Vascular transcriptome profiling identifies Sphingosine kinase 1 as a modulator of angiotensin II-induced vascular dysfunction

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Siedlinski, Mateusz ^a   Nosalski, Ryszard ^a,b   Szczepaniak, Piotr ^a   Ludwig Gałȩzowska, Agnieszka H ^a   Mikołajczyk, Tomasz ^a,b   Filip, Magdalena ^a   Osmenda, Grzegorz ^a   Wilk, Grzegorz ^a   Nowak, Michał ^a   Wołkow, Paweł ^a   Guzik, Tomasz J ^a,b  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE;

ANIMAL; CHEMICALLY INDUCED; DISSECTING ANEURYSM; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; HYPERTENSION; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; PATHOLOGY;

ANEURYSM, DISSECTING; ANGIOTENSIN II; ANIMALS; GENE EXPRESSION PROFILING; HYPERTENSION; MALE; MICE; MICE, KNOCKOUT; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR);

EID: 85014851149     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep44131     Document Type: Article

References (59)

1. Coffman, T. M. Under pressure: The search for the essential mechanisms of hypertension. Nat Med 17, 1402-1409 (2011).
2. Levy, D., et al. Genome-wide association study of blood pressure and hypertension. Nat Genet 41, 677-687 (2009).
3. Ehret, G. B., et al. Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature 478, 103-109 (2011).
4. Kato, N., et al. Meta-Analysis of genome-wide association studies identifies common variants associated with blood pressure variation in east asians. Nat Genet 43, 531-538 (2011).
5. Wain, L. V., et al. Genome-wide association study identifies six new loci influencing pulse pressure and mean arterial pressure. Nat Genet 43, 1005-1011 (2011).
6. Zeggini, E., et al. Meta-Analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40, 638-645 (2008).
7. Cho, M. H., et al. A genome-wide association study of copd identifies a susceptibility locus on chromosome 19q13. Hum Mol Genet 21, 947-957 (2012).
8. Guzik, T. J., et al. Role of the t cell in the genesis of angiotensin ii induced hypertension and vascular dysfunction. J Exp Med 204, 2449-2460 (2007).
9. Guzik, T. J., et al. Vascular superoxide production by nad (p)h oxidase: Association with endothelial dysfunction and clinical risk factors. Circ Res 86, E85-90 (2000).
10. Makhanova, N. A., Crowley, S. D., Griffiths, R. C., & Coffman, T. M. Gene expression profiles linked to at1 angiotensin receptors in the kidney. Physiol Genomics 42A, 211-218 (2010).
11. Larkin, J. E., Frank, B. C., Gavras, H., Sultana, R., & Quackenbush, J. Independence and reproducibility across microarray platforms. Nat Methods 2, 337-344 (2005).
12. Tsushima, K., et al. Irf3 regulates cardiac fibrosis but not hypertrophy in mice during angiotensin ii-induced hypertension. FASEB J 25, 1531-1543 (2011).
13. Rush, C., et al. Whole genome expression analysis within the angiotensin ii-Apolipoprotein e deficient mouse model of abdominal aortic aneurysm. BMC Genomics 10, 298 (2009).
14. Owens, A. P. 3rd, et al. Angiotensin ii induces a region-specific hyperplasia of the ascending aorta through regulation of inhibitor of differentiation 3. Circ Res 106, 611-619 (2010).
15. Zhou, Y., Chen, Y., Dirksen, W. P., Morris, M., & Periasamy, M. At1b receptor predominantly mediates contractions in major mouse blood vessels. Circ Res 93, 1089-1094 (2003).
16. Poduri, A., et al. Regional variation in aortic at1b receptor mrna abundance is associated with contractility but unrelated to atherosclerosis and aortic aneurysms. PLoS One 7, e48462 (2012).
17. Intengan, H. D., & Schiffrin, E. L. Structure and mechanical properties of resistance arteries in hypertension: Role of adhesion molecules and extracellular matrix determinants. Hypertension 36, 312-318 (2000).
18. Prewitt, R. L., Rice, D. C., & Dobrian, A. D. Adaptation of resistance arteries to increases in pressure. Microcirculation 9, 295-304 (2002).
