Data mining of atherosclerotic plaque transcriptomes predicts STAT1-dependent inflammatory signal integration in vascular disease

International Journal of Molecular Sciences

Volumn 15, Issue 8, 2014, Pages 14313-14331

  Sikorski, Krzysztof ^a,b   Wesoly, Joanna ^a   Bluyssen, Hans A R ^a  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Atherosclerosis; Diagnostic markers; IFN ; JAK STAT signalling; TLR4

Indexed keywords

CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; MACROPHAGE ACTIVATING FACTOR; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MATRIX METALLOPROTEINASE 19; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; NERVE CELL ADHESION MOLECULE; OSTEOPONTIN; OXIDIZED LOW DENSITY LIPOPROTEIN; RANTES; STAT1 PROTEIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTOME; VASCULAR CELL ADHESION MOLECULE 1; INTERFERON REGULATORY FACTOR; TLR4 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; CELL MIGRATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DATA MINING; DISEASE MARKER; GENE CONTROL; GENE EXPRESSION; GENE ONTOLOGY; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOMODULATION; INFERIOR MESENTERIC ARTERY; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR DISEASE; GENETICS; METABOLISM; PROMOTER REGION;

DATA MINING; HUMANS; INTERFERON REGULATORY FACTORS; INTERFERON-GAMMA; NF-KAPPA B; PLAQUE, ATHEROSCLEROTIC; PROMOTER REGIONS, GENETIC; STAT1 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 4; TRANSCRIPTOME; VASCULAR DISEASES;

EID: 84916895363     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150814313     Document Type: Article

References (70)

