Real-time imaging elucidates the role of H2O2 in regulating kinetics of epidermal growth factor-induced and Src-mediated tyrosine phosphorylation signaling

Journal of Biomedical Optics

Volumn 17, Issue 7, 2012, Pages

  Su, Ting ^a,b   Li, Xiangyong ^a,b   Liu, Nisha ^a,b   Pan, Shaotao ^a,b   Lu, Jinling ^a,b   Yang, Jie ^a,b   Zhang, Zhihong ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Fluorescence resonance energy transfer; H2O2; Kinetics; Protein tyrosine phosphatase; Protein tyrosine phosphorylation; Src

Indexed keywords

EPIDERMAL GROWTH FACTOR; HYDROGEN PEROXIDE; PROTEIN TYROSINE KINASE;

ARTICLE; COMPUTER SYSTEM; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC PROCEDURES; HELA CELL; HUMAN; KINETICS; METABOLISM; METHODOLOGY; MOLECULAR IMAGING; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN ANALYSIS; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

BIOSENSING TECHNIQUES; COMPUTER SYSTEMS; EPIDERMAL GROWTH FACTOR; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; KINETICS; MOLECULAR IMAGING; PHOSPHORYLATION; PROTEIN INTERACTION MAPPING; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84872043515     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.JBO.17.7.076015     Document Type: Article

References (58)

