Angiogenesis, Inflammation & Therapeutics | Online ISSN  2207-872X
REVIEWS   (Open Access)

Two Forms of C-Reactive Protein and Their Implication for Atherogenesis: Focus on Monomeric Form

Anastasia V. Poznyak 1*, Victoria A. Khotina 2, Anton Y Postnov 2, Vasily N. Sukhorukov 2, Nikolay Sadykhov 2, Alexander N. Orekhov 2*

+ Author Affiliations

Journal of Angiotherapy 8(1) 1-12 https://doi.org/10.25163/angiotherapy.819386

Submitted: 13 November 2023  Revised: 05 January 2024  Published: 22 January 2024 

Abstract

In this review, we discuss the role of C-reactive protein (CRP), a biomarker of inflammation, in the development of atherosclerosis. CRP exists in two forms: the native pentameric form (nCRP) and the non-native form (mCRP), which is formed during inflammatory processes. The article explores the functions of both forms in atherosclerosis. nCRP binds to molecules with uncoated phosphocholine groups and activates the classical complement pathway. It can bind to enzymatically-modified LDL (E-LDL) and ox-LDL, affecting their pro-inflammatory properties and reducing LDL oxidation. nCRP also interacts with endothelial cells and reduces the absorption of acetylated LDL by these cells. In contrast, mCRP, formed in the presence of pathological conditions, exhibits distinct pro-inflammatory characteristics. While the role of nCRP in atherosclerosis remains unclear in animal models, mCRP has been associated with inflammation and is found in atherosclerotic lesions. The study suggests that nCRP may have atheroprotective effects, while mCRP may contribute to the progression of atherosclerosis. Further research is needed to fully understand the complex mechanisms of CRP in atherosclerosis.

Keywords:  Atherosclerosis; C-reactive protein; Inflammation; CRP; Cardiovascular disease

References

Aday, A. W., & Ridker, P. M. (2018). Antiinflammatory Therapy in Clinical Care: The CANTOS Trial and Beyond. Frontiers in cardiovascular medicine, 5, 62. https://doi.org/10.3389/fcvm.2018.00062.

Agrawal, A., Gang, T. B., & Rusiñol, A. E. (2014). Recognition functions of pentameric C-reactive protein in cardiovascular disease. Mediators of inflammation, 2014, 319215. https://doi.org/10.1155/2014/319215

Agrawal, A., Hammond, D. J., Jr, & Singh, S. K. (2010). Atherosclerosis-related functions of C-reactive pro-tein. Cardiovascular & hematological disorders drug targets, 10(4), 235–240. https://doi.org/10.2174/187152910793743841

Ahmed, I., & Ismail, N. (2020). M1 and M2 Macrophages Polarization via mTORC1 Influences Innate Im-munity and Outcome of Ehrlichia Infection. Journal of cellular immunology, 2(3), 108–115. https://doi.org/10.33696/immunology.2.029

Akil, A., Gutiérrez-García, A. K., Guenter, R., Rose, J. B., Beck, A. W., Chen, H., & Ren, B. (2021). Notch Sig-naling in Vascular Endothelial Cells, Angiogenesis, and Tumor Progression: An Update and Prospective. Frontiers in cell and developmental biology, 9, 642352. https://doi.org/10.3389/fcell.2021.642352

Badimon, L., Padró, T., & Vilahur, G. (2012). Atherosclerosis, platelets and thrombosis in acute ischaemic heart disease. European heart journal. Acute cardiovascular care, 1(1), 60–74. https://doi.org/10.1177/2048872612441582

Badimon, L., Peña, E., Arderiu, G., Padró, T., Slevin, M., Vilahur, G., & Chiva-Blanch, G. (2018). C-Reactive Protein in Atherothrombosis and Angiogenesis. Frontiers in immunology, 9, 430. https://doi.org/10.3389/fimmu.2018.00430.

