Aqueous humor perturbations in chronic smokers: a proteomic study.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
17 May 2024
17 May 2024
Historique:
received:
21
08
2023
accepted:
13
05
2024
medline:
18
5
2024
pubmed:
18
5
2024
entrez:
17
5
2024
Statut:
epublish
Résumé
The detrimental effects of smoking are multisystemic and its effects on the eye health are significant. Smoking is a strong risk factor for age-related nuclear cataract, age-related macular degeneration, glaucoma, delayed corneal epithelial healing and increased risk of cystoid macular edema in patients with intermediate uveitis among others. We aimed to characterize the aqueous humor (AH) proteome in chronic smokers to gain insight into its perturbations and to identify potential biomarkers for smoking-associated ocular pathologies. Compared to the control group, chronic smokers displayed 67 (37 upregulated, 30 downregulated) differentially expressed proteins (DEPs). Analysis of DEPs from the biological point of view revealed that they were proteins involved in complement activation, lymphocyte mediated immunity, innate immune response, cellular oxidant detoxification, bicarbonate transport and platelet degranulation. From the molecular function point of view, DEPs were involved in oxygen binding, oxygen carrier activity, hemoglobin binding, peptidase/endopeptidase/cysteine-type endopeptidase inhibitory activity. Several of the upregulated proteins were acute phase reactant proteins such as clusterin, alpha-2-HS-glycoprotein, fibrinogen, alpha-1-antitrypsin, C4b-binding protein and serum amyloid A-2. Further research should confirm if these proteins might serve as biomarkers or therapeutic target for smoking-associated ocular diseases.
Identifiants
pubmed: 38760463
doi: 10.1038/s41598-024-62039-6
pii: 10.1038/s41598-024-62039-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
11279Informations de copyright
© 2024. The Author(s).
Références
World Health Organization. WHO Report on the Global Tobacco Epidemic 2019: Offer Help to Quit Tobacco Use (World Health Organization, 2020).
World Health Organization. WHO Global Report: Mortality Attributable to Tobacco (World Health Organization, 2012).
Barnes, P. J. Chronic obstructive pulmonary disease. N. Engl. J. Med. 343, 269–280 (2000).
pubmed: 10911010
doi: 10.1056/NEJM200007273430407
Hecht, S. S. Tobacco smoke carcinogens and lung cancer. J. Natl. Cancer Inst. 91, 1194–1210 (1999).
pubmed: 10413421
doi: 10.1093/jnci/91.14.1194
Lakier, J. B. Smoking and cardiovascular disease. Am. J. Med. 93, 8S-12S (1992).
pubmed: 1497005
doi: 10.1016/0002-9343(92)90620-Q
Chang, S. A. Smoking and type 2 diabetes mellitus. Diabetes Metab. J. 36, 399 (2012).
pubmed: 23275932
pmcid: 3530709
doi: 10.4093/dmj.2012.36.6.399
Rink, M. et al. Smoking and bladder cancer: A systematic review of risk and outcomes. Eur. Urol. Focus 1, 17–27 (2015).
pubmed: 28723350
doi: 10.1016/j.euf.2014.11.001
Fernández, J. A. et al. Systemic inflammation in 222.841 healthy employed smokers and nonsmokers: White blood cell count and relationship to spirometry. Tob. Induced Dis. 10, 7 (2012).
doi: 10.1186/1617-9625-10-7
Green, M. S., Peled, I. & Najenson, T. Gender differences in platelet count and its association with cigarette smoking in a large cohort in Israel. J. Clin. Epidemiol. 45, 77–84 (1992).
pubmed: 1738015
doi: 10.1016/0895-4356(92)90191-O
Higuchi, T. et al. Current cigarette smoking is a reversible cause of elevated white blood cell count: Cross-sectional and longitudinal studies. Prev. Med. Rep. 4, 417–422 (2016).
pubmed: 27583199
pmcid: 4995538
doi: 10.1016/j.pmedr.2016.08.009
Malenica, M. et al. Effect of cigarette smoking on haematological parameters in healthy population. Med. Arch. 71, 132 (2017).
pubmed: 28790546
pmcid: 5511531
doi: 10.5455/medarh.2017.71.132-136
Peres, F. S. et al. Time from smoking cessation and inflammatory markers: New evidence from a cross-sectional analysis of ELSA-Brasil. Nicotine Tob. Res. 19, 852–858 (2017).
pubmed: 28164227
doi: 10.1093/ntr/ntx032
Roethig, H. J. et al. Short term effects of reduced exposure to cigarette smoke on white blood cells, platelets and red blood cells in adult cigarette smokers. Regul. Toxicol. Pharmacol. 57, 333–337 (2010).
