Neutrophil extracellular traps in acrolein promoted hepatic ischemia reperfusion injury: Therapeutic potential of NOX2 and p38MAPK inhibitors

Journal of Cellular Physiology

Volumn 233, Issue 4, 2018, Pages 3244-3261

  Arumugam, Suyavaran ^a   Girish Subbiah, Kesthuru ^b   Kemparaju, Kempaiah ^c   Thirunavukkarasu, Chinnasamy ^a  

^a PONDICHERRY UNIVERSITY   (India)

^b TUMKUR UNIVERSITY   (India)

^c University of Mysoure   (India)

Author keywords

inflammation; ischemia reperfusion; necrosis; neutrophil extracellular trap

Indexed keywords

ACETOPHENONE DERIVATIVE; ACROLEIN; ANTIOXIDANT; APOCYNIN; AURANTIIN; AUTACOID; CYBB PROTEIN, RAT; ENZYME INHIBITOR; FLAVANONE DERIVATIVE; HISTONE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TUMOR NECROSIS FACTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CELL DEATH; CELL NUCLEUS; CHEMOTAXIS; DNA DAMAGE; DRUG EFFECT; EXTRACELLULAR TRAP; HEP-G2 CELL LINE; HUMAN; LIVER; MALE; MAPK SIGNALING; METABOLISM; MITOCHONDRION; NEUTROPHIL; PATHOLOGY; REPERFUSION INJURY; RESPIRATORY BURST; ULTRASTRUCTURE; VASCULARIZATION; WISTAR RAT;

ACETOPHENONES; ACROLEIN; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL DEATH; CELL NUCLEUS; CHEMOTAXIS; DNA DAMAGE; ENZYME INHIBITORS; EXTRACELLULAR TRAPS; FLAVANONES; HEP G2 CELLS; HISTONES; HUMANS; INFLAMMATION MEDIATORS; LIVER; MALE; MAP KINASE SIGNALING SYSTEM; MITOCHONDRIA; NADPH OXIDASE 2; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXIDASE; RATS, WISTAR; REPERFUSION INJURY; RESPIRATORY BURST; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85038929161     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.26167     Document Type: Article

References (77)