Bennett, M. R., Sinha, S., & Owens, G. K. (2016). Vascular Smooth Muscle Cells in Atherosclerosis. Circulation research, 118(4), 692–702. https://doi.org/10.1161/CIRCRESAHA.115.306361

Bian, F., Yang, X., Zhou, F., Wu, P. H., Xing, S., Xu, G., Li, W., Chi, J., Ouyang, C., Zhang, Y., Xiong, B., Li, Y., Zheng, T., Wu, D., Chen, X., & Jin, S. (2014). C-reactive protein promotes atherosclerosis by increasing LDL transcytosis across endothelial cells. British journal of pharmacology, 171(10), 2671–2684. https://doi.org/10.1111/bph.12616

Bisoendial, R. J., Kastelein, J. J., Levels, J. H., Zwaginga, J. J., van den Bogaard, B., Reitsma, P. H., Meijers, J. C., Hartman, D., Levi, M., & Stroes, E. S. (2005). Activation of inflammation and coagulation after infusion of C-reactive protein in humans. Circulation research, 96(7), 714–716. https://doi.org/10.1161/01.RES.0000163015.67711.AB

Boncler, M., Kehrel, B., Szewczyk, R., Stec-Martyna, E., Bednarek, R., Brodde, M., & Watala, C. (2018). Oxida-tion of C-reactive protein by hypochlorous acid leads to the formation of potent platelet activator. Interna-tional journal of biological macromolecules, 107(Pt B), 2701–2714. https://doi.org/10.1016/j.ijbiomac.2017.10.159

Boncler, M., Rywaniak, J., Szymanski, J., Potempa, L. A., Rychlik, B., & Watala, C. (2011). Modified C-reactive protein interacts with platelet glycoprotein Ibα. Pharmacological reports : PR, 63(2), 464–475. https://doi.org/10.1016/s1734-1140(11)70513-8

Boncler, M., Wu, Y., & Watala, C. (2019). The Multiple Faces of C-Reactive Protein-Physiological and Patho-physiological Implications in Cardiovascular Disease. Molecules (Basel, Switzerland), 24(11), 2062. https://doi.org/10.3390/molecules24112062

Boras, E., Slevin, M., Alexander, M. Y., Aljohi, A., Gilmore, W., Ashworth, J., Krupinski, J., Potempa, L. A., Al Abdulkareem, I., Elobeid, A., & Matou-Nasri, S. (2014). Monomeric C-reactive protein and Notch-3 co-operatively increase angiogenesis through PI3K signalling pathway. Cytokine, 69(2), 165–179. https://doi.org/10.1016/j.cyto.2014.05.027

Bottazzi, B., Garlanda, C., & Teixeira, M. M. (2019). Editorial: The Role of Pentraxins: From Inflammation, Tissue Repair and Immunity to Biomarkers. Frontiers in immunology, 10, 2817. https://doi.org/10.3389/fimmu.2019.02817

Braig, D., Nero, T. L., Koch, H. G., Kaiser, B., Wang, X., Thiele, J. R., Morton, C. J., Zeller, J., Kiefer, J., Potempa, L. A., Mellett, N. A., Miles, L. A., Du, X. J., Meikle, P. J., Huber-Lang, M., Stark, G. B., Parker, M. W., Peter, K., & Eisenhardt, S. U. (2017). Transitional changes in the CRP structure lead to the exposure of proinflammato-ry binding sites. Nature communications, 8, 14188. https://doi.org/10.1038/ncomms14188

Camaré, C., Pucelle, M., Nègre-Salvayre, A., & Salvayre, R. (2017). Angiogenesis in the atherosclerotic plaque. Redox biology, 12, 18–34. https://doi.org/10.1016/j.redox.2017.01.007

Chang, M. K., Hartvigsen, K., Ryu, J., Kim, Y., & Han, K. H. (2012). The pro-atherogenic effects of macro-phages are reduced upon formation of a complex between C-reactive protein and lysophosphatidylcholine. Journal of inflammation (London, England), 9(1), 42. https://doi.org/10.1186/1476-9255-9-42

Che Man, R., Sulaiman, N., Ishak, M. F., Bt Hj Idrus, R., Abdul Rahman, M. R., & Yazid, M. D. (2020). The Ef-fects of Pro-Inflammatory and Anti-Inflammatory Agents for the Suppression of Intimal Hyperplasia: An Evidence-Based Review. International journal of environmental research and public health, 17(21), 7825. https://doi.org/10.3390/ijerph17217825.