pubmed: 20394790
doi: 10.1016/j.yrtph.2010.04.005
Lakshmi, S. A. Effect of intensity of cigarette smoking on haematological and lipid parameters. J. Clin. Diagn. Res. https://doi.org/10.7860/jcdr/2014/9545.4612 (2014).
doi: 10.7860/jcdr/2014/9545.4612
pubmed: 25653949
pmcid: 4316255
Kroll, M. E. et al. Alcohol drinking, tobacco smoking and subtypes of haematological malignancy in the UK million women study. Br. J. Cancer 107, 879–887 (2012).
pubmed: 22878373
pmcid: 3425977
doi: 10.1038/bjc.2012.333
Pedersen, K. M. et al. Smoking is associated with increased risk of myeloproliferative neoplasms: A general population-based cohort study. Cancer Med. 7, 5796–5802 (2018).
pubmed: 30318865
pmcid: 6246929
doi: 10.1002/cam4.1815
Wang, P., Liu, H., Jiang, T. & Yang, J. Cigarette smoking and the risk of adult myeloid disease: A meta-analysis. PLoS ONE 10, e0137300 (2015).
pubmed: 26340093
pmcid: 4560392
doi: 10.1371/journal.pone.0137300
Pryor, W. A., Arbour, N. C., Upham, B. & Church, D. F. The inhibitory effect of extracts of cigarette tar on electron transport of mitochondria and submitochondrial particles. Free Radic. Biol. Med. 12, 365–372 (1992).
pubmed: 1317324
doi: 10.1016/0891-5849(92)90085-U
Lyons, M. J., Gibson, J. F. & Ingram, D. J. E. Free-radicals produced in cigarette smoke. Nature 181, 1003–1004 (1958).
pubmed: 13541350
doi: 10.1038/1811003a0
Cosgrove, J. P., Borish, E. T., Church, D. F. & Pryor, W. A. The metal-mediated formation of hydroxyl radical by aqueous extracts of cigarette tar. Biochem. Biophys. Res. Commun. 132, 390–396 (1985).
pubmed: 2998360
doi: 10.1016/0006-291X(85)91034-4
Gillespie, M. N., Owasoyo, J. O., Kojima, S. & Jay, M. Enhanced chemotaxis and superoxide anion production by polymorphonuclear leukocytes from nicotine-treated and smoke-exposed rats. Toxicology 45, 45–52 (1987).
pubmed: 3037731
doi: 10.1016/0300-483X(87)90113-2
Jay, M., Kojima, S. & Gillespie, M. N. Nicotine potentiates superoxide anion generation by human neutrophils. Toxicol. Appl. Pharmacol. 86, 484–487 (1986).
pubmed: 3024359
doi: 10.1016/0041-008X(86)90376-5
Kalra, J., Chaudhary, A. K. & Prasad, K. Increased production of oxygen free radicals in cigarette smokers. Int. J. Exp. Pathol. 72, 1–7 (1991).
pubmed: 1888662
pmcid: 2002262
Morrow, J. D. et al. Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers—Smoking as a cause of oxidative damage. N. Engl. J. Med. 332, 1198–1203 (1995).
pubmed: 7700313
doi: 10.1056/NEJM199505043321804
Loft, S., Astrup, A., Buemann, B. & Poulsen, H. E. Oxidative DNA damage correlates with oxygen consumption in humans. FASEB J. 8, 534–537 (1994).
pubmed: 8181672
doi: 10.1096/fasebj.8.8.8181672
Asami, S. et al. Increase of a type of oxidative DNA damage, 8-hydroxyguanine, and its repair activity in human leukocytes by cigarette smoking. Cancer Res. 56, 2546–2549 (1996).
pubmed: 8653695
Prieme, H. Effect of smoking cessation on oxidative DNA modification estimated by 8-oxo-7,8-dihydro-2’-deoxyguanosine excretion. Carcinogenesis 19, 347–351 (1998).
pubmed: 9498287
doi: 10.1093/carcin/19.2.347
Piperakis, S. Effects of smoking and aging on oxidative DNA damage of human lymphocytes. Carcinogenesis 19, 695–698 (1998).
pubmed: 9600358
doi: 10.1093/carcin/19.4.695
Vineis, P. & Caporaso, N. Tobacco and cancer: Epidemiology and the laboratory. Environ. Health Perspect. 103, 156–160 (1995).
