Rac2 GTPase activation by angiotensin II is modulated by Ca2+ calcineurin and mitogen-activated protein kinases in human neutrophils

Journal of Molecular Endocrinology

Volumn 39, Issue 5-6, 2007, Pages 351-363

  El Bekay, Rajaa ^a   Alba, Gonzalo ^a   Reyes, M Edith ^a   Chacón, Pedro ^a   Vega, Antonio ^a   Martín Nieto, José ^b   Jiménez, Juan ^a   Ramos, Eladio ^c   Oliván, Josefina ^c   Pintado, Elízabeth ^a   Sobrino, Francisco ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b UNIVERSITY OF ALICANTE   (Spain)

^c HOSPITAL UNIVERSITARIO VIRGEN MACARENA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANGIOTENSIN II; BOTULINUM TOXIN A; CALCINEURIN; CALCIUM ION; CYCLOSPORIN A; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 9; MITOGEN ACTIVATED PROTEIN KINASE P38; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; RAC PROTEIN; RAC2 PROTEIN; REACTIVE OXYGEN METABOLITE; RHO KINASE; STRESS ACTIVATED PROTEIN KINASE 1; WORTMANNIN;

ARTICLE; CARDIOVASCULAR DISEASE; CELL MEMBRANE; CONTROLLED STUDY; CYTOSOL; DRUG RESEARCH; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME PHOSPHORYLATION; HORMONE ACTION; HORMONE DETERMINATION; HUMAN; HUMAN CELL; INFLAMMATION; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANGIOTENSIN II; ANIMALS; CALCINEURIN; CALCIUM; CELL MEMBRANE; CYCLOSPORINE; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NEUTROPHILS; RAC GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 38449113370     PISSN: 09525041     EISSN: None     Source Type: Journal    
DOI: 10.1677/JME-07-0074     Document Type: Article

References (66)

