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Frontiers of Medicine

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Front. Med.    2020, Vol. 14 Issue (1) : 81-90    https://doi.org/10.1007/s11684-019-0692-x
RESEARCH ARTICLE
Plasma soluble C-type lectin-like receptor-2 is associated with the risk of coronary artery disease
Min Fei1,2, Li Xiang3, Xichen Chai4, Jingchun Jin5, Tao You1,2, Yiming Zhao2, Changgeng Ruan1,2, Yiwen Hao5(), Li Zhu1,2()
1. Cyrus Tang Medical Institute, Collaborative Innovation Center of Hematology, State Key Laboratory of Radiation Medicine and Protection, Soochow University, Suzhou 215123, China
2. Jiangsu Institute of Hematology, The First Affiliated Hospital, Soochow University, Suzhou 215006, China
3. Department of Cardiology, The Second Affiliated Hospital, Soochow University, Suzhou 215004, China
4. Department of Cardiology, The First Affiliated Hospital, Soochow University, Suzhou 215006, China
5. Department of Blood Transfusion, The First Affiliated Hospital, China Medical University, Shenyang 110001, China
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Abstract

Accumulating evidence suggests that C-type lectin-like receptor-2 (CLEC-2) plays an important role in atherothrombosis. In this case-control study, we investigated the association between CLEC-2 and incidence of coronary artery disease (CAD). A total of 216 patients, including 14 cases of stable angina pectoris (SAP, non-ACS) and 202 cases of acute coronary syndrome (ACS), and 89 non-CAD control subjects were enrolled. Plasma levels of soluble CLEC-2 (sCLEC-2) were measured using the enzyme-linked immunosorbent assay (ELISA). Compared with the control group (65.69 (55.36–143.22) pg/mL), the plasma levels of sCLEC-2 were significantly increased in patients with CAD (133.67 (88.76–220.09) pg/mL) and ACS (134.16 (88.88–225.81) pg/mL). The multivariate adjusted odds ratios (95% confidence interval) of CAD reached 2.01 (1.52–2.66) (Ptrend<0.001) for each 1-quartile increase in sCLEC-2. Restricted cubic splines showed a positive dose-response association between sCLEC2 and CAD incidence (Plinearity<0.001). The addition of sCLEC-2 to conventional risk factors improved the C statistic (0.821 vs. 0.761, P = 0.004) and reclassification ability (net reclassification improvement: 57.45%, P<0.001; integrated discrimination improvement: 8.27%, P<0.001) for CAD. In conclusion, high plasma sCLEC-2 is independently associated with CAD risk, and the prognostic value of sCLEC-2 may be evaluated in future prospective studies.
Keywords soluble C-type lectin-like receptor-2      coronary artery disease      risk factor     
Corresponding Author(s): Yiwen Hao,Li Zhu   
Just Accepted Date: 24 May 2019   Online First Date: 10 July 2019    Issue Date: 02 March 2020
 Cite this article:   
Min Fei,Li Xiang,Xichen Chai, et al. Plasma soluble C-type lectin-like receptor-2 is associated with the risk of coronary artery disease[J]. Front. Med., 2020, 14(1): 81-90.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-019-0692-x
https://academic.hep.com.cn/fmd/EN/Y2020/V14/I1/81
Variables non-CAD (n = 89) CAD (n = 216) P value
Age (year) 59.88±9.69 61.90±11.45 0.144
Male gender (n (%)) 52 (58.4) 158 (73.1) 0.012
Smoking (n (%)) 15 (16.9) 87 (40.3) <0.001
Hypertension (n (%)) 24 (27.0) 123 (56.9) <0.001
DM (n (%)) 6 (6.7) 55 (25.5) <0.001
Hyperlipidemia (n (%)) 15 (16.9) 39 (18.1) 0.803
NT-ProBNP (mmol/L) 60.00 (36.00–88.50) 161.90 (37.25–1123.50) <0.001
eGFR (mL/(min·1.73m2)) 116.00 (99.00–132.00) 71.00 (58.25–81.75) <0.001
Tab.1  Baseline characteristics of enrolled patients with CAD and control subjects
Fig.1  Plasma levels of sCLEC-2 were measured in CAD patients and control subjects. (A) Plasma sCLEC-2 was higher in CAD patients compared with control subjects. (B) No significant difference in plasma sCLEC-2 was detected between ACS and non-ACS patients. ****P<0.0001; N.S., not significant.
