NADPH oxidase mediates synergistic effects of IL-17 and TNF-α on CXCL1 expression by epithelial cells after lung ischemia-reperfusion

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 1, 2014, Pages

  Sharma, Ashish K ^a   Mulloy, Daniel P ^a   Le, Lamvy T ^a   Laubach, Victor E ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Alveolar epithelial cells; Ischemia reperfusion injury; Lung transplant; Primary graft dysfunction

Indexed keywords

CXCL1 CHEMOKINE; INTERLEUKIN 17; INTERLEUKIN 6; MYELOPEROXIDASE; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG EDEMA; LUNG FUNCTION; LUNG INJURY; LUNG LAVAGE; LUNG WEIGHT; MACROPHAGE; MALE; MOUSE; NATURAL KILLER CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REOXYGENATION; REPERFUSION INJURY;

EID: 84891498632     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00205.2013     Document Type: Article

References (44)

1. Awane M, Andres PG, Li DJ, Reinecker HC. NF-kappa B-inducing kinase is a common mediator of IL-17-, TNF-alpha-, and IL-1 betainduced chemokine promoter activation in intestinal epithelial cells. J Immunol 162: 5337-5344, 1999.
2. Belperio JA, Keane MP, Burdick MD, Gomperts BN, Xue YY, Hong K, Mestas J, Zisman D, Ardehali A, Saggar R, Lynch JP, 3rd Ross DJ, Strieter RM. CXCR2/CXCR2 ligand biology during lung transplant ischemia-reperfusion injury. J Immunol 175: 6931-6939, 2005.
3. Cao J, Ren G, Gong Y, Dong S, Yin Y, Zhang L. Bronchial epithelial cells release IL-6, CXCL1 and CXCL8 upon mast cell interaction. Cytokine 56: 823-831, 2011.
4. Chabaud M, Page G, Miossec P. Enhancing effect of IL-1, IL-17, and TNF-alpha on macrophage inflammatory protein-3alpha production in rheumatoid arthritis: regulation by soluble receptors and Th2 cytokines. J Immunol 167: 6015-6020, 2001.
5. Chiang CH, Chuang CH, Liu SL. Apocynin attenuates ischemia-reperfusion lung injury in an isolated and perfused rat lung model. Transl Res 158: 17-29, 2011.
6. Christie JD, Sager JS, Kimmel SE, Ahya VN, Gaughan C, Blumenthal NP, Kotloff RM. Impact of primary graft failure on outcomes following lung transplantation. Chest 127: 161-165, 2005.
7. Dodd OJ, Pearse DB. Effect of the NADPH oxidase inhibitor apocynin on ischemia-reperfusion lung injury. Am J Physiol Heart Circ Physiol 279: H303-H312, 2000.
8. El-Benna J, Dang PM, Gougerot-Pocidalo MA. Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol 30: 279-289, 2008.
9. Fischer H. Mechanisms and function of DUOX in epithelia of the lung. Antioxid Redox Signal 11: 2453-2465, 2009.
10. Fischer H, Gonzales LK, Kolla V, Schwarzer C, Miot F, Illek B, Ballard PL. Developmental regulation of DUOX1 expression and func-tion in human fetal lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 292: L1506-L1514, 2007.
11. Fisher AB, Al-Mehdi AB, Muzykantov V. Activation of endothelial NADPH oxidase as the source of a reactive oxygen species in lung ischemia. Chest 116: 25S-26S, 1999.
12. Forteza R, Salathe M, Miot F, Conner GE. Regulated hydrogen peroxide production by Duox in human airway epithelial cells. Am J Respir Cell Mol Biol 32: 462-469, 2005.
13. Fujie H, Niu K, Ohba M, Tomioka Y, Kitazawa H, Nagashima K, Ohrui T, Numasaki M. A distinct regulatory role of Th17 cytokines IL-17A and IL-17F in chemokine secretion from lung microvascular endothelial cells. Inflammation 35: 1119-1131, 2012.
