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Published in: Respiratory Research 1/2019

Open Access 01-12-2019 | Pulmonary Emphysema | Research

Loss of skin elasticity is associated with pulmonary emphysema, biomarkers of inflammation, and matrix metalloproteinase activity in smokers

Authors: Michael E. O’Brien, Divay Chandra, Robert C. Wilson, Chad M. Karoleski, Carl R. Fuhrman, Joseph K. Leader, Jiantao Pu, Yingze Zhang, Alison Morris, Seyed Nouraie, Jessica Bon, Zsolt Urban, Frank C. Sciurba

Published in: Respiratory Research | Issue 1/2019

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Abstract

Background

Elastin breakdown and the resultant loss of lung elastic recoil is a hallmark of pulmonary emphysema in susceptible individuals as a consequence of tobacco smoke exposure. Systemic alterations to the synthesis and degradation of elastin may be important to our understanding of disease phenotypes in chronic obstructive pulmonary disease. We investigated the association of skin elasticity with pulmonary emphysema, obstructive lung disease, and blood biomarkers of inflammation and tissue protease activity in tobacco-exposed individuals.

Methods

Two hundred and thirty-six Caucasian individuals were recruited into a sub-study of the University of Pittsburgh Specialized Center for Clinically Orientated Research in chronic obstructive pulmonary disease, a prospective cohort study of current and former smokers. The skin viscoelastic modulus (VE), a determinant of skin elasticity, was recorded from the volar forearm and facial wrinkling severity was determined using the Daniell scoring system.

Results

In a multiple regression analysis, reduced VE was significantly associated with cross-sectional measurement of airflow obstruction (FEV1/FVC) and emphysema quantified from computed tomography (CT) images, β = 0.26, p = 0.001 and β = 0.24, p = 0.001 respectively. In emphysema-susceptible individuals, elasticity-determined skin age was increased (median 4.6 years) compared to the chronological age of subjects without emphysema. Plasma biomarkers of inflammation (TNFR1, TNFR2, CRP, PTX3, and SAA) and matrix metalloproteinase activity (MMP1, TIMP1, TIMP2, and TIMP4) were inversely associated with skin elasticity.

