Distinguishing the impact of distinct obstructive sleep apnea syndrome (OSAS) and obesity related factors on human monocyte subsets.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
03 Jan 2024
03 Jan 2024
Historique:
received:
18
04
2023
accepted:
13
12
2023
medline:
4
1
2024
pubmed:
4
1
2024
entrez:
3
1
2024
Statut:
epublish
Résumé
Obstructive sleep apnea syndrome (OSAS) and obesity go hand in hand in the majority of patients and both are associated with a systemic inflammation, immune disturbance and comorbidities such as cardiovascular disease. However, the unambiguous impact of OSAS and obesity on the individual inflammatory microenvironment and the immunological consequences of human monocytes has not been distinguished yet. Therefore, aim of this study was to investigate the impact of OSAS and obesity related factors on the inflammatory microenvironment by performing flow cytometric whole blood measurements of CD14/CD16 monocyte subsets in normal weight OSAS patients, patients with obesity but without OSAS, and patients with OSAS and obesity, compared to healthy donors. Moreover, explicitly OSAS and obesity related plasma levels of inflammatory mediators adiponectin, leptin, lipocalin and metalloproteinase-9 were determined and the influence of different OSAS and obesity related factors on cytokine secretion and expression of different adhesion molecules by THP-1 monocytes was analysed. Our data revealed a significant redistribution of circulating classical and intermediate monocytes in all three patient cohorts, but differential effects in terms of monocytic adhesion molecules CD11a, CD11b, CD11c, CX3CR1, CD29, CD49d, and plasma cytokine levels. These data were reflected by differential effects of OSAS and obesity related factors leptin, TNFα and hypoxia on THP-1 cytokine secretion patterns and expression of adhesion molecules CD11b and CD49d. In summary, our data revealed differential effects of OSAS and obesity, which underlines the need for a customized therapeutic regimen with respect to the individual weighting of these overlapping diseases.
Identifiants
pubmed: 38172514
doi: 10.1038/s41598-023-49921-5
pii: 10.1038/s41598-023-49921-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
340Informations de copyright
© 2024. The Author(s).
Références
Kapur, V. K. et al. Clinical practice guideline for diagnostic testing for adult obstructive sleep apnea: An american academy of sleep medicine clinical practice guideline. J. Clin. Sleep Med. 13(3), 479–504 (2017).
pubmed: 28162150
pmcid: 5337595
doi: 10.5664/jcsm.6506
Gaines, J. et al. Inflammation mediates the association between visceral adiposity and obstructive sleep apnea in adolescents. Am. J. Physiol. Endocrinol. Metab. 311(5), E851–E858 (2016).
pubmed: 27651112
pmcid: 5130357
doi: 10.1152/ajpendo.00249.2016
Poitou, C. et al. CD14dimCD16+ and CD14+CD16+ monocytes in obesity and during weight loss: Relationships with fat mass and subclinical atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 31(10), 2322–2330 (2011).
pubmed: 21799175
doi: 10.1161/ATVBAHA.111.230979
Russo, L. & Lumeng, C. N. Properties and functions of adipose tissue macrophages in obesity. Immunology 155(4), 407–417 (2018).
pubmed: 30229891
pmcid: 6230999
doi: 10.1111/imm.13002
Xanthopoulos, M. S., Berkowitz, R. I. & Tapia, I. E. Effects of obesity therapies on sleep disorders. Metabol. Clin. Exp. 84, 109–117 (2018).
doi: 10.1016/j.metabol.2018.01.022
Muehlroth, B. E., Rasch, B. & Werkle-Bergner, M. Episodic memory consolidation during sleep in healthy aging. Sleep Med. Rev. 52, 101304 (2020).
pubmed: 32278267
doi: 10.1016/j.smrv.2020.101304
Gregor, M. F. & Hotamisligil, G. S. Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29, 415–445 (2011).
pubmed: 21219177
doi: 10.1146/annurev-immunol-031210-101322
Fantuzzi, G. Adipose tissue, adipokines, and inflammation. J. Allergy Clin. Immunol. 115(5), 911–919 (2005).
pubmed: 15867843
doi: 10.1016/j.jaci.2005.02.023
Kane, H. & Lynch, L. Innate immune control of adipose tissue homeostasis. Trends Immunol. 40(9), 857–872 (2019).
pubmed: 31399336
doi: 10.1016/j.it.2019.07.006
Kurobe, H. et al. Role of hypoxia-inducible factor 1alpha in T cells as a negative regulator in development of vascular remodeling. Arterioscleros. Thrombos. Vasc. Biol. 30(2), 210–217 (2010).
