MKK3 influences mitophagy and is involved in cigarette smoke-induced inflammation

Free Radical Biology and Medicine

Volumn 101, Issue , 2016, Pages 102-115

  Mannam, Praveen ^a   Rauniyar, Navin ^a   Lam, TuKiet T ^a   Luo, Ruiyan ^b   Lee, Patty J ^a   Srivastava, Anup ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Cigarette Smoke; Inflammation; MAP kinase Kinase 3; Mitochondria; Mitophagy

Indexed keywords

ADENOSINE TRIPHOSPHATE; CIGARETTE SMOKE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; IL1B PROTEIN, MOUSE; INTERLEUKIN-6, MOUSE; MAP2K3 PROTEIN, HUMAN; MAP2K3 PROTEIN, MOUSE; PLANT EXTRACT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN TISSUE; INFLAMMATION; ISOBARIC TAG FOR RELATIVE AND ABSOLUTE QUANTITATION; MITOCHONDRIAL RESPIRATION; MITOPHAGY; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEOMICS; UPREGULATION; AGONISTS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; MITOCHONDRION; PATHOLOGY; PRIMARY CELL CULTURE; SMOKING; TOBACCO;

ADENOSINE TRIPHOSPHATE; ANIMALS; CIGARETTE SMOKING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MACROPHAGES; MAP KINASE KINASE 3; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; NF-KAPPA B; OXIDATIVE PHOSPHORYLATION; PLANT EXTRACTS; PRIMARY CELL CULTURE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; REACTIVE OXYGEN SPECIES; TOBACCO; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84991608277     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.10.001     Document Type: Article

References (79)

1. [1] Donner, C.F., Virchow, J.C., Lusuardi, M., Pharmacoeconomics in COPD and inappropriateness of diagnostics, management and treatment. Respir. Med. 105 (2011), 828–837.
2. [2] Harrison, S.L., Robertson, N., Apps, L., M, C.S., Morgan, M.D., Singh, S.J., We are not worthy”-understanding why patients decline pulmonary rehabilitation following an acute exacerbation of COPD. Disabil. Rehabil. 37 (2015), 750–756.
3. [3] W.Macnee, Pathogenesis of chronic obstructive pulmonary disease. Clin. Chest Med. 28:479–513, v, 2007.
4. [4] Cano, M., Wang, L., Wan, J., Barnett, B.P., Ebrahimi, K., Qian, J., Handa, J.T., Oxidative stress induces mitochondrial dysfunction and a protective unfolded protein response in RPE cells. Free Radic. Biol. Med. 69 (2014), 1–14.
5. [5] Yao, H., Yang, S.R., Kode, A., Rajendrasozhan, S., Caito, S., Adenuga, D., Henry, R., Edirisinghe, I., Rahman, I., Redox regulation of lung inflammation: role of NADPH oxidase and NF-kappaB signalling. Biochem. Soc. Trans. 35 (2007), 1151–1155.
6. [6] Aravamudan, B., Kiel, A., Freeman, M., Delmotte, P., Thompson, M., Vassallo, R., Sieck, G.C., Pabelick, C.M., Prakash, Y.S., Cigarette smoke-induced mitochondrial fragmentation and dysfunction in human airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 306 (2014), L840–L854.
7. [7] K.BallwegK.MutzeM.KonigshoffO.EickelbergS.Meiners, Cigarette smoke extract affects mitochondrial function in alveolar epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 307:L895-L907, 2014.
8. [8] Hoffmann, R.F., Zarrintan, S., Brandenburg, S.M., Kol, A., de Bruin, H.G., Jafari, S., Dijk, F., Kalicharan, D., Kelders, M., Gosker, H.R., Ten Hacken, N.H., van der Want, J.J., van Oosterhout, A.J., Heijink, I.H., Prolonged cigarette smoke exposure alters mitochondrial structure and function in airway epithelial cells. Respir. Res., 14, 2013, 97.
9. [9] Mizumura, K., Cloonan, S.M., Nakahira, K., Bhashyam, A.R., Cervo, M., Kitada, T., Glass, K., Owen, C.A., Mahmood, A., Washko, G.R., Hashimoto, S., Ryter, S.W., Choi, A.M., Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J. Clin. Investig. 124 (2014), 3987–4003.
