Thioredoxin reductase linked to cytoskeleton by focal adhesion kinase reverses actin S-nitrosylation and restores neutrophil β2 integrin function

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30346-30357

  Thom, Stephen R ^a,b   Bhopale, Veena M ^a   Milovanova, Tatyana N ^a   Yang, Ming ^a   Bogush, Marina ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENT; CELL LYSATES; CYTOCHALASIN D; CYTOSKELETONS; CYTOSOLS; EX-VIVO; FOCAL ADHESION KINASE; HIGH OXYGEN PARTIAL PRESSURE; HYPEROXIA; IMMUNOPRECIPITATIONS; INTEGRINS; ISOLATED ENZYMES; KINASE DOMAINS; LATRUNCULIN B; PHYSICAL SEPARATION; S-NITROSYLATION; THIOREDOXIN REDUCTASE; VASODILATOR-STIMULATED PHOSPHOPROTEINS;

ADHESION; ENZYMES; SIGNAL TRANSDUCTION;

PROTEINS;

8 BROMO CYCLIC GMP; ACTIN; BETA2 INTEGRIN; CYTOCHALASIN D; FOCAL ADHESION KINASE; FORMYLMETHIONYLLEUCYLPHENYLALANINE; G ACTIN; LATRUNCULIN B; PHOSPHOPROTEIN; SHORT FILAMENTOUS ACTIN; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; DISSOCIATION; ENZYME ACTIVITY; EX VIVO STUDY; MOUSE; NEUTROPHIL; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TURNOVER TIME; ULTRAVIOLET RADIATION;

ACTINS; ANIMALS; ANTIGENS, CD18; CELL LINE; CYTOSKELETON; FOCAL ADHESION KINASE 1; HUMANS; NEUTROPHILS; PROTEIN TRANSPORT; RATS; THIOREDOXIN-DISULFIDE REDUCTASE;

EID: 84865773318     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.355875     Document Type: Article

References (64)