1. Agay, D., Andriollo-Sanchez, M., Claeyssen, R., Touvard, L., Denis, J., Roussel, A. M., & Chancerelle, Y. (2008). Interleukin-6, TNF-α and interleukin-1β levels in blood and tissue in severely burned rats. European Cytokine Network, 19(1), 1–7.
2. Alam, M. A., Subhan, N., Rahman, M. M., Uddin, S. J., Reza, H. M., & Sarker, S. D. (2014). Effect of citrus flavonoids, naringin and naringenin, on metabolic syndrome and their mechanisms of action. Advances in Nutrition, 5(4), 404–417.
3. Amin, A., & Hamza, A. A. (2005). Oxidative stress mediates drug-induced hepatotoxicity in rats: A possible role of DNA fragmentation. Toxicology, 208(3), 367–375.
4. Amir, M., Zhao, E., Fontana, L., Rosenberg, H., Tanaka, K., Gao, G., & Czaja, M. J. (2013). Inhibition of hepatocyte autophagy increases tumor necrosis factor-dependent liver injury by promoting caspase-8 activation. Cell Death & Differentiation, 20(7), 878–887.
5. Anastacio, L. R., Pereira, M. C., Vilela, E. G., Lima, A. S., & Correia, M. I. (2013). Overweight in liver transplant recipients. Revista Do Colegio Brasileiro De Cirurgioes, 40(6), 502–507.
6. Arai, T., Koyama, R., Yuasa, M., Kitamura, D., & Mizuta, R. (2014). Acrolein, a highly toxic aldehyde generated under oxidative stress in vivo, aggravates the mouse liver damage after acetaminophen overdose. Biomedical Research, 35(6), 389–395.
7. Avezov, K., Reznick, A. Z., & Aizenbud, D. (2015). Time and dose effects of cigarette smoke and acrolein on protein carbonyl formation in HaCaT keratinocytes. Advances in Experimental Medicine and Biology, 849, 57–64.
8. Awasthi, D., Nagarkoti, S., Kumar, A., Dubey, M., Singh, A. K., Pathak, P., … Dikshit, M. (2016). Oxidized LDL induced extracellular trap formation in human neutrophils via TLR-PKC-IRAK-MAPK and NADPH-oxidase activation. Free Radical Biology & Medicine, 93, 190–203.
9. Brandt, M., Garlapati, V., Oelze, M., Sotiriou, E., Knorr, M., Kroller-Schon, S., … Wenzel, P. (2016). NOX2 amplifies acetaldehyde-mediated cardiomyocyte mitochondrial dysfunction in alcoholic cardiomyopathy. Scientific Reports, 6, 32554.
10. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., … Zychlinsky, A. (2004). Neutrophil extracellular traps kill bacteria. Science, 303(5663), 1532–1535.
11. Carden, D. L., & Granger, D. N. (2000). Pathophysiology of ischaemia-reperfusion injury. The Journal of Pathology, 190(3), 255–266.
12. Cavia-Saiz, M., Busto, M. D., Pilar-Izquierdo, M. C., Ortega, N., Perez-Mateos, M., & Muniz, P. (2004). Antioxidant properties, radical scavenging activity and biomolecule protection capacity of flavonoid naringenin and its glycoside naringin: A comparative study. Journal of the Science of Food and Agriculture, 90(7), 1238–1244.
13. Chen, J., Guo, R., Yan, H., Tian, L., You, Q., Li, S., … Wu, K. (2013). Naringin inhibits ROS-activated MAPK pathway in high glucose-induced injuries in H9c2 cardiac cells. Basic & Clinical Pharmacology & Toxicology, 114(4), 293–304.
14. Chen, M., Suzuki, A., Borlak, J., Andrade, R. J., & Lucena, M. I. (2015). Drug-induced liver injury: Interactions between drug properties and host factors. Journal of Hepatology, 63(2), 503–514.
15. Covington, S. M., Bauler, L. D., & Toledo-Pereyra, L. H. (2017). Akt: A therapeutic target in hepatic ischemia-reperfusion injury. Journal of Investigative Surgery, 30(1), 47–55.
16. Daiber, A., Di Lisa, F., Oelze, M., Kroller-Schon, S., Steven, S., Schulz, E., & Munzel, T. (2015). Crosstalk of mitochondria with NADPH oxidase via reactive oxygen and nitrogen species signalling and its role for vascular function. British Journal of Pharmacology, 174(12), 1670–1689.
17. de Almeida, A. C., Cabral Marques, O., Arslanian, C., Condino-Neto, A., & Ximenes, V. F. (2011). 4-fluoro-2-methoxyphenol, an apocynin analog with enhanced inhibitory effect on leukocyte oxidant production and phagocytosis. European Journal of Pharmacology, 660(2–3), 445–453.
18. Doran, E., & Halestrap, A. P. (2000). Cytochrome c release from isolated rat liver mitochondria can occur independently of outer-membrane rupture: Possible role of contact sites. Biochemical Journal, 348(Pt 2), 343–350.