doi: 10.1161/ATVBAHA.109.192666
Domagala-Kulawik, J., Osinska, I., Piechuta, A., Bielicki, P. & Skirecki, T. T, B, and NKT cells in systemic inflammation in obstructive sleep apnoea. Mediat. Inflamm. 2015, 161579 (2015).
doi: 10.1155/2015/161579
Cubillos-Zapata, C. et al. Hypoxia-induced PD-L1/PD-1 crosstalk impairs T-cell function in sleep apnoea. Eur. Respir. J. 50, 4 (2017).
doi: 10.1183/13993003.00833-2017
Ryan, S., Taylor, C. T. & McNicholas, W. T. Systemic inflammation: A key factor in the pathogenesis of cardiovascular complications in obstructive sleep apnoea syndrome?. Thorax 64(7), 631–636 (2009).
pubmed: 19561283
Kapellos, T. S. et al. Human monocyte subsets and phenotypes in major chronic inflammatory diseases. Front. Immunol. 10, 2035 (2019).
pubmed: 31543877
pmcid: 6728754
doi: 10.3389/fimmu.2019.02035
Polasky, C. et al. Redistribution of monocyte subsets in obstructive sleep apnea syndrome patients leads to an imbalanced PD-1/PD-L1 cross-talk with CD4/CD8 T cells. J. Immunol. 206(1), 51–58 (2021).
pubmed: 33268482
doi: 10.4049/jimmunol.2001047
Meyhofer, S. et al. Plasma leptin levels, obstructive sleep apnea syndrome, and diabetes are associated with obesity-related alterations of peripheral blood monocyte subsets. ImmunoHorizons 7(3), 191–199 (2023).
pubmed: 36921085
pmcid: 10563442
doi: 10.4049/immunohorizons.2300009
Tsuchiya, S. et al. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26(2), 171–176 (1980).
pubmed: 6970727
doi: 10.1002/ijc.2910260208
Pries, R., Lange, C., Behn, N., Bruchhage, K. L. & Steffen, A. Dynamics of circulating CD14/CD16 monocyte subsets in obstructive sleep apnea syndrome patients upon hypoglossal nerve stimulation. Biomedicines 10, 8 (2022).
doi: 10.3390/biomedicines10081925
Germano, D. B. et al. Monocyte chemokine receptors as therapeutic targets in cardiovascular diseases. Immunol. Lett. 256–257, 1–8 (2023).
pubmed: 36893859
doi: 10.1016/j.imlet.2023.03.002
Zeng, L. et al. Loss of cAMP signaling in CD11c immune cells protects against diet-induced obesity. Diabetes 72(9), 1235–1250 (2023).
pubmed: 37257047
doi: 10.2337/db22-1035
Dupuy, A. G. & Caron, E. Integrin-dependent phagocytosis—spreading from microadhesion to new concepts. J. Cell Sci. 121(11), 1773–1783 (2008).
pubmed: 18492791
doi: 10.1242/jcs.018036
McDermott, D. H. et al. Association between polymorphism in the chemokine receptor CX3CR1 and coronary vascular endothelial dysfunction and atherosclerosis. Circ. Res. 89(5), 401–407 (2001).
pubmed: 11532900
doi: 10.1161/hh1701.095642
Tacke, F. et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117(1), 185–194 (2007).
pubmed: 17200718
pmcid: 1716202
doi: 10.1172/JCI28549
Auffray, C. et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317(5838), 666–670 (2007).
pubmed: 17673663
doi: 10.1126/science.1142883
Devevre, E. F. et al. Profiling of the three circulating monocyte subpopulations in human obesity. J. Immunol 194(8), 3917–3923 (2015).
pubmed: 25786686
doi: 10.4049/jimmunol.1402655
Bianchi, E., Bender, J. R., Blasi, F. & Pardi, R. Through and beyond the wall: Late steps in leukocyte transendothelial migration. Immunol. Today 18(12), 586–591 (1997).
pubmed: 9425737
doi: 10.1016/S0167-5699(97)01162-6
Sacco, R. E. et al. Reduction in inflammation following blockade of CD18 or CD29 adhesive pathways during the acute phase of a spirochetal-induced colitis in mice. Microb. Pathogenes. 29(5), 289–299 (2000).
doi: 10.1006/mpat.2000.0394
Friedemann, C. et al. Cardiovascular disease risk in healthy children and its association with body mass index: Systematic review and meta-analysis. BMJ 345, e4759 (2012).