Conclusions

We report that an objective non-invasive determinant of skin elasticity is independently associated with measures of lung function, pulmonary emphysema, and biomarkers of inflammation and tissue proteolysis in tobacco-exposed individuals. Loss of skin elasticity is a novel observation that may link the common pathological processes that drive tissue elastolysis in the extracellular matrix of the skin and lung in emphysema-susceptible individuals.
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Literature
1.
go back to reference Eisner MD, Anthonisen N, Coultas D, Kuenzli N, Perez-Padilla R, Postma D, et al. An official American Thoracic Society public policy statement: Novel risk factors and the global burden of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010 Sep 1;182(5):693–718.PubMedCrossRef Eisner MD, Anthonisen N, Coultas D, Kuenzli N, Perez-Padilla R, Postma D, et al. An official American Thoracic Society public policy statement: Novel risk factors and the global burden of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2010 Sep 1;182(5):693–718.PubMedCrossRef
2.
go back to reference Bon J, Fuhrman CR, Weissfeld JL, Duncan SR, Branch RA, Chang C-CH, et al. Radiographic emphysema predicts low bone mineral density in a tobacco-exposed cohort. Am J Respir Crit Care Med. 2011 Apr 1;183(7):885–90.PubMedCrossRef Bon J, Fuhrman CR, Weissfeld JL, Duncan SR, Branch RA, Chang C-CH, et al. Radiographic emphysema predicts low bone mineral density in a tobacco-exposed cohort. Am J Respir Crit Care Med. 2011 Apr 1;183(7):885–90.PubMedCrossRef
3.
go back to reference McAllister DA, Maclay JD, Mills NL, Mair G, Miller J, Anderson D, et al. Arterial stiffness is independently associated with emphysema severity in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007;176(12):1208–14.PubMedPubMedCentralCrossRef McAllister DA, Maclay JD, Mills NL, Mair G, Miller J, Anderson D, et al. Arterial stiffness is independently associated with emphysema severity in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007;176(12):1208–14.PubMedPubMedCentralCrossRef
4.
go back to reference Watz H, Waschki B, Kirsten A, Müller K-C, Kretschmar G, Meyer T, et al. The metabolic syndrome in patients with chronic bronchitis and COPD: frequency and associated consequences for systemic inflammation and physical inactivity. Chest. 2009;136(4):1039–46.PubMedCrossRef Watz H, Waschki B, Kirsten A, Müller K-C, Kretschmar G, Meyer T, et al. The metabolic syndrome in patients with chronic bronchitis and COPD: frequency and associated consequences for systemic inflammation and physical inactivity. Chest. 2009;136(4):1039–46.PubMedCrossRef
5.
go back to reference Frei A, Muggensturm P, Putcha N, Siebeling L, Zoller M, Boyd CM, et al. Five comorbidities reflected the health status in patients with chronic obstructive pulmonary disease: the newly developed COMCOLD index. J Clin Epidemiol. 2014;67(8):904–11.PubMedCrossRef Frei A, Muggensturm P, Putcha N, Siebeling L, Zoller M, Boyd CM, et al. Five comorbidities reflected the health status in patients with chronic obstructive pulmonary disease: the newly developed COMCOLD index. J Clin Epidemiol. 2014;67(8):904–11.PubMedCrossRef
6.
go back to reference Agusti A, Sobradillo P, Celli B. Addressing the complexity of chronic obstructive pulmonary disease: from phenotypes and biomarkers to scale-free networks, systems biology, and P4 medicine. Am J Respir Crit Care Med. 2011;183(9):1129–37.PubMedCrossRef Agusti A, Sobradillo P, Celli B. Addressing the complexity of chronic obstructive pulmonary disease: from phenotypes and biomarkers to scale-free networks, systems biology, and P4 medicine. Am J Respir Crit Care Med. 2011;183(9):1129–37.PubMedCrossRef
7.