19. Petnehazy, T., et al. Angiotensin ii type 1 receptors and the intestinal microvascular dysfunction induced by ischemia and reperfusion. Am J Physiol Gastrointest Liver Physiol 290, G1203-1210 (2006).
20. Wang, D., Chabrashvili, T., Borrego, L., Aslam, S., & Umans, J. G. Angiotensin ii infusion alters vascular function in mouse resistance vessels: Roles of o and endothelium. J Vasc Res 43, 109-119 (2006).
21. Peters, S. L., & Alewijnse, A. E. Sphingosine-1-phosphate signaling in the cardiovascular system. Current opinion in pharmacology 7, 186-192 (2007).
22. Moxon, J. V., et al. Comparison of the serum lipidome in patients with abdominal aortic aneurysm and peripheral artery disease. Circulation. Cardiovascular genetics 7, 71-79 (2014).
23. Xing, X. Q., et al. Sphingosine kinase 1/sphingosine 1-phosphate signalling pathway as a potential therapeutic target of pulmonary hypertension. International journal of clinical and experimental medicine 8, 11930-11935 (2015).
24. Gorshkova, I. A., et al. Inhibition of sphingosine-1-phosphate lyase rescues sphingosine kinase-1-knockout phenotype following murine cardiac arrest. Life sciences 93, 359-366 (2013).
25. Allende, M. L., et al. Mice deficient in sphingosine kinase 1 are rendered lymphopenic by fty720. The Journal of biological chemistry 279, 52487-52492 (2004).
26. Wilson, P. C., et al. Inhibition of sphingosine kinase 1 ameliorates angiotensin ii-induced hypertension and inhibits transmembrane calcium entry via store-operated calcium channel. Molecular endocrinology 29, 896-908 (2015).
27. Furuya, H., et al. Effect of sphingosine kinase 1 inhibition on blood pressure. FASEB J 27, 656-664 (2013).
28. Coussin, F., Scott, R. H., & Nixon, G. F. Sphingosine 1-phosphate induces creb activation in rat cerebral artery via a protein kinase c-mediated inhibition of voltage-gated k+ channels. Biochemical pharmacology 66, 1861-1870 (2003).
29. Salomone, S., & Waeber, C. Selectivity and specificity of sphingosine-1-phosphate receptor ligands: Caveats and critical thinking in characterizing receptor-mediated effects. Frontiers in pharmacology 2, 9 (2011).
30. Pyne, N. J., & Pyne, S. Selectivity and specificity of sphingosine 1-phosphate receptor ligands: ?Off-Targets? or complex pharmacology? Frontiers in pharmacology 2, 26 (2011).
31. Lorenz, J. N., Arend, L. J., Robitz, R., Paul, R. J., & MacLennan, A. J. Vascular dysfunction in s1p2 sphingosine 1-phosphate receptor knockout mice. American journal of physiology. Regulatory, integrative and comparative physiology 292, R440-446 (2007).
32. Sykes, D. A., et al. Investigating the molecular mechanisms through which fty720-p causes persistent s1p1 receptor internalization. British journal of pharmacology 171, 4797-4807 (2014).
33. Cantalupo, A., et al. Nogo-b regulates endothelial sphingolipid homeostasis to control vascular function and blood pressure. Nat Med 21, 1028-1037 (2015).
34. Tolle, M., et al. Immunomodulator fty720 induces enos-dependent arterial vasodilatation via the lysophospholipid receptor s1p3. Circ Res 96, 913-920 (2005).
35. Rikitake, Y., et al. Involvement of endothelial nitric oxide in sphingosine-1-phosphate-induced angiogenesis. Arteriosclerosis, thrombosis, and vascular biology 22, 108-114 (2002).
36. Mulders, A. C., et al. Sphingosine kinase-dependent activation of endothelial nitric oxide synthase by angiotensin ii. Arteriosclerosis, thrombosis, and vascular biology 26, 2043-2048 (2006).
37. Igarashi, J., & Michel, T. Sphingosine-1-phosphate and modulation of vascular tone. Cardiovasc Res 82, 212-220 (2009).
38. Tolle, M., et al. Regulation of endothelial nitric oxide synthase activation in endothelial cells by s1p1 and s1p3. Biochemical and biophysical research communications 476, 627-634 (2016).