pubmed: 23015032
pmcid: 3458230
doi: 10.1136/bmj.e4759
Hotamisligil, G. S. Foundations of immunometabolism and implications for metabolic health and disease. Immunity 47(3), 406–420 (2017).
pubmed: 28930657
pmcid: 5627521
doi: 10.1016/j.immuni.2017.08.009
Odegaard, J. I. & Chawla, A. Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339(6116), 172–177 (2013).
pubmed: 23307735
pmcid: 3725457
doi: 10.1126/science.1230721
Alexopoulos, N., Katritsis, D. & Raggi, P. Visceral adipose tissue as a source of inflammation and promoter of atherosclerosis. Atherosclerosis 233(1), 104–112 (2014).
pubmed: 24529130
doi: 10.1016/j.atherosclerosis.2013.12.023
Gustafson, B. Adipose tissue, inflammation and atherosclerosis. J.. Atheroscler. Thromb. 17(4), 332–341 (2010).
pubmed: 20124732
doi: 10.5551/jat.3939
Liao, J. K. Linking endothelial dysfunction with endothelial cell activation. J. Clin. Invest. 123(2), 540–541 (2013).
pubmed: 23485580
pmcid: 3561809
doi: 10.1172/JCI66843
Gast, K. B. et al. Individual contributions of visceral fat and total body fat to subclinical atherosclerosis: The NEO study. Atherosclerosis 241(2), 547–554 (2015).
pubmed: 26100677
doi: 10.1016/j.atherosclerosis.2015.05.026
Kranendonk, M. E. et al. Inflammatory characteristics of distinct abdominal adipose tissue depots relate differently to metabolic risk factors for cardiovascular disease: Distinct fat depots and vascular risk factors. Atherosclerosis 239(2), 419–427 (2015).
pubmed: 25682042
doi: 10.1016/j.atherosclerosis.2015.01.035
Kralova Lesna, I. et al. Characterisation and comparison of adipose tissue macrophages from human subcutaneous, visceral and perivascular adipose tissue. J. Transl. Med. 14(1), 208 (2016).
pubmed: 27400732
pmcid: 4940901
doi: 10.1186/s12967-016-0962-1
Maeda, N. et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8(7), 731–737 (2002).
pubmed: 12068289
doi: 10.1038/nm724
Park, P. H. et al. Suppression of lipopolysaccharide-stimulated tumor necrosis factor-alpha production by adiponectin is mediated by transcriptional and post-transcriptional mechanisms. J. Biol. Chem. 283(40), 26850–26858 (2008).
pubmed: 18678874
pmcid: 2556004
doi: 10.1074/jbc.M802787200
Tsatsanis, C. et al. Peripheral factors in the metabolic syndrome: The pivotal role of adiponectin. Ann. N. Y. Acad. Sci. 1083, 185–195 (2006).
pubmed: 17148740
doi: 10.1196/annals.1367.013
Najafi, A. et al. Evaluation of plasma/serum adiponectin (an anti-inflammatory factor) levels in adult patients with obstructive sleep apnea syndrome: A systematic review and meta-analysis. Life 12, 5 (2022).
doi: 10.3390/life12050738
Zhang, Y. & Chua, S. Jr. Leptin function and regulation. Compr. Physiol. 8(1), 351–369 (2017).
pubmed: 29357132
doi: 10.1002/cphy.c160041
Triantafyllou, G. A., Paschou, S. A. & Mantzoros, C. S. Leptin and hormones: Energy homeostasis. Endocrinol. Metabol. Clin. N. Am. 45(3), 633–645 (2016).
doi: 10.1016/j.ecl.2016.04.012
Fantuzzi, G. & Faggioni, R. Leptin in the regulation of immunity, inflammation, and hematopoiesis. J. Leukocyte Biol. 68(4), 437–446 (2000).
pubmed: 11037963
doi: 10.1189/jlb.68.4.437
Watanabe, K. et al. Leptin-producing monocytes in the airway submucosa may contribute to asthma pathogenesis. Respir. Investig. 61(1), 5–15 (2023).
pubmed: 36369154
doi: 10.1016/j.resinv.2022.09.005
Kapusuz Gencer, Z. et al. The correlation of serum levels of leptin, leptin receptor and NO x (NO 2 (-) and NO 3 (-)) in patients with obstructive sleep apnea syndrome. Eur. Arch. Oto-rhino-laryngol. 271(11), 2943–2948 (2014).