Di, X., Han, W., Liu, C. W., Ni, L., & Zhang, R. (2021). A systematic review and meta-analysis on the associa-tion between C-reactive protein levels and adverse limb events after revascularization in patients with periph-eral arterial disease. Journal of vascular surgery, 74(1), 317–326. https://doi.org/10.1016/j.jvs.2021.02.026

Eisenhardt, S. U., Starke, J., Thiele, J. R., Murphy, A., Björn Stark, G., Bassler, N., Sviridov, D., Winkler, K., & Peter, K. (2012). Pentameric CRP attenuates inflammatory effects of mmLDL by inhibiting mmLDL--monocyte interactions. Atherosclerosis, 224(2), 384–393. https://doi.org/10.1016/j.atherosclerosis.2012.07.039

Eisenhardt, S. U., Thiele, J. R., Bannasch, H., Stark, G. B., & Peter, K. (2009). C-reactive protein: how confor-mational changes influence inflammatory properties. Cell cycle (Georgetown, Tex.), 8(23), 3885–3892. https://doi.org/10.4161/cc.8.23.10068

Fernández-Bello, I., López-Longo, F. J., Arias-Salgado, E. G., Jiménez-Yuste, V., & Butta, N. V. (2013). Behçet's disease: new insight into the relationship between procoagulant state, endothelial activation/damage and dis-ease activity. Orphanet journal of rare diseases, 8, 81. https://doi.org/10.1186/1750-1172-8-81

Futosi, K., Fodor, S., & Mócsai, A. (2013). Neutrophil cell surface receptors and their intracellular signal transduction pathways. International immunopharmacology, 17(3), 638–650. https://doi.org/10.1016/j.intimp.2013.06.034

Gang, T. B., Hanley, G. A., & Agrawal, A. (2015). C-reactive protein protects mice against pneumococcal in-fection via both phosphocholine-dependent and phosphocholine-independent mechanisms. Infection and immunity, 83(5), 1845–1852. https://doi.org/10.1128/IAI.03058-14

Grufman, H., Gonçalves, I., Edsfeldt, A., Nitulescu, M., Persson, A., Nilsson, M., & Nilsson, J. (2014). Plasma levels of high-sensitive C-reactive protein do not correlate with inflammatory activity in carotid atheroscle-rotic plaques. Journal of internal medicine, 275(2), 127–133. https://doi.org/10.1111/joim.12133.

Harman, J. L., & Jørgensen, H. F. (2019). The role of smooth muscle cells in plaque stability: Therapeutic tar-geting potential. British journal of pharmacology, 176(19), 3741–3753. https://doi.org/10.1111/bph.14779

Head, B. P., Patel, H. H., & Insel, P. A. (2014). Interaction of membrane/lipid rafts with the cytoskeleton: im-pact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signal-ing. Biochimica et biophysica acta, 1838(2), 532–545. https://doi.org/10.1016/j.bbamem.2013.07.018

Heemskerk, N., & van Egmond, M. (2018). Monoclonal antibody-mediated killing of tumour cells by neu-trophils. European journal of clinical investigation, 48 Suppl 2(Suppl Suppl 2), e12962. https://doi.org/10.1111/eci.12962

Heuertz, R. M., Schneider, G. P., Potempa, L. A., & Webster, R. O. (2005). Native and modified C-reactive protein bind different receptors on human neutrophils. The international journal of biochemistry & cell biol-ogy, 37(2), 320–335. https://doi.org/10.1016/j.biocel.2004.07.002

Hirschfield, G. M., Gallimore, J. R., Kahan, M. C., Hutchinson, W. L., Sabin, C. A., Benson, G. M., Dhillon, A. P., Tennent, G. A., & Pepys, M. B. (2005). Transgenic human C-reactive protein is not proatherogenic in apolipoprotein E-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 102(23), 8309–8314. https://doi.org/10.1073/pnas.0503202102