1. Raines, E.W. The extracellular matrix can regulate vascular cell migration, proliferation, and survival: Relationships to vascular disease. Int. J. Exp. Pathol. 2000, 81, 173-182.
2. Ameriso, S.F.; Fridman, E.A.; Leiguarda, R.C.; Sevlever, G.E. Detection of helicobacter pylori in human carotid atherosclerotic plaques. Stroke J. Cereb. Circ. 2001, 32, 385-391.
3. Sitia, S.; Tomasoni, L.; Atzeni, F.; Ambrosio, G.; Cordiano, C.; Catapano, A.; Tramontana, S.; Perticone, F.; Naccarato, P.; Camici, P. et al. From endothelial dysfunction to atherosclerosis. Autoimmun. Rev. 2010, 9, 830-834.
4. Dauphinee, S.M.; Karsan, A. Lipopolysaccharide signaling in endothelial cells. Lab. Investig. J. Tech. Methods Pathol. 2006, 86, 9-22.
5. Robertson, A.K.; Hansson, G.K. T cells in atherogenesis: For better or for worse? Arterioscler. Thromb. Vasc. Biol. 2006, 26, 2421-2432.
6. Hansson, G.K.; Robertson, A.K.; Soderberg-Naucler, C. Inflammation and atherosclerosis. Annu. Rev. Pathol. 2006, 1, 297-329.
7. Hidalgo, L.G.; Halloran, P.F. Role of ifn-gamma in allograft rejection. Crit. Rev. Immunol. 2002, 22, 317-349.
8. Tellides, G.; Tereb, D.A.; Kirkiles-Smith, N.C.; Kim, R.W.; Wilson, J.H.; Schechner, J.S.; Lorber, M.I.; Pober, J.S. Interferon-gamma elicits arteriosclerosis in the absence of leukocytes. Nature 2000, 403, 207-211.
9. Tamura, T.; Yanai, H.; Savitsky, D.; Taniguchi, T. The irf family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 2008, 26, 535-584.
10. Liu, J.; Guan, X.; Ma, X. Interferon regulatory factor 1 is an essential and direct transcriptional activator for interferon {gamma}-induced rantes/ccl5 expression in macrophages. J. Biol. Chem. 2005, 280, 24347-24355.
11. Ohmori, Y.; Hamilton, T.A. The interferon-stimulated response element and a kappa b site mediate synergistic induction of murine ip-10 gene transcription by ifn-gamma and tnf-alpha. J. Immunol. 1995, 154, 5235-5244.
12. Methe, H.; Kim, J.O.; Kofler, S.; Weis, M.; Nabauer, M.; Koglin, J. Expansion of circulating toll-like receptor 4-positive monocytes in patients with acute coronary syndrome. Circulation 2005, 111, 2654-2661.
13. Michelsen, K.S.; Wong, M.H.; Shah, P.K.; Zhang, W.; Yano, J.; Doherty, T.M.; Akira, S.; Rajavashisth, T.B.; Arditi, M. Lack of toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein e. Proc. Natl. Acad. Sci. USA 2004, 101, 10679-10684.
14. Sakaguchi, S.; Negishi, H.; Asagiri, M.; Nakajima, C.; Mizutani, T.; Takaoka, A.; Honda, K.; Taniguchi, T. Essential role of irf-3 in lipopolysaccharide-induced interferon-beta gene expression and endotoxin shock. Biochem. Biophys. Res. Commun. 2003, 306, 860-866.
15. Sikorski, K.; Chmielewski, S.; Olejnik, A.; Wesoly, J.; Heemann, U.; Baumann, M.; Bluyssen, H.A. Stat1 as a central mediator of ifnγ and tlr4 signal integration in vascular dysfunction. JAK-STAT 2012, 1, 241-249.
16. Ohmori, Y.; Schreiber, R.D.; Hamilton, T.A. Synergy between interferon-gamma and tumor necrosis factor-alpha in transcriptional activation is mediated by cooperation between signal transducer and activator of transcription 1 and nuclear factor kappab. J. Biol. Chem. 1997, 272, 14899-14907.
17. Sikorski, K.; Chmielewski, S.; Przybyl, L.; Heemann, U.; Wesoly, J.; Baumann, M.; Bluyssen, H.A. Stat1-mediated signal integration between ifnγ and lps leads to increased ec and smc activation and monocyte adhesion. Am. J. Physiol. Cell Physiol. 2011, 300, C1337-C1344.
18. Hiroi, M.; Ohmori, Y. The transcriptional coactivator creb-binding protein cooperates with stat1 and nf-kappa b for synergistic transcriptional activation of the cxc ligand 9/monokine induced by interferon-gamma gene. J. Biol. Chem. 2003, 278, 651-660.