pubmed: 7737063
pmcid: 1518986
doi: 10.1289/ehp.95103156
Rojas, E., Valverde, M., Sordo, M. & Ostrosky-Wegman, P. DNA damage in exfoliated buccal cells of smokers assessed by the single cell gel electrophoresis assay. Mutat. Res. Genet. Toxicol. 370, 115–120 (1996).
doi: 10.1016/0165-1218(96)00062-6
Hsueh, Y.-J. et al. The pathomechanism, antioxidant biomarkers, and treatment of oxidative stress-related eye diseases. Int. J. Mol. Sci. 23, 1255 (2022).
pubmed: 35163178
pmcid: 8835903
doi: 10.3390/ijms23031255
Harding, J. J. & van Heyningen, R. Drugs, including alcohol, that act as risk factors for cataract, and possible protection against cataract by aspirin-like analgesics and cyclopenthiazide. Br. J. Ophthalmol. 72, 809–814 (1988).
pubmed: 3207655
pmcid: 1041596
doi: 10.1136/bjo.72.11.809
Myers, C. E. et al. Cigarette smoking and the natural history of age-related macular degeneration: The Beaver Dam Eye Study. Ophthalmology 121, 1949–1955 (2014).
pubmed: 24953792
doi: 10.1016/j.ophtha.2014.04.040
Pérez-de-Arcelus, M. et al. Smoking and incidence of glaucoma. Medicine 96, e5761 (2017).
pubmed: 28072720
pmcid: 5228680
doi: 10.1097/MD.0000000000005761
Thornton, J., Kelly, S. P., Harrison, R. A. & Edwards, R. Cigarette smoking and thyroid eye disease: A systematic review. Eye 21, 1135–1145 (2006).
pubmed: 16980921
doi: 10.1038/sj.eye.6702603
Grzybowski, A. & Nita, M. Smoking and eye pathologies. A systemic review. Part I. Anterior eye segment pathologies. Curr. Pharm. Des. 23, 629–638 (2017).
pubmed: 27897118
doi: 10.2174/1381612822666161129152041
Lin, P., Loh, A. R., Margolis, T. P. & Acharya, N. R. Cigarette smoking as a risk factor for uveitis. Ophthalmology 117, 585–590 (2010).
pubmed: 20036011
doi: 10.1016/j.ophtha.2009.08.011
Galor, A. et al. Adverse effects of smoking on patients with ocular inflammation. Br. J. Ophthalmol. 94, 848–853 (2010).
pubmed: 20606023
doi: 10.1136/bjo.2009.174466
Thorne, J. E. et al. Smoking as a risk factor for cystoid macular edema complicating intermediate uveitis. Am. J. Ophthalmol. 145, 841–846 (2008).
pubmed: 18321467
pmcid: 2574684
doi: 10.1016/j.ajo.2007.12.032
Bennett, K. L. et al. Proteomic analysis of human cataract aqueous humour: Comparison of one-dimensional gel LCMS with two-dimensional LCMS of unlabelled and iTRAQ®-labelled specimens. J. Proteom. 74, 151–166 (2011).
doi: 10.1016/j.jprot.2010.10.002
Pollreisz, A. et al. Quantitative proteomics of aqueous and vitreous fluid from patients with idiopathic epiretinal membranes. Exp. Eye Res. 108, 48–58 (2013).
pubmed: 23201028
doi: 10.1016/j.exer.2012.11.010
Yu, J., Peng, R., Chen, H., Cui, C. & Ba, J. Elucidation of the pathogenic mechanism of rhegmatogenous retinal detachment with proliferative vitreoretinopathy by proteomic analysis. Investig. Opthalmol. Vis. Sci. 53, 8146 (2012).
doi: 10.1167/iovs.12-10079
Nobi, M. et al. Proteomics of vitreous in neovascular age-related macular degeneration. Exp. Eye Res. 146, 107–117 (2016).
doi: 10.1016/j.exer.2016.01.001
Rinsky, B. et al. Analysis of the aqueous humor proteome in patients with age-related macular degeneration. Investig. Ophthalmol. Vis. Sci. 62, 18 (2021).
doi: 10.1167/iovs.62.10.18
Wang, H., Feng, L., Hu, J., Xie, C. & Wang, F. Differentiating vitreous proteomes in proliferative diabetic retinopathy using high-performance liquid chromatography coupled to tandem mass spectrometry. Exp. Eye Res. 108, 110–119 (2013).
pubmed: 23276812
doi: 10.1016/j.exer.2012.11.023
Futcher, B., Latter, G. I., Monardo, P., McLaughlin, C. S. & Garrels, J. I. A sampling of the yeast proteome. Mol. Cell. Biol. 19, 7357–7368 (1999).