Fig.2  Subgroup analyses of plasma sCLEC-2 levels in CAD patients. Plasma sCLEC-2 levels were compared among patient subgroups with different (A) affected coronary branches, (B) Gensini score classes, and (C) GRACE score classes. N.S., not significant.
Q1 Q2 Q3 Q4 P for trend Per SD increase
No. of CAD cases (%) 78 (25.6) 75 (24.6) 75 (24.6) 77 (25.2)
Odds of CAD
Unadjusted OR (CI) Reference 4.90 (2.43–9.92) 5.75 (2.79–11.86) 8.63 (3.95–18.84) 0.009 2.76 (1.71–4.45)
Adjusted OR (CI)a Reference 4.83 (2.21–10.53) 5.84 (2.60–13.11) 7.72 (3.26–18.28) <0.001 2.55 (1.58–4.13)
Tab.2  OR and 95% CI of CAD risk associated with CLEC-2
Fig.3  Association between plasma sCLEC-2 and CAD. (A) Forest plot of the multivariate logistic model for the association of sCLEC-2 with CAD. (B) The positive association between plasma sCLEC-2 and CAD was displayed in a restricted cubic spline.
C statistics NRI continuous NRI categoricala IDI
Estimate
(95% CI)		 P value Estimate
(95% CI)		 P value Estimate
(95% CI)		 P value Estimate
(95% CI)		 P value
Basic model 0.761 (0.709–0.808) Reference Reference Reference
Basic model+ CLEC-2 quartile 0.821 (0.774–0.863) 0.004 57.45 (34.15–80.75) <0.001 20.35 (11.22–29.49) <0.001 8.27 (4.73–11.82) <0.001
Tab.3  Reclassification and discrimination statistics for CAD incidence by plasma CLEC-2
Fig.4  Improvement distinguishing capacity for CAD by plasma sCLEC-2. (A) Addition of plasma sCLEC-2 to conventional risk factors improved the AUC of the receiver operating curve (ROC) for CAD. (B) Decision curve analyses for the odds of CAD by adding sCLEC-2 to a basic model. Basic model includes sex, age, smoking, hypertension, DM, and hyperlipidemia status.
1 JE Dalen, JS Alpert, RJ Goldberg, RS Weinstein. The epidemic of the 20(th) century: coronary heart disease. Am J Med 2014; 127(9): 807–812
https://doi.org/10.1016/j.amjmed.2014.04.015 pmid: 24811552
2 FB Hu, WC Willett. Optimal diets for prevention of coronary heart disease. JAMA 2002; 288(20): 2569–2578
https://doi.org/10.1001/jama.288.20.2569 pmid: 12444864
3 GLJ Fuller, JAE Williams, MG Tomlinson, JA Eble, SL Hanna, S Pöhlmann, K Suzuki-Inoue, Y Ozaki, SP Watson, AC Pearce. The C-type lectin receptors CLEC-2 and Dectin-1, but not DC-SIGN, signal via a novel YXXL-dependent signaling cascade. J Biol Chem 2007; 282(17): 12397–12409
https://doi.org/10.1074/jbc.M609558200 pmid: 17339324
4 C Weber, H Noels. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011; 17(11): 1410–1422
https://doi.org/10.1038/nm.2538 pmid: 22064431
5 E Falk, M Nakano, JF Bentzon, AV Finn, R Virmani. Update on acute coronary syndromes: the pathologists’ view. Eur Heart J 2013; 34(10): 719–728
https://doi.org/10.1093/eurheartj/ehs411 pmid: 23242196
6 KA Müller, M Chatterjee, D Rath, T Geisler. Platelets, inflammation and anti-inflammatory effects of antiplatelet drugs in ACS and CAD. Thromb Haemost 2015; 114(3): 498–518
https://doi.org/10.1160/TH14-11-0947 pmid: 26224127
7 MI Furman, SE Benoit, MR Barnard, CR Valeri, ML Borbone, RC Becker, HB Hechtman, AD Michelson. Increased platelet reactivity and circulating monocyte-platelet aggregates in patients with stable coronary artery disease. J Am Coll Cardiol 1998; 31(2): 352–358
https://doi.org/10.1016/S0735-1097(97)00510-X pmid: 9462579
