Protein kinase G increases antioxidant function in lung microvascular endothelial cells by inhibiting the c-Abl tyrosine kinase

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 6, 2014, Pages

  Scott Stephens, R ^a   Servinsky, Laura E ^a   Rentsendorj, Otgonchimeg ^a   Kolb, Todd M ^a   Pfeifer, Alexander ^b   Pearse, David B ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Acute lung injury; c Abl; Endothelium; Oxidant injury; Protein kinase G

Indexed keywords

ABELSON KINASE; ATRIAL NATRIURETIC FACTOR; CATALASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DERIVATIVE; GLUTATHIONE PEROXIDASE 1; HYDROGEN PEROXIDE; IMATINIB; OXIDIZING AGENT; PROTEIN KINASE G1; PROTEIN TYROSINE KINASE INHIBITOR; UNCLASSIFIED DRUG; BENZAMIDE DERIVATIVE; DRUG DERIVATIVE; GLUTATHIONE PEROXIDASE; MESSENGER RNA; PIPERAZINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DRUG MECHANISM; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ISOLATED LUNG; LUNG ENDOTHELIUM; MALE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WILD TYPE; ACTIVE TRANSPORT; ANIMAL; APOPTOSIS; BIOSYNTHESIS; C-ABL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENDOTHELIUM; ENDOTHELIUM CELL; GENETICS; KNOCKOUT MOUSE; LUNG; METABOLISM; OXIDANT INJURY; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ACUTE LUNG INJURY; C-ABL; ENDOTHELIUM; OXIDANT INJURY; PROTEIN KINASE G;

ACTIVE TRANSPORT, CELL NUCLEUS; ACUTE LUNG INJURY; ANIMALS; APOPTOSIS; ATRIAL NATRIURETIC FACTOR; BENZAMIDES; CATALASE; CELLS, CULTURED; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENDOTHELIAL CELLS; ENZYME ACTIVATION; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATION-REDUCTION; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-ABL; PYRIMIDINES; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84900035820     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00375.2012     Document Type: Article

References (62)

