Angiotensin-II and Marcks: A hydrogen peroxide- and Rac1-dependent signaling pathway in vascular endothelium

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 29147-29158

  Kalwa, Hermann ^a   Sartoretto, Juliano L ^a   Sartoretto, Simone M ^a   Michel, Thomas ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5-BISPHOSPHATE; ACTIN FIBERS; ACTIN-BINDING PROTEINS; CELL IMAGING; CYTOSKELETAL; CYTOSKELETONS; PATHOPHYSIOLOGY; PHOSPHOINOSITIDES; SIGNALING PATHWAYS; TYROSINE KINASE; VASCULAR ENDOTHELIAL CELLS; VASCULAR ENDOTHELIUM;

AMINO ACIDS; ENDOTHELIAL CELLS; HYDROGEN PEROXIDE; PHOSPHORYLATION; PROTEINS;

BIOSENSORS;

ABELSON KINASE; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; CATALASE; HYDROGEN PEROXIDE; MARCKS PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; RAC1 PROTEIN; SMALL INTERFERING RNA; VINCULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSENSOR; CELL ADHESION; CELL ASSAY; CONTROLLED STUDY; ENZYME ACTIVATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR ENDOTHELIUM;

ANGIOTENSIN II; ANIMALS; BIOSENSING TECHNIQUES; CATALASE; CATTLE; CYTOSKELETON; ENDOTHELIUM, VASCULAR; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; POLYETHYLENE GLYCOLS; PROTO-ONCOGENE PROTEINS C-ABL; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84865237234     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.381517     Document Type: Article

References (49)