14. Gelderblom M, Weymar A, Bernreuther C, Velden J, Arunachalam P, Steinbach K, Orthey E, Arumugam TV, Leypoldt F, Simova O, Thom V, Friese MA, Prinz I, Holscher C, Glatzel M, Korn T, Gerloff C, Tolosa E, Magnus T. Neutralization of the IL-17 axis diminishes neutrophil invasion and protects from ischemic stroke. Blood 120: 3793-3802, 2012.
15. Granton J. Update of early respiratory failure in the lung transplant recipient. Curr Opin Crit Care 12: 19-24, 2006.
16. Griffin GK, Newton G, Tarrio ML, Bu DX, Maganto-Garcia E, Azcutia V, Alcaide P, Grabie N, Luscinskas FW, Croce KJ, Lichtman AH. IL-17 and TNF-alpha sustain neutrophil recruitment during inflammation through synergistic effects on endothelial activation. J Immunol 188: 6287-6299, 2012.
17. Hartupee J, Liu C, Novotny M, Li X, Hamilton T. IL-17 enhances chemokine gene expression through mRNA stabilization. J Immunol 179: 4135-4141, 2007.
18. Hodge G, Hodge S, Li-Liew C, Reynolds PN, Holmes M. Increased natural killer T-like cells are a major source of pro-inflammatory cytokines and granzymes in lung transplant recipients. Respirology 17: 155-163, 2012.
19. Im J, Jeon JH, Cho MK, Woo SS, Kang SS, Yun CH, Lee K, Chung DK, Han SH. Induction of IL-8 expression by bacterial flagellin is mediated through lipid raft formation and intracellular TLR5 activation in A549 cells. Mol Immunol 47: 614-622, 2009.
20. Krause KH. Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn J Infect Dis 57: S28-S29, 2004.
21. Lee IT, Lin CC, Lee CY, Hsieh PW, Yang CM. Protective effects of (-)-epigallocatechin-3-gallate against TNF-alpha-induced lung inflammation via ROS-dependent ICAM-1 inhibition. J Nutr Biochem 24: 124-136, 2013.
22. Lee IT, Luo SF, Lee CW, Wang SW, Lin CC, Chang CC, Chen YL, Chau LY, Yang CM. Overexpression of HO-1 protects against TNFalpha-mediated airway inflammation by down-regulation of TNFR1-dependent oxidative stress. Am J Pathol 175: 519-532, 2009.
23. Leverence JT, Medhora M, Konduri GG, Sampath V. Lipopolysaccharide-induced cytokine expression in alveolar epithelial cells: role of PKCzeta-mediated p47phox phosphorylation. Chem Biol Interact 189: 72-81, 2011.
24. Liu Y, Mei J, Gonzales L, Yang G, Dai N, Wang P, Zhang P, Favara M, Malcolm KC, Guttentag S, Worthen GS. IL-17A and TNF-alpha exert synergistic effects on expression of CXCL5 by alveolar type II cells in vivo and in vitro. J Immunol 186: 3197-3205, 2011.
25. Nonaka M, Ogihara N, Fukumoto A, Sakanushi A, Kusama K, Pawankar R, Yagi T. Synergistic induction of macrophage inflammatory protein-3alpha;/CCL20 production by interleukin-17A and tumor necrosis factor-alpha; in nasal polyp fibroblasts. World Allergy Organ J 2: 218-223, 2009.
26. Onishi RM, Gaffen SL. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 129: 311-321, 2010.
27. Ovechkin AV, Lominadze D, Sedoris KC, Robinson TW, Tyagi SC, Roberts AM. Lung ischemia-reperfusion injury: implications of oxidative stress and platelet-arteriolar wall interactions. Arch Physiol Biochem 113: 1-12, 2007.
28. Papaiahgari S, Kleeberger SR, Cho HY, Kalvakolanu DV, Reddy SP. NADPH oxidase and ERK signaling regulates hyperoxia-induced Nrf2-ARE transcriptional response in pulmonary epithelial cells. J Biol Chem 279: 42302-42312, 2004.
