Novel proteolytic microvesicles released from human macrophages after exposure to tobacco smoke

American Journal of Pathology

Volumn 182, Issue 5, 2013, Pages 1552-1562

  Li, Chun Jun ^a,b   Liu, Yu ^a   Chen, Yan ^a   Yu, Demin ^b   Williams, Kevin Jon ^a   Liu, Ming Lin ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BEIJING HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX METALLOPROTEINASE 14; MITOGEN ACTIVATED PROTEIN KINASE P38; TOBACCO SMOKE;

APOPTOSIS; ARTICLE; CELL MEMBRANE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MACROPHAGE; MEMBRANE VESICLE; MICROVESICLE; PRIORITY JOURNAL; PROTEIN DEGRADATION; SMOKING;

APOPTOSIS; CELL LINE; CELL MEMBRANE; CELL-DERIVED MICROPARTICLES; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MACROPHAGES; MATRIX METALLOPROTEINASE 14; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEOLYSIS; SMOKING;

EID: 84876518109     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.01.035     Document Type: Article

References (70)

1. O. Morel, F. Toti, B. Hugel, and J.M. Freyssinet Cellular microparticles: a disseminated storage pool of bioactive vascular effectors Curr Opin Hematol 11 2004 156 164
2. M.C. Martinez, A. Tesse, F. Zobairi, and R. Andriantsitohaina Shed membrane microparticles from circulating and vascular cells in regulating vascular function Am J Physiol Heart Circ Physiol 288 2005 H1004 H1009
3. C.M. Boulanger, N. Amabile, and A. Tedgui Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease Hypertension 48 2006 180 186
4. M.L. Liu, M.P. Reilly, P. Casasanto, S.E. McKenzie, and K.J. Williams Cholesterol enrichment of human monocyte/macrophages induces surface exposure of phosphatidylserine and the release of biologically-active tissue factor-positive microvesicles Arterioscler Thromb Vasc Biol 27 2007 430 435
5. M. Li, D. Yu, K.J. Williams, and M.L. Liu Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages Arterioscler Thromb Vasc Biol 30 2010 1818 1824
6. A.P. Owens 3rd, and N. Mackman Microparticles in hemostasis and thrombosis Circ Res 108 2011 1284 1297
7. M.L. Liu, and K.J. Williams Microvesicles: potential markers and mediators of endothelial dysfunction Curr Opin Endocrinol Diabetes Obes 19 2012 121 127
8. C. Heiss, N. Amabile, A.C. Lee, W.M. Real, S.F. Schick, D. Lao, M.L. Wong, S. Jahn, F.S. Angeli, P. Minasi, M.L. Springer, S.K. Hammond, S.A. Glantz, W. Grossman, J.R. Balmes, and Y. Yeghiazarians Brief secondhand smoke exposure depresses endothelial progenitor cells activity and endothelial function: sustained vascular injury and blunted nitric oxide production J Am Coll Cardiol 51 2008 1760 1771
9. C. Gordon, K. Gudi, A. Krause, R. Sackrowitz, B.G. Harvey, Y. Strulovici-Barel, J.G. Mezey, and R.G. Crystal Circulating endothelial microparticles as a measure of early lung destruction in cigarette smokers Am J Respir Crit Care Med 184 2011 224 232
10. M.J. Davies, P.D. Richardson, N. Woolf, D.R. Katz, and J. Mann Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content Br Heart J 69 1993 377 381
11. J.L. Johnson, and A.C. Newby Macrophage heterogeneity in atherosclerotic plaques Curr Opin Lipidol 20 2009 370 378
12. K. Ley, Y.I. Miller, and C.C. Hedrick Monocyte and macrophage dynamics during atherogenesis Arterioscler Thromb Vasc Biol 31 2011 1506 1516
13. T.D. Tetley Macrophages and the pathogenesis of COPD Chest 121 2002 156S 159S
14. L. Landsman, and S. Jung Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages J Immunol 179 2007 3488 3494
15. R.D. Hautamaki, D.K. Kobayashi, R.M. Senior, and S.D. Shapiro Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice Science 277 1997 2002 2004
16. P.A. Snoek-van Beurden, and J.W. Von den Hoff Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors Biotechniques 38 2005 73 83
17. A.C. Newby Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture Physiol Rev 85 2005 1 31