1. S. G. Julien et al., "Inside the human cancer tyrosine phosphatome," Nat. Rev. Cancer 11(1), 35-49 (2011).
2. Y. S. Bae et al., "Epidermal growth factor (EGF)-induced generation of hydrogen peroxide-role in EGF receptor-mediated tyrosine phosphorylation, " J. Bio. Chem. 272(1), 217-221 (1997). (Pubitemid 27021147)
3. J. C. Juarez et al., "Superoxide dismutase 1 (SOD1) is essential for H2O2-mediated oxidation and inactivation of phosphatases in growth factor signaling," P. Natl. Acad. Sci. USA 105(20), 7147-7152 (2008). (Pubitemid 351754446)
4. 2 for platelet-derived growth factor signal transduction," Science 270(5234), 296-299 (1995).
5. P. Chiarugi and F. Buricchi, "Protein tyrosine phosphorylation and reversible oxidation: two cross-talking posttranslation modifications," Antioxid. Redox. Sign. 9(1), 1-24 (2007). (Pubitemid 44910992)
6. S. R. Lee et al., "Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor," J. Bio. Chem. 273(25), 15366-15372 (1998).
7. P. Chiarugi et al., "Two vicinal cysteines confer a peculiar redox regulation to low molecular weight protein tyrosine phosphatase in response to platelet-derived growth factor receptor stimulation," J. Bio. Chem. 276(36), 33478-33487 (2001).
8. J. J. Hornberg et al., "Principles behind the multifarious control of signal transduction-ERK phosphorylation and kinase/phosphatase control," Febs. J. 272(1), 244-258 (2005). (Pubitemid 40083081)
9. R. Heinrich, B. G. Neel, and T. A. Rapoport, "Mathematical models of protein kinase signal transduction," Mol. Cell 9(5), 957-970 (2002). (Pubitemid 34626667)
10. M. Ebisuya, K. Kondoh, and E. Nishida, "The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity," J. Cell. Sci. 118(14), 2997-3002 (2005). (Pubitemid 41149904)
11. C.J. Marshall, "Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation," Cell 80(2), 179-185 (1995).
12. Y. X. Wang, J. Y. J. Shyy, and S. Chien, "Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing," Annu. Rev. Biomed. Eng. 10, 1-38(2008).
13. J. Zhang et al., "Creating new fluorescent probes for cell biology," Nat. Rev. Mol. Cell. Bio. 3(12), 906-918 (2002). (Pubitemid 35477369)
14. A. Ibraheem and R. E. Campbell, "Designs and applications of fluorescent protein-based biosensors," Curr. Opin. Chem. Bio. 14(1), 30-36 (2010).
15. N. M. Mishina et al., "Does cellular hydrogen peroxide diffuse or act locally?," Antioxid. Redox. Sign. 14(1), 1-7 (2011).
16. D. Wang et al., "Genetically encoded ratiometric biosensors to measure intracellular exchangeable zinc in Escherichia coli," J. Biomed. Opt. 16(8), 087011 (2011).
17. T. Bruns et al., "Forster resonance energy transfer-based total internal reflection fluorescence reader for apoptosis," J. Biomed. Opt. 14(2), 021003 (2009).
18. G. S. Martin, "The road to Src," Oncogene. 23(48), 7910-7917 (2004). (Pubitemid 39468850)
19. T J. Yeatman, "A renaissance for SRC," Nat. Rev. Cancer 4(6), 470-480 (2004). (Pubitemid 38745532)
20. E. Giannoni, M. L. Taddei, and P. Chiarugi, "Src redox regulation: again in the front line," Free Radical Bio. Med. 49(4), 516-527 (2010).
21. E. Giannoni et al., "Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth," Mol. Cell. Bio. 25(15), 6391-6403 (2005). (Pubitemid 41023216)
22. J. Abe et al., "c-Src is required for oxidative stress-mediated activation of big mitogen-activated protein kinase 1 (BMK1)," J. Bio. Chem. 272(33), 20389-20394 (1997). (Pubitemid 27355589)
23. E. K. Krasnowska et al., "N-acetyl-l-cysteine fosters inactivation and transfer to endolysosomes of c-Src," Free Radical Bio. Med. 45(11), 1566-1572 (2008).
24. H. Tang et al., "Inactivation of Src family tyrosine kinases by reactive oxygen species in vivo," J. Biol. Chem. 280(25), 23918-23925 (2005). (Pubitemid 40884880)
25. D. J. Kemble and G. Q. Sun, "Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation," Proc. Natl. Acad. Sci. USA 106(13), 5070-5075 (2009).
26. Y X. Wang et al., "Visualizing the mechanical activation of Src," Nature 434(7036), 1040-1045 (2005).
27. M. X. Ouyang et al., "Determination of hierarchical relationship of Src and Rac at subcellular locations with FRET biosensors," P. Natl. Acad. Sci. USA 105(38), 14353-14358 (2008).
28. G. Huyer et al., "Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate," J. Bio. Chem. 272(2), 843-851 (1997). (Pubitemid 27034572)
29. J. Chu et al., "A novel far-red bimolecular fluorescence complementation system that allows for efficient visualization of protein interactions under physiological conditions," Biosens. Bioelectron. 25(1), 234-239 (2009).