29. Pearse DB, Dodd JM. Ischemia-reperfusion lung injury is prevented by apocynin, a novel inhibitor of leukocyte NADPH oxidase. Chest 116: 55S-56S, 1999.
30. Qian Y, Liu C, Hartupee J, Altuntas CZ, Gulen MF, Jane-Wit D, Xiao J, Lu Y, Giltiay N, Liu J, Kordula T, Zhang QW, Vallance B, Swaidani S, Aronica M, Tuohy VK, Hamilton T, Li X. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 8: 247-256, 2007.
31. Sedoris KC, Ovechkin AV, Gozal E, Roberts AM. Differential effects of nitric oxide synthesis on pulmonary vascular function during lung ischemia-reperfusion injury. Arch Physiol Biochem 115: 34-46, 2009.
32. Sharma AK, Fernandez LG, Awad AS, Kron IL, Laubach VE. Proinflammatory response of alveolar epithelial cells is enhanced by alveolar macrophage-produced TNF-alpha during pulmonary ischemiareperfusion injury. Am J Physiol Lung Cell Mol Physiol 293: L105-L113, 2007.
33. Sharma AK, LaPar DJ, Zhao Y, Li L, Lau CL, Kron IL, Iwakura Y, Okusa MD, Laubach VE. Natural killer T cell-derived IL-17 mediates lung ischemia-reperfusion injury. Am J Respir Crit Care Med 183: 1539-1549, 2011.
34. Shilling RA, Wilkes DS. Role of Th17 cells and IL-17 in lung transplant rejection. Semin Immunopathol 33: 129-134, 2011.
35. Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm 2008: 106507, 2008.
36. Sun D, Novotny M, Bulek K, Liu C, Li X, Hamilton T. Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat Immunol 12: 853-860, 2011.
37. Swaidani S, Bulek K, Kang Z, Liu C, Lu Y, Yin W, Aronica M, Li X. The critical role of epithelial-derived Act1 in IL-17-and IL-25-mediated pulmonary inflammation. J Immunol 182: 1631-1640, 2009.
38. Tarr JM, Ding N, Kaul K, Antonell A, Perez-Jurado LA, Chibber R. Cellular crosstalk between TNF-alpha, NADPH oxidase, PKCbeta2, and C2GNT in human leukocytes. Cell Signal 24: 873-878, 2012.
39. Trulock EP, Edwards LB, Taylor DO, Boucek MM, Keck BM, Hertz MI. Registry of the International Society for Heart and Lung Transplantation: twenty-third official adult lung and heart-lung transplantation report-2006. J Heart Lung Transplant 25: 880-892, 2006.
40. Whitson BA, Prekker ME, Herrington CS, Whelan TP, Radosevich DM, Hertz MI, Dahlberg PS. Primary graft dysfunction and long-term pulmonary function after lung transplantation. J Heart Lung Transplant 26: 1004-1011, 2007.
41. Yang Z, Sharma AK, Linden J, Kron IL, Laubach VE. CD4+ T lymphocytes mediate acute pulmonary ischemia-reperfusion injury. J Thorac Cardiovasc Surg 137: 695-702, 2009.
42. Yang Z, Sharma AK, Marshall M, Kron IL, Laubach VE. NADPH oxidase in bone marrow-derived cells mediates pulmonary ischemiareperfusion injury. Am J Respir Cell Mol Biol 40: 375-381, 2009.
43. Zhao M, Fernandez LG, Doctor A, Sharma AK, Zarbock A, Tribble CG, Kron IL, Laubach VE. Alveolar macrophage activation is a key initiation signal for acute lung ischemia-reperfusion injury. Am J Physiol Lung Cell Mol Physiol 291: L1018-L1026, 2006.
44. Zhu C, Bilali A, Georgieva GS, Kurata S, Mitaka C, Imai T. Salvage of nonischemic control lung from injury by unilateral ischemic lung with apocynin, a nicotinamide adenine dinucleotide phosphate (NADPH) oxidase inhibitor, in isolated perfused rat lung. Transl Res 152: 273-282, 2008.