19. Collins, T.; Read, M.A.; Neish, A.S.; Whitley, M.Z.; Thanos, D.; Maniatis, T. Transcriptional regulation of endothelial cell adhesion molecules: Nf-kappa b and cytokine-inducible enhancers. FASEB J. 1995, 9, 899-909.
20. Ganster, R.W.; Guo, Z.; Shao, L.; Geller, D.A. Differential effects of tnf-alpha and ifn-gamma on gene transcription mediated by nf-kappab-stat1 interactions. J. Interferon Cytokine Res. 2005, 25, 707-719.
21. Chon, S.Y.; Hassanain, H.H.; Gupta, S.L. Cooperative role of interferon regulatory factor 1 and p91 (stat1) response elements in interferon-gamma-inducible expression of human indoleamine 2,3-dioxygenase gene. J. Biol. Chem. 1996, 271, 17247-17252.
22. Brucet, M.; Marques, L.; Sebastian, C.; Lloberas, J.; Celada, A. Regulation of murine tap1 and lmp2 genes in macrophages by interferon gamma is mediated by stat1 and irf-1. Genes Immun. 2004, 5, 26-35.
23. Pietila, T.E.; Veckman, V.; Lehtonen, A.; Lin, R.; Hiscott, J.; Julkunen, I. Multiple nf-kappab and ifn regulatory factor family transcription factors regulate ccl19 gene expression in human monocyte-derived dendritic cells. J. Immunol. 2007, 178, 253-261.
24. Tamassia, N.; Calzetti, F.; Ear, T.; Cloutier, A.; Gasperini, S.; Bazzoni, F.; McDonald, P.P.; Cassatella, M.A. Molecular mechanisms underlying the synergistic induction of cxcl10 by lps and ifn-gamma in human neutrophils. Eur. J. Immunol. 2007, 37, 2627-2634.
25. Hagg, S.; Skogsberg, J.; Lundstrom, J.; Noori, P.; Nilsson, R.; Zhong, H.; Maleki, S.; Shang, M.M.; Brinne, B.; Bradshaw, M. et al. Multi-organ expression profiling uncovers a gene module in coronary artery disease involving transendothelial migration of leukocytes and lim domain binding 2: The stockholm atherosclerosis gene expression (stage) study. PLoS Genet. 2009, 5, e1000754.
26. Folkersen, L.; Persson, J.; Ekstrand, J.; Agardh, H.E.; Hansson, G.K.; Gabrielsen, A.; Hedin, U.; Paulsson-Berne, G. Prediction of ischemic events on the basis of transcriptomic and genomic profiling in patients undergoing carotid endarterectomy. Mol. Med. 2012, 18, 669-675.
27. Canfield, A.E.; Farrington, C.; Dziobon, M.D.; Boot-Handford, R.P.; Heagerty, A.M.; Kumar, S.N.; Roberts, I.S. The involvement of matrix glycoproteins in vascular calcification and fibrosis: An immunohistochemical study. J. Pathol. 2002, 196, 228-234.
28. Cantor, H.; Shinohara, M.L. Regulation of t-helper-cell lineage development by osteopontin: The inside story. Nat. Rev. Immunol. 2009, 9, 137-141.
29. Chen, T.; Yan, H.; Li, Z.; Jing, T.; Zhu, W.; Ge, J.; Zheng, X.; Pan, X.; Zhu, J. Microrna-155 regulates lipid uptake, adhesion/chemokine marker secretion and scg2 expression in oxldl-stimulated dendritic cells/macrophages. Int. J. Cardiol. 2011, 147, 446-447.
30. Scharl, M.; Hruz, P.; McCole, D.F. Protein tyrosine phosphatase non-receptor type 2 regulates ifn-gamma-induced cytokine signaling in thp-1 monocytes. Inflamm. Bowel Dis. 2010, 16, 2055-2064.
31. Kok, S.H.; Hong, C.Y.; Kuo, M.Y.; Wang, C.C.; Hou, K.L.; Lin, Y.T.; Galson, D.L.; Lin, S.K. Oncostatin m-induced ccl2 transcription in osteoblastic cells is mediated by multiple levels of stat-1 and stat-3 signaling: An implication for the pathogenesis of arthritis. Arthritis Rheumatol. 2009, 60, 1451-1462.
32. Dai, X.; Sayama, K.; Tohyama, M.; Shirakata, Y.; Yang, L.; Hirakawa, S.; Tokumaru, S.; Hashimoto, K. The nf-kappab, p38 mapk and stat1 pathways differentially regulate the dsrna-mediated innate immune responses of epidermal keratinocytes. Int. Immunol. 2008, 20, 901-909.
33. Fleetwood, A.J.; Dinh, H.; Cook, A.D.; Hertzog, P.J.; Hamilton, J.A. Gm-csf- and m-csf-dependent macrophage phenotypes display differential dependence on type i interferon signaling. J. Leukoc. Biol. 2009, 86, 411-421.