18. V. Muralidharan-Chari, J. Clancy, C. Plou, M. Romao, P. Chavrier, G. Raposo, and C. D'Souza-Schorey ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles Curr Biol 19 2009 1875 1885
19. J. Liu, G.K. Sukhova, J.S. Sun, W.H. Xu, P. Libby, and G.P. Shi Lysosomal cysteine proteases in atherosclerosis Arterioscler Thromb Vasc Biol 24 2004 1359 1366
20. B. Bauvois New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: outside-in signaling and relationship to tumor progression Biochim Biophys Acta 1825 2011 29 36
21. T. Sato, M. del Carmen Ovejero, P. Hou, A.M. Heegaard, M. Kumegawa, N.T. Foged, and J.M. Delaisse Identification of the membrane-type matrix metalloproteinase MT1-MMP in osteoclasts J Cell Sci 110 Pt 5 1997 589 596
22. C. Li, Y. Liu, D. Yu, K.J. Williams, and M.L. Liu Exposure of human macrophages to tobacco smoke induces MMP14 expression and generation of proteolytically active microvesicles Atheroscler Suppl 12 2011 69
23. H. Carp, and A. Janoff Possible mechanisms of emphysema in smokers. In vitro suppression of serum elastase-inhibitory capacity by fresh cigarette smoke and its prevention by antioxidants Am Rev Respir Dis 118 1978 617 621
24. K.K. Meja, S. Rajendrasozhan, D. Adenuga, S.K. Biswas, I.K. Sundar, G. Spooner, J.A. Marwick, P. Chakravarty, D. Fletcher, P. Whittaker, I.L. Megson, P.A. Kirkham, and I. Rahman Curcumin restores corticosteroid function in monocytes exposed to oxidants by maintaining HDAC2 Am J Respir Cell Mol Biol 39 2008 312 323
25. H. Yao, I. Edirisinghe, S.R. Yang, S. Rajendrasozhan, A. Kode, S. Caito, D. Adenuga, and I. Rahman Genetic ablation of NADPH oxidase enhances susceptibility to cigarette smoke-induced lung inflammation and emphysema in mice Am J Pathol 172 2008 1222 1237
26. S. Caito, S.R. Yang, A. Kode, I. Edirisinghe, S. Rajendrasozhan, R.P. Phipps, and I. Rahman Rosiglitazone and 15-deoxy-Delta12,14-prostaglandin J2. PPARgamma agonists, differentially regulate cigarette smoke-mediated pro-inflammatory cytokine release in monocytes/macrophages Antioxid Redox Signal 10 2008 253 260
27. C.J. Baglole, S.M. Bushinsky, T.M. Garcia, A. Kode, I. Rahman, P.J. Sime, and R.P. Phipps Differential induction of apoptosis by cigarette smoke extract in primary human lung fibroblast strains: implications for emphysema Am J Physiol Lung Cell Mol Physiol 291 2006 L19 L29
28. S.K. McMaster, M.J. Paul-Clark, M. Walters, M. Fleet, J. Anandarajah, S. Sriskandan, and J.A. Mitchell Cigarette smoke inhibits macrophage sensing of Gram-negative bacteria and lipopolysaccharide: relative roles of nicotine and oxidant stress Br J Pharmacol 153 2008 536 543
29. E.K. Park, H.S. Jung, H.I. Yang, M.C. Yoo, C. Kim, and K.S. Kim Optimized THP-1 differentiation is required for the detection of responses to weak stimuli Inflamm Res 56 2007 45 50
30. M. Daigneault, J.A. Preston, H.M. Marriott, M.K. Whyte, and D.H. Dockrell The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages PLoS One 5 2010 e8668
31. K.S. Akagawa, I. Komuro, H. Kanazawa, T. Yamazaki, K. Mochida, and F. Kishi Functional heterogeneity of colony-stimulating factor-induced human monocyte-derived macrophages Respirology 11 2006 S32 S36
32. C. Furman, C. Copin, M. Kandoussi, R. Davidson, M. Moreau, F. McTaggiart, M.J. Chapman, J.C. Fruchart, and M. Rouis Rosuvastatin reduces MMP-7 secretion by human monocyte-derived macrophages: potential relevance to atherosclerotic plaque stability Atherosclerosis 174 2004 93 98
33. W. Hadnagy, N.H. Seemayer, A. Happel, and A. Kiell Human monocyte-derived macrophage cultures: an alternative test system for the detection of pulmonary toxicity induced by inhaled particulate pollutants Toxicol In Vitro 7 1993 365 371
34. D. Klestadt, P. Laval-Gilly, L. Foucaud, and J. Falla Modification of membrane markers on THP-1 cells after ozone exposure in the presence or absence of fMLP Toxicol In Vitro 18 2004 279 283
