Storey B, Madden EA. Isolation of subcellular organelles. Methods Enzymol 182: 203-225, 1990.
50. Tang DD, Turner CE, Gunst SJ. Expression of non-phosphorylatable paxillin mutants in canine tracheal smooth muscle inhibits tension development. J Physiol 553: 21-35, 2003.
51. Thomas SM, Hagel M, Turner CE. Characterization of a focal adhesion protein, Hic-5, that shares extensive homology with paxillin. J Cell Sci 112: 181-190, 1999.
52. Walker AJ, Draeger A, Houssa B, van Blitterswijk WJ, Ohanian V, Ohanian J. Diacylglycerol kinase theta is translocated and phosphoinositide 3-kinase-dependently activated by noradrenaline but not angiotensin II in intact small arteries. Biochem J 353: 129-137, 2001.
53. Wang P, Bitar KN. Rho A regulates sustained smooth muscle contraction through cytoskeletal reorganization of HSP27. Am J Physiol Gastrointest Liver Physiol 275: G1454-G1462, 1998.
54. Ward DT, Alder AC, Ohanian J, Ohanian V. Noradrenaline-induced paxillin phosphorylation, ERK activation and MEK-regulated contraction in intact rat mesenteric arteries. J Vasc Res 39: 1-11, 2002.
55. Yamada H, Strahler J, Welsh MJ, Bitar KN. Activation of MAP kinase and translocation with HSP27 in bombesin-induced contraction of rectosigmoid smooth muscle. Am J Physiol Gastrointest Liver Physiol 269: G683-G691, 1995.
56. Yamboliev IA, Hedges JC, Mutnick JL, Adam LP, Gerthoffer WT. Evidence for modulation of smooth muscle force by the p38 MAP kinase/HSP27 pathway. Am J Physiol Heart Circ Physiol 278: H1899-H1907, 2000.
57. Yin HL, Janmey PA. Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65: 761-789, 2003.
58. Yuminamochi T, Yatomi Y, Osada M, Ohmori T, Ishii Y, Nakazawa K, Hosogaya S, Ozaki Y. Expression of the LIM proteins paxillin and Hic-5 in human tissues. J Histochem Cytochem 51: 513-521, 2003.
59. Zheng C, Xing Z, Bian C, Akbay A, Warner L, Guan J. Differential regulation of PYK2 and focal adhesion kinase (FAK). J Biol Chem 273: 2384-2389, 1998.