go back to reference Bon J, Kahloon R, Zhang Y, Xue J, Fuhrman CR, Tan J, et al. Autoreactivity to glucose regulated protein 78 links emphysema and osteoporosis in smokers. PLoS One. 2014;9(9):e105066.PubMedPubMedCentralCrossRef Bon J, Kahloon R, Zhang Y, Xue J, Fuhrman CR, Tan J, et al. Autoreactivity to glucose regulated protein 78 links emphysema and osteoporosis in smokers. PLoS One. 2014;9(9):e105066.PubMedPubMedCentralCrossRef
8.
go back to reference Brusselle GG, Joos GF, Bracke KR. New insights into the immunology of chronic obstructive pulmonary disease. Lancet. 2011;378(9795):1015–26.CrossRef Brusselle GG, Joos GF, Bracke KR. New insights into the immunology of chronic obstructive pulmonary disease. Lancet. 2011;378(9795):1015–26.CrossRef
9.
go back to reference Martinez FJ, Donohue JF, Rennard SI. The future of chronic obstructive pulmonary disease treatment--difficulties of and barriers to drug development. Lancet. 2011;378(9795):1027–37.PubMedCrossRef Martinez FJ, Donohue JF, Rennard SI. The future of chronic obstructive pulmonary disease treatment--difficulties of and barriers to drug development. Lancet. 2011;378(9795):1027–37.PubMedCrossRef
10.
go back to reference Viegi G, Pistelli F, Sherrill DL, Maio S, Baldacci S, Carrozzi L. Definition, epidemiology and natural history of COPD. Eur Respir J. 2007;30(5):993–1013.PubMedCrossRef Viegi G, Pistelli F, Sherrill DL, Maio S, Baldacci S, Carrozzi L. Definition, epidemiology and natural history of COPD. Eur Respir J. 2007;30(5):993–1013.PubMedCrossRef
11.
go back to reference Han MK, Agusti A, Calverley PM, Celli BR, Criner G, Curtis JL, et al. Chronic obstructive pulmonary disease phenotypes: the future of COPD. Am J Respir Crit Care Med. 2010;182(5):598–604.PubMedCrossRef Han MK, Agusti A, Calverley PM, Celli BR, Criner G, Curtis JL, et al. Chronic obstructive pulmonary disease phenotypes: the future of COPD. Am J Respir Crit Care Med. 2010;182(5):598–604.PubMedCrossRef
12.
go back to reference Smith BS, Williamson N, McConkey B. Dermal connective tissue in patients with chronic obstructive airways disease. Lancet. 1967 Feb 18;1(7486):341–3.PubMedCrossRef Smith BS, Williamson N, McConkey B. Dermal connective tissue in patients with chronic obstructive airways disease. Lancet. 1967 Feb 18;1(7486):341–3.PubMedCrossRef
13.
go back to reference Patel BD, Loo WJ, Tasker AD, Screaton NJ, Burrows NP, Silverman EK, et al. Smoking related COPD and facial wrinkling: is there a common susceptibility? Thorax. 2006;61(7):568–71.PubMedPubMedCentralCrossRef Patel BD, Loo WJ, Tasker AD, Screaton NJ, Burrows NP, Silverman EK, et al. Smoking related COPD and facial wrinkling: is there a common susceptibility? Thorax. 2006;61(7):568–71.PubMedPubMedCentralCrossRef
14.
go back to reference Imokawa G, Ishida K. Biological mechanisms underlying the ultraviolet radiation-induced formation of skin wrinkling and sagging I: reduced skin elasticity, highly associated with enhanced dermal elastase activity, triggers wrinkling and sagging. Int J Mol Sci. 2015;16(4):7753–75.PubMedPubMedCentralCrossRef Imokawa G, Ishida K. Biological mechanisms underlying the ultraviolet radiation-induced formation of skin wrinkling and sagging I: reduced skin elasticity, highly associated with enhanced dermal elastase activity, triggers wrinkling and sagging. Int J Mol Sci. 2015;16(4):7753–75.PubMedPubMedCentralCrossRef
15.
go back to reference Just M, Ribera M, Monsó E, Lorenzo JC, Ferrándiz C. Effect of smoking on skin elastic fibres: morphometric and immunohistochemical analysis. Br J Dermatol. 2007;156(1):85–91.PubMedCrossRef Just M, Ribera M, Monsó E, Lorenzo JC, Ferrándiz C. Effect of smoking on skin elastic fibres: morphometric and immunohistochemical analysis. Br J Dermatol. 2007;156(1):85–91.PubMedCrossRef
16.
go back to reference Kadunce DP, Burr R, Gress R, Kanner R, Lyon JL, Zone JJ. Cigarette smoking: risk factor for premature facial wrinkling. Ann Intern Med. 1991;114(10):840–4.PubMedCrossRef Kadunce DP, Burr R, Gress R, Kanner R, Lyon JL, Zone JJ. Cigarette smoking: risk factor for premature facial wrinkling. Ann Intern Med. 1991;114(10):840–4.PubMedCrossRef