10. [10] Pouwels, S.D., Heijink, I.H., ten Hacken, N.H., Vandenabeele, P., Krysko, D.V., Nawijn, M.C., van Oosterhout, A.J., DAMPs activating innate and adaptive immune responses in COPD. Mucosal Immunol. 7 (2014), 215–226.
11. [11] Zhang, X., Shan, P., Homer, R., Zhang, Y., Petrache, I., Mannam, P., Lee, P.J., Cathepsin E promotes pulmonary emphysema via mitochondrial fission. Am. J. Pathol. 184 (2014), 2730–2741.
12. [12] Hara, H., Araya, J., Ito, S., Kobayashi, K., Takasaka, N., Yoshii, Y., Wakui, H., Kojima, J., Shimizu, K., Numata, T., Kawaishi, M., Kamiya, N., Odaka, M., Morikawa, T., Kaneko, Y., Nakayama, K., Kuwano, K., Mitochondrial fragmentation in cigarette smoke-induced bronchial epithelial cell senescence. Am. J. Physiol. Lung Cell. Mol. Physiol. 305 (2013), L737–L746.
13. [13] Ahmad, T., Sundar, I.K., Lerner, C.A., Gerloff, J., Tormos, A.M., Yao, H., Rahman, I., Impaired mitophagy leads to cigarette smoke stress-induced cellular senescence: implications for chronic obstructive pulmonary disease. FASEB J. 29 (2015), 2912–2929.
14. [14] Gannon, A.M., Stampfli, M.R., Foster, W.G., Cigarette smoke exposure elicits increased autophagy and dysregulation of mitochondrial dynamics in murine granulosa cells. Biol. Reprod., 88, 2013, 63.
15. [15] Ito, S., Araya, J., Kurita, Y., Kobayashi, K., Takasaka, N., Yoshida, M., Hara, H., Minagawa, S., Wakui, H., Fujii, S., Kojima, J., Shimizu, K., Numata, T., Kawaishi, M., Odaka, M., Morikawa, T., Harada, T., Nishimura, S.L., Kaneko, Y., Nakayama, K., Kuwano, K., PARK2-mediated mitophagy is involved in regulation of HBEC senescence in COPD pathogenesis. Autophagy 11 (2015), 547–559.
16. [16] A.SrivastavaJ.McGinnissY.WongA.S.ShinnT.T.LamP.J.LeeP.Mannam, MKK3 deletion improves mitochondrial quality. Free Radic. Biol. Med. 87:373-384, 2015.
17. [17] Mannam, P., Shinn, A.S., Srivastava, A., Neamu, R.F., Walker, W.E., Bohanon, M., Merkel, J., Kang, M.J., Dela Cruz, C.S., Ahasic, A.M., Pisani, M.A., Trentalange, M., West, A.P., Shadel, G.S., Elias, J.A., Lee, P.J., MKK3 regulates mitochondrial biogenesis and mitophagy in sepsis-induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 306 (2014), L604–L619.
18. [18] Mannam, P., Zhang, X., Shan, P., Zhang, Y., Shinn, A.S., Zhang, Y., Lee, P.J., Endothelial MKK3 is a critical mediator of lethal murine endotoxemia and acute lung injury. J. Immunol. 190 (2013), 1264–1275.
19. [19] Zhang, X., Shan, P., Otterbein, L.E., Alam, J., Flavell, R.A., Davis, R.J., Choi, A.M., Lee, P.J., Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J. Biol. Chem. 278 (2003), 1248–1258.
20. [20] Otterbein, L.E., Otterbein, S.L., Ifedigbo, E., Liu, F., Morse, D.E., Fearns, C., Ulevitch, R.J., Knickelbein, R., Flavell, R.A., Choi, A.M., MKK3 mitogen-activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant-induced lung injury. Am. J. Pathol. 163 (2003), 2555–2563.