1. Agami R, Blandino G, Oren M, Shaul Y. Interaction of c-Abl and p73alpha and their collaboration to induce apoptosis. Nature 399: 809-813, 1999.
2. Akashi N, Matsumoto I, Tanaka Y, Inoue A, Yamamoto K, Umeda N, Tanaka Y, Hayashi T, Goto D, Ito S, Sekiguchi K, Sumida T. Comparative suppressive effects of tyrosine kinase inhibitors imatinib and nilotinib in models of autoimmune arthritis. Mod Rheumatol 21: 267-275, 2011.
3. Aman J, van BJ, Damanafshan A, Huveneers S, Eringa EC, Vogel SM, Groeneveld AB, Vonk NA, van Hinsbergh VW, van Nieuw Amerongen GP. Effective treatment of edema and endothelial barrier dysfunction with imatinib. Circulation 126: 2728-2738, 2012.
4. Awazu M. Inhibition of platelet-derived growth factor receptor tyrosine kinase by atrial natriuretic peptide. Kidney Int 52: 356-362, 1997.
5. Brasher BB, Van Etten RA. c-Abl has high intrinsic tyrosine kinase activity that is stimulated by mutation of the Src homology 3 domain and by autophosphorylation at two distinct regulatory tyrosines. J Biol Chem 275: 35631-35637, 2000.
6. Bruecher-Encke B, Griffin JD, Neel BG, Lorenz U. Role of the tyrosine phosphatase SHP-1 in K562 cell differentiation. Leukemia 15: 1424-1432, 2001.
7. Buchdunger E, O'Reilly T, Wood J. Pharmacology of imatinib (STI571). Eur J Cancer 38, Suppl 5: S28-S36, 2002.
8. Cao C, Leng Y, Huang W, Liu X, Kufe D. Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases. J Biol Chem 278: 39609-39614, 2003.
9. Cao C, Leng Y, Li C, Kufe D. Functional interaction between the c-Abl and Arg protein-tyrosine kinases in the oxidative stress response. J Biol Chem 278: 12961-12967, 2003.
10. Cao C, Leng Y, Liu X, Yi Y, Li P, Kufe D. Catalase is regulated by ubiquitination and proteosomal degradation. Role of the c-Abl and Arg tyrosine kinases. Biochemistry 42: 10348-10353, 2003.
11. Christofidou-Solomidou M, Scherpereel A, Wiewrodt R, Ng K, Sweitzer T, Arguiri E, Shuvaev V, Solomides CC, Albelda SM, Muzykantov VR. PECAM-directed delivery of catalase to endothelium protects against pulmonary vascular oxidative stress. Am J Physiol Lung Cell Mol Physiol 285: L283-L292, 2003.
12. Colicelli J. ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal 3: re6, 2010.
13. Conforti F, Sayan AE, Sreekumar R, Sayan BS. Regulation of p73 activity by post-translational modifications. Cell Death Dis 3: e285, 2012.
14. Cong F, Spencer S, Cote JF, Wu Y, Tremblay ML, Lasky LA, Goff SP. Cytoskeletal protein PSTPIP1 directs the PEST-type protein tyrosine phosphatase to the c-Abl kinase to mediate Abl dephosphorylation. Mol Cell 6: 1413-1423, 2000.
15. Costanzo A, Merlo P, Pediconi N, Fulco M, Sartorelli V, Cole PA, Fontemaggi G, Fanciulli M, Schiltz L, Blandino G, Balsano C, Levrero M. DNA damage-dependent acetylation of p73 dictates the selective activation of apoptotic target genes. Mol Cell 9: 175-186, 2002.
16. Das A, Smolenski A, Lohmann SM, Kukreja RC. Cyclic GMP-dependent protein kinase Ialpha attenuates necrosis and apoptosis following ischemia/reoxygenation in adult cardiomyocyte. J Biol Chem 281: 38644-38652, 2006.
17. Dodd-o JM, Hristopoulos ML, Kibler K, Gutkowska J, Mukaddam-Daher S, Gonzalez A, Welsh-Servinsky LE, Pearse DB. The role of natriuretic peptide receptor-A signaling in unilateral lung ischemia-reperfusion injury in the intact mouse. Am J Physiol Lung Cell Mol Physiol 294: L714-L723, 2008.
18. Dudek SM, Chiang ET, Camp SM, Guo Y, Zhao J, Brown ME, Singleton PA, Wang L, Desai A, Arce FT, Lal R, Van Eyk JE, Imam SZ, Garcia JG. Abl tyrosine kinase phosphorylates nonmuscle Myosin light chain kinase to regulate endothelial barrier function. Mol Biol Cell 21: 4042-4056, 2010.
19. Gajic O, Dabbagh O, Park PK, Adesanya A, Chang SY, Hou P, Anderson H, III, Hoth JJ, Mikkelsen ME, Gentile NT, Gong MN, Talmor D, Bajwa E, Watkins TR, Festic E, Yilmaz M, Iscimen R, Kaufman DA, Esper AM, Sadikot R, Douglas I, Sevransky J, Malinchoc M. Early identification of patients at risk of acute lung injury: evaluation of lung injury prediction score in a multicenter cohort study. Am J Respir Crit Care Med 183: 462-470, 2011.