19. Ermert, D., Zychlinsky, A., & Urban, C. (2009). Fungal and bacterial killing by neutrophils. Methods in Molecular Biology, 470, 293–312.
20. Faroon, O., Roney, N., Taylor, J., Ashizawa, A., Lumpkin, M. H., & Plewak, D. J. (2008). Acrolein environmental levels and potential for human exposure. Toxicology and Industrial Health, 24(8), 543–564.
21. Francoz, C., Valla, D., & Durand, F. (2012). Portal vein thrombosis, cirrhosis, and liver transplantation. Journal of Hepatology, 57(1), 203–212.
22. Fu, H., Bylund, J., Karlsson, A., Pellme, S., & Dahlgren, C. (2004). The mechanism for activation of the neutrophil NADPH-oxidase by the peptides formyl-Met-Leu-Phe and Trp-Lys-Tyr-Met-Val-Met differs from that for interleukin-8. Immunology, 112(2), 201–210.
23. Gobeil, S., Boucher, C. C., Nadeau, D., & Poirier, G. G. (2001). Characterization of the necrotic cleavage of poly(ADP-ribose) polymerase (PARP-1): Implication of lysosomal proteases. Cell Death Differ, 8(6), 588–594.
24. Haddad, L., Cassenote, A. J., Andraus, W., de Martino, R. B., Ortega, N. R., Abe, J. M., & D'Albuquerque, L. A. (2015). Factors associated with mortality and graft failure in liver transplants: A hierarchical approach. PLoS ONE, 10(8), e0134874.
25. Hakkim, A., Fuchs, T. A., Martinez, N. E., Hess, S., Prinz, H., Zychlinsky, A., & Waldmann, H. (2011). Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nature Chemical Biology, 7(2), 75–77.
26. Hattori, H., Subramanian, K. K., Sakai, J., & Luo, H. R. (2010). Reactive oxygen species as signaling molecules in neutrophil chemotaxis. Communicative & Integrative Biology, 3(3), 278–281.
27. Hirose, T., Hamaguchi, S., Matsumoto, N., Irisawa, T., Seki, M., Tasaki, O., … Shimazu, T. (2014). Presence of neutrophil extracellular traps and citrullinated histone H3 in the bloodstream of critically ill patients. PLoS ONE, 9(11), e111755.
28. Honda, M., Takeichi, T., Asonuma, K., Tanaka, K., Kusunoki, M., & Inomata, Y. (2013). Intravital imaging of neutrophil recruitment in hepatic ischemia-reperfusion injury in mice. Transplantation, 95(4), 551–558.
29. Huang, H., Tohme, S., Al-Khafaji, A. B., Tai, S., Loughran, P., Chen, L., … Tsung, A. (2015). Damage-associated molecular pattern-activated neutrophil extracellular trap exacerbates sterile inflammatory liver injury. Hepatology, 62(2), 600–614.
30. Jaeschke, H. (2011). Reactive oxygen and mechanisms of inflammatory liver injury: Present concepts. Journal of Gastroenterology and Hepatology, 26(Suppl 1), 173–179.
31. Jaeschke, H., & Hasegawa, T. (2006). Role of neutrophils in acute inflammatory liver injury. Liver International, 26(8), 912–919.
32. Jameel, N. M., Thirunavukkarasu, C., Wu, T., Watkins, S. C., Friedman, S. L., & Gandhi, C. R. (2009). P38-MAPK- and caspase-3-mediated superoxide-induced apoptosis of rat hepatic stellate cells: Reversal by retinoic acid. Journal of Cellular Physiology, 218(1), 157–166.
33. Jia, L., Liu, Z., Sun, L., Miller, S. S., Ames, B. N., Cotman, C. W., & Liu, J. (2007). Acrolein, a toxicant in cigarette smoke, causes oxidative damage and mitochondrial dysfunction in RPE cells: Protection by (R)-α-lipoic acid. Investigative Ophthalmology and Visual Science, 48(1), 339–348.
34. Kaplan, M. J., & Radic, M. (2012). Neutrophil extracellular traps: Double-edged swords of innate immunity. Journal of Immunology, 189(6), 2689–2695.
35. Katkar, G. D., Sundaram, M. S., NaveenKumar, S. K., Swethakumar, B., Sharma, R. D., Paul, M., … Kemparaju, K. (2016). NETosis and lack of DNase activity are key factors in Echis carinatus venom-induced tissue destruction. Nature Communications, 7, 11361.
36. Keshari, R. S., Verma, A., Barthwal, M. K., & Dikshit, M. (2013). Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. Journal of Cellular Biochemistry, 114(3), 532–540.
37. Kim, D., & Haynes, C. L. (2013). The role of p38 MAPK in neutrophil functions: Single cell chemotaxis and surface marker expression. Analyst, 138(22), 6826–6833.
38. Kolaczkowska, E., Jenne, C. N., Surewaard, B. G., Thanabalasuriar, A., Lee, W. Y., Sanz, M. J., … Kubes, P. (2015). Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nature Communications, 6, 6673.