pubmed: 10523624
pmcid: 84729
doi: 10.1128/MCB.19.11.7357
Gygi, S. P., Rochon, Y., Franza, B. R. & Aebersold, R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720–1730 (1999).
pubmed: 10022859
pmcid: 83965
doi: 10.1128/MCB.19.3.1720
Varshavsky, A. The N-end rule: Functions, mysteries, uses. Proc. Natl. Acad. Sci. 93, 12142–12149 (1996).
pubmed: 8901547
pmcid: 37957
doi: 10.1073/pnas.93.22.12142
Jomes, S. E. & Jomary, C. Clusterin. Int. J. Biochem. Cell Biol. 34, 427–431 (2002).
doi: 10.1016/S1357-2725(01)00155-8
Garden, G. A., Bothwell, M. & Rubel, E. W. Lack of correspondence between mRNA expression for a putative cell death molecule (SGP-2) and neuronal cell death in the central nervous system. J. Neurobiol. 22, 590–604 (1991).
pubmed: 1919566
doi: 10.1002/neu.480220605
Mackness, B., Hunt, R., Durrington, P. N. & Mackness, M. I. Increased immunolocalization of paraoxonase, clusterin, and apolipoprotein A-I in the human artery wall with the progression of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 17, 1233–1238 (1997).
pubmed: 9261251
doi: 10.1161/01.ATV.17.7.1233
Trougakos, I. P. et al. Serum levels of the senescence biomarker clusterin/apolipoprotein J increase significantly in diabetes type II and during development of coronary heart disease or at myocardial infarction. Exp. Gerontol. 37, 1175–1187 (2002).
pubmed: 12470829
doi: 10.1016/S0531-5565(02)00139-0
Antonelou, M. H., Kriebardis, A. G., Stamoulis, K. E., Trougakos, I. P. & Papassideri, I. S. Apolipoprotein J/clusterin is a novel structural component of human erythrocytes and a biomarker of cellular stress and senescence. PLoS ONE 6, e26032 (2011).
pubmed: 21998749
pmcid: 3188580
doi: 10.1371/journal.pone.0026032
Kim, T. W. et al. Proteomic analysis of the aqueous humor in age-related macular degeneration (AMD) patients. J. Proteome Res. 11, 4034–4043 (2012).
pubmed: 22702841
doi: 10.1021/pr300080s
Smith, W. et al. Risk factors for age-related macular degeneration: Pooled findings from three continents. Ophthalmology 108, 697–704 (2001).
pubmed: 11297486
doi: 10.1016/S0161-6420(00)00580-7
Mitchell, P. Smoking and the 5-year incidence of age-related maculopathy. Arch. Ophthalmol. 120, 1357 (2002).
pubmed: 12365915
doi: 10.1001/archopht.120.10.1357
Macular Photocoagulation Study Group. Recurrent choroidal neovascularization after argon laser photocoagulation for neovascular maculopathy. Arch. Ophthalmol. 104, 503–512 (1986).
doi: 10.1001/archopht.1986.01050160059012
Wang, L. et al. Abundant lipid and protein components of drusen. PLoS ONE 5, e10329 (2010).
pubmed: 20428236
pmcid: 2859054
doi: 10.1371/journal.pone.0010329
Sakaguchi, H. et al. Clusterin is present in drusen in age-related macular degeneration. Exp. Eye Res. 74, 547–549 (2002).
pubmed: 12076098
doi: 10.1006/exer.2002.1186
Yu, A. L., Birke, K., Burger, J. & Welge-Lussen, U. Biological effects of cigarette smoke in cultured human retinal pigment epithelial cells. PLoS ONE 7, e48501 (2012).
pubmed: 23155386
pmcid: 3498276
doi: 10.1371/journal.pone.0048501
Yanni, A. E., Agrogiannis, G., Gkekas, C. & Perrea, D. Clusterin/apolipoprotein J immunolocalization on carotid artery is affected by TNF-alpha, cigarette smoking and anti-platelet treatment. Lipids Health Dis. 13, 1 (2014).
doi: 10.1186/1476-511X-13-70
Carnevali, S. et al. Clusterin decreases oxidative stress in lung fibroblasts exposed to cigarette smoke. Am. J. Respir. Crit. Care Med. 174, 393–399 (2006).
pubmed: 16709934
doi: 10.1164/rccm.200512-1835OC
Tuut, M. Smoking, other risk factors and fibrinogen levels evidence of effect modification. Ann. Epidemiol. 11, 232–238 (2001).