1. Abo A, Pick E, Hall A, Totty N, Teahan CG & Segal AW 1991 Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 353 668-670.
2. Abo A, Boyhan A, West I, Thrasher AJ & Segal AW 1992 Reconstitution of neutrophil NADPH oxidase activity in the cell-free system by four components: p67-phox, p47-phox, p21rac1, and cytochrome b-245. Journal of Biological Chemistry 267 16767-16770.
3. Van Aelst L & D'Souza-Schorey C 1997 Rho GTPases and signaling networks. Genes and Development 11 2295-2322.
4. Akasaki T, Koga H & Sumimoto H 1999 Phosphoinositide 3-kinase-dependent and -independent activation of the small GTPase Rac2 in human neutrophils. Journal of Biological Chemistry 274 18055-18059.
5. Aktories K, Schmidt G & Just I 2000 Rho GTPases as targets of bacterial protein toxins. Biological Chemistry 381 421-426.
6. Ambruso DR, Knall C, Abell AN, Panepinto J, Kurkchubasche A, Thurman G, Gonzalez-Aller C, Hiester A, deBoer M, Harbeck RJ et al. 2000 Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. PNAS 97 4654-4659.
7. Babior BM 2000 Phagocytes and oxidative stress. American Journal of Medicine 109 33-44.
8. El Bekay R, Álvarez M, Monteseirin J, Alba G, Chacón P, Vega A, Martín-Nieto J, Jiménez J, Pintado E, Bedoya FJ et al. 2003 Oxidative stress is a critical mediator of the angiotensin II signal in human neutrophils: involvement of mitogen-activated protein kinase, calcineurin, and the transcription factor NF-κB. Blood 102 662-671.
9. Benard V, Bohl BP & Bokoch GM 1999 Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. Journal of Biological Chemistry 274 13198-13204.
10. El Benna J, Ruedi JM & Babior BM 1994 Cytosolic guanine nucleotide-binding protein Rac2 operates in vivo as a component of the neutrophil respiratory burst oxidase. Transfer of Rac2 and the cytosolic oxidase components p47phox and p67phox to the submembranous actin cytoskeleton during oxidase activation. Journal of Biological Chemistry 269 6729-6734.
11. Bokoch GM 1994 Regulation of the human neutrophil NADPH oxidase by the Rac GTP-binding proteins. Current Opinion in Cell Biology 6 212-218.
12. Bokoch GM 2003 Biology of the p21-activated kinases. Annual Review of Biochemistry 72 743-781.
13. Bokoch GM & Knaus UG 1994 Ras-related GTP-binding proteins and leukocyte signal transduction. Current Opinion in Hematology 1 53-60.
14. Bozem M, Kuhlmann S, Blum R, Feick P & Schulz I 2000 Hormone-stimulated calcium release is inhibited by cytoskeleton-disrupting toxins in AR4-2J cells. Cell Calcium 28 73-82.
15. Brooks DP, Ohlstein EH & Ruffolo RR, Jr. 1999 Pharmacology of eprosartan, an angiotensin II receptor antagonist: exploring hypotheses from clinical data. American Heart Journal 138 246-251.
16. Carballo M, Márquez G, Conde M, Martín-Nieto J, Monteseirín J, Conde J, Pintado E & Sobrino F 1999 Characterization of calcineurin in human neutrophils. Inhibitory effect of hydrogen peroxide on its enzyme activity and on NF-κB DNA binding. Journal of Biological Chemistry 274 93-100.
17. Curnutte JT, Kuver R & Babior BM 1987 Activation of the respiratory burst oxidase in a fully soluble system from human neutrophils. Journal of Biological Chemistry 262 6450-6452.
18. Didsbury J, Weber RF, Bokoch GM, Evans T & Snyderman R 1989 Rac, a novel ras-related family of proteins that are botulinum toxin substrates. Journal of Biological Chemistry 264 16378-16382.
19. Diekmann D, Abo A, Johnston C, Segal AW & Hall A 1994 Interaction of Rac with p67phox and regulation of phagocytic NADPH oxidase activity. Science 265 531-533.
20. Dusi S, Donini M & Rossi F 1995a Mechanisms of NADPH oxidase activation in human neutrophils: p67phox is required for the translocation of rac 1 but not of rac 2 from cytosol to the membranes. Biochemical Journal 308 991-994.
21. Dusi S, Donini M & Rossi F 1995b Mechanisms of NADPH oxidase activation: translocation of p40phox, Rac1 and Rac2 from the cytosol to the membranes in human neutrophils lacking p47phox or p67phox. Biochemical Journal 314 409-412.
22. Etienne-Manneville S & Hall A 2002 Rho GTPases in cell biology. Nature 420 629-635.
23. Finkel T 1998 Oxygen radicals and signaling. Current Opinion in Cell Biology 10 248-253.