39. Kudoh, K., Uchinami, H., Yoshioka, M., Seki, E., & Yamamoto, Y. (2014). Nrf2 activation protects the liver from ischemia/reperfusion injury in mice. Annals of Surgery, 260(1), 118–127.
40. Liang, S., Kisseleva, T., & Brenner, D. A. (2016). The role of NADPH oxidases (NOXs) in liver fibrosis and the activation of myofibroblasts. Frontiers in Physiology, 7, 17.
41. Liu, B., & Qian, J. M. (2015). Cytoprotective role of heme oxygenase-1 in liver ischemia reperfusion injury. International Journal of Clinical and Experimental Medicine, 8(11), 19867–19873.
42. Man, K., Fan, S. T., Ng, I. O., Lo, C. M., Liu, C. L., & Wong, J. (1997). Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Annals of Surgery, 226(6), 704–711;.
43. Marques, P. E., Amaral, S. S., Pires, D. A., Nogueira, L. L., Soriani, F. M., Lima, B. H., … Menezes, G. B. (2012). Chemokines and mitochondrial products activate neutrophils to amplify organ injury during mouse acute liver failure. Hepatology, 56(5), 1971–1982.
44. Moghe, A., Ghare, S., Lamoreau, B., Mohammad, M., Barve, S., McClain, C., & Joshi-Barve, S. (2015). Molecular mechanisms of acrolein toxicity: Relevance to human disease. Toxicological Sciences, 143(2), 242–255.
45. Obukhova, O., Kashiya, S., Gorojanskaya, E., Chekini, J., & Sviridova, S. (2011). Effects of high doses of selenium on the antioxidant status after liver resection. Critical Care, 15(Suppl 1), P374.
46. Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95(2), 351–358.
47. Papayannopoulos, V., Metzler, K. D., Hakkim, A., & Zychlinsky, A. (2010). Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. The Journal of Cell Biology, 191(3), 677–691.
48. Paugam-Burtz, C., Wendon, J., Belghiti, J., & Mantz, J. (2015). Case scenario: Postoperative liver failure after liver resection in a cirrhotic patient. Anesthesiology, 116(3), 705–711.
49. Pedersen, F., Marwitz, S., Holz, O., Kirsten, A., Bahmer, T., Waschki, B., … Watz, H. (2015). Neutrophil extracellular trap formation and extracellular DNA in sputum of stable COPD patients. Respiratory Medicine, 109(10), 1360–1362.
50. Qin, W. S., Deng, Y. H., & Cui, F. C. (2016). Sulforaphane protects against acrolein-induced oxidative stress and inflammatory responses: Modulation of Nrf-2 and COX-2 expression. Archives of Medical Science, 12(4), 871–880.
51. Ren, X., Shi, Y., Zhao, D., Xu, M., Li, X., Dang, Y., & Ye, X. (2016). Naringin protects ultraviolet B-induced skin damage by regulating p38 MAPK signal pathway. Journal of Dermatological Science, 82(2), 106–114.
52. Richards, J. A., Wigmore, S. J., & Devey, L. R. (2010). Heme oxygenase system in hepatic ischemia-reperfusion injury. World Journal of Gastroenterology, 16(48), 6068–6078.
53. Rohm, M., Grimm, M. J., D'Auria, A. C., Almyroudis, N. G., Segal, B. H., & Urban, C. F. (2014). NADPH oxidase promotes neutrophil extracellular trap formation in pulmonary aspergillosis. Infection and Immunity, 82(5), 1766–1777.
54. Rostas, A., Sabry, A., & Ghosh, S. (2016). The influence of heat shock proteins on hepatic ischaemia reperfusion injury. Orvosi Hetilap, 157(42), 1659–1666.
55. Roy, J., Pallepati, P., Bettaieb, A., Tanel, A., & Averill-Bates, D. A. (2009). Acrolein induces a cellular stress response and triggers mitochondrial apoptosis in A549 cells. Chemico-Biological Interactions, 181(2), 154–167.
56. Russmann, S., Kullak-Ublick, G. A., & Grattagliano, I. (2009). Current concepts of mechanisms in drug-induced hepatotoxicity. Current Medicinal Chemistry, 16(23), 3041–3053.
57. Saidi, R. F. (2013). Utilization of expanded criteria donors in liver transplantation. International Journal of Organ Transplantation Medicine, 4(2), 46–59.
58. Segal, A. W. (2005). How neutrophils kill microbes. Annual Review of Immunology, 23, 197–223.
59. Singh, A., Zarember, K. A., Kuhns, D. B., & Gallin, J. I. (2009). Impaired priming and activation of the neutrophil NADPH oxidase in patients with IRAK4 or NEMO deficiency. Journal of Immunology, 182(10), 6410–6417.