8 V Lorenz, D Stegner, S Stritt, T Vögtle, F Kiefer, W Witke, J Schymeinsky, SP Watson, B Walzog, B Nieswandt. Targeted downregulation of platelet CLEC-2 occurs through Syk-independent internalization. Blood 2015; 125(26): 4069–4077
https://doi.org/10.1182/blood-2014-11-611905 pmid: 25795918
9 M Colonna, J Samaridis, L Angman. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol 2000; 30(2): 697–704
https://doi.org/10.1002/1521-4141(200002)30:2<697::AID-IMMU697>3.0.CO;2-M pmid: 10671229
10 K Suzuki-Inoue, M Osada, Y Ozaki. Physiologic and pathophysiologic roles of interaction between C-type lectin-like receptor 2 and podoplanin: partners from in utero to adulthood. J Thromb Haemost 2017; 15(2): 219–229
https://doi.org/10.1111/jth.13590 pmid: 27960039
11 K Suzuki-Inoue, Y Kato, O Inoue, MK Kaneko, K Mishima, Y Yatomi, Y Yamazaki, H Narimatsu, Y Ozaki. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem 2007; 282(36): 25993–26001
https://doi.org/10.1074/jbc.M702327200 pmid: 17616532
12 K Suzuki-Inoue, GL Fuller, A García, JA Eble, S Pöhlmann, O Inoue, TK Gartner, SC Hughan, AC Pearce, GD Laing, RD Theakston, E Schweighoffer, N Zitzmann, T Morita, VL Tybulewicz, Y Ozaki, SP Watson. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood 2006; 107(2): 542–549
https://doi.org/10.1182/blood-2005-05-1994 pmid: 16174766
13 F May, I Hagedorn, I Pleines, M Bender, T Vögtle, J Eble, M Elvers, B Nieswandt. CLEC-2 is an essential platelet-activating receptor in hemostasis and thrombosis. Blood 2009; 114(16): 3464–3472
https://doi.org/10.1182/blood-2009-05-222273 pmid: 19641185
14 CE Hughes, JM Auger, J McGlade, JA Eble, AC Pearce, SP Watson. Differential roles for the adapters Gads and LAT in platelet activation by GPVI and CLEC-2. J Thromb Haemost 2008; 6(12): 2152–2159
https://doi.org/10.1111/j.1538-7836.2008.03166.x pmid: 18826392
15 AF Parguiña, J Alonso, I Rosa, P Vélez, MJ González-López, E Guitián, JA Eble, MI Loza, Á García. A detailed proteomic analysis of rhodocytin-activated platelets reveals novel clues on the CLEC-2 signalosome: implications for CLEC-2 signaling regulation. Blood 2012; 120(26): e117–e126
https://doi.org/10.1182/blood-2012-09-456004 pmid: 23053573
16 E Gitz, AY Pollitt, JJ Gitz-Francois, O Alshehri, J Mori, S Montague, GB Nash, MR Douglas, EE Gardiner, RK Andrews, CD Buckley, P Harrison, SP Watson. CLEC-2 expression is maintained on activated platelets and on platelet microparticles. Blood 2014; 124(14): 2262–2270
https://doi.org/10.1182/blood-2014-05-572818 pmid: 25150298
17 M Naghavi, P Libby, E Falk, SW Casscells, S Litovsky, J Rumberger, JJ Badimon, C Stefanadis, P Moreno, G Pasterkamp, Z Fayad, PH Stone, S Waxman, P Raggi, M Madjid, A Zarrabi, A Burke, C Yuan, PJ Fitzgerald, DS Siscovick, CL de Korte, M Aikawa, KE Airaksinen, G Assmann, CR Becker, JH Chesebro, A Farb, ZS Galis, C Jackson, IK Jang, W Koenig, RA Lodder, K March, J Demirovic, M Navab, SG Priori, MD Rekhter, R Bahr, SM Grundy, R Mehran, A Colombo, E Boerwinkle, C Ballantyne, W Insull Jr, RS Schwartz, R Vogel, PW Serruys, GK Hansson, DP Faxon, S Kaul, H Drexler, P Greenland, JE Muller, R Virmani, PM Ridker, DP Zipes, PK Shah, JT Willerson. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. Circulation 2003; 108(15): 1772–1778
https://doi.org/10.1161/01.CIR.0000087481.55887.C9 pmid: 14557340