24. Gao Y, Dickerson JB, Gut F, Zheng J & Zheng Y 2004 Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. PNAS 101 7618--7623.
25. Geijsen N, van Delft S, Raaijmakers JA, Lammers JW, Collard JG, Koenderman L & Coffer PJ 1999 Regulation of p21rac activation in human neutrophils. Blood 94 1121-1130.
26. Gualberto A, Marquez G, Carballo M, Youngblood GL, Hunt SW, Baldwin AS & Sobrino F 1998 p53 transactivation of the HIV-1 long terminal repeat is blocked by PD 144795, a calcineurin-inhibitor with anti-HIV properties. Journal of Biological Chemistry 273 7088-7093.
27. Haataja L, Groffen J & Heisterkamp N 1997 Characterization of RAC3, a novel member of the Rho family. Journal of Biological Chemistry 272 20384-20388.
28. Hahn AW, Johas U, Buhler FR & Resink TJ 1994 Activation of human peripheral monocytes by angiotensin II. FEBS Letters 347 178-180.
29. Heyworth PG, Bohl BP, Bokoch GM & Curnutte JT 1994 Rac translocates independently of the neutrophil NADPH oxidase components p47phox and p67phox. Evidence for its interaction with flavocytochrome b558. Journal of Biological Chemistry 269 30749-30752.
30. Inanami O, Johnson JL & Babior BM 1998a The leukocyte NADPH oxidase subunit p47PHOX: the role of the cysteine residues. Archives of Biochemistry and Biophysics 350 36-40.
31. Inanami O, Johnson JL, McAdara JK, Benna JE, Faust LR, Newburger PE & Babior BM 1998b Activation of the leukocyte NADPH oxidase by phorbol ester requires the phosphorylation of p47PHOX on serine 303 or 304. Journal of Biological Chemistry 273 9539-9543.
32. Inanami O, Yamamori T, Takahashi TA, Nagahata H & Kuwabara M 2001 ESR detection of intraphagosomal superoxide in polymorphonuclear leukocytes using 5-(diethoxyphosphoryl)-5-methyl-L-pyrroline-N-oxide. Free Radical Research 34 81-92.
33. Ito H, Takemory K & Suzuki T 2001 Role of angiotensin II type I receptor in the leukocytes and endothelial cells of brain microvessels in the pathogenesis of hypertensive cerebral injury. Journal of Hypertension 19 591-597.
34. Johnson JL, Park JW, Benna JE, Faust LP, Inanami O & Babior BM 1998 Activation of p47(PHOX), a cytosolic subunit of the leukocyte NADPH oxidase. Phosphorylation of ser-359 or ser-370 precedes phosphorylation at other sites and is required for activity. Journal of Biological Chemistry 273 35147-35152.
35. Just I, Selzer J, Eichel-Streiber C & Aktories K 1995 The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile. Journal of Clinical Investigation 95 1026-1031.
36. Kim C & Dinauer MC 2001 Rac2 is an essential regulator of neutrophil nicotinamide adenine dinucleotide phosphate oxidase activation in response to specific signaling pathways. Immunology 166 1223-1232.
37. Kim C & Dinauer MC 2006 Impaired NADPH oxidase activity in Rac2-deficient murine neutrophils does not result from defective translocation of p47phox and p67phox and can be rescued by exogenous arachidonic acid. Journal of Leukocyte Biology 79 223-234.
38. Knans UG, Heyworth PG, Evans T, Curnutte JT & Bokoch GM 1991 Regulation of phagocyte oxygen radical production by the GTP-binding protein Rac 2. Science 254 1512-1515.
39. Koga H, Terasawa H, Nunoi H, Takeshige K, Inagaki F & Sumimoto H 1999 Tetratricopeptide repeat (TPR) motifs of p67(phox) participate in interaction with the small GTPase Rac and activation of the phagocyte NADPH oxidase. Journal of Biological Chemistry 274 25051-25060.
40. Kwong CH, Malech HL, Rotrosen D & Leto TL 1993 Regulation of the human neutrophil NADPH oxidase by rho-related G-proteins. Biochemistry 32 5711-5717.
41. Li Y, Zhu H, Kuppusamy P, Roubaud V, Zweier JL & Trush MA 1998 Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. Journal of Biological Chemistry 273 2015-2023.
42. Lim HW, New L, Han J & Molkentin JD 2001 Calcineurin enhances MAPK phosphatase-1 expression and p38 MAPK inactivation in cardiac myocytes. Journal of Biological Chemistry 276 15913-15919.
43. Mankelow TJ & Henderson LM 2001 Inhibition of the neutrophil NADPH oxidase and associated H+ channel by diethyl pyrocarbonate (DEPC), a histidine-modifying agent: evidence for at least two target sites. Biochemical Journal 358 315-324.