doi: 10.1007/s00405-014-2946-1
Ursavas, A., Ilcol, Y. O., Nalci, N., Karadag, M. & Ege, E. Ghrelin, leptin, adiponectin, and resistin levels in sleep apnea syndrome: Role of obesity. Ann. Thorac. Med. 5(3), 161–165 (2010).
pubmed: 20835311
pmcid: 2930655
doi: 10.4103/1817-1737.65050
Haas, P., Straub, R. H., Bedoui, S. & Nave, H. Peripheral but not central leptin treatment increases numbers of circulating NK cells, granulocytes and specific monocyte subpopulations in non-endotoxaemic lean and obese LEW-rats. Regul. Peptides 151(1–3), 26–34 (2008).
doi: 10.1016/j.regpep.2008.05.004
An, H. S. et al. Lipocalin-2 promotes acute lung inflammation and oxidative stress by enhancing macrophage iron accumulation. Int. J. Biol. Sci. 19(4), 1163–1177 (2023).
pubmed: 36923935
pmcid: 10008694
doi: 10.7150/ijbs.79915
Javaid, H. M. A. et al. TNFalpha-induced NLRP3 inflammasome mediates adipocyte dysfunction and activates macrophages through adipocyte-derived lipocalin 2. Metabol. Clin. Exp. 142, 155527 (2023).
doi: 10.1016/j.metabol.2023.155527
Ye, J., Liu, H., Li, Y., Liu, X. & Zhu, J. M. Increased serum levels of C-reactive protein and matrix metalloproteinase-9 in obstructive sleep apnea syndrome. Chin. Med. J. 120(17), 1482–1486 (2007).
pubmed: 17908454
doi: 10.1097/00029330-200709010-00003
Zysk, B. et al. Pro-inflammatory adipokine and cytokine profiles in the saliva of obese patients with non-alcoholic fatty liver disease (NAFLD)—a pilot study. Int. J. Mol. Sci. 24, 3 (2023).
doi: 10.3390/ijms24032891
Zhang, Y. et al. KCNQ1OT1, HIF1A-AS2 and APOA1-AS are promising novel biomarkers for diagnosis of coronary artery disease. Clin. Exp. Pharmacol. Physiol. 46(7), 635–642 (2019).
pubmed: 30941792
doi: 10.1111/1440-1681.13094
Hu, J. et al. Apolipoprotein A1 suppresses the hypoxia-induced angiogenesis of human retinal endothelial cells by targeting PlGF. Int. J. Ophthalmol. 16(1), 33–39 (2023).
pubmed: 36659935
pmcid: 9815967
doi: 10.18240/ijo.2023.01.05
Ottria, A. et al. Hypoxia and TLR9 activation drive CXCL4 production in systemic sclerosis plasmacytoid dendritic cells via mtROS and HIF-2alpha. Rheumatology 61(6), 2682–2693 (2022).
pubmed: 34559222
doi: 10.1093/rheumatology/keab532
Tsai, C. L. et al. TNF-alpha induces matrix metalloproteinase-9-dependent soluble intercellular adhesion molecule-1 release via TRAF2-mediated MAPKs and NF-kappaB activation in osteoblast-like MC3T3-E1 cells. J. Biomed. Sci. 21(1), 12 (2014).
pubmed: 24502696
pmcid: 3926355
doi: 10.1186/1423-0127-21-12
O’Hara, A. M. et al. Tumor necrosis factor (TNF)-alpha-induced IL-8 expression in gastric epithelial cells: Role of reactive oxygen species and AP endonuclease-1/redox factor (Ref)-1. Cytokine 46(3), 359–369 (2009).
pubmed: 19376732
pmcid: 2846768
doi: 10.1016/j.cyto.2009.03.010
Silber, M. H. et al. The visual scoring of sleep in adults. J. Clin. sleep Med. 3(2), 121–131 (2007).
pubmed: 17557422
doi: 10.5664/jcsm.26814
Temirbekov, D., Gunes, S., Yazici, Z. M. & Sayin, I. The ignored parameter in the diagnosis of obstructive sleep apnea syndrome: The oxygen desaturation index. Turk. Arch. Otorhinolaryngol. 56(1), 1–6 (2018).
pubmed: 29988275
pmcid: 6017211
doi: 10.5152/tao.2018.3025
Johns, M. W. A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep 14(6), 540–545 (1991).
pubmed: 1798888
doi: 10.1093/sleep/14.6.540
Sauter, C. P. R. et al. Normative values of the German Epworth Sleepiness Scale. Somnologie 11, 272–278 (2007).
doi: 10.1007/s11818-007-0322-8