pubmed: 11306341
doi: 10.1016/S1047-2797(00)00226-X
Hunter, K. A., Garlick, P. J., Broom, I., Anderson, S. E. & McNurlan, M. A. Effects of smoking and abstention from smoking on fibrinogen synthesis in humans. Clin. Sci. 100, 459 (2001).
doi: 10.1042/cs1000459
Csordas, A. & Bernhard, D. The biology behind the atherothrombotic effects of cigarette smoke. Nat. Rev. Cardiol. 10, 219–230 (2013).
pubmed: 23380975
doi: 10.1038/nrcardio.2013.8
Delgado, D. et al. Alterations in the coagulation system of active smokers from the Ludwigshafen risk and cardiovascular health (LURIC) study. Adv. Exp. Med. Biol. 832, 9–14 (2015).
pubmed: 25300683
doi: 10.1007/5584_2014_5
Green, D., Foiles, N., Chan, C., Schreiner, P. J. & Liu, K. Elevated fibrinogen levels and subsequent subclinical atherosclerosis: The CARDIA study. Atherosclerosis 202, 623–631 (2009).
pubmed: 18602107
doi: 10.1016/j.atherosclerosis.2008.05.039
Folsom, A. R. et al. Distributions of hemostatic variables in blacks and whites: Population reference values from the atherosclerosis risk in communities (ARIC) study. Ethn. Dis. 2, 35–46 (1992).
pubmed: 1458214
Heinrich, J., Balleisen, L., Schulte, H., Assmann, G. & van de Loo, J. Fibrinogen and factor VII in the prediction of coronary risk. Results from the PROCAM study in healthy men. Arterioscler. Thromb. J. Vasc. Biol. 14, 54–59 (1994).
doi: 10.1161/01.ATV.14.1.54
Stone, M. C. & Thorp, J. M. Plasma fibrinogen—A major coronary risk factor. J. R. Coll. Gen. Pract. 35, 565–569 (1985).
pubmed: 4093900
pmcid: 1961456
Muddathir, A. R. M., Abd Alla, M. I. & Khabour, O. F. Waterpipe smoking is associated with changes in fibrinogen, FVII, and FVIII levels. Acta Haematol. 140, 159–165 (2018).
pubmed: 30261515
doi: 10.1159/000492740
Csordas, A., Wick, G., Laufer, G. & Bernhard, D. An evaluation of the clinical evidence on the role of inflammation and oxidative stress in smoking-mediated cardiovascular disease. Biomark. Insights 3, S480 (2008).
doi: 10.4137/BMI.S480
Fusegawa, Y., Goto, S., Handa, S., Kawada, T. & Ando, Y. Platelet spontaneous aggregation in platelet-rich plasma is increased in habitual smokers. Thromb. Res. 93, 271–278 (1999).
pubmed: 10093968
doi: 10.1016/S0049-3848(98)00184-4
Tapson, V. F. The role of smoking in coagulation and thromboembolism in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 2, 71–77 (2005).
pubmed: 16113472
doi: 10.1513/pats.200407-038MS
Ermert, D. & Blom, A. M. C4b-binding protein: The good, the bad and the deadly. Novel functions of an old friend. Immunol. Lett. 169, 82–92 (2016).
pubmed: 26658464
doi: 10.1016/j.imlet.2015.11.014
Scott, B. D., Esmon, C. T. & Comp, P. C. The natural anticoagulant protein S is decreased in male smokers. Am. Heart J. 122, 76–80 (1991).
pubmed: 1829572
doi: 10.1016/0002-8703(91)90761-6
Suankratay, C., Mold, C., Zhang, Y., Lint, T. F. & Gewurz, H. Mechanism of complement-dependent haemolysis via the lectin pathway: Role of the complement regulatory proteins. Clin. Exp. Immunol. 117, 442–448 (1999).
pubmed: 10469045
pmcid: 1905373
doi: 10.1046/j.1365-2249.1999.00998.x
Fujita, T., Gigli, I. & Nussenzweig, V. Human C4-binding protein. II. Role in proteolysis of C4b by C3b-inactivator. J. Exp. Med. 148, 1044–1051 (1978).
pubmed: 702059
doi: 10.1084/jem.148.4.1044
Scharfstein, J., Ferreira, A., Gigli, I. & Nussenzweig, V. Human C4-binding protein. I. Isolation and characterization. J. Exp. Med. 148, 207–222 (1978).