34. Hardison, S.E.; Herrera, G.; Young, M.L.; Hole, C.R.; Wozniak, K.L.; Wormley, F.L., Jr. Protective immunity against pulmonary cryptococcosis is associated with stat1-mediated classical macrophage activation. J. Immunol. 2012, 189, 4060-4068.
35. Tyagi, A.; Agarwal, C.; Dwyer-Nield, L.D.; Singh, R.P.; Malkinson, A.M.; Agarwal, R. Silibinin modulates tnf-alpha and ifn-gamma mediated signaling to regulate cox2 and inos expression in tumorigenic mouse lung epithelial lm2 cells. Mol. Carcinog. 2012, 51, 832-842.
36. Kosaka, H.; Yoshimoto, T.; Fujimoto, J.; Nakanishi, K. Interferon-gamma is a therapeutic target molecule for prevention of postoperative adhesion formation. Nat. Med. 2008, 14, 437-441.
37. Eastabrook, G.D.; Hu, Y.; Tan, R.; Dutz, J.P.; Maccalman, C.D.; von Dadelszen, P. Decidual nk cell-derived conditioned medium (dnk-cm) mediates vegf-c secretion in extravillous cytotrophoblasts. Am. J. Reprod. Immunol. 2012, 67, 101-111.
38. Hu, X.; Ivashkiv, L.B. Cross-regulation of signaling pathways by interferon-gamma: Implications for immune responses and autoimmune diseases. Immunity 2009, 31, 539-550.
39. Schroder, K.; Sweet, M.J.; Hume, D.A. Signal integration between ifngamma and tlr signalling pathways in macrophages. Immunobiology 2006, 211, 511-524.
40. Cagnin, S.; Biscuola, M.; Patuzzo, C.; Trabetti, E.; Pasquali, A.; Laveder, P.; Faggian, G.; Iafrancesco, M.; Mazzucco, A.; Pignatti, P.F. et al. Reconstruction and functional analysis of altered molecular pathways in human atherosclerotic arteries. BMC Genomics 2009, 10, 13.
41. Hansson, G.K. Immune mechanisms in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2001, 21, 1876-1890.
42. Poston, R.N.; Davies, D.F. Immunity and inflammation in the pathogenesis of atherosclerosis. A review. Atherosclerosis 1974, 19, 353-367.
43. Toshchakov, V.; Jones, B.W.; Perera, P.Y.; Thomas, K.; Cody, M.J.; Zhang, S.; Williams, B.R.; Major, J.; Hamilton, T.A.; Fenton, M.J. et al. Tlr4, but not tlr2, mediates ifn-beta-induced stat1alpha/beta-dependent gene expression in macrophages. Nat. Immunol. 2002, 3, 392-398.
44. Clarke, D.L.; Clifford, R.L.; Jindarat, S.; Proud, D.; Pang, L.; Belvisi, M.; Knox, A.J. Tnfalpha and ifngamma synergistically enhance transcriptional activation of cxcl10 in human airway smooth muscle cells via stat-1, nf-kappab, and the transcriptional coactivator creb-binding protein. J. Biol. Chem. 2010, 285, 29101-29110.
45. Qi, X.F.; Kim, D.H.; Yoon, Y.S.; Jin, D.; Huang, X.Z.; Li, J.H.; Deung, Y.K.; Lee, K.J. Essential involvement of cross-talk between ifn-gamma and tnf-alpha in cxcl10 production in human thp-1 monocytes. J. Cell. Physiol. 2009, 220, 690-697.
46. Gao, J.; Morrison, D.C.; Parmely, T.J.; Russell, S.W.; Murphy, W.J. An interferon-gamma-activated site (gas) is necessary for full expression of the mouse inos gene in response to interferon-gamma and lipopolysaccharide. J. Biol. Chem. 1997, 272, 1226-1230.
47. Butcher, M.J.; Galkina, E.V. Phenotypic and functional heterogeneity of macrophages and dendritic cell subsets in the healthy and atherosclerosis-prone aorta. Front. Physiol. 2012, 3, 44.
48. Rohde, L.E.; Lee, R.T. Pathophysiology of atherosclerotic plaque development and rupture: An overview. Semin. Vasc. Med. 2003, 3, 347-354.
49. Jashari, F.; Ibrahimi, P.; Nicoll, R.; Bajraktari, G.; Wester, P.; Henein, M.Y. Coronary and carotid atherosclerosis: Similarities and differences. Atherosclerosis 2013, 227, 193-200.
50. Prasad, A.; Zhu, J.; Halcox, J.P.; Waclawiw, M.A.; Epstein, S.E.; Quyyumi, A.A. Predisposition to atherosclerosis by infections: Role of endothelial dysfunction. Circulation 2002, 106, 184-190.