17.
go back to reference Ernster VL, Grady D, Miike R, Black D, Selby J, Kerlikowske K. Facial wrinkling in men and women, by smoking status. Am J Public Health. 1995;85(1):78–82.PubMedPubMedCentralCrossRef Ernster VL, Grady D, Miike R, Black D, Selby J, Kerlikowske K. Facial wrinkling in men and women, by smoking status. Am J Public Health. 1995;85(1):78–82.PubMedPubMedCentralCrossRef
18.
go back to reference Aizen E, Gilhar A. Smoking effect on skin wrinkling in the aged population. Int J Dermatol. 2001;40(7):431–3.PubMedCrossRef Aizen E, Gilhar A. Smoking effect on skin wrinkling in the aged population. Int J Dermatol. 2001;40(7):431–3.PubMedCrossRef
19.
go back to reference Maclay JD, McAllister DA, Rabinovich R, Haq I, Maxwell S, Hartland S, et al. Systemic elastin degradation in chronic obstructive pulmonary disease. Thorax BMJ Publishing Group Ltd. 2012;67(7):606–12. Maclay JD, McAllister DA, Rabinovich R, Haq I, Maxwell S, Hartland S, et al. Systemic elastin degradation in chronic obstructive pulmonary disease. Thorax BMJ Publishing Group Ltd. 2012;67(7):606–12.
20.
go back to reference Kozel BA, Su C-T, Danback JR, Minster RL, Madan-Khetarpal S, McConnell JS, et al. Biomechanical properties of the skin in cutis laxa. J Investig Dermatol. 2014;134(11):2836–8.PubMedCrossRef Kozel BA, Su C-T, Danback JR, Minster RL, Madan-Khetarpal S, McConnell JS, et al. Biomechanical properties of the skin in cutis laxa. J Investig Dermatol. 2014;134(11):2836–8.PubMedCrossRef
21.
go back to reference Chandra D, Gupta A, Strollo PJ, Fuhrman CR, Leader JK, Bon J, et al. Airflow limitation and endothelial dysfunction. Unrelated and independent predictors of atherosclerosis. Am J Respir Crit Care Med. 2016 Jul 1;194(1):38–47.PubMedPubMedCentralCrossRef Chandra D, Gupta A, Strollo PJ, Fuhrman CR, Leader JK, Bon J, et al. Airflow limitation and endothelial dysfunction. Unrelated and independent predictors of atherosclerosis. Am J Respir Crit Care Med. 2016 Jul 1;194(1):38–47.PubMedPubMedCentralCrossRef
22.
go back to reference Urban Z, Davis EC. Cutis laxa: intersection of elastic fiber biogenesis, TGFβ signaling, the secretory pathway and metabolism. Matrix Biol. 2014;33:16–22.PubMedCrossRef Urban Z, Davis EC. Cutis laxa: intersection of elastic fiber biogenesis, TGFβ signaling, the secretory pathway and metabolism. Matrix Biol. 2014;33:16–22.PubMedCrossRef
23.
go back to reference Daniell HW. Smoker’s wrinkles. A study in the epidemiology of “crow’s feet”. Ann Intern Med. 1971;75(6):873–80.PubMedCrossRef Daniell HW. Smoker’s wrinkles. A study in the epidemiology of “crow’s feet”. Ann Intern Med. 1971;75(6):873–80.PubMedCrossRef
24.
go back to reference Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Vol. 26, The European respiratory journal : official journal of the European Society for Clinical Respiratory Physiology. 2005. pp. 319–38.PubMedCrossRef Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Vol. 26, The European respiratory journal : official journal of the European Society for Clinical Respiratory Physiology. 2005. pp. 319–38.PubMedCrossRef
25.
go back to reference Hankinson JL, Odencrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med. 1999;159(1):179–87.PubMedCrossRef Hankinson JL, Odencrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med. 1999;159(1):179–87.PubMedCrossRef
26.
go back to reference Wanger J, Clausen JL, Coates A, Pedersen OF, Brusasco V, Burgos F, et al. Standardisation of the measurement of lung volumes. Eur Respir J. 2005;26(3):511–22.PubMedCrossRef Wanger J, Clausen JL, Coates A, Pedersen OF, Brusasco V, Burgos F, et al. Standardisation of the measurement of lung volumes. Eur Respir J. 2005;26(3):511–22.PubMedCrossRef
27.