pubmed: 670886
pmcid: 2184907
doi: 10.1084/jem.148.1.207
Nagasawa, S., Ichihara, C. & Stroud, R. M. Cleavage of C4b by C3b inactivator: Production of a nicked form of C4b, C4b’, as an intermediate cleavage product of C4b by C3b inactivator. J. Immunol. 125, 578–582 (1980).
pubmed: 7391570
doi: 10.4049/jimmunol.125.2.578
Daha, M. R. & van Es, L. A. Relative resistance of the F-42-stabilized classical pathway C3 convertase to inactivation by C4-binding protein. J. Immunol. 125, 2051–2054 (1980).
pubmed: 6903579
doi: 10.4049/jimmunol.125.5.2051
Gigli, I., Fujita, T. & Nussenzweig, V. Modulation of the classical pathway C3 convertase by plasma proteins C4 binding protein and C3b inactivator. Proc. Natl. Acad. Sci. 76, 6596–6600 (1979).
pubmed: 293746
pmcid: 411913
doi: 10.1073/pnas.76.12.6596
Sjöholm, K. et al. A microarray search for genes predominantly expressed in human omental adipocytes: Adipose tissue as a major production site of serum amyloid A. J. Clin. Endocrinol. Metab. 90, 2233–2239 (2005).
pubmed: 15623807
doi: 10.1210/jc.2004-1830
Urieli-Shoval, S., Cohen, P., Eisenberg, S. & Matzner, Y. Widespread expression of serum amyloid A in histologically normal human tissues: Predominant localization to the epithelium. J. Histochem. Cytochem. 46, 1377–1384 (1998).
pubmed: 9815279
doi: 10.1177/002215549804601206
Elias, D., Navarro, S., España, F., Griffin, J. & Deguchi, H. Elevated serum amyloid A is associated with venous thromboembolism. Thromb. Haemost. 109, 358–359 (2013).
pubmed: 23255027
doi: 10.1160/TH12-10-0722
Song, C. et al. Serum amyloid A may potentiate prothrombotic and proinflammatory events in acute coronary syndromes. Atherosclerosis 202, 596–604 (2009).
pubmed: 18571179
doi: 10.1016/j.atherosclerosis.2008.04.049
Page, M. J. et al. Serum amyloid A binds to fibrin(ogen), promoting fibrin amyloid formation. Sci. Rep. 9, 3102 (2019).
pubmed: 30816210
pmcid: 6395759
doi: 10.1038/s41598-019-39056-x
Al-Sieni, A. I., Al-Alawy, A. I., Al-Shehri, Z. S. & Al-Abbasi, F. A. Serum amyloid-A protein and serum rheumatoid factor as serological surrogate markers for smoking risk factor in Saudi population. Pak. J. Phram. Sci. 26, 239–243 (2013).
Wilson, P. G. et al. Serum amyloid A is an exchangeable apolipoprotein. Arterioscler. Thromb. Vasc. Biol. 38, 1890–1900 (2018).
pubmed: 29976766
pmcid: 6202200
doi: 10.1161/ATVBAHA.118.310979
Kotani, K., Satoh, N., Yamada, T. & Gugliucci, A. The potential of serum amyloid A—LDL as a novel biomarker for cardiovascular disease risk. Clin. Lipidol. 5, 489–495 (2010).
doi: 10.2217/clp.10.42
Kotani, K. et al. Serum amyloid a low-density lipoprotein levels and smoking status in obese Japanese patients. J. Int. Med. Res. 39, 1917–1922 (2011).
pubmed: 22117994
doi: 10.1177/147323001103900536
Huber, R. & Carrell, R. W. Implications of the three-dimensional structure of alpha.1-antitrypsin for structure and function of serpins. Biochemistry 28, 8951–8966 (1989).
pubmed: 2690952
doi: 10.1021/bi00449a001
Perlmutter, D. H. Alpha-1-antitrypsin deficiency: Diagnosis and treatment. Clin. Liver Dis. 8, 839–859 (2004).
pubmed: 15464658
doi: 10.1016/j.cld.2004.06.001
Voulgari, F. et al. Serum levels of acute phase and cardiac proteins after myocardial infarction, surgery, and infection. Heart 48, 352–356 (1982).
doi: 10.1136/hrt.48.4.352
Correale, M., Totaro, A., Abruzzese, S., Di Biase, M. & Daniele Brunetti, N. Acute phase proteins in acute coronary syndrome: An up-to-date. Cardiovasc. Hematol. Agents Med. Chem. 10, 352–361 (2012).
pubmed: 22721440
doi: 10.2174/187152512803530298
Wolf, G. T., Chretien, P. B., Weiss, J. F., Edwards, B. K. & Spiegel, H. E. Effects of smoking and age on serum levels of immune reactive proteins. Otolaryngol. Head Neck Surg. 90, 319–326 (1982).