1. Brown, E. J., and Lindberg, F. P. (1996) Leukocyte adhesion molecules in host defence against infection. Ann. Med. 28, 201-208
2. Thom, S. R. (1993) Functional inhibition of leukocyte B2 integrins by hyperbaric oxygen in carbon monoxide-mediated brain injury in rats. Toxicol. Appl. Pharmacol. 123, 248-256
3. 2. Am. J. Physiol. 272, C770-C777
4. Kalns, J., Lane, J., Delgado, A., Scruggs, J., Ayala, E., Gutierrez, E., Warren, D., Niemeyer, D., George Wolf, E., and Bowden, R. A. (2002) Hyperbaric oxygen exposure temporarily reduces Mac-1-mediated functions of human neutrophils. Immunol. Lett. 83, 125-131
5. Labrouche, S., Javorschi, S., Leroy, D., Gbikpi-Benissan, G., and Freyburger, G. (1999) Influence of hyperbaric oxygen on leukocyte functions and hemostasis in normal volunteer divers. Thromb. Res. 96, 309-315
6. Zamboni, W. A., Roth, A. C., Russell, R. C., Graham, B., Suchy, H., and Kucan, J. O. (1993) Morphologic analysis of the microcirculation during reperfusion of ischemic skeletal muscle and the effect of hyperbaric oxygen. Plast. Reconstr. Surg. 91, 1110-1123
7. Martin, J. D., and Thom, S. R. (2002) Vascular leukocyte sequestration in decompression sickness and prophylactic hyperbaric oxygen therapy in rats. Aviat. Space Environ. Med. 73, 565-569
8. Atochin, D. N., Fisher, D., Demchenko, I. T., and Thom, S. R. (2000) Neutrophil sequestration and the effect of hyperbaric oxygen in a rat model of temporary middle cerebral artery occlusion. Undersea Hyperb. Med. 27, 185-190
9. Tähepõld, P., Vaage, J., Starkopf, J., and Valen, G. (2003) Hyperoxia elicits myocardial protection through a nuclear factor κB-dependent mechanism in the rat heart. J. Thorac. Cardiovasc Surg. 125, 650-660
10. Tähepold, P., Valen, G., Starkopf, J., Kairane, C., Zilmer, M., and Vaage, J. (2001) Pretreating rats with hyperoxia attenuates inschemia- reperfusion injury of the heart. Life Sci. 68, 1629-1640
11. Ueno, S., Tanabe, G., Kihara, K., Aoki, D., Arikawa, K., Dogomori, H., and Aikou, T. (1999) Early postoperative hyperbaric oxygen therapy modifies neutrophile activation. Hepatol. Gastroenterology 46, 1798-1799
12. Wong, H. P., Zamboni, W. A., and Stephenson, L. L. (1996) Effect of hyperbaric oxygen on skeletal muscle necrosis following primary and secondary ischemia in a rat model. Surg. Forum 705-707
13. 2 reduces intestinal ischemia-reperfusion-induced TNF-α production and lung neutrophil sequestration. Eur. J. Appl. Physiol. 85, 96-103
14. Sharifi, M., Fares, W., Abdel-Karim, I., Koch, J. M., Sopko, J., Adler, D., and the Hyperbaric Oxygen Therapy in Percutaneous Coronary Interventions Investigators (2004) Usefulness of hyperbaric oxygen therapy to inhibit restenosis after percutaneous coronary intervention for acute myocardial infarction or unstable angina pectoris. Am. J. Cardiol. 93, 1533-1535
15. Sharifi, M., Fares, W., Abdel-Karim, I., Petrea, D., Koch, J. M., Adler, D., Sopko, J., and the Hyperbaric Oxygen Therapy in Percutaneous Coronary Interventions (HOT-PI) Investigators (2002) Inhibition of restenosis by hyperbaric oxygen. A novel indication for an old modality. Cardiovasc. Radiat. Med. 3, 124-126
16. Shandling, A. H., Ellestad, M. H., Hart, G. B., Crump, R., Marlow, D., Van Natta, B., Messenger, J. C., Strauss, M., and Stavitsky, Y. (1997) Hyperbaric oxygen and thrombolysis in myocardial infarction. The HOT MI pilot study. Am. Heart J. 134, 544-550
17. Stavitsky, Y., Shandling, A. H., Ellestad, M. H., Hart, G. B., Van Natta, B., Messenger, J. C., Strauss, M., Dekleva, M. N., Alexander, J. M., Mattice, M., and Clarke, D. (1998) Hyperbaric oxygen and thrombolysis in myocardial infarction. The "HOT MI" randomized multicenter study. Cardiology 90, 131-136
18. Weaver, L. K., Hopkins, R. O., Chan, K. J., Churchill, S., Elliott, C. G., Clemmer, T. P., Orme, J. F., Jr., Thomas, F. O., and Morris, A. H. (2002) Hyperbaric oxygen for acute carbon monoxide poisoning. N. Engl. J. Med. 347, 1057-1067
19. Alex, J., Laden, G., Cale, A. R., Bennett, S., Flowers, K., Madden, L., Gardiner, E., McCollum, P. T., and Griffin, S. C. (2005) Pretreatment with hyperbaric oxygen and its effect on neuropsychometric dysfunction and systemic inflammatory response after cardiopulmonary bypass. A prospective randomized double-blind trial. J. Thorac. Cardiovasc. Surg. 130, 1623-1630