Jaipuria, G., Leonov, A., Giller, K., Vasa, S. K., Jaremko, L., Jaremko, M., Linser, R., Becker, S., & Zweckstetter, M. (2017). Cholesterol-mediated allosteric regulation of the mitochondrial translocator protein structure. Nature communications, 8, 14893. https://doi.org/10.1038/ncomms14893

Kamath, D. Y., Xavier, D., Sigamani, A., & Pais, P. (2015). High sensitivity C-reactive protein (hsCRP) & car-diovascular disease: An Indian perspective. The Indian journal of medical research, 142(3), 261–268. https://doi.org/10.4103/0971-5916.166582

Karar, J., & Maity, A. (2011). PI3K/AKT/mTOR Pathway in Angiogenesis. Frontiers in molecular neuroscience, 4, 51. https://doi.org/10.3389/fnmol.2011.00051

Keshavarz-Motamed, Z., Saijo, Y., Majdouline, Y., Riou, L., Ohayon, J., & Cloutier, G. (2014). Coronary artery atherectomy reduces plaque shear strains: an endovascular elastography imaging study. Atherosclerosis, 235(1), 140–149. https://doi.org/10.1016/j.atherosclerosis.2014.04.022.

Khreiss, T., József, L., Potempa, L. A., & Filep, J. G. (2004). Conformational rearrangement in C-reactive pro-tein is required for proinflammatory actions on human endothelial cells. Circulation, 109(16), 2016–2022. https://doi.org/10.1161/01.CIR.0000125527.41598.68

Koike, T., Kitajima, S., Yu, Y., Nishijima, K., Zhang, J., Ozaki, Y., Morimoto, M., Watanabe, T., Bhakdi, S., Asa-da, Y., Chen, Y. E., & Fan, J. (2009). Human C-reactive protein does not promote atherosclerosis in transgenic rabbits. Circulation, 120(21), 2088–2094. https://doi.org/10.1161/CIRCULATIONAHA.109.872796

Kovacs, A., Tornvall, P., Nilsson, R., Tegnér, J., Hamsten, A., & Björkegren, J. (2007). Human C-reactive pro-tein slows atherosclerosis development in a mouse model with human-like hypercholesterolemia. Proceed-ings of the National Academy of Sciences of the United States of America, 104(34), 13768–13773. https://doi.org/10.1073/pnas.0706027104

Kürsat Kirkgöz. C-Reactive Protein in Atherosclerosis—More than a Biomarker, but not Just a Culprit. Rev. Cardiovasc. Med. 2023, 24(10), 297.https://doi.org/10.31083/j.rcm2410297

Lin, P., Ji, H. H., Li, Y. J., & Guo, S. D. (2021). Macrophage Plasticity and Atherosclerosis Therapy. Frontiers in molecular biosciences, 8, 679797. https://doi.org/10.3389/fmolb.2021.679797

Linton, M. F., Yancey, P. G., Davies, S. S., Jerome, W. G., Linton, E. F., Song, W. L., Doran, A. C., & Vickers, K. C. (2019). The Role of Lipids and Lipoproteins in Atherosclerosis. In K. R. Feingold (Eds.) et. al., Endotext. MDText.com, Inc.

Marchini, T., Mitre, L. S., & Wolf, D. (2021). Inflammatory Cell Recruitment in Cardiovascular Dis-ease. Frontiers in cell and developmental biology, 9, 635527. https://doi.org/10.3389/fcell.2021.635527

McFadyen, J. D., Kiefer, J., Braig, D., Loseff-Silver, J., Potempa, L. A., Eisenhardt, S. U., & Peter, K. (2018). Dissociation of C-Reactive Protein Localizes and Amplifies Inflammation: Evidence for a Direct Biological Role of C-Reactive Protein and Its Conformational Changes. Frontiers in immunology, 9, 1351. https://doi.org/10.3389/fimmu.2018.01351

Melnikov, I. S., Kozlov, S. G., Saburova, O. S., Avtaeva, Y. N., Prokofieva, L. V., & Gabbasov, Z. A. (2020). Current Position on the Role of Monomeric C-reactive Protein in Vascular Pathology and Atherothrombosis. Current pharmaceutical design, 26(1), 37–43. https://doi.org/10.2174/1381612825666191216144055.