30. J. Brons-Poulsen et al., "An improved PCR-based method for site directed mutagenesis using megaprimers," Mol. Cell. Probe. 12(6), 345-348 (1998). (Pubitemid 29010195)
31. Y C. Poh et al., "Rapid activation of rac GTPase in living cells by force is independent of Src," Plos. One. 4(11), e7886-e7886 (2009).
32. O. Pertz et al., "Spatiotemporal dynamics of RhoA activity in migrating cells," Nature 440(7087), 1069-1072 (2006).
33. R. H. Cool et al., "Rac1, and not Rac2, is involved in the regulation of the intracellular hydrogen peroxide level in HepG2 cells," Biochem. J. 332(Pt 1), 5-8 (1998). (Pubitemid 28239312)
34. 2 production requires the activation of phosphatidylinositol 3-kinase," J. Bio. Chem. 275(14), 10527-10531 (2000). (Pubitemid 30202116)
35. 2," Mol. Cell Bio. 24(10), 4384-4394 (2004).
36. T. L. Leto et al., "Targeting and regulation of reactive oxygen species generation by nox family NADPH oxidases," Antioxid. Redox. Sign. 11(10), 2607-2619 (2009).
37. S. G. Rhee, H. Z. Chae, and K. Kim, "Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling," Free Radical Bio. Med. 38(12), 1543-1552 (2005). (Pubitemid 40726061)
38. 2 accumulation for cell signaling," Cell 140(4), 517-528 (2010).
39. 2 in studies of signal transduction," Free Radical Bio. Med. 42(7), 926-932 (2007). (Pubitemid 46356902)
40. S. Cuddihy, C. C. Winterbourn, and M. B. Hampton, "Assessment of redox changes to hydrogen peroxide-sensitive proteins during EGF signaling," Antioxid. Redox. Sign. 15(1), 167-174 (2011).
41. 2: regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification," Antioxid. Redox. Sign. 7(5-6), 619-626 (2005). (Pubitemid 40563199)
42. 2 and GPx concentrations," Free Radical Res. 41(11), 1201-1211 (2007). (Pubitemid 350090774)
43. M. Gutscher et al., "Real-time imaging of the intracellular glutathione redox potential," Nat. Meth. 5(6), 553-559 (2008). (Pubitemid 351761764)
44. W. C. Barrett et al., "Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B," J. Bio. Chem. 274(49), 34543-34546 (1999). (Pubitemid 129509489)
45. H. Tang et al., "Inactivation of Src family tyrosine kinases by reactive oxygen species in vivo," J. Bio. Chem. 280(25), 23918-23925 (2005). (Pubitemid 40884880)
46. J. M. Cunnick et al., "Role of tyrosine kinase activity of epidermal growth factor receptor in the lysophosphatidic acid-stimulated mitogen-activated protein kinase pathway," J. Bio. Chem. 273(23), 14468-14475 (1998). (Pubitemid 28319168)
47. G. Q. Sun et al., "Effect of autophosphorylation on the catalytic and regulatory properties of protein tyrosine kinase Src," Arch. Biochem. Biophys. 397(1), 11-17 (2002).
48. J. S. Hardwick and B. M. Sefton, "The activated form of the Lck tyrosine protein kinase in cells exposed to hydrogen peroxide is phos-phorylated at both Tyr-394 and Tyr-505," J. Bio. Chem. 272(41), 25429-25432 (1997). (Pubitemid 27438844)
49. J. D. Bjorge, A. Pang, and D. J. Fujita, "Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines," J. Bio. Chem. 275(52), 41439-41446 (2000). (Pubitemid 32054980)
50. X. M. Zheng, R. J. Resnick, and D. Shalloway, "A phosphotyrosine displacement mechanism for activation of Src by PTP alpha," Embo. J. 19(5), 964-978 (2000). (Pubitemid 30119822)
51. J. R. Stone, "An assessment of proposed mechanisms for sensing hydrogen peroxide in mammalian systems," Arch. Biochem. Biophys. 422(2), 119-124 (2004). (Pubitemid 38169357)
52. J. N. LaButti et al., "Redox regulation of protein tyrosine phosphatase 1B by peroxymonophosphate (-O3POOH)," J. Am. Chem. Soc. 129(17), 5320-5321 (2007).
53. H. E. Grecco, M. Schmick, and P. I. H. Bastiaens, "Signaling from the living plasma membrane," Cell 144(6), 897-909 (2011).
54. E. H. Fischer, H. Charbonneau, and N. K. Tonks, "Protein tyrosine phosphatases: a diverse family of intracellular and transmembrane enzymes," Science 253(5018), 401-406 (1991). (Pubitemid 21917164)
55. P. J. Halvey et al., "Compartmental oxidation of thiol-disulphide redox couples during epidermal growth factor signalling," Biochem. J. 386(Pt 2), 215-219 (2005). (Pubitemid 40343778)
56. R. Brigelius-Flohe and A. Kipp, "Glutathione peroxidases in different stages of carcinogenesis," Bba-Gen. Subjects 1790(11), 1555-1568 (2009).
57. C. Cao et al., "Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases," J. Bio. Chem. 278(41), 39609-39614 (2003). (Pubitemid 37248520)
58. X. G. Sun et al., "Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species," J. Bio. Chem. 275(23), 17237-17240 (2000).