35. T.H. Sulahian, A. Imrich, G. Deloid, A.R. Winkler, and L. Kobzik Signaling pathways required for macrophage scavenger receptor-mediated phagocytosis: analysis by scanning cytometry Respir Res 9 2008 59
36. H. Zhou, G. Deloid, E. Browning, D.J. Gregory, F. Tan, A.S. Bedugnis, A. Imrich, H. Koziel, I. Kramnik, Q. Lu, and L. Kobzik Genome-wide RNAi screen in IFN-gamma-treated human macrophages identifies genes mediating resistance to the intracellular pathogen francisella tularensis PLoS One 7 2012 e31752
37. S.P. Hawkes, H. Li, and G.T. Taniguchi Zymography and reverse zymography for detecting MMPs and TIMPs Methods Mol Biol 622 2010 257 269
38. K. Kupai, G. Szucs, S. Cseh, I. Hajdu, C. Csonka, T. Csont, and P. Ferdinandy Matrix metalloproteinase activity assays: importance of zymography J Pharmacol Toxicol Methods 61 2010 205 209
39. B. Gogly, N. Groult, W. Hornebeck, G. Godeau, and B. Pellat Collagen zymography as a sensitive and specific technique for the determination of subpicogram levels of interstitial collagenase Anal Biochem 255 1998 211 216
40. W.H. Yu, and J.F. Woessner Jr. Heparin-enhanced zymographic detection of matrilysin and collagenases Anal Biochem 293 2001 38 42
41. T.B. Rajavashisth, X.P. Xu, S. Jovinge, S. Meisel, X.O. Xu, N.N. Chai, M.C. Fishbein, S. Kaul, B. Cercek, B. Sharifi, and P.K. Shah Membrane type 1 matrix metalloproteinase expression in human atherosclerotic plaques: evidence for activation by proinflammatory mediators Circulation 99 1999 3103 3109
42. E.D. Karagiannis, and A.S. Popel A theoretical model of type I collagen proteolysis by matrix metalloproteinase (MMP) 2 and membrane type 1 MMP in the presence of tissue inhibitor of metalloproteinase 2 J Biol Chem 279 2004 39105 39114
43. F. Schneider, G.K. Sukhova, M. Aikawa, J. Canner, N. Gerdes, S.M. Tang, G.P. Shi, S.S. Apte, and P. Libby Matrix-metalloproteinase-14 deficiency in bone-marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques Circulation 117 2008 931 939
44. J.J. Atkinson, K. Holmbeck, S. Yamada, H. Birkedal-Hansen, W.C. Parks, and R.M. Senior Membrane-type 1 matrix metalloproteinase is required for normal alveolar development Dev Dyn 232 2005 1079 1090
45. H.S. Deshmukh, A. McLachlan, J.J. Atkinson, W.D. Hardie, T.R. Korfhagen, M. Dietsch, Y. Liu, P.Y. Di, S.C. Wesselkamper, M.T. Borchers, and G.D. Leikauf Matrix metalloproteinase-14 mediates a phenotypic shift in the airways to increase mucin production Am J Respir Crit Care Med 180 2009 834 845
46. S. Loffek, O. Schilling, and C.W. Franzke Series "matrix metalloproteinases in lung health and disease": Biological role of matrix metalloproteinases: a critical balance Eur Respir J 38 2011 191 208
47. J.L. Johnson, G.B. Sala-Newby, Y. Ismail, C.M. Aguilera, and A.C. Newby Low tissue inhibitor of metalloproteinases 3 and high matrix metalloproteinase 14 levels defines a subpopulation of highly invasive foam-cell macrophages Arterioscler Thromb Vasc Biol 28 2008 1647 1653
48. J. Llodra, V. Angeli, J. Liu, E. Trogan, E.A. Fisher, and G.J. Randolph Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques Proc Natl Acad Sci USA 101 2004 11779 11784
49. K.J. Williams, J.E. Feig, and E.A. Fisher Rapid regression of atherosclerosis: insights from the clinical and experimental literature Nat Clin Pract Cardiovasc Med 5 2008 91 102
50. J.E. Feig, J.X. Rong, R. Shamir, M. Sanson, Y. Vengrenyuk, J. Liu, K. Rayner, K. Moore, M. Garabedian, and E.A. Fisher HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells Proc Natl Acad Sci USA 108 2011 7166 7171
51. J. Huber, A. Vales, G. Mitulovic, M. Blumer, R. Schmid, J.L. Witztum, B.R. Binder, and N. Leitinger Oxidized membrane vesicles and blebs from apoptotic cells contain biologically active oxidized phospholipids that induce monocyte-endothelial interactions Arterioscler Thromb Vasc Biol 22 2002 101 107
52. M.L. Liu, R. Scalia, J.L. Mehta, and K.J. Williams Cholesterol-induced membrane microvesicles as novel carriers of damage-associated molecular patterns: mechanisms of formation, action, and detoxification Arterioscler Thromb Vasc Biol 32 2012 2113 2121