20. Garcia JG, Davis HW, Patterson CE. Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol 163: 510-522, 1995.
21. Hantschel O, Superti-Furga G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 5: 33-44, 2004.
22. Huang P, Zhao XS, Fields M, Ransohoff RM, Zhou L. Imatinib attenuates skeletal muscle dystrophy in mdx mice. FASEB J 23: 2539-2548, 2009.
23. Jacob M, Todd LA, Majumdar RS, Li Y, Yamamoto K, Pure E. Endogenous cAbl regulates receptor endocytosis. Cell Signal 21: 1308-1316, 2009.
24. Kharbanda S, Bharti A, Pei D, Wang J, Pandey P, Ren R, Weichselbaum R, Walsh CT, Kufe D. The stress response to ionizing radiation involoves c-Abl-dependent phosphorylation of SHPTP1. Proc Natl Acad Sci USA 93: 6898-6901, 1996.
25. Koleske AJ, Gifford AM, Scott ML, Nee M, Bronson RT, Miczek KA, Baltimore D. Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21: 1259-1272, 1998.
26. Kozower BD, Christofidou-Solomidou M, Sweitzer TD, Muro S, Buerk DG, Solomides CC, Albelda SM, Patterson GA, Muzykantov VR. Immunotargeting of catalase to the pulmonary endothelium alleviates oxidative stress and reduces acute lung transplantation injury. Nat Biotechnol 21: 392-398, 2003.
27. Kumar S, Bharti A, Mishra NC, Raina D, Kharbanda S, Saxena S, Kufe D. Targeting of the c-Abl tyrosine kinase to mitochondria in the necrotic cell death response to oxidative stress. J Biol Chem 276: 17281-17285, 2001.
28. Kumar S, Mishra N, Raina D, Saxena S, Kufe D. Abrogation of the cell death response to oxidative stress by the c-Abl tyrosine kinase inhibitor STI571. Mol Pharmacol 63: 276-282, 2003.
29. LaMontagne KR Jr, Flint AJ, Franza BR Jr, Pandergast AM, Tonks NK. Protein tyrosine phosphatase 1B antagonizes signalling by oncoprotein tyrosine kinase p210 bcr-abl in vivo. Mol Cell Biol 18: 2965-2975, 1998.
30. Lee JC, Christie JD. Primary graft dysfunction. Clin Chest Med 32: 279-293, 2011.
31. Levrero M, De L, V, Costanzo A, Gong J, Melino G, Wang JY. Structure, function and regulation of p63 and p73. Cell Death Differ 6: 1146-1153, 1999.
32. Li M, Abdollahi A, Grone HJ, Lipson KE, Belka C, Huber PE. Late treatment with imatinib mesylate ameliorates radiation-induced lung fibrosis in a mouse model. Radiat Oncol 4: 66, 2009.
33. Lunghi P, Costanzo A, Mazzera L, Rizzoli V, Levrero M, Bonati A. The p53 family protein p73 provides new insights into cancer chemosensitivity and targeting. Clin Cancer Res 15: 6495-6502, 2009.
34. Mahon FX, Deininger MW, Schultheis B, Chabrol J, Reiffers J, Goldman JM, Melo JV. Selection and characterization of BCR-ABL positive cell lines with differential sensitivity to the tyrosine kinase inhibitor STI571: diverse mechanisms of resistance. Blood 96: 1070-1079, 2000.
35. Moldobaeva A, Welsh-Servinsky LE, Shimoda LA, Stephens RS, Verin AD, Tuder RM, Pearse DB. Role of protein kinase G in barrierprotective effects of cGMP in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 290: L919-L930, 2006.
36. Motiwala T, Majumder S, Ghoshal K, Kutay H, Datta J, Roy S, Lucas DM, Jacob ST. PTPROt inactivates the oncogenic fusion protein BCR/ ABL and suppresses transformation of K562 cells. J Biol Chem 284: 455-464, 2009.
37. Pearse DB, Shimoda LA, Verin AD, Bogatcheva N, Moon C, Ronnett GV, Welsh LE, Becker PM. Effect of cGMP on lung microvascular endothelial barrier dysfunction following hydrogen peroxide. Endothelium 10: 309-317, 2003.
38. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, Wang GX, Korth M, Aszodi A, Andersson KE, Krombach F, Mayerhofer A, Ruth P, Fassler R, Hofmann F. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 17: 3045-3051, 1998.
39. Pilz RB, Casteel DE. Regulation of gene expression by cyclic GMP. Circ Res 93: 1034-1046, 2003.
40. Pinsky DJ, Naka Y, Chowdhury NC, Liao H, Oz MC, Michler RE, Kubaszewski E, Malinski T, Stern DM. The nitric oxide/cyclic GMP pathway in organ transplantation: critical role in successful lung preservation. Proc Natl Acad Sci USA 91: 12086-12090, 1994.
41. Plattner R, Koleske AJ, Kazlauskas A, Pendergast AM. Bidirectional signaling links the Abelson kinases to the platelet-derived growth factor receptor. Mol Cell Biol 24: 2573-2583, 2004.