pubmed: 6813806
Bergin, D. A., Hurley, K., McElvaney, N. G. & Reeves, E. P. Alpha-1 antitrypsin: A potent anti-inflammatory and potential novel therapeutic agent. Arch. Immunol. Therap. Exp. 60, 81–97 (2012).
doi: 10.1007/s00005-012-0162-5
O’Dwyer, C. A., McElvaney, N. G. & Reeves, E. P. Alpha-1 antitrypsin inhibits leukotriene B4 induced neutrophil signalling through a mechanism that involves direct complexation of the two molecules. In B39. Neutrophils: New Insights into Their Activation and Contribution to Lung Injury (eds O’Dwyer, C. A. et al.) (American Thoracic Society, 2013).
Bergin, D. A. et al. The circulating proteinase inhibitor α-1 antitrypsin regulates neutrophil degranulation and autoimmunity. Sci. Transl. Med. 6, 217 (2014).
doi: 10.1126/scitranslmed.3007116
Griese, M. et al. Alpha1-antitrypsin inhalation reduces airway inflammation in cystic fibrosis patients. Eur. Respir. J. 29, 240–250 (2007).
pubmed: 17050563
doi: 10.1183/09031936.00047306
Kalis, M., Kumar, R., Janciauskiene, S., Salehi, A. & Cilio, C. M. α 1-antitrypsin enhances insulin secretion and prevents cytokine-mediated apoptosis in pancreatic β-cells. Islets 2, 185–189 (2010).
pubmed: 21099312
doi: 10.4161/isl.2.3.11654
Bergin, D. A. et al. α-1 antitrypsin regulates human neutrophil chemotaxis induced by soluble immune complexes and IL-8. J. Clin. Investig. 120, 4236–4250 (2010).
pubmed: 21060150
pmcid: 2993580
doi: 10.1172/JCI41196
Al-Omari, M. et al. Acute-phase protein α1-antitrypsin inhibits neutrophil calpain I and induces random migration. Mol. Med. 17, 865–874 (2011).
pubmed: 21494752
pmcid: 3188872
doi: 10.2119/molmed.2011.00089
Zhang, B. et al. Alpha1-antitrypsin protects beta-cells from apoptosis. Diabetes 56, 1316–1323 (2017).
doi: 10.2337/db06-1273
Perlmutter, D. H., May, L. T. & Sehgal, P. B. Interferon beta 2/interleukin 6 modulates synthesis of alpha 1-antitrypsin in human mononuclear phagocytes and in human hepatoma cells. J. Clin. Investig. 84, 138–144 (1989).
pubmed: 2472425
pmcid: 303963
doi: 10.1172/JCI114133
Perlmutter, D. H. et al. Induction of the stress response in alpha 1-antitrypsin deficiency. Trans. Assoc. Am. Phys. 101, 33–41 (1988).
pubmed: 2855901
Perlmutter, D. H., Travis, J. & Punsal, P. I. Elastase regulates the synthesis of its inhibitor, alpha 1-proteinase inhibitor, and exaggerates the defect in homozygous PiZZ alpha 1 PI deficiency. J. Clin. Investig. 81, 1774–1780 (1988).
pubmed: 3260245
pmcid: 442624
doi: 10.1172/JCI113519
Knoell, D. L., Ralston, D. R., Coulter, K. R. & Wewers, M. D. Alpha 1-antitrypsin and protease complexation is induced by lipopolysaccharide, interleukin-1 β, and tumor necrosis factor-α in monocytes. Am. J. Respir. Crit. Care Med. 157, 246–255 (1998).
pubmed: 9445306
doi: 10.1164/ajrccm.157.1.9702033
Boutten, A. et al. Oncostatin M is a potent stimulator of α1-antitrypsin secretion in lung epithelial cells: Modulation by transforming growth factor-β and interferon-γ. Am. J. Respir. Cell Mol. Biol. 18, 511–520 (1998).
pubmed: 9533938
doi: 10.1165/ajrcmb.18.4.2772
Ix, J. H. et al. Association between human fetuin-A and the metabolic syndrome. Circulation 113, 1760–1767 (2006).
pubmed: 16567568
pmcid: 2776669
doi: 10.1161/CIRCULATIONAHA.105.588723
Dziegielewska, K. M., Møllgård, K., Reynolds, M. L. & Saunders, N. R. A fetuin-related glycoprotein (2HS) in human embryonic and fetal development. Cell Tissue Res. 248, 33–41 (1987).