51. Xu, Q. Role of heat shock proteins in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2002, 22, 1547-1559.
52. Frantz, S.; Ertl, G.; Bauersachs, J. Mechanisms of disease: Toll-like receptors in cardiovascular disease. Nat. Clin. Pract. Cardiovasc. Med. 2007, 4, 444-454.
53. Rauch, S.J.; Rosenkranz, A.C.; Bohm, A.; Meyer-Kirchrath, J.; Hohlfeld, T.; Schror, K.; Rauch, B.H. Cholesterol induces apoptosis-associated loss of the activated leukocyte cell adhesion molecule (alcam) in human monocytes. Vasc. Pharmacol. 2011, 54, 93-99.
54. Kurata, H.; Matsumoto, A.; Fujiwara, Y.; Kondo, K.; Itakura, H.; Mitchell, A.; Fidge, N. A candidate high density lipoprotein (hdl) receptor, hb2, with possible multiple functions shows sequence homology with adhesion molecules. J. Atheroscler. Thromb. 1998, 4, 112-117.
55. Barks, J.L.; McQuillan, J.J.; Iademarco, M.F. Tnf-alpha and il-4 synergistically increase vascular cell adhesion molecule-1 expression in cultured vascular smooth muscle cells. J. Immunol. 1997, 159, 4532-4538.
56. Murooka, T.T.; Rahbar, R.; Platanias, L.C.; Fish, E.N. Ccl5-mediated t-cell chemotaxis involves the initiation of mrna translation through mtor/4e-bp1. Blood 2008, 111, 4892-4901.
57. Yurchenko, E.; Tritt, M.; Hay, V.; Shevach, E.M.; Belkaid, Y.; Piccirillo, C.A. Ccr5-dependent homing of naturally occurring cd4+ regulatory t cells to sites of leishmania major infection favors pathogen persistence. J. Exp. Med. 2006, 203, 2451-2460.
58. Ottoson, N.C.; Pribila, J.T.; Chan, A.S.; Shimizu, Y. Cutting edge: T cell migration regulated by cxcr4 chemokine receptor signaling to zap-70 tyrosine kinase. J. Immunol. 2001, 167, 1857-1861.
59. Cangemi, C.; Skov, V.; Poulsen, M.K.; Funder, J.; Twal, W.O.; Gall, M.A.; Hjortdal, V.; Jespersen, M.L.; Kruse, T.A.; Aagard, J. et al. Fibulin-1 is a marker for arterial extracellular matrix alterations in type 2 diabetes. Clin. Chem. 2011, 57, 1556-1565.
60. Kallio, M.A.; Tuimala, J.T.; Hupponen, T.; Klemela, P.; Gentile, M.; Scheinin, I.; Koski, M.; Kaki, J.; Korpelainen, E.I. Chipster: User-friendly analysis software for microarray and other high-throughput data. BMC Genomics 2011, 12, 507.
61. Johnson, W.E.; Li, C.; Rabinovic, A. Adjusting batch effects in microarray expression data using empirical bayes methods. Biostatistics 2007, 8, 118-127.
62. Zheng, Q.; Wang, X.J. Goeast: A web-based software toolkit for gene ontology enrichment analysis. Nucleic Acids Res. 2008, 36, W358-W363.
63. Data Analysis Suite GENOMATIX. Avaliable online: www.genomatix.de (accessed on 14 August 2014).
64. Kanehisa, M.; Goto, S. Kegg: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000, 28, 27-30.
65. BioCarta. Available online: http://www.biocarta.com (accessed on 20 February 2014).
66. Croft, D.; O'Kelly, G.; Wu, G.; Haw, R.; Gillespie, M.; Matthews, L.; Caudy, M.; Garapati, P.; Gopinath, G.; Jassal, B. et al. Reactome: A database of reactions, pathways and biological processes. Nucleic Acids Res. 2011, 39, D691-D697.
67. Krzywinski, M.; Schein, J.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S.J.; Marra, M.A. Circos: An information aesthetic for comparative genomics. Genome Res. 2009, 19, 1639-1645.
68. Genomatix Regionminer Manual. Available online: http://www.genomatix.de/online_help/help_regionminer/overrepresented_TFs.html (accessed on 20 February 2014).
69. Sikorski, K.; Czerwoniec, A.; Bujnicki, J.M.; Wesoly, J.; Bluyssen, H.A. Stat1 as a novel therapeutical target in pro-atherogenic signal integration of ifngamma, tlr4 and il-6 in vascular disease. Cytokine Growth Factor Rev. 2011, 22, 211-219.
70. Kuvin, J.T.; Karas, R.H. Clinical utility of endothelial function testing: Ready for prime time? Circulation 2003, 107, 3243-3247.