39. Camm, J., Hla, T., Bakshi, R., & Brinkmann, V. Cardiac and vascular effects of fingolimod: Mechanistic basis and clinical implications. American heart journal 168, 632-644 (2014).
40. Hoefer, J., et al. Sphingosine-1-phosphate-dependent activation of p38 mapk maintains elevated peripheral resistance in heart failure through increased myogenic vasoconstriction. Circ Res 107, 923-933 (2010).
41. Drummond, G. R., & Sobey, C. G. Endothelial nadph oxidases: Which nox to target in vascular disease? Trends in endocrinology and metabolism: TEM 25, 452-463 (2014).
42. Galougahi, K. K., et al. Glutathionylation mediates angiotensin ii-induced enos uncoupling, amplifying nadph oxidase-dependent endothelial dysfunction. Journal of the American Heart Association 3, e000731 (2014).
43. Schenten, V., Melchior, C., Steinckwich, N., Tschirhart, E. J., & Brechard, S. Sphingosine kinases regulate nox2 activity via p38 mapkdependent translocation of s100a8/a9. Journal of leukocyte biology 89, 587-596 (2011).
44. Denzel, M. S., et al. T-cadherin is critical for adiponectin-mediated cardioprotection in mice. The Journal of clinical investigation 120, 4342-4352 (2010).
45. Chung, C. M., et al. A genome-wide association study reveals a quantitative trait locus of adiponectin on cdh13 that predicts cardiometabolic outcomes. Diabetes 60, 2417-2423 (2011).
46. Org, E., et al. Genome-wide scan identifies cdh13 as a novel susceptibility locus contributing to blood pressure determination in two european populations. Hum Mol Genet 18, 2288-2296 (2009).
47. Carlstrom, M., et al. Superoxide dismutase 1 limits renal microvascular remodeling and attenuates arteriole and blood pressure responses to angiotensin ii via modulation of nitric oxide bioavailability. Hypertension 56, 907-913 (2010).
48. Guzik, T. J., et al. Superoxide dismutase activity and expression in human venous and arterial bypass graft vessels. Journal of physiology and pharmacology: an official journal of the Polish Physiological Society 56, 313-323 (2005).
49. Crassous, P. A., et al. Soluble guanylyl cyclase is a target of angiotensin ii-induced nitrosative stress in a hypertensive rat model. Am J Physiol Heart Circ Physiol 303, H597-604 (2012).
50. Ramanathan, S., Mazzalupo, S., Boitano, S., & Montfort, W. R. Thrombospondin-1 and angiotensin ii inhibit soluble guanylyl cyclase through an increase in intracellular calcium concentration. Biochemistry 50, 7787-7799 (2011).
51. Stuiver, M., et al. Cnnm2, encoding a basolateral protein required for renal mg2+ handling, is mutated in dominant hypomagnesemia. Am J Hum Genet 88, 333-343 (2011).
52. Obinata, H., et al. Individual variation of human s1p (1) coding sequence leads to heterogeneity in receptor function and drug interactions. Journal of lipid research 55, 2665-2675 (2014).
53. Hartono, S. P., Knudsen, B. E., Lerman, L. O., Textor, S. C., & Grande, J. P. Combined effect of hyperfiltration and renin angiotensin system activation on development of chronic kidney disease in diabetic db/db mice. BMC nephrology 15, 58 (2014).
54. Andersen, C. L., Jensen, J. L., & Orntoft, T. F. Normalization of real-Time quantitative reverse transcription-pcr data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer research 64, 5245-5250 (2004).
55. Nazarewicz, R. R., Bikineyeva, A., & Dikalov, S. I. Rapid and specific measurements of superoxide using fluorescence spectroscopy. Journal of biomolecular screening 18, 498-503 (2013).
56. Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. Nih image to imagej: 25 years of image analysis. Nat Methods 9, 671-675 (2012).
57. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/(2013).
58. Mootha, V. K., et al. Pgc-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34, 267-273 (2003).
59. Subramanian, A., et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102, 15545-15550 (2005).