18 JD Schuijf, D Poldermans, LJ Shaw, JW Jukema, HJ Lamb, A de Roos, W Wijns, EE van der Wall, JJ Bax. Diagnostic and prognostic value of non-invasive imaging in known or suspected coronary artery disease. Eur J Nucl Med Mol Imaging 2006; 33(1): 93–104
https://doi.org/10.1007/s00259-005-1965-y pmid: 16320016
19 SP Chao, WY Law, CJ Kuo, HF Hung, JJ Cheng, HM Lo, KG Shyu. The diagnostic accuracy of 256-row computed tomographic angiography compared with invasive coronary angiography in patients with suspected coronary artery disease. Eur Heart J 2010; 31(15): 1916–1923
https://doi.org/10.1093/eurheartj/ehq072 pmid: 20233790
20 S Goodacre, P Thokala, C Carroll, JW Stevens, J Leaviss, M Al Khalaf, P Collinson, F Morris, P Evans, J Wang. Systematic review, meta-analysis and economic modelling of diagnostic strategies for suspected acute coronary syndrome. Health Technol Assess 2013; 17(1): v–vi, 1–188
https://doi.org/10.3310/hta17010 pmid: 23331845
21 M Rubini Gimenez, R Twerenbold, C Mueller. Beyond cardiac troponin: recent advances in the development of alternative biomarkers for cardiovascular disease. Expert Rev Mol Diagn 2015; 15(4): 547–556
https://doi.org/10.1586/14737159.2015.1010519 pmid: 25676700
22 DA Gorog. Prognostic value of plasma fibrinolysis activation markers in cardiovascular disease. J Am Coll Cardiol 2010; 55(24): 2701–2709
https://doi.org/10.1016/j.jacc.2009.11.095 pmid: 20538163
23 EA Amsterdam, NK Wenger, RG Brindis, DE Casey Jr, TG Ganiats, DR Holmes Jr, AS Jaffe, H Jneid, RF Kelly, MC Kontos, GN Levine, PR Liebson, D Mukherjee, ED Peterson, MS Sabatine, RW Smalling, SJ Zieman; ACC/AHA Task Force Members; Society for Cardiovascular Angiography and Interventions and the Society of Thoracic Surgeons. 2014 AHA/ACC guideline for the management of patients with non-ST-elevation acute coronary syndromes: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 2014; 130(25): 2354–2394
https://doi.org/10.1161/CIR.0000000000000133 pmid: 25249586
24 EM Antman, DT Anbe, PW Armstrong, ER Bates, LA Green, M Hand, JS Hochman, HM Krumholz, FG Kushner, GA Lamas, CJ Mullany, JP Ornato, DL Pearle, MA Sloan, SC Smith Jr, JS Alpert, JL Anderson, DP Faxon, V Fuster, RJ Gibbons, G Gregoratos, JL Halperin, LF Hiratzka, SA Hunt, AK Jacobs; American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 1999 Guidelines for the Management of Patients With Acute Myocardial Infarction). ACC/AHA guidelines for the management of patients with ST-elevation myocardial infarction--executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 1999 Guidelines for the Management of Patients With Acute Myocardial Infarction). Circulation 2004; 110(5): 588–636
https://doi.org/10.1161/01.CIR.0000134791.68010.FA pmid: 15289388
25 SD Fihn, JC Blankenship, KP Alexander, JA Bittl, JG Byrne, BJ Fletcher, GC Fonarow, RA Lange, GN Levine, TM Maddox, SS Naidu, EM Ohman, PK Smith. 2014 ACC/AHA/AATS/PCNA/SCAI/STS focused update of the guideline for the diagnosis and management of patients with stable ischemic heart disease: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines, and the American Association for Thoracic Surgery, Preventive Cardiovascular Nurses Association, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons. J Am Coll Cardiol 2014; 64(18): 1929–1949
