Stress-induced release of matrix metalloproteinase-9 in patients with coronary artery disease: The possible influence of cortisol
Open accessAbstract
Stress and inflammation are both important risk factors for coronary artery disease (CAD). However, the susceptibility to stress-induced inflammation and its determinants have been little explored in patients with CAD. Here, our aim was to study the stress-induced inflammatory response, more precisely the early release of matrix metalloproteinase (MMP)-9, and its association with cortisol response in patients with CAD. Sixty-four patients underwent a standardized laboratory stress test. The stress-induced release of MMP-9 was closely associated with the release of other neutrophil-associated proteins, MMP-8 and myeloperoxidase (MPO). It also showed a large variation among patients, as did cortisol. Twenty minutes after stress, a negative association between changes in MMP-9 and cortisol was seen (p<0.01). In vitro, dexamethasone reduced the IL-8-mediated release of MMP-9 from neutrophils, indicating that glucocorticoids may exert rapid effects on neutrophil activation. Further characterization of patients revealed that stress-induced release of MMP-9 was related to leukocyte telomere shortening and increased ultrasound-assessed plaque occurrence in the carotid arteries, but not to other characteristics such as age, gender or psychological background factors. The susceptibility to stress-induced release of MMP-9 may thus have impact on disease phenotype. Stress tests can be useful to identify CAD patients in need of novel prevention and treatment strategies.
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Cites
The CES-D Scale: A Self-Report Depression Scale for Research in the General Population
Radloff, L. S. (1977) · Applied Psychological Measurement · doi:10.1177/014662167700100306 · Cited by 53,267 · see citing works
Pearlin, L. I., & Schooler, C. (1978) · Journal of Health and Social Behavior · doi:10.2307/2136319 · Cited by 7,791 · see citing works
Salivary cortisol as a biomarker in stress research
Hellhammer, D. H., Wüst, S., & Kudielka, B. M. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.10.026 · Cited by 1,925 · see citing works
Mannheim Carotid Intima-Media Thickness and Plaque Consensus (2004–2006–2011)
Touboul, P., Hennerici, M. G., Meairs, S. P., Adams, H., Amarenco, P., Bornstein, N. M., Csiba, L., Desvarieux, M., Ebrahim, S. B. J., Hernandez, R. H., et al. (2012) · Cerebrovascular Diseases · doi:10.1159/000343145 · Cited by 1,818 · see citing works
Proposed hostility and Pharisaic-virtue scales for the MMPI.
Cook, W. W., & Medley, D. M. (1954) · Journal of Applied Psychology · doi:10.1037/h0060667 · Cited by 1,489 · see citing works
Steptoe, A., Hamer, M., & Chida, Y. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.03.011 · Cited by 1,278 · see citing works
Chronic variable stress activates hematopoietic stem cells
Heidt, T., Sager, H. B., Courties, G., Dutta, P., Iwamoto, Y., Zaltsman, A., von zur Muhlen, C., Bode, C., Fricchione, G. L., Denninger, J., et al. (2014) · Nature Medicine · doi:10.1038/nm.3589 · Cited by 803 · see citing works
Blankenberg, S., Rupprecht, H. J., Poirier, O., Bickel, C., Smieja, M., Hafner, G., Meyer, J., Cambien, F., & Tiret, L. (2003) · Circulation · doi:10.1161/01.cir.0000058700.41738.12 · Cited by 755 · see citing works
HMG-CoA Reductase Inhibitors Reduce MMP-9 Secretion by Macrophages
Bellosta, S., Via, D. P., Canavesi, M., Pfister, P., Fumagalli, R., Paoletti, R., & Bernini, F. (1998) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.18.11.1671 · Cited by 512 · see citing works
Multiple Roles for Neutrophils in Atherosclerosis
Soehnlein, O. (2012) · Circulation Research · doi:10.1161/circresaha.111.257535 · Cited by 498 · see citing works
Stimulation of systemic low-grade inflammation by psychosocial stress.
