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The Characteristics and Roles of Advanced Oxidation Protein Products in Atherosclerosis

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Abstract

Advanced oxidation protein products (AOPPs) are novel biomarkers of oxidative damage to proteins and a novel class of inflammatory mediators. AOPPs can promote oxidative stress (OS) and inflammation and thus participate in many pathophysiological disease processes. Atherosclerosis is a chronic inflammatory disease of blood vessels that is characterized by low-density lipoprotein infiltration into the endothelial intima and the formation of atherosclerotic plaques. Inflammation and OS are established risk factors for the formation of atherosclerosis. Accumulated studies show that AOPPs can accelerate the progression of atherosclerosis through OS and inflammation. Additionally, AOPPs can accelerate the formation of atherosclerotic plaques by inhibiting high-density lipoprotein receptor scavenger receptor class B type I-mediated high-density lipoprotein cholesterol reverse transport, leading to metabolic disturbances. Some studies have suggested that plasma AOPPs levels are independently positively correlated with blood pressure and are also independent risk factors for cardiovascular disease. AOPPs can trigger oxidative bursts of neutrophils, monocytes and phagocytic cells, increase the generation of reactive oxygen species and promote the secretion of cytokines to accelerate endothelial cell injury. Detecting the levels and inhibiting the formation of AOPPs may provide a novel approach to monitor the progress and improve the prognosis of atherosclerosis.

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Abbreviations

AOPPs:

Advanced oxidation protein products

OS:

Oxidative stress

LDL:

Low-density lipoprotein

HDL:

High-density lipoprotein

SR-BI:

Scavenger receptor class B type I

HDL-C:

High-density lipoprotein cholesterol

CVD:

Cardiovascular disease

CRF:

Chronic renal failure

HAS:

Human serum albumin

FB:

Fibrinogen

HOCL:

Hypochlorous acid

NO:

Nitric oxide

ROS:

Reactive oxygen species

OH:

Hydroxyl radical

MPO:

Myeloperoxidase

CPR:

C-reactive protein

CAD:

Coronary artery disease

ABCA1:

ATP-binding cassette transporter A1

ABCG1:

ATP-binding cassette transporter G1

O2−:

Superoxide

H2O2 :

Peroxide ions

PPP:

Platelet poor plasma

WB:

Whole blood

ICAM-1:

Intercellular adhesion molecule-1

VSMCs:

Vascular smooth muscle cells

PD:

Peritoneal dialysis

HD:

Hemodialysis

SOD:

Superoxide dismutase

VC:

Vascular calcification

RCT:

Reverse cholesterol transport

VEGF:

Vascular endothelial growth factor

VCAM-1:

Vascular cellular adhesion molecule 1

HASMCs:

Human umbilical smooth muscle cells

References

  1. Mangge, H., Becker, K., Fuchs, D., & Gostner, J. M. (2014). Antioxidants, inflammation and cardiovascular disease. World Journal of Cardiology, 6, 462–477.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hansson, G. K. (2005). Inflammation, atherosclerosis, and coronary artery disease. New England Journal of Medicine, 352, 1685–1695.

    Article  CAS  PubMed  Google Scholar 

  3. Vasdev, S., Gill, V., & Singal, P. (2007). Role of advanced glycation end products in hypertension and atherosclerosis: Therapeutic implications. Cell Biochemistry and Biophysics, 49, 48–63.

    Article  CAS  PubMed  Google Scholar 

  4. Jamkhande, P. G., Chandak, P. G., Dhawale, S. C., Barde, S. R., Tidke, P. S., & Sakhare, R. S. (2014). Therapeutic approaches to drug targets in atherosclerosis. Saudi Pharmaceutical Journal, 22, 179–190.

    Article  PubMed  Google Scholar 

  5. Bandeali, S., & Farmer, J. (2012). High-density lipoprotein and atherosclerosis: The role of antioxidant activity. Current Atherosclerosis Reports, 14, 101–107.

    Article  CAS  PubMed  Google Scholar 

  6. Witko-Sarsat, V., Friedlander, M., Capeillere-Blandin, C., Nguyen-Khoa, T., Nguyen, A. T., Zingraff, J., et al. (1996). Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney International, 49, 1304–1313.

    Article  CAS  PubMed  Google Scholar 

  7. Piwowar, A. (2010). Advanced oxidation protein products. Part I. Mechanism of the formation, characteristics and property. Polski Merkuriusz Lekarski, 28, 166–169.

    CAS  PubMed  Google Scholar 

  8. Selmeci, L. (2011). Advanced oxidation protein products (AOPP): Novel uremic toxins, or components of the non-enzymatic antioxidant system of the plasma proteome? Free Radical Research, 45, 1115–1123.

    Article  CAS  PubMed  Google Scholar 

  9. Selmeci, L., Szekely, M., Soos, P., Seres, L., Klinga, N., Geiger, A., & Acsady, G. (2006). Human blood plasma advanced oxidation protein products (AOPP) correlates with fibrinogen levels. Free Radical Research, 40, 952–958.

    Article  CAS  PubMed  Google Scholar 

  10. Witko-Sarsat, V., Friedlander, M., Nguyen, K. T., Capeillere-Blandin, C., Nguyen, A. T., Canteloup, S., et al. (1998). Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. The Journal of Immunology, 161, 2524–2532.

    CAS  PubMed  Google Scholar 

  11. Valente, A. J., Yoshida, T., Clark, R. A., Delafontaine, P., Siebenlist, U., & Chandrasekar, B. (2013). Advanced oxidation protein products induce cardiomyocyte death via Nox2/Rac1/superoxide-dependent TRAF3IP2/JNK signaling. Free Radical Biology and Medicine, 60, 125–135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Halliwell, B. (1988). Albumin—An important extracellular antioxidant? Biochemical Pharmacology, 37, 569–571.

    Article  CAS  PubMed  Google Scholar 

  13. Sciskalska, M., Zalewska, M., Grzelak, A., & Milnerowicz, H. (2014). The influence of the occupational exposure to heavy metals and tobacco smoke on the selected oxidative stress markers in smelters. Biological Trace Element Research, 159, 59–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Anraku, M., Chuang, V. T., Maruyama, T., & Otagiri, M. (2013). Redox properties of serum albumin. Biochimica et Biophysica Acta, 1830, 5465–5472.

    Article  CAS  PubMed  Google Scholar 

  15. Himmelfarb, J., & McMonagle, E. (2001). Albumin is the major plasma protein target of oxidant stress in uremia. Kidney International, 60, 358–363.

    Article  CAS  PubMed  Google Scholar 

  16. Liu, B., Hou, X., Zhou, Q., Tian, J., Zhu, P., Xu, J., et al. (2011). Detection of advanced oxidation protein products in patients with chronic kidney disease by a novel monoclonal antibody. Free Radical Research, 45, 662–671.

    Article  CAS  PubMed  Google Scholar 

  17. Torbitz, V. D., Bochi, G. V., de Carvalho, J. A., de Almeida, V. R., Da, S. J., & Moresco, R. N. (2015). In vitro oxidation of fibrinogen promotes functional alterations and formation of advanced oxidation protein products, an inflammation mediator. Inflammation, 38, 1201–1206.

    Article  CAS  PubMed  Google Scholar 

  18. Liu, S. X., Hou, F. F., Guo, Z. J., Nagai, R., Zhang, W. R., Liu, Z. Q., et al. (2006). Advanced oxidation protein products accelerate atherosclerosis through promoting oxidative stress and inflammation. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 1156–1162.

    Article  CAS  PubMed  Google Scholar 

  19. Bochi, G. V., Torbitz, V. D., de Campos, L. P., Sangoi, M. B., Fernandes, N. F., Gomes, P., et al. (2016). In vitro oxidation of collagen promotes the formation of advanced oxidation protein products and the activation of human neutrophils. Inflammation, 39, 916–927.

    Article  CAS  PubMed  Google Scholar 

  20. Bochi, G. V., Torbitz, V. D., Cargnin, L. P., de Carvalho, J. A., Gomes, P., & Moresco, R. N. (2014). An alternative pathway through the Fenton reaction for the formation of advanced oxidation protein products, a new class of inflammatory mediators. Inflammation, 37, 512–521.

    Article  CAS  PubMed  Google Scholar 

  21. Capeillere-Blandin, C., Gausson, V., Descamps-Latscha, B., & Witko-Sarsat, V. (2004). Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochimica et Biophysica Acta, 1689, 91–102.

    Article  CAS  PubMed  Google Scholar 

  22. Heinecke, J. W., Li, W., Daehnke, H. R., & Goldstein, J. A. (1993). Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. Journal of Biological Chemistry, 268, 4069–4077.

    CAS  PubMed  Google Scholar 

  23. Ohkubo, Y., Kishikawa, H., Araki, E., Miyata, T., Isami, S., Motoyoshi, S., et al. (1995). Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: A randomized prospective 6-year study. Diabetes Research and Clinical Practice, 28, 103–117.

    Article  CAS  PubMed  Google Scholar 

  24. Witko, V., Nguyen, A. T., & Descamps-Latscha, B. (1992). Microtiter plate assay for phagocyte-derived taurine-chloramines. Journal of Clinical Laboratory Analysis, 6, 47–53.

    Article  CAS  PubMed  Google Scholar 

  25. Anderstam, B., Ann-Christin, B. H., Valli, A., Stenvinkel, P., Lindholm, B., & Suliman, M. E. (2008). Modification of the oxidative stress biomarker AOPP assay: Application in uremic samples. Clinica Chimica Acta, 393, 114–118.

    Article  CAS  Google Scholar 

  26. Valli, A., Suliman, M. E., Meert, N., Vanholder, R., Lindholm, B., Stenvinkel, P., et al. (2007). Overestimation of advanced oxidation protein products in uremic plasma due to presence of triglycerides and other endogenous factors. Clinica Chimica Acta, 379, 87–94.

    Article  CAS  Google Scholar 

  27. Witko-Sarsat, V., & Descamps-Latscha, B. (1997). Advanced oxidation protein products: Novel uraemic toxins and pro-inflammatory mediators in chronic renal failure? Nephrology, Dialysis, Transplantation, 12, 1310–1312.

    Article  CAS  PubMed  Google Scholar 

  28. Iwao, Y., Anraku, M., Hiraike, M., Kawai, K., Nakajou, K., Kai, T., et al. (2006). The structural and pharmacokinetic properties of oxidized human serum albumin, advanced oxidation protein products (AOPP). Drug Metabolism and Pharmacokinetics, 21, 140–146.

    Article  CAS  PubMed  Google Scholar 

  29. Matteucci, E., Biasci, E., & Giampietro, O. (2001). Advanced oxidation protein products in plasma: Stability during storage and correlation with other clinical characteristics. Acta Diabetologica, 38, 187–189.

    Article  CAS  PubMed  Google Scholar 

  30. Kadowaki, D., Anraku, M., Sakaya, M., Hirata, S., Maruyama, T., & Otagiri, M. (2015). Olmesartan protects endothelial cells against oxidative stress-mediated cellular injury. Clinical and Experimental Nephrology, 19, 1007–1014.

    Article  CAS  PubMed  Google Scholar 

  31. Suzuki, M., Minami, A., Nakanishi, A., Kobayashi, K., Matsuda, S., Ogura, Y., & Kitagishi, Y. (2014). Atherosclerosis and tumor suppressor molecules (Review). International Journal of Molecular Medicine, 34, 934–940.

    CAS  PubMed  Google Scholar 

  32. Komosinska-Vassev, K., Olczyk, P., Winsz-Szczotka, K., Kuznik-Trocha, K., Klimek, K., & Olczyk, K. (2012). Age- and gender-related alteration in plasma advanced oxidation protein products (AOPP) and glycosaminoglycan (GAG) concentrations in physiological ageing. Clinical Chemistry and Laboratory Medicine, 50, 557–563.

    Article  CAS  PubMed  Google Scholar 

  33. Yang, X. B., Hou, F. F., Wu, Q., Zhou, H., Liu, Z. R., Yang, Y., & Zhang, X. (2005). Increased levels of advanced oxidation protein products are associated with atherosclerosis in chronic kidney disease. Zhonghua Nei Ke Za Zhi, 44, 342–346.

    CAS  PubMed  Google Scholar 

  34. Peng, K. F., Wu, X. F., Zhao, H. W., & Sun, Y. (2006). Advanced oxidation protein products induce monocyte chemoattractant protein-1 expression via p38 mitogen-activated protein kinase activation in rat vascular smooth muscle cells. Chinese Medical Journal, 119, 1088–1093.

    CAS  PubMed  Google Scholar 

  35. Descamps-Latscha, B., Witko-Sarsat, V., Nguyen-Khoa, T., Nguyen, A. T., Gausson, V., Mothu, N., et al. (2005). Advanced oxidation protein products as risk factors for atherosclerotic cardiovascular events in nondiabetic predialysis patients. American Journal of Kidney Diseases, 45, 39–47.

    Article  CAS  PubMed  Google Scholar 

  36. Kaneda, H., Taguchi, J., Ogasawara, K., Aizawa, T., & Ohno, M. (2002). Increased level of advanced oxidation protein products in patients with coronary artery disease. Atherosclerosis, 162, 221–225.

    Article  CAS  PubMed  Google Scholar 

  37. Mo, Z. C., Xiao, J., Tang, S. L., Ouyang, X. P., He, P. P., Lv, Y. C., et al. (2014). Advanced oxidation protein products exacerbates lipid accumulation and atherosclerosis through downregulation of ATP-binding cassette transporter A1 and G1 expression in apolipoprotein E knockout mice. Circulation Journal, 78, 2760–2770.

    Article  PubMed  Google Scholar 

  38. Guo, Z. J., Hou, F. F., Liu, S. X., Zhang, W. R., Zhou, Z. M., & Liu, Z. Q. (2004). Proteins modified with glycation or oxidation products accelerate atherosclerosis in experimental hypercholesterolemic rabbits. Beijing Da Xue Xue Bao, 36, 127–130.

    CAS  PubMed  Google Scholar 

  39. Chen, S., Liu, L., Sun, X., Liu, Y., & Song, T. (2005). Captopril restores endothelium-dependent relaxation induced by advanced oxidation protein products in rat aorta. Journal of Cardiovascular Pharmacology, 46, 803–809.

    Article  CAS  PubMed  Google Scholar 

  40. Piwowar, A. (2010). Advanced oxidation protein products. Part II. The significance of oxidation protein products in the pathomechanism of diabetes and its complications. Polski Merkuriusz Lekarski, 28, 227–230.

    CAS  PubMed  Google Scholar 

  41. Skvarilova, M., Bulava, A., Stejskal, D., Adamovska, S., & Bartek, J. (2005). Increased level of advanced oxidation products (AOPP) as a marker of oxidative stress in patients with acute coronary syndrome. Biomedical papers of the Medical Faculty of the University Palacký, Olomouc, Czechoslovakia Republic, 149, 83–87.

    Article  CAS  Google Scholar 

  42. Sugiura, T., Dohi, Y., Yamashita, S., Hirowatari, Y., Fujii, S., & Ohte, N. (2016). Serotonin in peripheral blood reflects oxidative stress and plays a crucial role in atherosclerosis: Novel insights toward holistic anti-atherothrombotic strategy. Atherosclerosis, 246, 157–160.

    Article  CAS  PubMed  Google Scholar 

  43. Liang, M., Wang, J., Xie, C., Yang, Y., Tian, J. W., Xue, Y. M., & Hou, F. F. (2014). Increased plasma advanced oxidation protein products is an early marker of endothelial dysfunction in type 2 diabetes patients without albuminuria. Journal of Diabetes, 6, 417–426.

    Article  CAS  PubMed  Google Scholar 

  44. Kocak, H., Gumuslu, S., Sahin, E., Ceken, K., Gocmen, Y. A., Yakupoglu, G., et al. (2009). Advanced oxidative protein products are independently associated with endothelial function in peritoneal dialysis patients. Nephrology (Carlton), 14, 273–280.

    Article  CAS  Google Scholar 

  45. Yuan, F., Liu, S. X., & Tian, J. W. (2004). Advanced oxidation protein products induce reactive oxygen species production in endothelial cells. Di Yi Jun Yi Da Xue Xue Bao, 24, 1350–1352.

    CAS  PubMed  Google Scholar 

  46. Piwowar, A. (2014). Biochemical and clinical aspects of advanced oxidation protein products in kidney diseases and metabolic disturbances. Postepy Higieny i Medycyny Doswiadczalnej (Online), 68, 179–190.

    Article  Google Scholar 

  47. Descamps-Latscha, B., & Witko-Sarsat, V. (2003). Oxidative stress in chronic renal failure and hemodialysis. Nephrologie, 24, 377–379.

    CAS  PubMed  Google Scholar 

  48. Krasniak, A., Drozdz, M., Pasowicz, M., Chmiel, G., Kowalczyk-Michalek, M., Szumilak, D., et al. (2007). Influence of microinflammation and oxidative stress on atherosclerosis progression and calcifications in cardiovascular system of hemodialyzed patients during two years follow-up. Przeglad Lekarski, 64, 140–147.

    PubMed  Google Scholar 

  49. Marsche, G., Frank, S., Hrzenjak, A., Holzer, M., Dirnberger, S., Wadsack, C., et al. (2009). Plasma-advanced oxidation protein products are potent high-density lipoprotein receptor antagonists in vivo. Circulation Research, 104, 750–757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zadrazil, J., Horak, P., Strebl, P., Krejci, K., Kajabova, M., Schneiderka, P., et al. (2012). In vivo oxidized low-density lipoprotein (ox-LDL) aopp and tas after kidney transplantation: A prospective, randomized one year study comparing cyclosporine A and tacrolimus based regiments. Biomedical papers of the Medical Faculty of the University Palacky, Olomouc, Czechoslovakia Republic, 156, 14–20.

    Article  CAS  Google Scholar 

  51. Le Bras, M., Clement, M. V., Pervaiz, S., & Brenner, C. (2005). Reactive oxygen species and the mitochondrial signaling pathway of cell death. Histology and Histopathology, 20, 205–219.

    PubMed  Google Scholar 

  52. Sun, N., Yang, L., Li, Y., Cheng, Y., Zhang, Z., & Cai, D. (2013). Advanced oxidation protein products inhibit proliferation and differentiation of rat osteoblasts through oxidative stress. Nan Fang Yi Ke Da Xue Xue Bao, 33, 356–359.

    CAS  PubMed  Google Scholar 

  53. Witko-Sarsat, V., Gausson, V., & Descamps-Latscha, B. (2003). Are advanced oxidation protein products potential uremic toxins? Kidney International, 84, S11–S14.

    Article  CAS  Google Scholar 

  54. Witko-Sarsat, V., Gausson, V., Nguyen, A. T., Touam, M., Drueke, T., Santangelo, F., & Descamps-Latscha, B. (2003). AOPP-induced activation of human neutrophil and monocyte oxidative metabolism: A potential target for N-acetylcysteine treatment in dialysis patients. Kidney International, 64, 82–91.

    Article  CAS  PubMed  Google Scholar 

  55. Werner-Felmayer, G., Werner, E. R., Fuchs, D., Hausen, A., Reibnegger, G., & Wachter, H. (1989). Tumour necrosis factor-alpha and lipopolysaccharide enhance interferon-induced tryptophan degradation and pteridine synthesis in human cells. Biological Chemistry Hoppe-Seyler, 370, 1063–1069.

    Article  CAS  PubMed  Google Scholar 

  56. Sugioka, K., Naruko, T., Matsumura, Y., Shirai, N., Hozumi, T., Yoshiyama, M., & Ueda, M. (2010). Neopterin and atherosclerotic plaque instability in coronary and carotid arteries. Journal of Atherosclerosis and Thrombosis, 17, 1115–1121.

    Article  CAS  PubMed  Google Scholar 

  57. Wirleitner, B., Reider, D., Ebner, S., Bock, G., Widner, B., Jaeger, M., et al. (2002). Monocyte-derived dendritic cells release neopterin. Journal of Leukocyte Biology, 72, 1148–1153.

    CAS  PubMed  Google Scholar 

  58. Fuchs, D., Avanzas, P., Arroyo-Espliguero, R., Jenny, M., Consuegra-Sanchez, L., & Kaski, J. C. (2009). The role of neopterin in atherogenesis and cardiovascular risk assessment. Current Medicinal Chemistry, 16, 4644–4653.

    Article  CAS  PubMed  Google Scholar 

  59. Murr, C., Winklhofer-Roob, B. M., Schroecksnadel, K., Maritschnegg, M., Mangge, H., Bohm, B. O., et al. (2009). Inverse association between serum concentrations of neopterin and antioxidants in patients with and without angiographic coronary artery disease. Atherosclerosis, 202, 543–549.

    Article  CAS  PubMed  Google Scholar 

  60. Adachi, T., Naruko, T., Itoh, A., Komatsu, R., Abe, Y., Shirai, N., et al. (2007). Neopterin is associated with plaque inflammation and destabilisation in human coronary atherosclerotic lesions. Heart, 93, 1537–1541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Cirillo, P., Pacileo, M., de Rosa, S., Calabro, P., Gargiulo, A., Angri, V., et al. (2006). Neopterin induces pro-atherothrombotic phenotype in human coronary endothelial cells. Journal of Thrombosis and Haemostasis, 4, 2248–2255.

    Article  CAS  PubMed  Google Scholar 

  62. Libby, P., Ridker, P. M., & Maseri, A. (2002). Inflammation and atherosclerosis. Circulation, 105, 1135–1143.

    Article  CAS  PubMed  Google Scholar 

  63. Matuszkiewicz-Rowinska, J. (2002). The association between malnutrition, inflammation, and atherosclerosis in chronic renal failure. Polskie Archiwum Medycyny Wewnetrznej, 108, 901–905.

    PubMed  Google Scholar 

  64. Henaut, L., Sanchez-Nino, M. D., Aldamiz-Echevarria, C. G., Sanz, A. B., & Ortiz, A. (2016). Targeting local vascular and systemic consequences of inflammation on vascular and cardiac valve calcification. Expert Opinion on Therapeutic Targets, 20, 89–105.

    Article  CAS  PubMed  Google Scholar 

  65. Frostegard, J. (2013). Immunity, atherosclerosis and cardiovascular disease. BMC Medicine, 11, 117.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Conti, P., & Shaik-Dasthagirisaeb, Y. (2015). Atherosclerosis: A chronic inflammatory disease mediated by mast cells. Central European Journal of Immunology, 40, 380–386.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Descamps-Latscha, B., & Witko-Sarsat, V. (2001). Importance of oxidatively modified proteins in chronic renal failure. Kidney International, 78, S108–S113.

    Article  CAS  PubMed  Google Scholar 

  68. Kirichenko, T. V., Sobenin, I. A., Nikolic, D., Rizzo, M., & Orekhov, A. N. (2015). Anti-cytokine therapy for prevention of atherosclerosis. Phytomedicine. doi:10.1016/j.phymed.2015.12.002.

    PubMed  Google Scholar 

  69. Krzystek-Korpacka, M., Neubauer, K., Berdowska, I., Boehm, D., Zielinski, B., Petryszyn, P., et al. (2008). Enhanced formation of advanced oxidation protein products in IBD. Inflammatory Bowel Diseases, 14, 794–802.

    Article  PubMed  Google Scholar 

  70. Tesarova, P., Kalousova, M., Trnkova, B., Soukupova, J., Argalasova, S., Mestek, O., et al. (2007). Carbonyl and oxidative stress in patients with breast cancer—Is there a relation to the stage of the disease? Neoplasma, 54, 219–224.

    CAS  PubMed  Google Scholar 

  71. Fenyo, I. M., & Gafencu, A. V. (2013). The involvement of the monocytes/macrophages in chronic inflammation associated with atherosclerosis. Immunobiology, 218, 1376–1384.

    Article  CAS  PubMed  Google Scholar 

  72. Rolin, J., & Maghazachi, A. A. (2014). Implications of chemokines, chemokine receptors, and inflammatory lipids in atherosclerosis. Journal of Leukocyte Biology, 95, 575–585.

    Article  PubMed  CAS  Google Scholar 

  73. Zernecke, A., & Weber, C. (2014). Chemokines in atherosclerosis: Proceedings resumed. Arteriosclerosis, Thrombosis, and Vascular Biology, 34, 742–750.

    Article  CAS  PubMed  Google Scholar 

  74. Shi, C. H., Jiang, Y. N., Shan, L. J., Lu, Y., Zhang, Y., & Gao, Y. G. (2013). Advanced oxidation protein products promote expression of stromal-cell derived factor-1alpha of ECV304 cells through ERK signal pathway. Zhongguo Ying Yong Sheng Li Xue Za Zhi, 29, 142–146.

    PubMed  Google Scholar 

  75. Kalousova, M., Zima, T., Tesar, V., & Lachmanova, J. (2002). Advanced glycation end products and advanced oxidation protein products in hemodialyzed patients. Blood Purification, 20, 531–536.

    Article  CAS  PubMed  Google Scholar 

  76. Hazell, L. J., Arnold, L., Flowers, D., Waeg, G., Malle, E., & Stocker, R. (1996). Presence of hypochlorite-modified proteins in human atherosclerotic lesions. Journal of Clinical Investigation, 97, 1535–1544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Chisolm, G. M., & Steinberg, D. (2000). The oxidative modification hypothesis of atherogenesis: An overview. Free Radical Biology and Medicine, 28, 1815–1826.

    Article  CAS  PubMed  Google Scholar 

  78. Yu, L., Cecil, J., Peng, S. B., Schrementi, J., Kovacevic, S., Paul, D., et al. (2006). Identification and expression of novel isoforms of human stromal cell-derived factor 1. Gene, 374, 174–179.

    Article  CAS  PubMed  Google Scholar 

  79. Juarez, J., Bendall, L., & Bradstock, K. (2004). Chemokines and their receptors as therapeutic targets: The role of the SDF-1/CXCR4 axis. Current Pharmaceutical Design, 10, 1245–1259.

    Article  CAS  PubMed  Google Scholar 

  80. Ma, Q., Jones, D., Borghesani, P. R., Segal, R. A., Nagasawa, T., Kishimoto, T., et al. (1998). Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proceedings of the National Academy of Sciences USA, 95, 9448–9453.

    Article  CAS  Google Scholar 

  81. Holvoet, P., Mertens, A., Verhamme, P., Bogaerts, K., Beyens, G., Verhaeghe, R., et al. (2001). Circulating oxidized LDL is a useful marker for identifying patients with coronary artery disease. Arteriosclerosis, Thrombosis, and Vascular Biology, 21, 844–848.

    Article  CAS  PubMed  Google Scholar 

  82. Fraley, A. E., & Tsimikas, S. (2006). Clinical applications of circulating oxidized low-density lipoprotein biomarkers in cardiovascular disease. Current Opinion in Lipidology, 17, 502–509.

    Article  CAS  PubMed  Google Scholar 

  83. Holvoet, P., Vanhaecke, J., Janssens, S., Van de Werf, F., & Collen, D. (1998). Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation, 98, 1487–1494.

    Article  CAS  PubMed  Google Scholar 

  84. Ferretti, G., Bacchetti, T., Masciangelo, S., & Bicchiega, V. (2010). HDL-paraoxonase and membrane lipid peroxidation: A comparison between healthy and obese subjects. Obesity (Silver Spring), 18, 1079–1084.

    Article  CAS  Google Scholar 

  85. Zelzer, S., Fuchs, N., Almer, G., Raggam, R. B., Pruller, F., Truschnig-Wilders, M., et al. (2011). High density lipoprotein cholesterol level is a robust predictor of lipid peroxidation irrespective of gender, age, obesity, and inflammatory or metabolic biomarkers. Clinica Chimica Acta, 412, 1345–1349.

    Article  CAS  Google Scholar 

  86. Jun, H. J., Hoang, M. H., Lee, J. W., Yaoyao, J., Lee, J. H., Lee, D. H., et al. (2012). Iristectorigenin B isolated from Belamcanda chinensis is a liver X receptor modulator that increases ABCA1 and ABCG1 expression in macrophage RAW 264.7 cells. Biotechnology Letters, 34, 2213–2221.

    Article  CAS  PubMed  Google Scholar 

  87. Wang, J. C., Zhao, Y., Chen, S. J., Long, J., Jia, Q. Q., Zhai, J. D., et al. (2013). AOPPs induce MCP-1 expression by increasing ROS-mediated activation of the NF-kappaB pathway in rat mesangial cells: Inhibition by sesquiterpene lactones. Cellular Physiology and Biochemistry, 32, 1867–1877.

    Article  CAS  PubMed  Google Scholar 

  88. Zhang, J., Guo, T. T., Yang, L., Du, Q. S., Hua, J., Liu, R. Z., & Tang, X. (2012). Effect of arctiin on mouse podocyte epithelial-mesenchymal transition induced by advanced oxidation protein products. Nan Fang Yi Ke Da Xue Xue Bao, 32, 379–382.

    PubMed  Google Scholar 

  89. Avci, B., Akar, A., Bilgici, B., & Tuncel, O. K. (2012). Oxidative stress induced by 1.8 GHz radio frequency electromagnetic radiation and effects of garlic extract in rats. International Journal of Radiation Biology, 88, 799–805.

    Article  CAS  PubMed  Google Scholar 

  90. Camps, J., Marsillach, J., & Joven, J. (2009). The paraoxonases: Role in human diseases and methodological difficulties in measurement. Critical Reviews in Clinical Laboratory Sciences, 46, 83–106.

    Article  CAS  PubMed  Google Scholar 

  91. Esteghamati, A., Eskandari, D., Mirmiranpour, H., Noshad, S., Mousavizadeh, M., Hedayati, M., & Nakhjavani, M. (2013). Effects of metformin on markers of oxidative stress and antioxidant reserve in patients with newly diagnosed type 2 diabetes: A randomized clinical trial. Clinical Nutrition, 32, 179–185.

    Article  CAS  PubMed  Google Scholar 

  92. Bochi, G. V., Torbitz, V. D., Cargnin, L. P., Sangoi, M. B., Santos, R. C., Gomes, P., & Moresco, R. N. (2012). Fructose-1,6-bisphosphate and N-acetylcysteine attenuate the formation of advanced oxidation protein products, a new class of inflammatory mediators, in vitro. Inflammation, 35, 1786–1792.

    Article  CAS  PubMed  Google Scholar 

  93. Lazarova, M., Stejskal, D., Lacnak, B., Vaclavik, J., Adamovska, S., Ochmanova, R., et al. (2004). The antioxidant acetylcysteine reduces oxidative stress by decreasing level of AOPPs. Biomedical papers of the Medical Faculty of the University Palacky, Olomouc, Czechoslovakia Republic 148, 131–133.

    Article  CAS  PubMed  Google Scholar 

  94. Bordignon, M., Da Dalt, L., Marinelli, L., & Gabai, G. (2013). Advanced oxidation protein products are generated by bovine neutrophils and inhibit free radical production in vitro. The Veterinary Journal, 199, 162–168.

    Article  PubMed  CAS  Google Scholar 

  95. Rimm, E. B., Stampfer, M. J., Ascherio, A., Giovannucci, E., Colditz, G. A., & Willett, W. C. (1993). Vitamin E consumption and the risk of coronary heart disease in men. New England Journal of Medicine, 328, 1450–1456.

    Article  CAS  PubMed  Google Scholar 

  96. Stampfer, M. J., Hennekens, C. H., Manson, J. E., Colditz, G. A., Rosner, B., & Willett, W. C. (1993). Vitamin E consumption and the risk of coronary disease in women. New England Journal of Medicine, 328, 1444–1449.

    Article  CAS  PubMed  Google Scholar 

  97. Liu, J., Zhang, L., Ren, Y., Gao, Y., Kang, L., & Lu, S. (2016). Matrine inhibits the expression of adhesion molecules in activated vascular smooth muscle cells. Molecular Medicine Reports, 13, 2313–2319.

    CAS  PubMed  Google Scholar 

  98. Byeon, H. E., Park, B. K., Yim, J. H., Lee, H. K., Moon, E. Y., Rhee, D. K., & Pyo, S. (2012). Stereocalpin A inhibits the expression of adhesion molecules in activated vascular smooth muscle cells. International Immunopharmacology, 12, 315–325.

    Article  CAS  PubMed  Google Scholar 

  99. Kim, J. Y., Park, H. J., Um, S. H., Sohn, E. H., Kim, B. O., Moon, E. Y., et al. (2012). Sulforaphane suppresses vascular adhesion molecule-1 expression in TNF-alpha-stimulated mouse vascular smooth muscle cells: Involvement of the MAPK, NF-kappaB and AP-1 signaling pathways. Vascular Pharmacology, 56, 131–141.

    Article  CAS  PubMed  Google Scholar 

  100. Kishimoto, Y., Yoshida, H., & Kondo, K. (2016). Potential anti-atherosclerotic properties of astaxanthin. Marine Drugs, 14, 345.

    Article  Google Scholar 

  101. Owens, C. D. (2012). Statins and other agents for vascular inflammation. Journal of Vascular Surgery, 56, 1799–1806.

    Article  PubMed  Google Scholar 

  102. Huang, Y., Li, W., Dong, L., Li, R., & Wu, Y. (2013). Effect of statin therapy on the progression of common carotid artery intima-media thickness: An updated systematic review and meta-analysis of randomized controlled trials. Journal of Atherosclerosis and Thrombosis, 20, 108–121.

    Article  CAS  PubMed  Google Scholar 

  103. Profumo, E., Buttari, B., Saso, L., & Rigano, R. (2014). Pleiotropic effects of statins in atherosclerotic disease: Focus on the antioxidant activity of atorvastatin. Current Topics in Medicinal Chemistry, 14, 2542–2551.

    Article  CAS  PubMed  Google Scholar 

  104. Violi, F., Carnevale, R., Pastori, D., & Pignatelli, P. (2014). Antioxidant and antiplatelet effects of atorvastatin by Nox2 inhibition. Trends in Cardiovascular Medicine, 24, 142–148.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by financial support from the Natural Sciences Foundation of Hunan Province (2016JJ6133), the National Natural Sciences Foundation of China (81100211), the Science and Technology Plan Projects of Hengyang City (Nos. 2013KJ04 and 2014KS34), the Construct Program of the Key Discipline in Hunan Province (Basic Medicine Sciences in University of South China) and the Zhengxiang Scholar (Xiangyang Tang) Program of the University of South China.

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    1. Department of Histology and Embryology, Laboratory of Reproductive Medicine, University of South China, Hengyang, 421001, China

      Hanxiao Ou & Zhongcheng Mo

    2. Department of Anesthesiology, Loudi Central Hospital, Loudi, 417000, China

      Zhuping Huang

    3. Department of Anesthesiology, the Second Affiliated Hospital, University of South China, Hengyang, 421001, China

      Ji Xiao

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    1. Hanxiao Ou
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    Hanxiao Ou and Zhuping Huang have contributed equally to this work.

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    Ou, H., Huang, Z., Mo, Z. et al. The Characteristics and Roles of Advanced Oxidation Protein Products in Atherosclerosis. Cardiovasc Toxicol 17, 1–12 (2017). https://doi.org/10.1007/s12012-016-9377-8

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