https://doi.org/10.1016/j.jacc.2014.07.017 pmid: 25077860
26 World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 2013; 310(20): 2191–2194
https://doi.org/10.1001/jama.2013.281053 pmid: 24141714
27 KA Fox, FA Anderson Jr, OH Dabbous, PG Steg, J López-Sendón, F Van de Werf, A Budaj, EP Gurfinkel, SG Goodman, D Brieger; GRACE investigators. Intervention in acute coronary syndromes: do patients undergo intervention on the basis of their risk characteristics? The Global Registry of Acute Coronary Events (GRACE). Heart 2007; 93(2): 177–182
https://doi.org/10.1136/hrt.2005.084830 pmid: 16757543
28 MS Anvari, MA Boroumand, A karimi, M Alidoosti, P Yazdanifard, M Shirzad, SH Abbasi, A Soleymani. Aortic and mitral valve atherosclerosis: predictive factors and associations with coronary atherosclerosis using Gensini score. Arch Med Res 2009; 40(2): 124–127
https://doi.org/10.1016/j.arcmed.2008.12.003 pmid: 19237022
29 P Seizer, C Fuchs, SN Ungern-Sternberg, D Heinzmann, H Langer, M Gawaz, AE May, T Geisler. Platelet-bound cyclophilin A in patients with stable coronary artery disease and acute myocardial infarction. Platelets 2016; 27(2): 155–158
pmid: 26084004
30 D Rath, M Chatterjee, O Borst, K Müller, H Langer, AF Mack, M Schwab, S Winter, M Gawaz, T Geisler. Platelet surface expression of stromal cell-derived factor-1 receptors CXCR4 and CXCR7 is associated with clinical outcomes in patients with coronary artery disease. J Thromb Haemost 2015; 13(5): 719–728
https://doi.org/10.1111/jth.12870 pmid: 25660395
31 R George, A Bhatt, J Narayani, JV Thulaseedharan, H Sivadasanpillai, JA Tharakan. Enhanced P-selectin expression on platelet––a marker of platelet activation, in young patients with angiographically proven coronary artery disease. Mol Cell Biochem 2016; 419(1-2): 125–133
https://doi.org/10.1007/s11010-016-2756-4 pmid: 27406211
32 F Kazama, J Nakamura, M Osada, O Inoue, M Oosawa, S Tamura, N Tsukiji, K Aida, A Kawaguchi, S Takizawa, M Kaneshige, S Tanaka, K Suzuki-Inoue, Y Ozaki. Measurement of soluble C-type lectin-like receptor 2 in human plasma. Platelets 2015; 26(8): 711–719
https://doi.org/10.3109/09537104.2015.1021319 pmid: 25856065
33 CE Hughes, U Sinha, A Pandey, JA Eble, CA O’Callaghan, SP Watson. Critical role for an acidic amino acid region in platelet signaling by the HemITAM (hemi-immunoreceptor tyrosine-based activation motif) containing receptor CLEC-2 (C-type lectin receptor-2). J Biol Chem 2013; 288(7): 5127–5135
https://doi.org/10.1074/jbc.M112.411462 pmid: 23264619
34 MK Kaneko, Y Kato, T Kitano, M Osawa. Conservation of a platelet activating domain of Aggrus/podoplanin as a platelet aggregation-inducing factor. Gene 2006; 378: 52–57
https://doi.org/10.1016/j.gene.2006.04.023 pmid: 16766141
35 H Payne, T Ponomaryov, SP Watson, A Brill. Mice with a deficiency in CLEC-2 are protected against deep vein thrombosis. Blood 2017; 129(14): 2013–2020
https://doi.org/10.1182/blood-2016-09-742999 pmid: 28104688
36 J Riedl, M Preusser, PM Nazari, F Posch, S Panzer, C Marosi, P Birner, J Thaler, C Brostjan, D Lötsch, W Berger, JA Hainfellner, I Pabinger, C Ay. Podoplanin expression in primary brain tumors induces platelet aggregation and increases risk of venous thromboembolism. Blood 2017; 129(13): 1831–1839