21. [21] Srivastava, A., Shinn, A.S., Lee, P.J., Mannam, P., MKK3 mediates inflammatory response through modulation of mitochondrial function. Free Radic. Biol. Med. 83 (2015), 139–148.
22. [22] Yang, S.R., Chida, A.S., Bauter, M.R., Shafiq, N., Seweryniak, K., Maggirwar, S.B., Kilty, I., Rahman, I., Cigarette smoke induces proinflammatory cytokine release by activation of NF-kappaB and posttranslational modifications of histone deacetylase in macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 291 (2006), L46–L57.
23. [23] Kent, L., Smyth, L., Clayton, C., Scott, L., Cook, T., Stephens, R., Fox, S., Hext, P., Farrow, S., Singh, D., Cigarette smoke extract induced cytokine and chemokine gene expression changes in COPD macrophages. Cytokine 42 (2008), 205–216.
24. [24] Kent, L.M., Fox, S.M., Farrow, S.N., Singh, D., The effects of dexamethasone on cigarette smoke induced gene expression changes in COPD macrophages. Int. Immunopharmacol. 10 (2010), 57–64.
25. [25] Metcalfe, H.J., Lea, S., Hughes, D., Khalaf, R., Abbott-Banner, K., Singh, D., Effects of cigarette smoke on Toll-like receptor (TLR) activation of chronic obstructive pulmonary disease (COPD) macrophages. Clin. Exp. Immunol. 176 (2014), 461–472.
26. [26] Brancho, D., Tanaka, N., Jaeschke, A., Ventura, J.J., Kelkar, N., Tanaka, Y., Kyuuma, M., Takeshita, T., Flavell, R.A., Davis, R.J., Mechanism of p38 MAP kinase activation in vivo. Genes Dev. 17 (2003), 1969–1978.
27. [27] Valcarcel-Ares, M.N., Riveiro-Naveira, R.R., Vaamonde-Garcia, C., Loureiro, J., Hermida-Carballo, L., Blanco, F.J., Lopez-Armada, M.J., Mitochondrial dysfunction promotes and aggravates the inflammatory response in normal human synoviocytes. Rheumatology 53 (2014), 1332–1343.
28. [28] Moerloose, K.B., Pauwels, R.A., Joos, G.F., Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 172 (2005), 168–172.
29. [29] Yao, H., Hwang, J.W., Moscat, J., Diaz-Meco, M.T., Leitges, M., Kishore, N., Li, X., Rahman, I., Protein kinase C zeta mediates cigarette smoke/aldehyde- and lipopolysaccharide-induced lung inflammation and histone modifications. J. Biol. Chem. 285 (2010), 5405–5416.
30. [30] Vassallo, R., Tamada, K., Lau, J.S., Kroening, P.R., Chen, L., Cigarette smoke extract suppresses human dendritic cell function leading to preferential induction of Th-2 priming. J. Immunol. 175 (2005), 2684–2691.
31. [31] Aravamudan, B., Thompson, M.A., Pabelick, C.M., Prakash, Y.S., Mitochondria in lung diseases. Expert Rev. Respir. Med. 7 (2013), 631–646.
32. [32] Allen, G.F., Toth, R., James, J., Ganley, I.G., Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. 14 (2013), 1127–1135.
33. [33] Sargsyan, A., Cai, J., Fandino, L.B., Labasky, M.E., Forostyan, T., Colosimo, L.K., Thompson, S.J., Graham, T.E., Rapid parallel measurements of macroautophagy and mitophagy in mammalian cells using a single fluorescent biosensor. Sci. Rep., 5, 2015, 12397.
34. [34] Kalucka, S., The occurrence of chronic obstructive pulmonary disease (COPD) in cigarette smoking families. Prz. Lek. 63 (2006), 848–857.
35. [35] V.KimT.J.RogersG.J.Criner, New concepts in the pathobiology of chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 5:478-485, 2008.
36. [36] Comer, D.M., Kidney, J.C., Ennis, M., Elborn, J.S., Airway epithelial cell apoptosis and inflammation in COPD, smokers and nonsmokers. Eur. Respir. J. 41 (2013), 1058–1067.