go back to reference Wilson DO, Weissfeld JL, Balkan A, Schragin JG, Fuhrman CR, Fisher SN, et al. Association of radiographic emphysema and airflow obstruction with lung cancer. Am J Respir Crit Care Med. 2008;178(7):738–44.PubMedPubMedCentralCrossRef Wilson DO, Weissfeld JL, Balkan A, Schragin JG, Fuhrman CR, Fisher SN, et al. Association of radiographic emphysema and airflow obstruction with lung cancer. Am J Respir Crit Care Med. 2008;178(7):738–44.PubMedPubMedCentralCrossRef
28.
go back to reference Kennedy C, Bastiaens MT, Bajdik CD, Willemze R, Westendorp RGJ, Bouwes Bavinck JN, et al. Effect of smoking and sun on the aging skin. J Invest Dermatol. 2003;120(4):548–54.PubMedCrossRef Kennedy C, Bastiaens MT, Bajdik CD, Willemze R, Westendorp RGJ, Bouwes Bavinck JN, et al. Effect of smoking and sun on the aging skin. J Invest Dermatol. 2003;120(4):548–54.PubMedCrossRef
29.
go back to reference Pedersen L, Hansen B, Jemec GBE. Mechanical properties of the skin: a comparison between two suction cup methods. Skin Res Technol. 2003;9(2):111–5.PubMedCrossRef Pedersen L, Hansen B, Jemec GBE. Mechanical properties of the skin: a comparison between two suction cup methods. Skin Res Technol. 2003;9(2):111–5.PubMedCrossRef
30.
go back to reference Grove G, Damia J, Grove M, Zerweck C. Suction Chamber Method for Measurement of Skin Mechanics. In: Handbook of Non-Invasive Methods and the Skin, Second Edition. CRC Press; 2013. pp. 593–9. (The DermaLab). Grove G, Damia J, Grove M, Zerweck C. Suction Chamber Method for Measurement of Skin Mechanics. In: Handbook of Non-Invasive Methods and the Skin, Second Edition. CRC Press; 2013. pp. 593–9. (The DermaLab).
31.
go back to reference Anthonissen M, Daly D, Fieuws S, Massagé P, Van Brussel M, Vranckx J, et al. Measurement of elasticity and transepidermal water loss rate of burn scars with the Dermalab®. Burns. 2013;39(3):420–8.PubMedCrossRef Anthonissen M, Daly D, Fieuws S, Massagé P, Van Brussel M, Vranckx J, et al. Measurement of elasticity and transepidermal water loss rate of burn scars with the Dermalab®. Burns. 2013;39(3):420–8.PubMedCrossRef
32.
go back to reference Gankande TU, Duke JM, Danielsen PL, DeJong HM, Wood FM, Wallace HJ. Reliability of scar assessments performed with an integrated skin testing device - the DermaLab combo(®). Burns. 2014;40(8):1521–9.PubMedCrossRef Gankande TU, Duke JM, Danielsen PL, DeJong HM, Wood FM, Wallace HJ. Reliability of scar assessments performed with an integrated skin testing device - the DermaLab combo(®). Burns. 2014;40(8):1521–9.PubMedCrossRef
33.
go back to reference Francès C, Boisnic S, Hartmann DJ, Dautzenberg B, Branchet MC, Charpentier YL, et al. Changes in the elastic tissue of the non-sun-exposed skin of cigarette smokers. Br J Dermatol. 1991;125(1):43–7.PubMedCrossRef Francès C, Boisnic S, Hartmann DJ, Dautzenberg B, Branchet MC, Charpentier YL, et al. Changes in the elastic tissue of the non-sun-exposed skin of cigarette smokers. Br J Dermatol. 1991;125(1):43–7.PubMedCrossRef
34.
go back to reference O'Donnell DE, Revill SM, Webb KA. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;164(5):770–7.PubMedCrossRef O'Donnell DE, Revill SM, Webb KA. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;164(5):770–7.PubMedCrossRef
35.
go back to reference Houghton AM, Quintero PA, Perkins DL, Kobayashi DK, Kelley DG, Marconcini LA, et al. Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest. 2006;116(3):753–9.PubMedPubMedCentralCrossRef Houghton AM, Quintero PA, Perkins DL, Kobayashi DK, Kelley DG, Marconcini LA, et al. Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest. 2006;116(3):753–9.PubMedPubMedCentralCrossRef
36.
go back to reference Rabinovich RA, Miller BE, Wrobel K, Ranjit K, Williams MC, Drost E, et al. Circulating desmosine levels do not predict emphysema progression but are associated with cardiovascular risk and mortality in COPD. Eur Respir J. 2016;47(5):1365–73.PubMedCrossRef Rabinovich RA, Miller BE, Wrobel K, Ranjit K, Williams MC, Drost E, et al. Circulating desmosine levels do not predict emphysema progression but are associated with cardiovascular risk and mortality in COPD. Eur Respir J. 2016;47(5):1365–73.PubMedCrossRef