60. Singh, D., Cho, W. C., & Upadhyay, G. (2009). Drug-induced liver toxicity and prevention by herbal antioxidants: An overview. Frontiers in Physiology, 6, 363.
61. Stevens, J. F., & Maier, C. S. (2008). Acrolein: Sources, metabolism, and biomolecular interactions relevant to human health and disease. Molecular Nutrition and Food Research, 52(1), 7–25.
62. Stutchfield, B. M., Antoine, D. J., Mackinnon, A. C., Gow, D. J., Bain, C. C., Hawley, C. A., … Forbes, S. J. (2015). CSF1 restores innate immunity after liver injury in mice and serum levels indicate outcomes of patients with acute liver failure. Gastroenterology, 149(7), 1896–1909.
63. Sun, Y., Ito, S., Nishio, N., Tanaka, Y., Chen, N., Liu, L., & Isobe, K. (2015). Enhancement of the acrolein-induced production of reactive oxygen species and lung injury by GADD34. Oxidative Medicine and Cellular Longevity, 2015, 170309.
64. Sur Chowdhury, C., Giaglis, S., Walker, U. A., Buser, A., Hahn, S., & Hasler, P. (2004). Enhanced neutrophil extracellular trap generation in rheumatoid arthritis: analysis of underlying signal transduction pathways and potential diagnostic utility. Arthritis Research & Therapy, 16(3), R122.
65. Suyavaran, A., Ramamurthy, C., Mareeswaran, R., Subastri, A., Lokeswara Rao, P., & Thirunavukkarasu, C. (2015). TNF-α suppression by glutathione preconditioning attenuates hepatic ischemia reperfusion injury in young and aged rats. Inflammation Research, 64(1), 71–81.
66. Suyavaran, A., & Thirunavukkarasu, C. (2017a). Preconditioning methods in the management of hepatic ischemia reperfusion- induced injury: Update on molecular and future perspectives. Hepatology Research, 47(1), 31–48.
67. Suyavaran, A., & Thirunavukkarasu, C. (2017b). Inhibition of NADPH oxidase-2 and P38 mitogen activated protein kinase suppresses acrolein aggravated hepatic ischemia reperfusion injury through neutrophil extracellular traps. Journal of Hepatology, 66(1), S201–S202.
68. Tang, M. S., Wang, H. T., Hu, Y., Chen, W. S., Akao, M., Feng, Z., & Hu, W. (2011). Acrolein induced DNA damage, mutagenicity and effect on DNA repair. Molecular Nutrition and Food Research, 55(9), 1291–1300.
69. Tomiyama, K., Ikeda, A., Ueki, S., Nakao, A., Stolz, D. B., Koike, Y., … Murase, N. (2008). Inhibition of Kupffer cell-mediated early proinflammatory response with carbon monoxide in transplant-induced hepatic ischemia/reperfusion injury in rats. Hepatology, 48(5), 1608–1620.
70. Uemura, T., Watanabe, K., Ishibashi, M., Saiki, R., Kuni, K., Nishimura, K., … Igarashi, K. (2016). Aggravation of brain infarction through an increase in acrolein production and a decrease in glutathione with aging. Biochemical and Biophysical Research Communications, 473(2), 630–635.
71. Valatas, V., Kolios, G., Manousou, P., Notas, G., Xidakis, C., Diamantis, I., & Kouroumalis, E. (2004). Octreotide regulates CC but not CXC LPS-induced chemokine secretion in rat Kupffer cells. British Journal of Pharmacology, 141(3), 477–487.
72. von Kockritz-Blickwede, M., Blodkamp, S., & Nizet, V. (2016). Interaction of bacterial exotoxins with neutrophil extracellular traps: Impact for the infected host. Frontiers in Microbiology, 7, 402.
73. Wang, Y., Wysocka, J., Sayegh, J., Lee, Y. H., Perlin, J. R., Leonelli, L., … Coonrod, S. A. (2004). Human PAD4 regulates histone arginine methylation levels via demethylimination. Science, 306(5694), 279–283.
74. Wong, S. L., Demers, M., Martinod, K., Gallant, M., Wang, Y., Goldfine, A. B., … Wagner, D. D. (2015). Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nature Medicine, 21(7), 815–819.
75. Yang, H., Biermann, M. H., Brauner, J. M., Liu, Y., Zhao, Y., & Herrmann, M. (2016). New insights into neutrophil extracellular traps: Mechanisms of formation and role in inflammation. Frontiers in Immunology, 7, 302.
76. Zawrotniak, M., & Rapala-Kozik, M. (2013). Neutrophil extracellular traps (NETs)—formation and implications. Acta Biochimica Polonica, 60(3), 277–284.
77. Zhai, Y., Petrowsky, H., Hong, J. C., Busuttil, R. W., & Kupiec-Weglinski, J. W. (2013). Ischaemia-reperfusion injury in liver transplantation-from bench to bedside. Nature Reviews. Gastroenterology & Hepatology, 10(2), 79–89.