https://doi.org/10.1182/blood-2016-06-720714 pmid: 28073783
37 K Suzuki-Inoue. CLEC-2/podoplanin and thromboinflammation. Blood 2017; 129(14): 1896–1898
https://doi.org/10.1182/blood-2017-02-764670 pmid: 28385772
38 JR Hitchcock, CN Cook, S Bobat, EA Ross, A Flores-Langarica, KL Lowe, M Khan, CC Dominguez-Medina, S Lax, M Carvalho-Gaspar, S Hubscher, GE Rainger, M Cobbold, CD Buckley, TJ Mitchell, A Mitchell, ND Jones, N Van Rooijen, D Kirchhofer, IR Henderson, DH Adams, SP Watson, AF Cunningham. Inflammation drives thrombosis after Salmonella infection via CLEC-2 on platelets. J Clin Invest 2015; 125(12): 4429–4446
https://doi.org/10.1172/JCI79070 pmid: 26571395
39 O Inoue, K Hokamura, T Shirai, M Osada, N Tsukiji, K Hatakeyama, K Umemura, Y Asada, K Suzuki-Inoue, Y Ozaki. Vascular smooth muscle cells stimulate platelets and facilitate thrombus formation through platelet CLEC-2: implications in atherothrombosis. PLoS One 2015; 10(9): e0139357
https://doi.org/10.1371/journal.pone.0139357 pmid: 26418160
40 AM Kerrigan, KM Dennehy, D Mourão-Sá, I Faro-Trindade, JA Willment, PR Taylor, JA Eble, C Reis e Sousa, GD Brown. CLEC-2 is a phagocytic activation receptor expressed on murine peripheral blood neutrophils. J Immunol 2009; 182(7): 4150–4157
https://doi.org/10.4049/jimmunol.0802808 pmid: 19299712
41 Y Ozaki, S Tamura, K Suzuki-Inoue. New horizon in platelet function: with special reference to a recently-found molecule, CLEC-2. Thromb J 2016; 14(Suppl 1): 27
https://doi.org/10.1186/s12959-016-0099-8 pmid: 27766053
42 B Pamukcu, GYH Lip, V Snezhitskiy, E Shantsila. The CD40-CD40L system in cardiovascular disease. Ann Med 2011; 43(5): 331–340
https://doi.org/10.3109/07853890.2010.546362 pmid: 21244217
43 WS Choi, OH Jeon, DS Kim. CD40 ligand shedding is regulated by interaction between matrix metalloproteinase-2 and platelet integrin α(IIb)β(3). J Thromb Haemost 2010; 8(6): 1364–1371
https://doi.org/10.1111/j.1538-7836.2010.03837.x pmid: 20230421
44 C Heeschen, S Dimmeler, CW Hamm, MJ van den Brand, E Boersma, AM Zeiher, ML Simoons; CAPTURE Study Investigators. Soluble CD40 ligand in acute coronary syndromes. N Engl J Med 2003; 348(12): 1104–1111
https://doi.org/10.1056/NEJMoa022600 pmid: 12646667
45 P Napoleão, LB Cabral, M Selas, C Freixo, MC Monteiro, MB Criado, MC Costa, FJ Enguita, AM Viegas-Crespo, C Saldanha, MM Carmo, RC Ferreira, T Pinheiro. Stratification of ST-elevation myocardial infarction patients based on soluble CD40L longitudinal changes. Transl Res 2016; 176: 95–104
https://doi.org/10.1016/j.trsl.2016.04.005 pmid: 27172386
46 S Lindberg. Prognostic utility of the soluble CD40 ligand in acute coronary syndrome. Coron Artery Dis 2014; 25(7): 548–549
https://doi.org/10.1097/MCA.0000000000000155 pmid: 25248136
47 N Gerdes, T Seijkens, D Lievens, MJ Kuijpers, H Winkels, D Projahn, H Hartwig, L Beckers, RT Megens, L Boon, RJ Noelle, O Soehnlein, JW Heemskerk, C Weber, E Lutgens. Platelet CD40 exacerbates atherosclerosis by transcellular activation of endothelial cells and leukocytes. Arterioscler Thromb Vasc Biol 2016; 36(3): 482–490
https://doi.org/10.1161/ATVBAHA.115.307074 pmid: 26821950