1. Blackshear, P. J. (1993) The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268, 1501-1504
2. Arnold, T. P., Standaert, M. L., Hernandez, H., Watson, J., Mischak, H., Kazanietz, M. G., Zhao, L., Cooper, D. R., and Farese, R. V. (1993) Effects of insulin and phorbol esters on MARCKS (myristoylated alanine-rich C-kinase substrate) phosphorylation (and other parameters of protein kinase C activation) in rat adipocytes, rat soleus muscle, and BC3H-1 myocytes. Biochem. J. 295, 155-164
3. Arbuzova, A., Schmitz, A. A., and Vergeres, G. (2002) Cross-talk unfolded: MARCKS proteins. Biochem. J. 362, 1-12
4. Lu, D., Yang, H., Lenox, R. H., and Raizada, M. K. (1998) Regulation of angiotensin II-induced neuromodulation by MARCKS in brain neurons. J. Cell Biol. 142, 217
5. Shiraishi, M., Tanabe, A., Saito, N., and Sasaki, Y. (2006) Unphosphorylated MARCKS is involved in neurite initiation induced by insulin-like growth factor-I in SH-SY5Y cells. J. Cell. Physiol. 209, 1029-1038
6. Yamaguchi, H., Shiraishi, M., Fukami, K., Tanabe, A., Ikeda-Matsuo, Y., Naito, Y., and Sasaki, Y. (2009)MARCKSregulates lamellipodia formation induced by IGF-I via association with PIP2 and β-actin at membrane microdomains. J. Cell. Physiol. 220, 748-755
7. Finlayson, A. E., and Freeman, K. W. (2009) A cell motility screen reveals role for MARCKS-related protein in adherens junction formation and tumorigenesis. PLoS One 4, e7833
8. Tzlil, S., Murray, D., and Ben-Shaul, A. (2008) The "electrostatic- switch" mechanism: Monte Carlo study of MARCKS-membrane interaction. Biophys. J. 95, 1745-1757
9. Calabrese, B., and Halpain, S. (2005) Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron 48, 77-90
10. Gadi, D., Wagenknecht-Wiesner, A., Holowka, D., and Baird, B. (2011) Sequestration of phosphoinositides by mutated MARCKS effector domain inhibits stimulated Ca(2+) mobilization and degranulation in mast cells. Mol. Biol. Cell 22, 4908-4917
11. Hussain, R. J., Stumpo, D. J., Blackshear, P. J., Lenox, R. H., Abel, T., and McNamara, R. K. (2006) Myristoylated alanine-rich C kinase substrate (MARCKS) heterozygous mutant mice exhibit deficits in hippocampal mossy fiber-CA3 long-term potentiation. Hippocampus 16, 495-503
12. Kalwa, H., and Michel, T. (2011) The MARCKS protein plays a critical role in phosphatidylinositol 4,5-bisphosphate metabolism and directed cell movement in vascular endothelial cells. J. Biol. Chem. 286, 2320-2330
13. Monahan, T. S., Andersen, N. D., Martin, M. C., Malek, J. Y., Shrikhande, G. V., Pradhan, L., Ferran, C., and LoGerfo, F. W. (2009) MARCKS silencing differentially affects human vascular smooth muscle and endothelial cell phenotypes to inhibit neointimal hyperplasia in saphenous vein. FASEB J., 23, 557-564
14. Tanabe, A., Shiraishi, M., Negishi, M., Saito, N., Tanabe, M., and Sasaki, Y. (2012) MARCKS dephosphorylation is involved in bradykinin-induced neurite outgrowth in neuroblastoma SH-SY5Y cells. J. Cell. Physiol. 227, 618-629
15. Cai, H. (2005) Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc. Res. 68, 26-36
16. Finkel, T. (2001) Reactive oxygen species and signal transduction. IUBMB Life 52, 3-6
17. Mehta, P. K., and Griendling, K. K. (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am. J. Physiol. Cell Physiol. 292, C82-C97
18. Nathan, C. (2003) Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 111, 769-778
19. Desideri, G., Bravi, M. C., Tucci, M., Croce, G., Marinucci, M. C., Santucci, A., Alesse, E., and Ferri, C. (2003) Angiotensin II inhibits endothelial cell motility through an AT1-dependent oxidant-sensitive decrement of nitric oxide availability. Arterioscler. Thromb. Vasc. Biol. 23, 1218-1223
20. Rateri, D. L., Moorleghen, J. J., Balakrishnan, A., Owens, A. P., 3rd, Howatt, D. A., Subramanian, V., Poduri, A., Charnigo, R., Cassis, L. A., and Daugherty, A. (2011) Endothelial cell-specific deficiency of Ang II type 1a receptors attenuates Ang II-induced ascending aortic aneurysms in LDL receptor-/- mice. Circ. Res., 108, 574-581
21. Al Ghouleh, I., Khoo, N. K., Knaus, U. G., Griendling, K. K., Touyz, R. M., Thannickal, V. J., Barchowsky, A., Nauseef, W. M., Kelley, E. E., Bauer, P. M., Darley-Usmar, V., Shiva, S., Cifuentes-Pagano, E., Freeman, B. A., Gladwin, M. T., and Pagano, P. J. (2011) Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radic. Biol. Med. 51, 1271-1288
22. Apel, K., and Hirt, H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399
23. Amanso, A. M., and Griendling, K. K. (2012) Differential roles of NADPH oxidases in vascular physiology and pathophysiology. Front. Biosci. 4, 1044-1064