42. Pluk H, Dorey K, Superti-Furga G. Autoinhibition of c-Abl. Cell 108: 247-259, 2002.
43. Polte T, Oberle S, Schroder H. Nitric oxide protects endothelial cells from tumor necrosis factor-alpha-mediated cytotoxicity: possible involvement of cyclic GMP. FEBS Lett 409: 46-48, 1997.
44. Raina D, Mishra N, Kumar S, Kharbanda S, Saxena S, Kufe D. Inhibition of c-Abl with STI571 attenuates stress-activated protein kinase activation and apoptosis in the cellular response to 1-beta-D-arabinofuranosylcytosine. Mol Pharmacol 61: 1489-1495, 2002.
45. Shuvaev VV, Christofidou-Solomidou M, Bhora F, Laude K, Cai H, Dikalov S, Arguiri E, Solomides CC, Albelda SM, Harrison DG, Muzykantov VR. Targeted detoxification of selected reactive oxygen species in the vascular endothelium. J Pharmacol Exp Ther 331: 404-411, 2009.
46. Stephens RS, Rentsendorj O, Servinsky LE, Moldobaeva A, Damico R, Pearse DB. cGMP increases antioxidant function and attenuates oxidant cell death in mouse lung microvascular endothelial cells by a protein kinase G-dependent mechanism. Am J Physiol Lung Cell Mol Physiol 299: L323-L333, 2010.
47. Sun X, Majumder P, Shioya H, Wu F, Kumar S, Weichselbaum R, Kharbanda S, Kufe D. Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J Biol Chem 275: 17237-17240, 2000.
48. Sun X, Wu F, Datta R, Kharbanda S, Kufe D. Interaction between protein kinase C delta and the c-Abl tyrosine kinase in the cellular response to oxidative stress. J Biol Chem 275: 7470-7473, 2000.
49. Sun Y, Hu G, Zhang X, Minshall RD. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ Res 105: 676-85, 15, 2009.
50. Taagepera S, McDonald D, Loeb JE, Whitaker LL, McElroy AK, Wang JY, Hope TJ. Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc Natl Acad Sci USA 95: 7457-7462, 1998.
51. Takuma K, Phuagphong P, Lee E, Mori K, Baba A, Matsuda T. Anti-apoptotic Effect of cGMP in cultured astrocytes. Inhibition by cgmp-dependent protein kinase of mitochondrial permeable transition pore. J Biol Chem 276: 48093-48099, 2001.
52. Tang PS, Mura M, Seth R, Liu M. Acute lung injury and cell death: how many ways can cells die? Am J Physiol Lung Cell Mol Physiol 294: L632-L641, 2008.
53. Van Etten RA, Jackson PK, Baltimore D, Sanders MC, Matsudaira PT, Janmey PA. The COOH terminus of the c-Abl tyrosine kinase contains distinct F-and G-actin binding domains with bundling activity. J Cell Biol 124: 325-340, 1994.
54. Vittal R, Zhang H, Han MK, Moore BB, Horowitz JC, Thannickal VJ. Effects of the protein kinase inhibitor, imatinib mesylate, on epithelial/ mesenchymal phenotypes: implications for treatment of fibrotic diseases. J Pharmacol Exp Ther 321: 35-44, 2007.
55. Wang L, Chiang ET, Simmons JT, Garcia JG, Dudek SM. FTY720-induced human pulmonary endothelial barrier enhancement is mediated by c-Abl. Eur Respir J 2010.
56. Weiss ES, Champion HC, Williams JA, Baumgartner WA, Shah AS. Long-acting oral phosphodiesterase inhibition preconditions against reperfusion injury in an experimental lung transplantation model. J Thorac Cardiovasc Surg 137: 1249-1257, 2009.
57. Woodring PJ, Hunter T, Wang JY. Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J Cell Sci 116: 2613-2626, 2003.
58. Xing H, Yang X, Liu T, Lin J, Chen X, Gong Y. The study of resistant mechanisms and reversal in an imatinib resistant Ph acute lymphoblastic leukemia cell line. Leuk Res 36: 509-513, 2012.
59. Xu J, Millard M, Ren X, Cox OT, Erdreich-Epstein A. c-Abl mediates endothelial apoptosis induced by inhibition of integrins alphavbeta3 and alphavbeta5 and by disruption of actin. Blood 115: 2709-2718, 2010.
60. Yuan ZM, Shioya H, Ishiko T, Sun X, Gu J, Huang YY, Lu H, Kharbanda S, Weichselbaum R, Kufe D. p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature 399: 814-817, 1999.
61. Zhu B, Zhang L, Alexeyev M, Alvarez DF, Strada SJ, Stevens T. Type 5 phosphodiesterase expression is a critical determinant of the endothelial cell angiogenic phenotype. Am J Physiol Lung Cell Mol Physiol 296: L220-L228, 2009.
62. 2 levels in NO-induced inhibition of rat aortic smooth muscle cell motility. Am J Physiol Heart Circ Physiol 288: H1859-H1866, 2005.