48 D Lievens, A Zernecke, T Seijkens, O Soehnlein, L Beckers, IC Munnix, E Wijnands, P Goossens, R van Kruchten, L Thevissen, L Boon, RA Flavell, RJ Noelle, N Gerdes, EA Biessen, MJ Daemen, JW Heemskerk, C Weber, E Lutgens. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood 2010; 116(20): 4317–4327
https://doi.org/10.1182/blood-2010-01-261206 pmid: 20705757
49 PJ Mason, S Chakrabarti, AA Albers, S Rex, O Vitseva, S Varghese, JE Freedman. Plasma, serum, and platelet expression of CD40 ligand in adults with cardiovascular disease. Am J Cardiol 2005; 96(10): 1365–1369
https://doi.org/10.1016/j.amjcard.2005.07.039 pmid: 16275179
50 SP Levine, J Lindenfeld, JB Ellis, NM Raymond, LS Krentz. Increased plasma concentrations of platelet factor 4 in coronary artery disease: a measure of in vivo platelet activation and secretion. Circulation 1981; 64(3): 626–632
https://doi.org/10.1161/01.CIR.64.3.626 pmid: 6973419
51 WE Strauss, G Cella, AF Parisi, AA Sasahara. Serial studies of platelet factor 4 and beta thromboglobulin during exercise in patients with coronary artery disease. Am Heart J 1985; 110(2): 293–299
https://doi.org/10.1016/0002-8703(85)90147-4 pmid: 2411121
52 M Shechter, CN Bairey Merz, MJ Paul-Labrador, PK Shah, S Kaul. Plasma apolipoprotein B levels predict platelet-dependent thrombosis in patients with coronary artery disease. Cardiology 1999; 92(3): 151–155
https://doi.org/10.1159/000006964 pmid: 10754344
53 S Fichtlscherer, S De Rosa, H Fox, T Schwietz, A Fischer, C Liebetrau, M Weber, CW Hamm, T Röxe, M Müller-Ardogan, A Bonauer, AM Zeiher, S Dimmeler. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010; 107(5): 677–684
https://doi.org/10.1161/CIRCRESAHA.109.215566 pmid: 20595655
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[7] David P. Taggart. Contemporary coronary artery bypass grafting[J]. Front. Med., 2014, 8(4): 395-398.
[8] Zhiming Zhu, Peijian Wang, Shuangtao Ma. Metabolic hypertension: concept and practice[J]. Front Med, 2013, 7(2): 201-206.
[9] Jin Gao, Ben Panizza, Newell W. Johnson, Scott Coman, Alan R. Clough. Basic consideration of research strategies for head and neck cancer[J]. Front Med, 2012, 6(4): 339-353.
[10] Marie-Germaine Bousser. Stroke prevention: an update[J]. Front Med, 2012, 6(1): 22-34.
[11] Qin-Yan GAO, Hui-Min CHEN, Jing-Yuan FANG, Jian-Qiu SHENG, Ping ZHENG, Cheng-Gong YU, Bo JIANG, . The first year follow-up after colorectal adenoma polypectomy is important: A multiple-center study in symptomatic hospital-based individuals in China[J]. Front. Med., 2010, 4(4): 436-442.
[12] Wei HAN MM, Ming-Xing XIE MD, Qing LV MD, Xin-Fang WANG MD, Li ZHANG MM, . Assessment of global and regional left ventricular twist and displacement in anterior myocardial infarction using 2-dimensional strain imaging[J]. Front. Med., 2010, 4(1): 71-76.
[13] Chen WANG PhD, MD, Zhen-Guo ZHAI PhD, MD, Ying H. SHEN PhD, MD, Lan ZHAO PhD, MD, . Clinical and genetic risk factors for venous thromboembolism in Chinese population[J]. Front. Med., 2010, 4(1): 29-35.
[14] Jun-Jie XIAO MD, Yi-Han CHEN MD, PhD, . Prevalence of cardiovascular diseases in China[J]. Front. Med., 2010, 4(1): 16-20.
[15] Qiong DAI MD, Bei LIU MD, Yukai DU MM, . Meta-analysis of the risk factors of breast cancer concerning reproductive factors and oral contraceptive use[J]. Front. Med., 2009, 3(4): 452-458.
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