44. Mansfield MA 1995 Rapid immunodetection on polyvinylidene fluoride membrane blots without blocking. Analytical Biochemistry 229 140-143.
45. Mazzone A, De Servi S, Ricevuti G, Mazzucchelli I, Fossati G, Pasotti D, Bramucci E, Angoli L, Marsico F & Specchia G 1993 Increased expression of neutrophil and monocyte adhesion molecules in unstable coronary artery disease. Circulation 88 358-363.
46. Monteseirín J, Camacho MJ, Montaño R, Llamas E, Conde M, Carballo M, Guardia P, Conde J & Sobrino F 1996 Enhancement of antigen-specific functional responses by neutrophils from allergic patients. Journal of Experimental Medicine 183 2571-2579.
47. Murat A, Pellieux C, Brunner HR & Pedrazzini T 2000 Calcineurin blockade prevents cardiac mitogen-activated protein kinase activation and hypertrophy in renovascular hypertension. Journal of Biological Chemistry 275 40867-40873.
48. Nataraj C, Oliverio MI & Mannon RB 1999 Angiotensin II regulates cellular immune responses through a calcineurin-dependent pathway. Journal of Clinical Investigation 104 1693-1701.
49. Nguyen NS, Pulido SM & Ruegg UT 1998 Biphasic effects of cyclosporin A on formyl-methionyl-leucyl-phenylalanine stimulated responses in HL-60 cells differentiated into neutrophils. British Journal of Pharmacology 124 1774-1780.
50. Northup JK, Smigel MD & Gilman AG 1982 The guanine nucleotide activating site of the regulatory component of adenylate cyclase. Identification by ligand binding. Journal of Biological Chemistry 257 11416-11423.
51. Price LS, Langeslag M, ten Klooster JP, Hordijk PL, Jalink K & Collard JG 2003 Calcium signaling regulates translocation and activation of Rac. Journal of Biological Chemistry 278 39413-39421.
52. Roberts AW, Kim C, Zhen L, Lowe JB, Kapur R, Petryniak B, Spaetti A, Pollock JD, Borneo JB, Bradford GB et al. 1999 Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity 10 183-196.
53. Ross R 1999 Atherosclerosis-an inflammatory disease. New England Journal of Medicine 340 115-126.
54. 2+ concentration in fura-2-loaded human neutrophils. Biochemical Journal 265 915-918.
55. Schmitz U, Thommes K, Beier I, Wagner W, Sachinidis A, Dusing R & Vetter H 2001 Angiotensin II-induced stimulation of p21-activated kinase and c-Jun NH2-terminal kinase is mediated by Rac1 and Nck. Journal of Biological Chemistry 276 22003-22010.
56. Segal AW & Abo A 1993 The biochemical basis of the NADPH oxidase of phagocytes. Trends in Biochemical Sciences 18 43-47.
57. Shimada K & Yakazi Y 1978 Binding sites for angiotensin II in human mononuclear leucocytes. Journal of Biochemistry 84 1013-1015.
58. Timmermans PB, Wong PC, Chiu AT, Herblin WF, Benfield P, Carini DJ, Lee RJ, Wexler RR, Saye JA & Smith RD 1993 Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacological Reviews 45 205-251.
59. Touyz RM 2003 Recent advances in intracellular signalling in hypertension. Current Opinion in Nephrology and Hypertension 12 165-174.
60. Vega A, Chacón P, Monteseirín J, El Bekay R, Alvarez M, Alba G, Conde J, Martín-Nieto J, Bedoya FJ, Pintado E et al. 2004 A new role for monoamine oxidases in the modulation of macrophage-inducible nitric oxide synthase gene expression. Journal of Leukocyte Biology 75 1093-1101.
61. Voth DE & Ballard JD 2005 Clostridium difficile toxins: mechanism of action and role in disease. Clinical Microbiology Reviews 18 247-263.
62. Werlen G, Jacinto E, Xia Y & Karin M 1998 Calcineurin preferentially synergizes with PKC-theta to activate JNK and IL-2 promoter in T lymphocytes. EMBO Journal 17 3101-3111.
63. Williams DA, Tao W, Yang F, Kim C, Gu Y, Mansfield P, Levine JE, Petryniak B, Derrow CW, Harris C et al. 2000 Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood 96 1646-1654.
64. 2+ and protein kinase C {delta} in vascular smooth muscle cells. American Journal of Physiology. Cell Physiology 289 C1286-C1294.
65. Yang FC, Kapur R, King AJ, Tao W, Kim C, Borneo J, Breese R, Marshall M, Dinauer MC & Williams DA 2000 Rac2 stimulates Akt activation affecting BAD/Bcl-XL expression while mediating survival and actin function in primary mast cells. Immunity 12 557-568.
66. Yu H, Leitenberg D, Li B & Flavell RA 2001 Deficiency of small GTPase Rac2 affects T cell activation. Journal of Experimental Medicine 194 915-926.