53. K. Aoshiba, J. Tamaoki, and A. Nagai Acute cigarette smoke exposure induces apoptosis of alveolar macrophages Am J Physiol Lung Cell Mol Physiol 281 2001 L1392 L1401
54. T. Rangasamy, C.Y. Cho, R.K. Thimmulappa, L. Zhen, S.S. Srisuma, T.W. Kensler, M. Yamamoto, I. Petrache, R.M. Tuder, and S. Biswal Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice J Clin Invest 114 2004 1248 1259
55. M. Fujihara, N. Nagai, T.E. Sussan, S. Biswal, and J.T. Handa Chronic cigarette smoke causes oxidative damage and apoptosis to retinal pigmented epithelial cells in mice PLoS One 3 2008 e3119
56. H. Kim, X. Liu, T. Kohyama, T. Kobayashi, H. Conner, S. Abe, Q. Fang, F.Q. Wen, and S.I. Rennard Cigarette smoke stimulates MMP-1 production by human lung fibroblasts through the ERK1/2 pathway COPD 1 2004 13 23
57. B.A. Mercer, A.M. Wallace, C.E. Brinckerhoff, and J.M. D'Armiento Identification of a cigarette smoke-responsive region in the distal MMP-1 promoter Am J Respir Cell Mol Biol 40 2009 4 12
58. L. O'Rourke, and P.R. Shepherd Biphasic regulation of extracellular-signal-regulated protein kinase by leptin in macrophages: role in regulating STAT3 Ser727 phosphorylation and DNA binding Biochem J 364 2002 875 879
59. R.P. Dai, C.Q. Li, J.W. Zhang, F. Li, X.D. Shi, J.Y. Zhang, and X.F. Zhou Biphasic activation of extracellular signal-regulated kinase in anterior cingulate cortex distinctly regulates the development of pain-related anxiety and mechanical hypersensitivity in rats after incision Anesthesiology 115 2011 604 613
60. A.M. Preaux, M.P. D'Ortho, M.P. Bralet, Y. Laperche, and P. Mavier Apoptosis of human hepatic myofibroblasts promotes activation of matrix metalloproteinase-2 Hepatology 36 2002 615 622
61. E. Ispanovic, and T.L. Haas JNK and PI3K differentially regulate MMP-2 and MT1-MMP mRNA and protein in response to actin cytoskeleton reorganization in endothelial cells Am J Physiol Cell Physiol 291 2006 C579 C588
62. S.J. Tudhope, T.K. Finney-Hayward, A.G. Nicholson, R.J. Mayer, M.S. Barnette, P.J. Barnes, and L.E. Donnelly Different mitogen-activated protein kinase-dependent cytokine responses in cells of the monocyte lineage J Pharmacol Exp Ther 324 2008 306 312
63. M. Jin, J.M. Opalek, C.B. Marsh, and H.M. Wu Proteome comparison of alveolar macrophages with monocytes reveals distinct protein characteristics Am J Respir Cell Mol Biol 31 2004 322 329
64. S. Seshadri, M.D. Duncan, J.M. Hart, M.A. Gavrilin, and M.D. Wewers Pyrin levels in human monocytes and monocyte-derived macrophages regulate IL-1beta processing and release J Immunol 179 2007 1274 1281
65. A. Lehtonen, H. Ahlfors, V. Veckman, M. Miettinen, R. Lahesmaa, and I. Julkunen Gene expression profiling during differentiation of human monocytes to macrophages or dendritic cells J Leukoc Biol 82 2007 710 720
66. F.D. Kolodgie, J. Narula, A.P. Burke, N. Haider, A. Farb, Y. Hui-Liang, J. Smialek, and R. Virmani Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death Am J Pathol 157 2000 1259 1268
67. J.H. Park, S.M. Park, S.H. Park, K.H. Cho, and S.T. Lee Cleavage and functional loss of human apolipoprotein E by digestion of matrix metalloproteinase-14 Proteomics 8 2008 2926 2935
68. S. Fazio, V.R. Babaev, A.B. Murray, A.H. Hasty, K.J. Carter, L.A. Gleaves, J.B. Atkinson, and M.F. Linton Increased atherosclerosis in mice reconstituted with apolipoprotein E null macrophages Proc Natl Acad Sci USA 94 1997 4647 4652
69. K. Aupeix, B. Hugel, T. Martin, P. Bischoff, H. Lill, J.L. Pasquali, and J.M. Freyssinet The significance of shed membrane particles during programmed cell death in vitro, and in vivo, in HIV-1 infection J Clin Invest 99 1997 1546 1554
70. K. Lauber, S.G. Blumenthal, M. Waibel, and S. Wesselborg Clearance of apoptotic cells: getting rid of the corpses Mol Cell 14 2004 277 287