Rohleder, N. (2014) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000049 · Cited by 497 · see citing works
Lin, J., Epel, E., Cheon, J., Kroenke, C., Sinclair, E., Bigos, M., Wolkowitz, O., Mellon, S., & Blackburn, E. (2010) · Journal of Immunological Methods · doi:10.1016/j.jim.2009.09.012 · Cited by 426 · see citing works
The roles of senescence and telomere shortening in cardiovascular disease
Fyhrquist, F., Saijonmaa, O. J., & Strandberg, T. E. (2013) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2013.30 · Cited by 368 · see citing works
Acute mental stress elicits delayed increases in circulating inflammatory cytokine levels
STEPTOE, A., WILLEMSEN, G., OWEN, N., FLOWER, L., & MOHAMED-ALI, V. (2001) · Clinical Science · doi:10.1042/cs1010185 · Cited by 354 · see citing works
Domenici, E., Willé, D. R., Tozzi, F., Prokopenko, I., Miller, S. L., McKeown, A., Brittain, C. F., Rujescu, D., Giegling, I., Turck, C. W., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009166 · Cited by 347 · see citing works
Atherosclerotic Plaque Destabilization
Silvestre-Roig, C., de Winther, M. P. J., Weber, C., Daemen, M. J. A. P., Lutgens, E., & Soehnlein, O. (2014) · Circulation Research · doi:10.1161/circresaha.114.302355 · Cited by 334 · see citing works
Ionita, M. G., van den Borne, P., Catanzariti, L. M., Moll, F. L., de Vries, J. P. P. M., Pasterkamp, G., Vink, A., & de Kleijn, D. P. V. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.209296 · Cited by 304 · see citing works
Kunz-Ebrecht, S., Mohamed‐Ali, V., Feldman, P. J., Kirschbaum, C., & Steptoe, A. (2003) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(03)00029-1 · Cited by 290 · see citing works
Lagraauw, H. M., Kuiper, J., & Bot, I. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.08.007 · Cited by 265 · see citing works
Does cellular aging relate to patterns of allostasis?
Tomiyama, A. J., O’Donovan, A., Lin, J., Puterman, E. M., Lazaro, A., Chan, J. L., Dhabhar, F. S., Wolkowitz, O. M., Kirschbaum, C., Blackburn, E. H., et al. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.11.016 · Cited by 206 · see citing works
Schleimer, R. P., Freeland, H. S., Peters, S. P., Brown, K. E., & Derse, C. P. (1989) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22251-0 · Cited by 193 · see citing works
Wikgren, M., Maripuu, M., Karlsson, T., Nordfjäll, K., Bergdahl, J., Hultdin, J., Del‐Favero, J., Roos, G., Nilsson, L., Adolfsson, R., et al. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.015 · Cited by 173 · see citing works
Regulation of matrix metalloproteinase-9 release from IL-8-stimulated human neutrophils
Chakrabarti, S., & Patel, K. D. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.1004612 · Cited by 164 · see citing works
Depressive symptoms enhance stress-induced inflammatory responses.
Fagundes, C. P., Glaser, R., Hwang, B. S., Malarkey, W. B., & Kiecolt-Glaser, J. K. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.05.006 · Cited by 151 · see citing works
Pathophysiological processes underlying emotional triggering of acute cardiac events
Strike, P. C., Magid, K. S., Whitehead, D. L., Brydon, L., Bhattacharyya, M. R., & Steptoe, A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507097103 · Cited by 123 · see citing works
Newby, A. C. (2015) · Matrix Biology · doi:10.1016/j.matbio.2015.01.015 · Cited by 119 · see citing works
The Role of Matrix Metalloproteinases in Atherothrombosis
Ketelhuth, D. F. J., & Bäck, M. (2011) · Current Atherosclerosis Reports · doi:10.1007/s11883-010-0159-7 · Cited by 98 · see citing works
Nijm, J., Kristenson, M., OLSSON, A. G., & Jonasson, L. (2007) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01817.x · Cited by 97 · see citing works
Self-citationRapid non-genomic inhibitory effects of glucocorticoids on human neutrophil degranulation
Liu, L., Wang, Y. X., Zhou, J., Long, F., Sun, H., Liu, Y., Chen, Y. Z., & Jiang, C. (2005) · Inflammation Research · doi:10.1007/s00011-004-1320-y · Cited by 93 · see citing works
Kuebler, U., Zuccarella-Hackl, C., Arpagaus, A., Wolf, J. M., Farahmand, F., von Känel, R., Ehlert, U., & Wirtz, P. H. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.12.024 · Cited by 91 · see citing works
Determinants of the NF-κB response to acute psychosocial stress in humans
Wolf, J. M., Rohleder, N., Bierhaus, A., Nawroth, P. P., & Kirschbaum, C. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2008.09.009 · Cited by 87 · see citing works
Davidson, K. W., Schwartz, J. E., Kirkland, S., Mostofsky, E., Fink, D. L., Guernsey, D. L., & Shimbo, D. (2009) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2008.11.035 · Cited by 80 · see citing works
Emotional triggers in myocardial infarction: do they matter?