37. [37] Kelsen, S.G., Duan, X., Ji, R., Perez, O., Liu, C., Merali, S., Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am. J. Respir. Cell Mol. Biol. 38 (2008), 541–550.
38. [38] Ojo, O., Lagan, A.L., Rajendran, V., Spanjer, A., Chen, L., Sohal, S.S., Heijink, I., Jones, R., Maarsingh, H., Hackett, T.L., Pathological changes in the COPD lung mesenchyme-novel lessons learned from in vitro and in vivo studies. Pulm. Pharmacol. Ther. 29 (2014), 121–128.
39. [39] Tanabe, N., Muro, S., Sato, S., Tanaka, S., Oguma, T., Kiyokawa, H., Takahashi, T., Kinose, D., Hoshino, Y., Kubo, T., Hirai, T., Mishima, M., Longitudinal study of spatially heterogeneous emphysema progression in current smokers with chronic obstructive pulmonary disease. PLoS One, 7, 2012, e44993.
40. [40] Mansoor, S., Gupta, N., Falatoonzadeh, P., Kuppermann, B.D., Kenney, M.C., 2-ethylpyridine, a cigarette smoke component, causes mitochondrial damage in human retinal pigment epithelial cells in vitro. Indian J. Ophthalmol. 62 (2014), 16–22.
41. [41] Nguyen, L.T., Stangenberg, S., Chen, H., Al-Odat, I., Chan, Y.L., Gosnell, M.E., Anwer, A.G., Goldys, E.M., Pollock, C.A., Saad, S., l-Carnitine reverses maternal cigarette smoke exposure-induced renal oxidative stress and mitochondrial dysfunction in mouse offspring. Am. J. Physiol. Ren. Physiol. 308 (2015), F689–F696.
42. [42] Pei, Z., Zhuang, Z., Sang, H., Wu, Z., Meng, R., He, E.Y., Scott, G.I., Maris, J.R., Li, R., Ren, J., alpha,beta-Unsaturated aldehyde crotonaldehyde triggers cardiomyocyte contractile dysfunction: role of TRPV1 and mitochondrial function. Pharmacol. Res. 82 (2014), 40–50.
43. [43] Xuan, L.L., Shi, J., Yao, C.S., Bai, J.Y., Qu, F., Zhang, J.L., Hou, Q., Vam3, a resveratrol dimer, inhibits cigarette smoke-induced cell apoptosis in lungs by improving mitochondrial function. Acta Pharmacol. Sin. 35 (2014), 779–791.
44. [44] Yang, J., Yu, H.M., Zhou, X.D., Huang, H.P., Han, Z., Kolosov, V.P., Perelman, J.M., Cigarette smoke induces mucin hypersecretion and inflammatory response through the p66shc adaptor protein-mediated mechanism in human bronchial epithelial cells. Mol. Immunol. 69 (2016), 86–98.
45. [45] Arnoult, D., Soares, F., Tattoli, I., Girardin, S.E., Mitochondria in innate immunity. EMBO Rep. 12 (2011), 901–910.
46. [46] Chung, S.D., Lai, T.Y., Chien, C.T., Yu, H.J., Activating Nrf-2 signaling depresses unilateral ureteral obstruction-evoked mitochondrial stress-related autophagy, apoptosis and pyroptosis in kidney. PLoS One, 7, 2012, e47299.
47. [47] Hattori, N., Saiki, S., Imai, Y., Regulation by mitophagy. Int. J. Biochem. Cell Biol. 53 (2014), 147–150.
48. [48] Lionaki, E., Markaki, M., Palikaras, K., Tavernarakis, N., Mitochondria, autophagy and age-associated neurodegenerative diseases: new insights into a complex interplay. Biochim. Biophys. Acta 1847 (2015), 1412–1423.
49. [49] S.Von StockumA.NardinE.SchrepferE.Ziviani, Mitochondrial dynamics and mitophagy in Parkinson's disease: A fly point of view. Neurobiol. Dis., 2015.
50. [50] Scarffe, L.A., Stevens, D.A., Dawson, V.L., Dawson, T.M., Parkin and PINK1: much more than mitophagy. Trends Neurosci. 37 (2014), 315–324.