20. Juttner, B., Scheinichen, D., Bartsch, S., Heine, J., Ruschulte, H., Elsner, H., Franko, W., and Jaeger, K. (2003) Lack of toxic side effects in neutrophils following hyperbaric oxygen. Undersea Hyperbar. Med. 30, 305-311
21. Mileski, W. J., Sikes, P., Atiles, L., Lightfoot, E., Lipsky, P., and Baxter, C. (1993) Inhibition of leukocyte adherence and susceptibility to infection. J. Surg. Res. 54, 349-354
22. Mileski, W. J., Winn, R. K., Vedder, N. B., Pohlman, T. H., Harlan, J. M., and Rice, C. L. (1990) Inhibition of CD18-dependent neutrophil adherence reduces organ injury after hemorrhagic shock in primates. Surgery 108, 206-212
23. Thom, S. R., Lauermann, M. W., and Hart, G. B. (1986) Intermittent hyperbaric oxygen therapy for reduction of mortality in experimental polymicrobial sepsis. J. Infect. Dis. 154, 504-510
24. Ross, R. M., and McAllister, T. A. (1965) Protective action of hyperbaric oxygen in mice with pneumococcal septicemia Lancet 1, 579-581
25. Buras, J., Holt, D., Orlow, D., Belikoff, B., Pavlides, S., and Reenstra, W. (2006) Hyperbaric oxygen protects from sepsis mortality via an interleukin- 10-dependent mechanism. Crit. Care Med. 34, 2624-2629
26. Thom, S. R., Bhopale, V. M., Mancini, D. J., and Milovanova, T. N. (2008) Actin S-nitrosylation inhibits neutrophil β-2 integrin function. J. Biol. Chem. 283, 10822-10834
27. Thom, S. R., Bhopale, V. M., Yang, M., Bogush, M., Huang, S., and Milovanova, T. (2011) Neutrophil β2 integrin inhibition by enhanced interactions of vasodilator stimulated phosphoprotein with S-nitrosylated actin. J. Biol. Chem. 286, 32854-32865
28. Thom, S. R. (2009) Oxidative stress is fundamental to hyperbaric oxygen therapy. J. Appl. Physiol. 106, 988-995
29. Marasco, W. A., Phan, S. H., Krutzsch, H., Showell, H. J., Feltner, D. E., Nairn, R., Becker, E. L., and Ward, P. A. (1984) Purification and identification of formyl-methionyl-leucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J. Biol. Chem. 259, 5430-5439
30. Stoyanovsky, D. A., Tyurina, Y. Y., Tyurin, V. A., Anand, D., Mandavia, D. N., Gius, D., Ivanova, J., Pitt, B., Billiar, T. R., and Kagan, V. E. (2005) Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols. J. Am. Chem. Soc. 127, 15815-15823
31. Matuda, S., and Saheki, T. (1982) Intracellular distribution and biosynthesis of lipoamide dehydrogenase in rat liver. J. Biochem. 91, 553-561
32. Sun, Q. A., Su, D., Novoselov, S. V., Carlson, B. A., Hatfield, D. L., and Gladyshev, V. N. (2005) Reaction mechanism and regulation of mammalian thioredoxin/glutathione reductase. Biochemistry 44, 14528-14537
33. Sun, Q. A., Kirnarsky, L., Sherman, S., and Gladyshev, V. N. (2001) Selenoprotein oxidoreductase with specificity for thioredoxin and glutathione systems. Proc. Natl. Acad. Sci. U.S.A. 98, 3673-3678
34. Arnér, E. S., and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109
35. Rigobello, M. P., Callegaro, M. T., Barzon, E., Benetti, M., and Bindoli, A. (1998) Purification of mitochondrial thioredoxin reductase and its involvement in the redox regulation of membrane permeability. Free Radic. Biol. Med. 24, 370-376
36. Benhar, M., Forrester, M. T., and Stamler, J. S. (2009) Protein denitrosylation. Enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 10
37. Foster, M. W., Liu, L., Zeng, M., Hess, D. T., and Stamler, J. S. (2009) A genetic analysis of nitrosative stress. Biochemistry 48, 792-799
38. Schlaepfer, D. D., Mitra, S. K., and Ilic, D. (2004) Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim. Biophys. Acta 1692, 77-102
39. FAK) in PHA-activated T cells. Cell Immunol. 193, 179-184
40. Sada, K., Minami, Y., and Yamamura, H. (1997) Relocation of Syk proteintyrosine kinase to the actin filament network and subsequent association with Fak. Eur. J. Biochem. 248, 827-833
41. Totani, L., Piccoli, A., Manarini, S., Federico, L., Pecce, R., Martelli, N., Cerletti, C., Piccardoni, P., Lowell, C. A., Smyth, S. S., Berton, G., and Evangelista, V. (2006) Src-family kinases mediate an outside-in signal necessary for B2 integrins to achieve full activation and sustain firm adhesion of polymorphonuclear leukocytes tethered on E-selectin. Biochem. J. 396, 89-98
42. Serrels, B., Serrels, A., Brunton, V. G., Holt, M., McLean, G. W., Gray, C. H., Jones, G. E., and Frame, M. C. (2007) Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol. 9, 1046-1056
43. Ilić, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544