24. Garrido, A. M., and Griendling, K. K. (2009) NADPH oxidases and angiotensin II receptor signaling. Mol. Cell. Endocrinol. 302, 148-158
25. Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V., and Lukyanov, S. (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281-286
26. Choi, H., Kim, S., Mukhopadhyay, P., Cho, S., Woo, J., Storz, G., and Ryu, S. E. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105, 103-113
27. 2 with expanded dynamic range. Bioorg. Med. Chem. 19, 1079-1084
28. Sartoretto, J. L., Kalwa, H., Pluth, M. D., Lippard, S. J., and Michel, T. (2011) Hydrogen peroxide differentially modulates cardiac myocyte ni-tric- oxide synthesis. Proc. Natl. Acad. Sci. U.S.A. 108, 15792-15797
29. Dietrich, U., Krüger, P., Gutberlet, T., and Käs, J. A. (2009) Interaction of the MARCKS peptide with PIP2 in phospholipid monolayers. Biochim. Biophys. Acta 1788, 1474-1481
30. Aoki, K., Nakamura, T., Inoue, T., Meyer, T., and Matsuda, M. (2007) An essential role for the SHIP2-dependent negative feedback loop in neuritogenesis of nerve growth factor-stimulated PC12 cells. J. Cell Biol. 177, 817-827
31. Sato, M., Ueda, Y., Takagi, T., and Umezawa, Y. (2003) Production of PtdInsP3 at endomembranes is triggered by receptor endocytosis. Nat. Cell Biol. 5, 1016-1022
32. Gonzalez, E., Kou, R., and Michel, T. (2006) Rac1 modulates sphingosine 1-phosphate-mediated activation of phosphoinositide 3-kinase/Akt signaling pathways in vascular endothelial cells. J. Biol. Chem., 281, 3210-3216
33. Aoki, K., and Matsuda, M. (2009) Visualization of small GTPase activity with fluorescence resonance energy transfer-based biosensors. Nat. Protoc. 4, 1623-1631
34. Aoki, K., Nakamura, T., and Matsuda, M. (2004) Spatio-temporal regulation of Rac1 and Cdc42 activity during nerve growth factor-induced neurite outgrowth in PC12 cells. J. Biol. Chem. 279, 713-719
35. Itoh, R. E., Fujioka, A., Sharma, A., Mayer, B. J., and Matsuda, M. (2005) A FRET-based probe for epidermal growth factor receptor bound non-covalently to a pair of synthetic amphipathic helixes. Exp. Cell Res. 307, 142-152
36. Colicelli, J. (2010) ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal. 3, re6
37. Schlatterer, S. D., Acker, C. M., and Davies, P. (2011) c-Abl in neurodegenerative disease. J. Mol. Neurosci. 45, 445-452
38. Wang, B., E., Golemis, E. A., and Kruh, G. D. (1997) ArgBP2, a multiple Src homology 3 domain-containing, Arg/Abl-interacting protein, is phosphorylated in v-Abl-transformed cells and localized in stress fibers and cardiocyte Z-disks. J. Biol. Chem. 272, 17542-17550
39. Zandy, N. L., and Pendergast, A. M. (2008) Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases. Cell Cycle 7, 444-448
40. Pluk, H., Dorey, K., and Superti-Furga, G. (2002) Autoinhibition of c-Abl. Cell 108, 247-259
41. Izard, T., Evans, G., Borgon, R. A., Rush, C. L., Bricogne, G., and Bois, P. R. (2004) Vinculin activation by talin through helical bundle conversion. Nature 427, 171-175
42. Yang, H. J., Chen, J. Z., Zhang, W. L., and Ding, Y. Q. (2010) Focal adhesion plaque associated cytoskeletons are involved in the invasion and metastasis of human colorectal carcinoma. Cancer Invest. 28, 127-134
43. Blackshear, P. J., Lai, W. S., Tuttle, J. S., Stumpo, D. J., Kennington, E., Nairn, A. C., and Sulik, K. K. (1996) Developmental expression of MARCKS and protein kinase C in mice in relation to the exencephaly resulting from MARCKS deficiency. Brain Res. Dev. Brain. Res. 96, 62-75
44. Sechi, A. S., and Wehland, J. (2000) The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113, 3685-3695
45. Niethammer, P., Grabher, C., Look, A. T., and Mitchison, T. J. (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996-999
46. Aoki, K., Kiyokawa, E., Nakamura, T., and Matsuda, M. (2008) Visualization of growth signal transduction cascades in living cells with genetically encoded probes based on Forster resonance energy transfer. Philos. Trans R Soc. Lond. B Biol. Sci. 363, 2143-2151
47. Yoshizaki, H., Mochizuki, N., Gotoh, Y., and Matsuda, M. (2007) Akt- PDK1 complex mediates epidermal growth factor-induced membrane protrusion through Ral activation. Mol. Biol. Cell 18, 119-128
48. Cowen, T., Haven, A. J., and Burnstock, G. (1985) Pontamine sky blue: a counterstain for background autofluorescence in fluorescence and immunofluorescence histochemistry. Histochemistry 82, 205-208
49. Jin, B. Y., Sartoretto, J. L., Gladyshev, V. N., and Michel, T. (2009) Endothelial nitric oxide synthase negatively regulates hydrogen peroxide-stimulated AMP-activated protein kinase in endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 106, 17343-17348