Meuwissen, M., van der Wal, A. C., Niessen, H. W., Koch, K. T., de Winter, R. J., van der Loos, C. M., Ritters-ma, S. Z., Chamuleau, S. A., Tijssen, J. G., Becker, A. E., & Piek, J. J. (2006). Colocalisation of intraplaque C re-active protein, complement, oxidised low density lipoprotein, and macrophages in stable and unstable angina and acute myocardial infarction. Journal of clinical pathology, 59(2), 196–201. https://doi.org/10.1136/jcp.2005.027235

Molins, B., Peña, E., Vilahur, G., Mendieta, C., Slevin, M., & Badimon, L. (2008). C-reactive protein isoforms differ in their effects on thrombus growth. Arteriosclerosis, thrombosis, and vascular biology, 28(12), 2239–2246. https://doi.org/10.1161/ATVBAHA.108.174359

Muraille, E., Leo, O., & Moser, M. (2014). TH1/TH2 paradigm extended: macrophage polarization as an un-appreciated pathogen-driven escape mechanism?. Frontiers in immunology, 5, 603. https://doi.org/10.3389/fimmu.2014.00603

Musunuru, K., Kral, B. G., Blumenthal, R. S., Fuster, V., Campbell, C. Y., Gluckman, T. J., Lange, R. A., Topol, E. J., Willerson, J. T., Desai, M. Y., Davidson, M. H., & Mora, S. (2008). The use of high-sensitivity assays for C-reactive protein in clinical practice. Nature clinical practice. Cardiovascular medicine, 5(10), 621–635. https://doi.org/10.1038/ncpcardio1322

Nakamura, M., Fukukawa, T., Kitagawa, K., Nagai, Y., Hosomi, N., Minematsu, K., Uchiyama, S., Matsumoto, M., Miyamoto, Y., & for J-STARS collaborators (2018). Ten-year standardization of lipids and high-sensitivity C-reactive protein in a randomized controlled trial to assess the effects of statins on secondary stroke preven-tion: Japan Statin Treatment Against Recurrent Stroke. Annals of clinical biochemistry, 55(1), 128–135. https://doi.org/10.1177/0004563217693651

Nambiar, S. S., Shetty, N. P., Bhatt, P., & Neelwarne, B. (2014). Inhibition of LDL oxidation and oxidized LDL-induced foam cell formation in RAW 264.7 cells show anti-atherogenic properties of a foliar methanol extract of Scoparia dulcis. Pharmacognosy magazine, 10(Suppl 2), S240–S248. https://doi.org/10.4103/0973-1296.133241

Nehring, S. M., Goyal, A., & Patel, B. C. (2023). C Reactive Protein. In StatPearls. StatPearls Publishing.

O'Keefe, J. H., Carter, M. D., Lavie, C. J., & Bell, D. S. (2009). The gravity of JUPITER (Justification for the Use of Statins in Primary Prevention: An Intervention Trial Evaluating Rosuvastatin). Postgraduate medicine, 121(3), 113–118. https://doi.org/10.3810/pgm.2009.05.2010

Orekhov, A. N., Nikiforov, N. G., Sukhorukov, V. N., Kubekina, M. V., Sobenin, I. A., Wu, W. K., Foxx, K. K., Pintus, S., Stegmaier, P., Stelmashenko, D., Kel, A., Gratchev, A. N., Melnichenko, A. A., Wetzker, R., Summerhill, V. I., Manabe, I., & Oishi, Y. (2020). Role of Phagocytosis in the Pro-Inflammatory Response in LDL-Induced Foam Cell Formation; a Transcriptome Analysis. International journal of molecular sciences, 21(3), 817. https://doi.org/10.3390/ijms21030817

Pathak, A., Singh, S. K., Thewke, D. P., & Agrawal, A. (2020). Conformationally Altered C-Reactive Protein Capable of Binding to Atherogenic Lipoproteins Reduces Atherosclerosis. Frontiers in immunology, 11, 1780. https://doi.org/10.3389/fimmu.2020.01780

Patibandla, S., Gupta, K., & Alsayouri, K. (2023). Cardiac Biomarkers. In StatPearls. StatPearls Publishing.