44. Clark, E. A., and Brugge, J. S. (1995) Integrins and signal transduction pathways. The road taken. Science 268, 233-239
45. García-Alvarez, B., de Pereda, J. M., Calderwood, D. A., Ulmer, T. S., Critchley, D., Campbell, I. D., Ginsberg, M. H., and Liddington, R. C. (2003) Structural determinants of integrin recognition by talin. Mol. Cell 11, 49-58
46. Arold, S. T. (2011) How focal adhesion kinase achieves regulation by linking ligand binding, localization and action. Curr. Opin. Struct. Biol. 21, 808-813
47. Schaller, M. D., Otey, C. A., Hildebrand, J. D., and Parsons, J. T. (1995) Focal adhesion kinase and paxillin bind to peptides mimicking β integrin cytoplasmic domains. J. Cell Biol. 130, 1181-1187
48. Parsons, J. T. (2003) Focal adhesion kinase. The first ten years. J. Cell Sci. 116, 1409-1416
49. Zheng, D., Kurenova, E., Ucar, D., Golubovskaya, V., Magis, A., Ostrov, D., Cance, W. G., and Hochwald, S. N. (2009) Targeting of the protein interaction site between FAK and IGF-1R. Biochem. Biophys. Res. Commun. 388, 301-305
50. Wang, X., Kettenhofen, N. J., Shiva, S., Hogg, N., and Gladwin, M. T. (2008) Copper dependence of the biotin switch assay. Modified assay for measuring cellular and blood nitrosated proteins. Free Radic. Biol. Med. 44, 1362-1372
51. Hill, K. E., McCollum, G. W., and Burk, R. F. (1997) Determination of thioredoxin reductase activity in rat liver supernatant. Anal. Biochem. 253, 123-125
52. Thom, S. R., Bhopale, V. M., Fisher, D., Zhang, J., and Gimotty, P. (2004) Delayed neuropathology after carbon monoxide poisoning is immune-mediated. Proc. Natl. Acad. Sci. U.S.A. 101, 13660-13665
53. Slack-Davis, J. K., Martin, K. H., Tilghman, R. W., Iwanicki, M., Ung, E. J., Autry, C., Luzzio, M. J., Cooper, B., Kath, J. C., Roberts, W. G., and Parsons, J. T. (2007) Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem. 282, 14845-14852
54. Su, Y., Kondrikov, D., and Block, E. R. (2005) Cytoskeletal regulation of nitric-oxide synthase. Cell Biochem. Biophys. 43, 439-449
55. Kone, B. C., Kuncewicz, T., Zhang, W., and Yu, Z. Y. (2003) Protein interactions with nitric oxide synthases. Controlling the right time, the right place, and the right amount of nitric oxide. Am. J. Physiol. 285, F178-F190
56. Abbi, S., Ueda, H., Zheng, C., Cooper, L. A., Zhao, J., Christopher, R., and Guan, J. L. (2002) Regulation of focal adhesion kinase by a novel protein inhibitor, FIP200. Mol. Biol. Cell 13, 3178-3191
57. Volonte, D., and Galbiati, F. (2009) Inhibition of thioredoxin reductase 1 by caveolin 1 promotes stress-induced premature senescence. EMBORep. 10, 1334-1340
58. Du, P., Loulakis, P., Luo, C., Mistry, A., Simons, S. P., LeMotte, P. K., Rajamohan, F., Rafidi, K., Coleman, K. G., Geoghegan, K. F., and Xie, Z. (2005) Phosphorylation of serine residues in histidine tag sequences attached to recombinant protein kinases. A cause of heterogeneity in mass and complications in function. Protein Expr. Purif. 44, 121-129
59. Kanchanawong, P., Shtengel, G., Pasapera, A. M., Ramko, E. B., Davidson, M. W., Hess, H. F., and Waterman, C. M. (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584
60. Toutant, M., Costa, A., Studler, J. M., Kadaré, G., Carnaud, M., and Girault, J. A. (2002) Alternative splicing controls the mechanisms of FAK autophosphorylation. Mol. Cell Biol. 22, 7731-7743
61. Sroka, J., Antosik, A., Czyz, J., Nalvarte, I., Olsson, J. M., Spyrou, G., and Madeja, Z. (2007) Overexpression of thioredoxin reductase 1 inhibits migration of HEK-293 cells. Biol. Cell 99, 677-687
62. Dammeyer, P., Damdimopoulos, A. E., Nordman, T., Jiménez, A., Miranda- Vizuete, A., and Arnér, E. S. (2008) Induction of cell membrane protrusions by the N-terminal glutaredoxin domain of a rare splice variant of human thioredoxin reductase 1. J. Biol. Chem. 283, 2814-2821
63. Damdimopoulou, P. E., Miranda-Vizuete, A., Arnér, E. S., Gustafsson, J. A., and Damdimopoulos, A. E. (2009) The human thioredoxin reductase- 1 splice variant TXNRD1-v3 is an atypical inducer of cytoplasmic filaments and cell membrane filopodia. Biochim. Biophys. Acta 1793, 1588-1596
64. Wang, X., Ling, S., Zhao, D., Sun, Q., Li, Q., Wu, F., Nie, J., Qu, L., Wang, B., Shen, X., Bai, Y., Li, Y., and Li, Y. (2010) Redox regulation of actin by thioredoxin-1 is mediated by the interaction of the proteins via cysteine 62. Antioxid. Redox Signal. 13, 565-573