37.
go back to reference Boyd AS, Stasko T, King LE, Cameron GS, Pearse AD, Gaskell SA. Cigarette smoking-associated elastotic changes in the skin. J Am Acad Dermatol. 1999;41(1):23–6.PubMedCrossRef Boyd AS, Stasko T, King LE, Cameron GS, Pearse AD, Gaskell SA. Cigarette smoking-associated elastotic changes in the skin. J Am Acad Dermatol. 1999;41(1):23–6.PubMedCrossRef
38.
go back to reference Laurent P, Janoff A, Kagan HM. Cigarette smoke blocks cross-linking of elastin in vitro. Am Rev Respir Dis. 1983;127(2):189–92.PubMed Laurent P, Janoff A, Kagan HM. Cigarette smoke blocks cross-linking of elastin in vitro. Am Rev Respir Dis. 1983;127(2):189–92.PubMed
39.
go back to reference Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun. 2010;34(3):J258–65.PubMedCrossRef Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun. 2010;34(3):J258–65.PubMedCrossRef
40.
go back to reference Chung KF, Adcock IM. Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. Eur Respir J. 2008;31(6):1334–56.PubMedCrossRef Chung KF, Adcock IM. Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. Eur Respir J. 2008;31(6):1334–56.PubMedCrossRef
41.
go back to reference Agusti A, Edwards LD, Rennard SI, MacNee W, Tal-Singer R, Miller BE, et al. Persistent systemic inflammation is associated with poor clinical outcomes in COPD: a novel phenotype. PLoS One. 2012;7(5):e37483.PubMedPubMedCentralCrossRef Agusti A, Edwards LD, Rennard SI, MacNee W, Tal-Singer R, Miller BE, et al. Persistent systemic inflammation is associated with poor clinical outcomes in COPD: a novel phenotype. PLoS One. 2012;7(5):e37483.PubMedPubMedCentralCrossRef
42.
go back to reference Bond M, Fabunmi RP, Baker AH, Newby AC. Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEBS Lett. 1998;435(1):29–34.PubMedCrossRef Bond M, Fabunmi RP, Baker AH, Newby AC. Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEBS Lett. 1998;435(1):29–34.PubMedCrossRef
43.
go back to reference Han YP, Tuan TL, Hughes M, Wu H, Garner WL. Transforming growth factor-beta - and tumor necrosis factor-alpha -mediated induction and proteolytic activation of MMP-9 in human skin. J Biol Chem American Society for Biochemistry and Molecular Biology. 2001;276(25):22341–50. Han YP, Tuan TL, Hughes M, Wu H, Garner WL. Transforming growth factor-beta - and tumor necrosis factor-alpha -mediated induction and proteolytic activation of MMP-9 in human skin. J Biol Chem American Society for Biochemistry and Molecular Biology. 2001;276(25):22341–50.
44.
go back to reference Russell REK, Culpitt SV, DeMatos C, Donnelly L, Smith M, Wiggins J, et al. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2002;26(5):602–9.PubMedCrossRef Russell REK, Culpitt SV, DeMatos C, Donnelly L, Smith M, Wiggins J, et al. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2002;26(5):602–9.PubMedCrossRef
45.
go back to reference Simó R, Barbosa-Desongles A, Lecube A, Hernandez C, Selva DM. Potential role of tumor necrosis factor-α in downregulating sex hormone-binding globulin. Diabetes. 2012;61(2):372–82.PubMedPubMedCentralCrossRef Simó R, Barbosa-Desongles A, Lecube A, Hernandez C, Selva DM. Potential role of tumor necrosis factor-α in downregulating sex hormone-binding globulin. Diabetes. 2012;61(2):372–82.PubMedPubMedCentralCrossRef
46.
go back to reference Aderka D, Engelmann H, Maor Y, Brakebusch C, Wallach D. Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors. J Exp Med. 1992;175(2):323–9.PubMedCrossRef Aderka D, Engelmann H, Maor Y, Brakebusch C, Wallach D. Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors. J Exp Med. 1992;175(2):323–9.PubMedCrossRef
47.