pubmed: 3552239
doi: 10.1007/BF01239959
Denecke, B. et al. Tissue distribution and activity testing suggest a similar but not identical function of fetuin-B and fetuin-A. Biochem. J. 376, 135–145 (2003).
pubmed: 12943536
pmcid: 1223762
doi: 10.1042/bj20030676
Wang, H. & Sama, E. A. Anti-inflammatory role of fetuin-A in injury and infection. Curr. Mol. Med. 12, 625–633 (2012).
pubmed: 22292896
pmcid: 3349766
doi: 10.2174/156652412800620039
Li, W. et al. A hepatic protein, fetuin-A, occupies a protective role in lethal systemic inflammation. PLoS ONE 6, e16945 (2011).
pubmed: 21347455
pmcid: 3035675
doi: 10.1371/journal.pone.0016945
Chang, W. C., Lee, C. H., Chiou, S. H., Liao, C. C. & Cheng, C. W. Proteomic analysis of aqueous humor proteins in association with cataract risks: Diabetes and smoking. J. Clin. Med. 10, 5731 (2021).
pubmed: 34945026
pmcid: 8703435
doi: 10.3390/jcm10245731
Mackiewicz, A. Acute phase proteins and transformed cells. Int. Rev. Cytol. 170, 225–300 (1997).
pubmed: 9002238
doi: 10.1016/S0074-7696(08)61623-X
Thompson, D. & Bird, H. A. Acute phase response. In Oxford Textbook of Rheumatology 3rd edn (eds Isenberg, D. A. et al.) 473–478 (Oxford University Press, 2004).
Kushner, I., Ganapathi, M. & Schultz, D. The acute phase response is mediated by heterogeneous mechanisms. Ann. N. Y. Acad. Sci. 557, 10–29 (1989).
doi: 10.1111/j.1749-6632.1989.tb23996.x
Yanbaeva, D. G., Dentener, M. A., Creutzberg, E. C., Wesseling, G. & Wouters, E. F. M. Systemic effects of smoking. Chest 131, 1557–1566 (2007).
pubmed: 17494805
doi: 10.1378/chest.06-2179
Arnson, Y., Shoenfeld, Y. & Amital, H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J. Autoimmunity 34, J258–J265 (2010).
doi: 10.1016/j.jaut.2009.12.003
Wannamethee, S. G. et al. Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. Eur. Heart J. 26, 1765–1773 (2005).
pubmed: 15817606
doi: 10.1093/eurheartj/ehi183
Petrescu, F., Voican, C. S. & Silosi, I. Tumor necrosis factor-α serum levels in healthy smokers and nonsmokers. Int. J. Chronic Obstruct. Pulm. Dis. 2010, 217–222 (2010).
Barbieri, S. S. et al. Cytokines present in smokers’ serum interact with smoke components to enhance endothelial dysfunction. Cardiovasc. Res. 90, 475–483 (2011).
pubmed: 21285293
doi: 10.1093/cvr/cvr032
Nordenberg, D. et al. The effect of cigarette smoking on hemoglobin levels and anemia screening. J. Am. Med. Assoc. 264, 1556 (1990).
doi: 10.1001/jama.1990.03450120068031
Brody, J. S. & Coburn, R. F. Carbon monoxide-induced arterial hypoxemia. Science 164, 1297–1298 (1969).
pubmed: 5770624
doi: 10.1126/science.164.3885.1297
Tyagi, S., Salier, J.-P. & Lal, S. K. The liver-specific human α1-microglobulin/bikunin precursor (AMBP) is capable of self-association. Arch. Biochem. Biophys. 399, 66–72 (2002).
pubmed: 11883904
doi: 10.1006/abbi.2001.2745
Olsson, M. G. et al. Pathological conditions involving extracellular hemoglobin: Molecular mechanisms, clinical significance, and novel therapeutic opportunities for α1-microglobulin. Antioxid. Redox Signal. 17, 813–846 (2012).
pubmed: 22324321
doi: 10.1089/ars.2011.4282
Brady, J. P. et al. Targeted disruption of the mouse αA-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein αB-crystallin. Proc. Natl. Acad. Sci. 94, 884–889 (1997).
pubmed: 9023351
pmcid: 19608
doi: 10.1073/pnas.94.3.884
Zhang, J. et al. Targeted knockout of the mouse βB2-crystallin gene (Crybb2) induces age-related cataract. Investig. Ophthalmol. Vis. Sci. 49, 5476 (2008).
doi: 10.1167/iovs.08-2179