51. [51] Wu, W., Xu, H., Wang, Z., Mao, Y., Yuan, L., Luo, W., Cui, Z., Cui, T., Wang, X.L., Shen, Y.H., PINK1-Parkin-mediated mitophagy protects mitochondrial integrity and prevents metabolic stress-induced endothelial injury. PLoS One, 10, 2015, e0132499.
52. [52] Hamacher-Brady, A., Brady, N.R., Mitophagy programs: mechanisms and physiological implications of mitochondrial targeting by autophagy. Cell Mol. Life Sci. 73 (2016), 775–795.
53. [53] Lee, J., Giordano, S., Zhang, J., Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J. 441 (2012), 523–540.
54. [54] Dias, V., Junn, E., Mouradian, M.M., The role of oxidative stress in Parkinson's disease. J. Park. Dis. 3 (2013), 461–491.
55. [55] Mitchell, T., Chacko, B., Ballinger, S.W., Bailey, S.M., Zhang, J., Darley-Usmar, V., Convergent mechanisms for dysregulation of mitochondrial quality control in metabolic disease: implications for mitochondrial therapeutics. Biochem. Soc. Trans. 41 (2013), 127–133.
56. [56] Victorino, V.J., Mencalha, A.L., Panis, C., Post-translational modifications disclose a dual role for redox stress in cardiovascular pathophysiology. Life Sci. 129 (2015), 42–47.
57. [57] Ryter, S.W., Choi, A.M., Autophagy in lung disease pathogenesis and therapeutics. Redox Biol. 4 (2015), 215–225.
58. [58] Sticozzi, C., Pecorelli, A., Belmonte, G., Valacchi, G., Cigarette smoke affects ABCAl expression via liver X receptor nuclear translocation in human keratinocytes. Int. J. Mol. Sci. 11 (2010), 3375–3386.
59. [59] La Maestra, S., Micale, R.T., De Flora, S., D'Agostini, F., Ganchev, G., Iltcheva, M., Petkov, N., Steele, V.E., Balansky, R., DNA damage in exfoliated cells and histopathological alterations in the urinary tract of mice exposed to cigarette smoke and treated with chemopreventive agents. Carcinogenesis 34 (2013), 183–189.
60. [60] Boue, S., Tarasov, K., Janis, M., Lebrun, S., Hurme, R., Schlage, W., Lietz, M., Vuillaume, G., Ekroos, K., Steffen, Y., Peitsch, M.C., Laaksonen, R., Hoeng, J., Modulation of atherogenic lipidome by cigarette smoke in apolipoprotein E-deficient mice. Atherosclerosis 225 (2012), 328–334.
61. [61] Damasceno, D.C., Sinzato, Y.K., Bueno, A., Dallaqua, B., Lima, P.H., Calderon, I.M., Rudge, M.V., Campos, K.E., Metabolic profile and genotoxicity in obese rats exposed to cigarette smoke. Obesity 21 (2013), 1596–1601.
62. [62] Ghezzi, S., Rise, P., Ceruti, S., Galli, C., Effects of cigarette smoke on cell viability, linoleic acid metabolism and cholesterol synthesis, in THP-1 cells. Lipids 42 (2007), 629–636.
63. [63] Jean-Baptiste, E., Cellular mechanisms in sepsis. J. Intensive Care Med. 22 (2007), 63–72.
64. [64] Hoonhorst, S.J., Timens, W., Koenderman, L., Lo Tam Loi, A.T., Lammers, J.W., Boezen, H.M., van Oosterhout, A.J., Postma, D.S., Ten Hacken, N.H., Increased activation of blood neutrophils after cigarette smoking in young individuals susceptible to COPD. Respir. Res., 15, 2014, 121.
65. [65] John, G., Kohse, K., Orasche, J., Reda, A., Schnelle-Kreis, J., Zimmermann, R., Schmid, O., Eickelberg, O., Yildirim, A.O., The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models. Clin. Sci. 126 (2014), 207–221.