go back to reference Vierkötter A, Schikowski T, Sugiri D, Matsui MS, Krämer U, Krutmann J. MMP-1 and -3 promoter variants are indicative of a common susceptibility for skin and lung aging: results from a cohort of elderly women (SALIA). J Investig Dermatol. 2015;135(5):1268–74.PubMedCrossRef Vierkötter A, Schikowski T, Sugiri D, Matsui MS, Krämer U, Krutmann J. MMP-1 and -3 promoter variants are indicative of a common susceptibility for skin and lung aging: results from a cohort of elderly women (SALIA). J Investig Dermatol. 2015;135(5):1268–74.PubMedCrossRef
48.
go back to reference Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, et al. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med. 2006;12(3):317–23.PubMedCrossRef Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, et al. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med. 2006;12(3):317–23.PubMedCrossRef
49.
go back to reference Barnes PJ. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2016;138(1):16–27.PubMedCrossRef Barnes PJ. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2016;138(1):16–27.PubMedCrossRef
50.
go back to reference Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT. Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Lab Investig. 1998;78(9):1077–87.PubMed Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT. Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Lab Investig. 1998;78(9):1077–87.PubMed
51.
go back to reference Han YP, Tuan TL, Wu H, Hughes M, Garner WL. TNF-alpha stimulates activation of pro-MMP2 in human skin through NF-(kappa)B mediated induction of MT1-MMP. J Cell Sci. 2001;114(Pt 1):131–9.PubMedPubMedCentral Han YP, Tuan TL, Wu H, Hughes M, Garner WL. TNF-alpha stimulates activation of pro-MMP2 in human skin through NF-(kappa)B mediated induction of MT1-MMP. J Cell Sci. 2001;114(Pt 1):131–9.PubMedPubMedCentral
52.
go back to reference Hoonhorst SJM, Tam Loi Lo AT, Hartman JE, Telenga ED, van den Berge M, Koenderman L, et al. Advanced glycation end products in the skin are enhanced in COPD. Metab Clin Exp. 2014;63(9):1149–56.PubMedCrossRef Hoonhorst SJM, Tam Loi Lo AT, Hartman JE, Telenga ED, van den Berge M, Koenderman L, et al. Advanced glycation end products in the skin are enhanced in COPD. Metab Clin Exp. 2014;63(9):1149–56.PubMedCrossRef
53.
go back to reference Wesley NO, Maibach HI. Racial (ethnic) differences in skin properties: the objective data. Am J Clin Dermatol. 2003;4(12):843–60.PubMedCrossRef Wesley NO, Maibach HI. Racial (ethnic) differences in skin properties: the objective data. Am J Clin Dermatol. 2003;4(12):843–60.PubMedCrossRef
54.
go back to reference Bruse S, Moreau M, Bromberg Y, Jang J-H, Wang N, Ha H, et al. Whole exome sequencing identifies novel candidate genes that modify chronic obstructive pulmonary disease susceptibility. Hum Genomics. 2016;10(1):1.PubMedPubMedCentralCrossRef Bruse S, Moreau M, Bromberg Y, Jang J-H, Wang N, Ha H, et al. Whole exome sequencing identifies novel candidate genes that modify chronic obstructive pulmonary disease susceptibility. Hum Genomics. 2016;10(1):1.PubMedPubMedCentralCrossRef
55.
go back to reference Demierre MF, Brooks D, Koh HK, Geller AC. Public knowledge, awareness, and perceptions of the association between skin aging and smoking. J Am Acad Dermatol. 1999;41(1):27–30.PubMedCrossRef Demierre MF, Brooks D, Koh HK, Geller AC. Public knowledge, awareness, and perceptions of the association between skin aging and smoking. J Am Acad Dermatol. 1999;41(1):27–30.PubMedCrossRef
Metadata
Title
Loss of skin elasticity is associated with pulmonary emphysema, biomarkers of inflammation, and matrix metalloproteinase activity in smokers
Authors
Michael E. O’Brien
Divay Chandra
Robert C. Wilson
Chad M. Karoleski
Carl R. Fuhrman
Joseph K. Leader
Jiantao Pu
Yingze Zhang
Alison Morris
Seyed Nouraie
Jessica Bon
Zsolt Urban
Frank C. Sciurba
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2019
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-019-1098-7

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WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine