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Gene dysregulation in peripheral blood of moyamoya disease and comparison with other vascular disorders


Autoři: Xing Peng aff001;  Zhengshan Zhang aff003;  Dongqing Ye aff001;  Peiqi Xing aff001;  Zhengxing Zou aff003;  Hongxing Lei aff001;  Lian Duan aff003
Působiště autorů: CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China aff001;  University of Chinese Academy of Sciences, Beijing, China aff002;  Department of Neurosurgery, the Fifth Medical Center, Chinese PLA General Hospital, Beijing, China aff003;  Center of Alzheimer’s Disease, Beijing Institute for Brain Disorders, Beijing, China aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221811

Souhrn

Objective

Moyamoya disease (MMD) is a chronic occlusive cerebrovascular disease with unknown etiology, sharing many similar clinical symptoms with other vascular disorders. This study aimed to investigate gene dysregulation in peripheral blood of MMD and compare it with other vascular disorders.

Methods

Transcriptomic profiles of 12 MMD patients and 8 healthy controls were obtained using RNA sequencing. Differentially expressed genes (DEGs) were identified and several were validated by quantitative real-time PCR in independent samples. Biological pathway enrichment analysis of DEGs and deconvolution of leukocyte subsets in peripheral blood were performed. Expression profiles for other vascular diseases were downloaded from public database and consistent DEGs were calculated. Gene set enrichment analysis (GSEA) was conducted to compare gene dysregulation pattern between MMD and other vascular diseases.

Results

A total of 533 DEGs were identified for MMD. Up-regulated genes were mainly involved in extracellular matrix (ECM) organization, whereas down-regulated genes were primarily associated with inflammatory and immune responses. As for cell populations, significantly increased naïve B cells and naïve CD4 cells as well as obviously decreased resting natural killer cells were observed in peripheral blood of MMD patients. GSEA analysis indicated that only up-regulated genes of ischemic stroke and down-regulated genes of coronary artery disease and myocardial infarction were enriched in up-regulated and down-regulated genes of MMD, respectively.

Conclusion

Dysregulated genes in peripheral blood of MMD mainly played key roles in ECM organization, inflammatory and immune responses. This gene dysregulation pattern was specific compared with other vascular diseases. Besides, naïve B cells, naïve CD4 cells and resting natural killer cells were aberrantly disrupted in peripheral blood of MMD patients. These results will help elucidate the complicated pathogenic mechanism of MMD.

Klíčová slova:

Medicine and health sciences – Neurology – Brain diseases – Vascular medicine – Coronary heart disease – Cardiology – Myocardial infarction – Immunology – Immune response – Biology and life sciences – Anatomy – Body fluids – Blood – Physiology – Genetics – Gene expression – Genomics – Genome analysis – Gene ontologies – Cell biology – Cellular types – Animal cells – Blood cells – White blood cells – Immune cells – Computational biology


Zdroje

1. Suzuki J, Takaku A. Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Archives of neurology. 1969;20(3):288–99. Epub 1969/03/01. doi: 10.1001/archneur.1969.00480090076012 5775283.

2. Bao XY, Duan L, Yang WZ, Li DS, Sun WJ, Zhang ZS, et al. Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China. Cerebrovascular diseases (Basel, Switzerland). 2015;39(2):75–81. Epub 2015/01/13. doi: 10.1159/000369524 25573764.

3. Bao XY, Duan L, Li DS, Yang WZ, Sun WJ, Zhang ZS, et al. Clinical features, surgical treatment and long-term outcome in adult patients with Moyamoya disease in China. Cerebrovascular diseases (Basel, Switzerland). 2012;34(4):305–13. Epub 2012/11/14. doi: 10.1159/000343225 23146868.

4. Duan L, Bao XY, Yang WZ, Shi WC, Li DS, Zhang ZS, et al. Moyamoya disease in China: its clinical features and outcomes. Stroke. 2012;43(1):56–60. Epub 2011/10/25. doi: 10.1161/STROKEAHA.111.621300 22020027.

5. Miao W, Zhao PL, Zhang YS, Liu HY, Chang Y, Ma J, et al. Epidemiological and clinical features of Moyamoya disease in Nanjing, China. Clinical neurology and neurosurgery. 2010;112(3):199–203. Epub 2009/12/17. doi: 10.1016/j.clineuro.2009.11.009 20004511.

6. Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, et al. A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. Journal of human genetics. 2011;56(1):34–40. Epub 2010/11/05. doi: 10.1038/jhg.2010.132 21048783.

7. Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PloS one. 2011;6(7):e22542. Epub 2011/07/30. doi: 10.1371/journal.pone.0022542 21799892; PubMed Central PMCID: PMC3140517.

8. Zhang Q, Liu Y, Zhang D, Wang R, Zhang Y, Wang S, et al. RNF213 as the major susceptibility gene for Chinese patients with moyamoya disease and its clinical relevance. Journal of neurosurgery. 2017;126(4):1106–13. Epub 2016/04/30. doi: 10.3171/2016.2.JNS152173 27128593.

9. Wu Z, Jiang H, Zhang L, Xu X, Zhang X, Kang Z, et al. Molecular analysis of RNF213 gene for moyamoya disease in the Chinese Han population. PloS one. 2012;7(10):e48179. Epub 2012/10/31. doi: 10.1371/journal.pone.0048179 23110205; PubMed Central PMCID: PMC3479116.

10. Miyatake S, Miyake N, Touho H, Nishimura-Tadaki A, Kondo Y, Okada I, et al. Homozygous c.14576G>A variant of RNF213 predicts early-onset and severe form of moyamoya disease. Neurology. 2012;78(11):803–10. Epub 2012/03/02. doi: 10.1212/WNL.0b013e318249f71f 22377813.

11. Moteki Y, Onda H, Kasuya H, Yoneyama T, Okada Y, Hirota K, et al. Systematic Validation of RNF213 Coding Variants in Japanese Patients With Moyamoya Disease. Journal of the American Heart Association. 2015;4(5). Epub 2015/05/13. doi: 10.1161/jaha.115.001862 25964206; PubMed Central PMCID: PMC4599414.

12. Sonobe S, Fujimura M, Niizuma K, Nishijima Y, Ito A, Shimizu H, et al. Temporal profile of the vascular anatomy evaluated by 9.4-T magnetic resonance angiography and histopathological analysis in mice lacking RNF213: a susceptibility gene for moyamoya disease. Brain research. 2014;1552:64–71. Epub 2014/01/21. doi: 10.1016/j.brainres.2014.01.011 24440776.

13. Kim SJ, Heo KG, Shin HY, Bang OY, Kim GM, Chung CS, et al. Association of thyroid autoantibodies with moyamoya-type cerebrovascular disease: a prospective study. Stroke. 2010;41(1):173–6. Epub 2009/11/21. doi: 10.1161/STROKEAHA.109.562264 19926842.

14. Chen JB, Liu Y, Zhou LX, Sun H, He M, You C. Prevalence of autoimmune disease in moyamoya disease patients in Western Chinese population. Journal of the neurological sciences. 2015;351(1–2):184–6. Epub 2015/03/07. doi: 10.1016/j.jns.2015.02.037 25743224.

15. Bower RS, Mallory GW, Nwojo M, Kudva YC, Flemming KD, Meyer FB. Moyamoya disease in a primarily white, midwestern US population: increased prevalence of autoimmune disease. Stroke. 2013;44(7):1997–9. Epub 2013/05/09. doi: 10.1161/STROKEAHA.111.000307 23652271.

16. Mejia-Munne JC, Ellis JA, Feldstein NA, Meyers PM, Connolly ES. Moyamoya and Inflammation. World neurosurgery. 2017;100:575–8. Epub 2017/01/18. doi: 10.1016/j.wneu.2017.01.012 28093343.

17. Bersano A, Guey S, Bedini G, Nava S, Herve D, Vajkoczy P, et al. Research Progresses in Understanding the Pathophysiology of Moyamoya Disease. Cerebrovascular diseases (Basel, Switzerland). 2016;41(3–4):105–18. Epub 2016/01/13. doi: 10.1159/000442298 26756907.

18. Kang HS, Kim JH, Phi JH, Kim YY, Kim JE, Wang KC, et al. Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. Journal of neurology, neurosurgery, and psychiatry. 2010;81(6):673–8. Epub 2009/12/08. doi: 10.1136/jnnp.2009.191817 19965844.

19. Hojo M, Hoshimaru M, Miyamoto S, Taki W, Nagata I, Asahi M, et al. Role of transforming growth factor-beta1 in the pathogenesis of moyamoya disease. Journal of neurosurgery. 1998;89(4):623–9. Epub 1998/10/07. doi: 10.3171/jns.1998.89.4.0623 9761057.

20. Malek AM, Connors S, Robertson RL, Folkman J, Scott RM. Elevation of cerebrospinal fluid levels of basic fibroblast growth factor in moyamoya and central nervous system disorders. Pediatric neurosurgery. 1997;27(4):182–9. Epub 1998/05/13. doi: 10.1159/000121249 9577971.

21. Yoshimoto T, Houkin K, Takahashi A, Abe H. Angiogenic factors in moyamoya disease. Stroke. 1996;27(12):2160–5. Epub 1996/12/01. doi: 10.1161/01.str.27.12.2160 8969773.

22. Jiang T, Perry A, Dacey RG Jr., Zipfel GJ, Derdeyn CP. Intracranial atherosclerotic disease associated with moyamoya collateral formation: histopathological findings. Journal of neurosurgery. 2013;118(5):1030–4. Epub 2013/02/12. doi: 10.3171/2013.1.JNS12565 23394336; PubMed Central PMCID: PMC4598180.

23. Roder C, Peters V, Kasuya H, Nishizawa T, Takehara Y, Berg D, et al. Common genetic polymorphisms in moyamoya and atherosclerotic disease in Europeans. Child's nervous system: ChNS: official journal of the International Society for Pediatric Neurosurgery. 2011;27(2):245–52. Epub 2010/08/10. doi: 10.1007/s00381-010-1241-8 20694560.

24. Lee JH, Youn TJ, Yoon YE, Park JJ, Hong SJ, Chun EJ, et al. Coronary artery stenosis in moyamoya disease: tissue characterization by 256-slice multi-detector CT and virtual histology. Circulation. 2013;127(20):2063–5. Epub 2013/05/22. doi: 10.1161/CIRCULATIONAHA.112.136473 23690454.

25. Livesay J, Johnson J. ST-Elevation Myocardial Infarction (STEMI) in a Patient with Moyamoya Disease. Case reports in cardiology. 2019;2019:7124072. Epub 2019/03/14. doi: 10.1155/2019/7124072 30863645; PubMed Central PMCID: PMC6378792.

26. Murakami T, Ueno M, Takeda A, Yakuwa S, Kuroda S. Image in cardiovascular medicine. Multiple coronary stenosis in infantile Moyamoya disease. Circulation. 2009;119(12):1689. Epub 2009/04/01. doi: 10.1161/CIRCULATIONAHA.108.827782 19332482.

27. Nam TM, Jo KI, Yeon JY, Hong SC, Kim JS. Coronary heart disease in moyamoya disease: are they concomitant or coincidence? Journal of Korean medical science. 2015;30(4):470–4. Epub 2015/04/02. doi: 10.3346/jkms.2015.30.4.470 25829816; PubMed Central PMCID: PMC4366969.

28. St Goar FG, Gominak SC, Potkin BN. Bilateral aortoostial coronary artery disease: moyamoya of the heart? The American journal of cardiology. 1999;83(8):1296–9, a10. Epub 1999/04/24. doi: 10.1016/s0002-9149(99)00081-8 10215306.

29. Komiyama M, Nishikawa M, Yasui T, Otsuka M, Haze K. Moyamoya disease and coronary artery disease—case report. Neurologia medico-chirurgica. 2001;41(1):37–41. Epub 2001/02/24. doi: 10.2176/nmc.41.37 11218639.

30. Ikeda E. Systemic vascular changes in spontaneous occlusion of the circle of Willis. Stroke. 1991;22(11):1358–62. Epub 1991/11/01. doi: 10.1161/01.str.22.11.1358 1750042.

31. Aziz H, Zaas A, Ginsburg GS. Peripheral blood gene expression profiling for cardiovascular disease assessment. Genomic medicine. 2007;1(3–4):105–12. Epub 2008/10/17. doi: 10.1007/s11568-008-9017-x 18923935; PubMed Central PMCID: PMC2269039.

32. Barr TL, Conley Y, Ding J, Dillman A, Warach S, Singleton A, et al. Genomic biomarkers and cellular pathways of ischemic stroke by RNA gene expression profiling. Neurology. 2010;75(11):1009–14. Epub 2010/09/15. doi: 10.1212/WNL.0b013e3181f2b37f 20837969; PubMed Central PMCID: PMC2942033.

33. Huang CC, Lloyd-Jones DM, Guo X, Rajamannan NM, Lin S, Du P, et al. Gene expression variation between African Americans and whites is associated with coronary artery calcification: the multiethnic study of atherosclerosis. Physiological genomics. 2011;43(13):836–43. Epub 2011/04/28. doi: 10.1152/physiolgenomics.00243.2010 21521779; PubMed Central PMCID: PMC3132836.

34. Lewis DA, Stashenko GJ, Akay OM, Price LI, Owzar K, Ginsburg GS, et al. Whole blood gene expression analyses in patients with single versus recurrent venous thromboembolism. Thrombosis research. 2011;128(6):536–40. Epub 2011/07/09. doi: 10.1016/j.thromres.2011.06.003 21737128; PubMed Central PMCID: PMC3726737.

35. Park HJ, Noh JH, Eun JW, Koh YS, Seo SM, Park WS, et al. Assessment and diagnostic relevance of novel serum biomarkers for early decision of ST-elevation myocardial infarction. Oncotarget. 2015;6(15):12970–83. Epub 2015/05/31. doi: 10.18632/oncotarget.4001 26025919; PubMed Central PMCID: PMC4536992.

36. Sinnaeve PR, Donahue MP, Grass P, Seo D, Vonderscher J, Chibout SD, et al. Gene expression patterns in peripheral blood correlate with the extent of coronary artery disease. PloS one. 2009;4(9):e7037. Epub 2009/09/15. doi: 10.1371/journal.pone.0007037 19750006; PubMed Central PMCID: PMC2736586.

37. Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis, Health Labour Sciences Research Grant for Research on Measures for Intractable Diseases. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurologia medico-chirurgica. 2012;52(5):245–66. Epub 2012/08/09. doi: 10.2176/nmc.52.245 22870528.

38. Wang Y, Song F, Zhu J, Zhang S, Yang Y, Chen T, et al. GSA: Genome Sequence Archive. Genomics, proteomics & bioinformatics. 2017;15(1):14–8. Epub 2017/04/08. doi: 10.1016/j.gpb.2017.01.001 28387199; PubMed Central PMCID: PMC5339404.

39. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 2011;17(1):10–2. Epub 2011-08-02. doi: 10.14806/ej.17.1.200

40. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics (Oxford, England). 2013;29(1):15–21. Epub 2012/10/30. doi: 10.1093/bioinformatics/bts635 23104886; PubMed Central PMCID: PMC3530905.

41. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics (Oxford, England). 2015;31(2):166–9. Epub 2014/09/28. doi: 10.1093/bioinformatics/btu638 25260700; PubMed Central PMCID: PMC4287950.

42. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome biology. 2014;15(12):550. Epub 2014/12/18. doi: 10.1186/s13059-014-0550-8 25516281; PubMed Central PMCID: PMC4302049.

43. Jansen R, Batista S, Brooks AI, Tischfield JA, Willemsen G, van Grootheest G, et al. Sex differences in the human peripheral blood transcriptome. BMC genomics. 2014;15:33. Epub 2014/01/21. doi: 10.1186/1471-2164-15-33 24438232; PubMed Central PMCID: PMC3904696.

44. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics (Oxford, England). 2003;4(2):249–64. Epub 2003/08/20. doi: 10.1093/biostatistics/4.2.249 12925520.

45. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics (Oxford, England). 2006;22(22):2825–7. Epub 2006/09/20. doi: 10.1093/bioinformatics/btl476 16982708.

46. Westra HJ, Peters MJ, Esko T, Yaghootkar H, Schurmann C, Kettunen J, et al. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nature genetics. 2013;45(10):1238–43. Epub 2013/09/10. doi: 10.1038/ng.2756 24013639; PubMed Central PMCID: PMC3991562.

47. Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, et al. Robust enumeration of cell subsets from tissue expression profiles. Nature methods. 2015;12:453. doi: 10.1038/nmeth.3337 https://www.nature.com/articles/nmeth.3337#supplementary-information. 25822800

48. Song F, Qian Y, Peng X, Li X, Xing P, Ye D, et al. The frontline of immune response in peripheral blood. 2017;12(8):e0182294. doi: 10.1371/journal.pone.0182294 28771541.

49. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovascular research. 2006;69(3):562–73. Epub 2006/01/13. doi: 10.1016/j.cardiores.2005.12.002 16405877.

50. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T. Increased expression of serum Matrix Metalloproteinase-9 in patients with moyamoya disease. Surgical neurology. 2009;72(5):476–80; discussion 80. Epub 2009/01/17. doi: 10.1016/j.surneu.2008.10.009 19147196.

51. Masuda J, Ogata J, Yutani C. Smooth muscle cell proliferation and localization of macrophages and T cells in the occlusive intracranial major arteries in moyamoya disease. Stroke. 1993;24(12):1960–7. Epub 1993/12/01. doi: 10.1161/01.str.24.12.1960 7902623.

52. Im SH, Oh CW, Kwon OK, Kim JE, Han DH. Moyamoya disease associated with Graves disease: special considerations regarding clinical significance and management. Journal of neurosurgery. 2005;102(6):1013–7. Epub 2005/07/21. doi: 10.3171/jns.2005.102.6.1013 16028759.

53. Houkin K, Ito M, Sugiyama T, Shichinohe H, Nakayama N, Kazumata K, et al. Review of past research and current concepts on the etiology of moyamoya disease. Neurologia medico-chirurgica. 2012;52(5):267–77. Epub 2012/06/13. doi: 10.2176/nmc.52.267 22688062.

54. Fujimura M, Fujimura T, Kakizaki A, Sato-Maeda M, Niizuma K, Tomata Y, et al. Increased serum production of soluble CD163 and CXCL5 in patients with moyamoya disease: Involvement of intrinsic immune reaction in its pathogenesis. Brain research. 2018;1679:39–44. Epub 2017/11/28. doi: 10.1016/j.brainres.2017.11.013 29174692.

55. Kang HS, Moon YJ, Kim YY, Park WY, Park AK, Wang KC, et al. Smooth-muscle progenitor cells isolated from patients with moyamoya disease: novel experimental cell model. Journal of neurosurgery. 2014;120(2):415–25. Epub 2013/10/29. doi: 10.3171/2013.9.JNS131000 24160477.

56. Hynes RO. The extracellular matrix: not just pretty fibrils. Science (New York, NY). 2009;326(5957):1216–9. Epub 2009/12/08. doi: 10.1126/science.1176009 19965464; PubMed Central PMCID: PMC3536535.

57. Rasmussen LM, Wolf YG, Ruoslahti E. Vascular smooth muscle cells from injured rat aortas display elevated matrix production associated with transforming growth factor-beta activity. The American journal of pathology. 1995;147(4):1041–8. Epub 1995/10/01. 7573349; PubMed Central PMCID: PMC1871016.

58. Nabel EG, Shum L, Pompili VJ, Yang ZY, San H, Shu HB, et al. Direct transfer of transforming growth factor beta 1 gene into arteries stimulates fibrocellular hyperplasia. Proceedings of the National Academy of Sciences of the United States of America. 1993;90(22):10759–63. Epub 1993/11/15. doi: 10.1073/pnas.90.22.10759 8248168; PubMed Central PMCID: PMC47857.

59. Davidson JM, Zoia O, Liu JM. Modulation of transforming growth factor-beta 1 stimulated elastin and collagen production and proliferation in porcine vascular smooth muscle cells and skin fibroblasts by basic fibroblast growth factor, transforming growth factor-alpha, and insulin-like growth factor-I. Journal of cellular physiology. 1993;155(1):149–56. Epub 1993/04/01. doi: 10.1002/jcp.1041550119 8468360.

60. Folkman J, Klagsbrun M. Angiogenic factors. Science (New York, NY). 1987;235(4787):442–7. Epub 1987/01/23. doi: 10.1126/science.2432664 2432664.

61. Lawrence R, Hartmann DJ, Sonenshein GE. Transforming growth factor beta 1 stimulates type V collagen expression in bovine vascular smooth muscle cells. The Journal of biological chemistry. 1994;269(13):9603–9. Epub 1994/04/01. 8144547.

62. Fukui M, Kono S, Sueishi K, Ikezaki K. Moyamoya disease. Neuropathology: official journal of the Japanese Society of Neuropathology. 2000;20 Suppl:S61–4. Epub 2000/10/19. 11037190.

63. Jung KH, Chu K, Lee ST, Park HK, Kim DH, Kim JH, et al. Circulating endothelial progenitor cells as a pathogenetic marker of moyamoya disease. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2008;28(11):1795–803. Epub 2008/07/10. doi: 10.1038/jcbfm.2008.67 18612318.

64. Kim JH, Jung JH, Phi JH, Kang HS, Kim JE, Chae JH, et al. Decreased level and defective function of circulating endothelial progenitor cells in children with moyamoya disease. Journal of neuroscience research. 2010;88(3):510–8. Epub 2009/09/24. doi: 10.1002/jnr.22228 19774676.

65. Rafat N, Beck G, Pena-Tapia PG, Schmiedek P, Vajkoczy P. Increased levels of circulating endothelial progenitor cells in patients with Moyamoya disease. Stroke. 2009;40(2):432–8. Epub 2008/12/20. doi: 10.1161/STROKEAHA.108.529420 19095988.

66. Yoshihara T, Taguchi A, Matsuyama T, Shimizu Y, Kikuchi-Taura A, Soma T, et al. Increase in circulating CD34-positive cells in patients with angiographic evidence of moyamoya-like vessels. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2008;28(6):1086–9. Epub 2008/01/31. doi: 10.1038/jcbfm.2008.1 18231114.

67. Weng L, Cao X, Han L, Zhao H, Qiu S, Yan Y, et al. Association of increased Treg and Th17 with pathogenesis of moyamoya disease. Scientific reports. 2017;7(1):3071. Epub 2017/06/10. doi: 10.1038/s41598-017-03278-8 28596558; PubMed Central PMCID: PMC5465197.

68. Christodoulidis G, Vittorio TJ, Fudim M, Lerakis S, Kosmas CE. Inflammation in coronary artery disease. Cardiology in review. 2014;22(6):279–88. Epub 2014/01/21. doi: 10.1097/CRD.0000000000000006 24441047.

69. Fioranelli M, Bottaccioli AG, Bottaccioli F, Bianchi M, Rovesti M, Roccia MG. Stress and Inflammation in Coronary Artery Disease: A Review Psychoneuroendocrineimmunology-Based. Frontiers in immunology. 2018;9:2031. Epub 2018/09/22. doi: 10.3389/fimmu.2018.02031 30237802; PubMed Central PMCID: PMC6135895.

70. Li JJ. Inflammation in coronary artery diseases. Chinese medical journal. 2011;124(21):3568–75. Epub 2012/02/22. 22340179.

71. Libby P. Inflammation and cardiovascular disease mechanisms. The American journal of clinical nutrition. 2006;83(2):456s–60s. Epub 2006/02/14. doi: 10.1093/ajcn/83.2.456S 16470012.

72. Ikonomidis I, Michalakeas CA, Parissis J, Paraskevaidis I, Ntai K, Papadakis I, et al. Inflammatory markers in coronary artery disease. BioFactors (Oxford, England). 2012;38(5):320–8. Epub 2012/05/26. doi: 10.1002/biof.1024 22628054.

73. Li H, Sun K, Zhao R, Hu J, Hao Z, Wang F, et al. Inflammatory biomarkers of coronary heart disease. Frontiers in bioscience (Scholar edition). 2018;10:185–96. Epub 2017/09/21. 28930526.

74. Madjid M, Willerson JT. Inflammatory markers in coronary heart disease. British medical bulletin. 2011;100:23–38. Epub 2011/10/20. doi: 10.1093/bmb/ldr043 22010105.

75. Voudris KV, Chanin J, Feldman DN, Charitakis K. Novel Inflammatory Biomarkers in Coronary Artery Disease: Potential Therapeutic Approaches. Current medicinal chemistry. 2015;22(22):2680–9. Epub 2015/04/22. doi: 10.2174/0929867322666150420124427 25891107.

76. Subirana I, Fito M, Diaz O, Vila J, Frances A, Delpon E, et al. Prediction of coronary disease incidence by biomarkers of inflammation, oxidation, and metabolism. Scientific reports. 2018;8(1):3191. Epub 2018/02/18. doi: 10.1038/s41598-018-21482-y 29453342; PubMed Central PMCID: PMC5816603.


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