66. [66] Huang, C., Wang, J.J., Ma, J.H., Jin, C., Yu, Q., Zhang, S.X., Activation of the UPR protects against cigarette smoke-induced RPE apoptosis through up-regulation of Nrf2. J. Biol. Chem. 290 (2015), 5367–5380.
67. [67] Kojima, T., Dogru, M., Higuchi, A., Nagata, T., Ibrahim, O.M., Inaba, T., Tsubota, K., The effect of Nrf2 knockout on ocular surface protection from acute tobacco smoke exposure: evidence from Nrf2 knockout mice. Am. J. Pathol. 185 (2015), 776–785.
68. [68] Pascual, M.B., Mata-Cabana, A., Florencio, F.J., Lindahl, M., Cejudo, F.J., A comparative analysis of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system from plants and cyanobacteria. Plant Physiol. 155 (2011), 1806–1816.
69. [69] Tomanek, L., Proteomic responses to environmentally induced oxidative stress. J. Exp. Biol. 218 (2015), 1867–1879.
70. [70] Agarwal, A.R., Zhao, L., Sancheti, H., Sundar, I.K., Rahman, I., Cadenas, E., Short-term cigarette smoke exposure induces reversible changes in energy metabolism and cellular redox status independent of inflammatory responses in mouse lungs. Am. J. Physiol. Lung Cell. Mol. Physiol. 303 (2012), L889–L898.
71. [71] Chen, Z.H., Lam, H.C., Jin, Y., Kim, H.P., Cao, J., Lee, S.J., Ifedigbo, E., Parameswaran, H., Ryter, S.W., Choi, A.M., Autophagy protein microtubule-associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc. Natl. Acad. Sci. USA 107 (2010), 18880–18885.
72. [72] Hwang, J.W., Chung, S., Sundar, I.K., Yao, H., Arunachalam, G., McBurney, M.W., Rahman, I., Cigarette smoke-induced autophagy is regulated by SIRT1-PARP-1-dependent mechanism: implication in pathogenesis of COPD. Arch. Biochem. Biophys. 500 (2010), 203–209.
73. [73] Zhu, L., Barrett, E.C., Xu, Y., Liu, Z., Manoharan, A., Chen, Y., Regulation of cigarette smoke (CS)-induced autophagy by Nrf2. PLoS One, 8, 2013, e55695.
74. [74] Furlong, H.C., Stampfli, M.R., Gannon, A.M., Foster, W.G., Cigarette smoke exposure triggers the autophagic cascade via activation of the AMPK pathway in mice. Biol. Reprod., 93, 2015, 93.
75. [75] Lee, K., Hong, S., Seong, G.J., Kim, C.Y., Cigarette smoke extract causes injury in primary retinal ganglion cells via apoptosis and autophagy. Curr. Eye Res., 2016, 1–6.
76. [76] Wang, J., Fang, R., Peterson, A., Jiang, J.J., The protective role of autophagy in human vocal fold fibroblasts under cigarette smoke extract exposure: a new insight into the study of Reinke's Edema. J. Oto-Rhino-Laryngol. Relat. Spec. 78 (2016), 26–35.
77. [77] Bortner, J.D., J.P. Richie, A. Das, J. Liao, T.M. Umstead, A. Stanley, B.A. Stanley, C.P. Belani, K. El-Bayoumy, Proteomic profiling of human plasma by iTRAQ reveals down-regulation of ITI-HC3 and VDBP by cigarette smoking. J. Proteome Res. 10:1151–1159, 2011.
78. [78] Franciosi, L., Postma, D.S., van den Berge, M., Govorukhina, N., Horvatovich, P.L., Fusetti, F., Poolman, B., Lodewijk, M.E., Timens, W., Bischoff, R., ten Hacken, N.H., Susceptibility to COPD: differential proteomic profiling after acute smoking. PLoS One, 9, 2014, e102037.
79. [79] Sexton, K., Balharry, D., Brennan, P., McLaren, J., Brewis, I.A., BeruBe, K.A., Proteomic profiling of human respiratory epithelia by iTRAQ reveals biomarkers of exposure and harm by tobacco smoke components. Biomark.: Biochem. Indic. Expo. Response Susceptibility Chem. 16 (2011), 567–576.