Poznyak, A. V., Bharadwaj, D., Prasad, G., Grechko, A. V., Sazonova, M. A., & Orekhov, A. N. (2021). An-ti-Inflammatory Therapy for Atherosclerosis: Focusing on Cytokines. International journal of molecular sci-ences, 22(13), 7061. https://doi.org/10.3390/ijms22137061

Ridker P. M. (2016). From C-Reactive Protein to Interleukin-6 to Interleukin-1: Moving Upstream To Identi-fy Novel Targets for Atheroprotection. Circulation research, 118(1), 145–156. https://doi.org/10.1161/CIRCRESAHA.115.306656.

Saha, D., S, S., Sergeeva, E. G., Ionova, Z. I., & Gorbach, A. V. (2015). Tissue factor and atherothrombosis. Current pharmaceutical design, 21(9), 1152–1157. https://doi.org/10.2174/1381612820666141013154946.

Schwedler, S. B., Amann, K., Wernicke, K., Krebs, A., Nauck, M., Wanner, C., Potempa, L. A., & Galle, J. (2005). Native C-reactive protein increases whereas modified C-reactive protein reduces atherosclerosis in apolipo-protein E-knockout mice. Circulation, 112(7), 1016–1023. https://doi.org/10.1161/CIRCULATIONAHA.105.556530

Singh, S. K., & Agrawal, A. (2019). Functionality of C-Reactive Protein for Atheroprotection. Frontiers in immunology, 10, 1655. https://doi.org/10.3389/fimmu.2019.01655

Singh, S. K., Suresh, M. V., Hammond, D. J., Jr, Rusiñol, A. E., Potempa, L. A., & Agrawal, A. (2009). Binding of the monomeric form of C-reactive protein to enzymatically-modified low-density lipoprotein: effects of phosphoethanolamine. Clinica chimica acta; international journal of clinical chemistry, 406(1-2), 151–155. https://doi.org/10.1016/j.cca.2009.06.018.

Singh, S. K., Suresh, M. V., Prayther, D. C., Moorman, J. P., Rusiñol, A. E., & Agrawal, A. (2008). C-reactive protein-bound enzymatically modified low-density lipoprotein does not transform macrophages into foam cells. Journal of immunology (Baltimore, Md. : 1950), 180(6), 4316–4322. https://doi.org/10.4049/jimmunol.180.6.4316.

Slevin, M., Iemma, R. S., Zeinolabediny, Y., Liu, D., Ferris, G. R., Caprio, V., Phillips, N., Di Napoli, M., Guo, B., Zeng, X., AlBaradie, R., Binsaleh, N. K., McDowell, G., & Fang, W. H. (2018). Acetylcholine Inhibits Mon-omeric C-Reactive Protein Induced Inflammation, Endothelial Cell Adhesion, and Platelet Aggregation; A Potential Therapeutic?. Frontiers in immunology, 9, 2124. https://doi.org/10.3389/fimmu.2018.02124

Sproston, N. R., & Ashworth, J. J. (2018). Role of C-Reactive Protein at Sites of Inflammation and Infection. Frontiers in immunology, 9, 754. https://doi.org/10.3389/fimmu.2018.00754

Sproston, N. R., & Ashworth, J. J. (2018). Role of C-Reactive Protein at Sites of Inflammation and Infection. Frontiers in immunology, 9, 754. https://doi.org/10.3389/fimmu.2018.00754

Taskinen, S., Hyvönen, M., Kovanen, P. T., Meri, S., & Pentikäinen, M. O. (2005). C-reactive protein binds to the 3beta-OH group of cholesterol in LDL particles. Biochemical and biophysical research communications, 329(4), 1208–1216. https://doi.org/10.1016/j.bbrc.2005.02.091

Teupser, D., Weber, O., Rao, T. N., Sass, K., Thiery, J., & Fehling, H. J. (2011). No reduction of atherosclerosis in C-reactive protein (CRP)-deficient mice. The Journal of biological chemistry, 286(8), 6272–6279. https://doi.org/10.1074/jbc.M110.161414.