Edmondson, D. E., Newman, J. D., Whang, W., & Davidson, K. W. (2012) · European Heart Journal · doi:10.1093/eurheartj/ehs398 · Cited by 77 · see citing works
Hostility and physiological responses to laboratory stress in acute coronary syndrome patients
Brydon, L., Strike, P. C., Bhattacharyya, M. R., Whitehead, D. L., McEwan, J. R., Zachary, I. C., & Steptoe, A. (2009) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2009.06.007 · Cited by 73 · see citing works
Hirsch, G., Lavoie‐Lamoureux, A., Beauchamp, G., & Lavoie, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044606 · Cited by 62 · see citing works
Do Psychological Factors Affect Inflammation and Incident Coronary Heart Disease
Nabi, H., Singh‐Manoux, A., Shipley, M. J., Gimeno, D., Marmot, M. G., & Mika Kivimaki, B. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.167239 · Cited by 61 · see citing works
Hua, Y., Xue, J., Sun, F., et al. (2008) · Pharmacology · doi:10.1159/000166183 · Cited by 53 · see citing works
Kristenson, M., OLSSON, A. G., & Kučinskienė, Z. A. (2005) · International Journal of Behavioral Medicine · doi:10.1207/s15327558ijbm1203_4 · Cited by 51 · see citing works
Self-citationGarvin, P., Nilsson, L., Carstensen, J. M., Jonasson, L., & Kristenson, M. (2009) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181960e7f · Cited by 51 · see citing works
Self-citationIncreased Levels of Leukocyte-Derived MMP-9 in Patients with Stable Angina Pectoris
Jönsson, S., Lundberg, A., Kälvegren, H., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019340 · Cited by 50 · see citing works
Self-citationResponse and habituation of pro- and anti-inflammatory gene expression to repeated acute stress
McInnis, C. M., Wang, D., Gianferante, D., Hanlin, L. C., Chen, X., Thoma, M. V., & Rohleder, N. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.006 · Cited by 49 · see citing works
Hellberg, L., Samavedam, U. K. S. R. L., Holdorf, K., Hänsel, M., Recke, A., Beckmann, T., Steinhorst, K., Boehncke, W., Kirchner, T., Möckel, N., et al. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.91 · Cited by 48 · see citing works
The effect of a short-term mental stressor on neutrophil activation
Ellard, D. R., Castle, P. C., & Mian, R. (2001) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(00)00180-x · Cited by 46 · see citing works
Garvin, P., Jonasson, L., Nilsson, L. E., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138290 · Cited by 35 · see citing works
Self-citationPolymorphonuclear neutrophils and instability of the atherosclerotic plaque: a causative role?
Bona, R. D., Cardillo, M. T., Leo, M., Biasillo, G., Gustapane, M., Trotta, F., & Biasucci, L. M. (2013) · Inflammation Research · doi:10.1007/s00011-013-0617-0 · Cited by 30 · see citing works
Mian, R., Shelton-Rayner, G. K., Harkin, B., et al. (2003) · Stress · doi:10.1080/1025389031000101349 · Cited by 25 · see citing works
Szymanowski, A., Nijm, J., Kristenson, M., & Jonasson, L. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.012 · Cited by 20 · see citing works
Self-citationKeresztes, M., Horváth, T., Ocsovszki, I., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071902 · Cited by 17 · see citing works
Matrix metalloproteinases and psychosocial factors in acute coronary syndrome patients
Machulsky, N. F., Gagliardi, J., Fabre, B. R., Miksztowicz, V., Lombardo, M., Escudero, A. G., Gigena, G. E., Blanco, F., Gelpi, R. J., Schreier, L. E., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.09.015 · Cited by 12 · see citing works
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Beroun, A., Mitra, S., Michaluk, P., Pijet, B., Stefaniuk, M., & Kaczmarek, L. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03180-8 · Cited by 207 · see citing works
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Peng, Z., Peng, S., Lin, K., Zhao, B., Wei, L., Tuo, Q., Liao, D., Yuan, T., & Shi, Z. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02543-6 · Cited by 95 · see citing works
- Authors
- Lundberg, A. K., Jönsson, S., Stenmark, J., Kristenson, M., & Jonasson, L.
- Affiliations
- Linköping University (SE)
- Corresponding author
- Jonasson, Lena
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2016-11
- Volume
- 73
- Pages
- 117-124
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2492075907
- Cited by
- 24
- References
- 49
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 1 · 2020: 1 · 2019: 3 · 2018: 2 · 2017: 2 · 2016: 1
- FWCI
- 1.70
- Type
- journal article
- Language
- en
- Open access
- green
- urn.kb.se
- Licence
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Health and Mental Health
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Keywords
- coronary artery disease, MMP-9, stress-induced inflammation, cortisol, glucocorticoids, neutrophils, myeloperoxidase, MMP-8, dexamethasone, carotid plaque, stress testing, interleukin-8, disease phenotypes
- MeSH terms
- Aged, Coronary Artery Disease, Female, Follow-Up Studies, Humans, Hydrocortisone, Inflammation, Male, Middle Aged, Stress, Psychological, Matrix Metalloproteinase 9
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