Thiele, J. R., Zeller, J., Bannasch, H., Stark, G. B., Peter, K., & Eisenhardt, S. U. (2015). Targeting C-Reactive Protein in Inflammatory Disease by Preventing Conformational Changes. Mediators of inflammation, 2015, 372432. https://doi.org/10.1155/2015/372432

Torzewski, M., Reifenberg, K., Cheng, F., Wiese, E., Küpper, I., Crain, J., Lackner, K. J., & Bhakdi, S. (2008). No effect of C-reactive protein on early atherosclerosis in LDLR-/- / human C-reactive protein transgenic mice. Thrombosis and haemostasis, 99(1), 196–201. https://doi.org/10.1160/TH07-10-0595.

Torzewski, M., Waqar, A. B., & Fan, J. (2014). Animal models of C-reactive protein. Mediators of inflammation, 2014, 683598. https://doi.org/10.1155/2014/683598

Wirtz, P. H., & von Känel, R. (2017). Psychological Stress, Inflammation, and Coronary Heart Disease. Cur-rent cardiology reports, 19(11), 111. https://doi.org/10.1007/s11886-017-0919-x.

Wu, M. Y., Li, C. J., Hou, M. F., & Chu, P. Y. (2017). New Insights into the Role of Inflammation in the Patho-genesis of Atherosclerosis. International journal of molecular sciences, 18(10), 2034. https://doi.org/10.3390/ijms18102034

Yousuf, O., Mohanty, B. D., Martin, S. S., Joshi, P. H., Blaha, M. J., Nasir, K., Blumenthal, R. S., & Budoff, M. J. (2013). High-sensitivity C-reactive protein and cardiovascular disease: a resolute belief or an elusive link?. Journal of the American College of Cardiology, 62(5), 397–408. https://doi.org/10.1016/j.jacc.2013.05.016

Yu, Q., Liu, Z., Waqar, A. B., Ning, B., Yang, X., Shiomi, M., Graham, M. J., Crooke, R. M., Liu, E., Dong, S., & Fan, J. (2014). Effects of antisense oligonucleotides against C-reactive protein on the development of athero-sclerosis in WHHL rabbits. Mediators of inflammation, 2014, 979132. https://doi.org/10.1155/2014/979132

Yu, Y., & Su, K. (2013). Neutrophil Extracellular Traps and Systemic Lupus Erythematosus. Journal of clinical & cellular immunology, 4, 139. https://doi.org/10.4172/2155-9899.1000139

Zha, Z., Cheng, Y., Cao, L., Qian, Y., Liu, X., Guo, Y., & Wang, J. (2021). Monomeric CRP Aggravates Myocar-dial Injury After Myocardial Infarction by Polarizing the Macrophage to Pro-Inflammatory Phenotype Through JNK Signaling Pathway. Journal of inflammation research, 14, 7053–7064. https://doi.org/10.2147/JIR.S316816

Zha, Z., Cheng, Y., Cao, L., Qian, Y., Liu, X., Guo, Y., & Wang, J. (2021). Monomeric CRP Aggravates Myocar-dial Injury After Myocardial Infarction by Polarizing the Macrophage to Pro-Inflammatory Phenotype Through JNK Signaling Pathway. Journal of inflammation research, 14, 7053–7064. https://doi.org/10.2147/JIR.S316816

PDF
Full Text
Export Citation

View Dimensions


View Plumx



View Altmetric



7
Save
0
Citation
555
View
0
Share