Atlas of tissue renin-angiotensin-aldosterone system in human: A transcriptomic meta-analysis

Ali Nehme; Catherine Cerutti; Nedra Dhaouadi; Marie Paule Gustin; Pierre-Yves Courand; Kazem Zibara; Giampiero Bricca

doi:10.1038/srep10035

journal article Open Access May 20, 2015

Atlas of tissue renin-angiotensin-aldosterone system in human: A transcriptomic meta-analysis

Ali Nehme Catherine Cerutti Nedra Dhaouadi Marie Paule Gustin Pierre-Yves Courand Kazem Zibara Giampiero Bricca

Scientific Reports Vol. 5 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep10035

Abstract

AbstractTissue renin-angiotensin-aldosterone system (RAAS) has attracted much attention because of its physiological and pharmacological implications; however, a clear definition of tissue RAAS is still missing. We aimed to establish a preliminary atlas for the organization of RAAS across 23 different normal human tissues. A set of 37 genes encoding classical and novel RAAS participants including gluco- and mineralo-corticoids were defined as extended RAAS (extRAAS) system. Microarray data sets containing more than 10 normal tissues were downloaded from the GEO database. R software was used to extract expression levels and construct dendrograms of extRAAS genes within each data set. Tissue co-expression modules were then extracted from reproducible gene clusters across data sets. An atlas of the maps of tissue-specific organization of extRAAS was constructed from gene expression and coordination data. Our analysis included 143 data sets containing 4933 samples representing 23 different tissues. Expression data provided an insight on the favored pathways in a given tissue. Gene coordination indicated the existence of tissue-specific modules organized or not around conserved core groups of transcripts. The atlas of tissue-specific organization of extRAAS will help better understand tissue-specific effects of RAAS. This will provide a frame for developing more effective and selective pharmaceuticals targeting extRAAS.

Topics

No keywords indexed for this article. Browse by subject →

References

42

[1]

Robertson, J. I. S., Nichools, M. G. & August, P. The renin-angiotensin system . Mosby1993).

[2]

Michel, J.-B. Médecine cardiovasculaire du système rénine angiotensine. (Ed. Pradel, 1992).

[3]

Paul, M., Mehr, A. P. & Kreutz, R. Physiology of Local Renin-Angiotensin Systems. Physiol. Rev. 86, 747–803 (2006). 10.1152/physrev.00036.2005

[4]

Ahmad, S. et al. Chymase-dependent generation of angiotensin II from angiotensin-(1–12) in human atrial tissue. PloS One, 6, e28501 (2011). 10.1371/journal.pone.0028501

[5]

Uehara, Y., Miura, S., Yahiro, E. & Saku, K. Non-ACE pathway-induced angiotensin II production. Curr. Pharm. Des. 19, 3054–3059 (2013). 10.2174/1381612811319170012

[6]

Kramkowski, K., Mogielnicki, A. & Buczko, W. The physiological significance of the alternative pathways of angiotensin II production. J. Physiol. Pharmacol. Off. J. Pol. Physiol. Soc. 57, 529–539 (2006).

[7]

Akasu, M. et al. Differences in tissue angiotensin II-forming pathways by species and organs in vitro. Hypertension 32, 514–520 (1998). 10.1161/01.hyp.32.3.514

[8]

Engeli, S. et al. Co-expression of renin-angiotensin system genes in human adipose tissue. J. Hypertens. 17, 555–560 (1999). 10.1097/00004872-199917040-00014

[9]

Legedz, L. et al. Cathepsin G is associated with atheroma formation in human carotid artery. J. Hypertens. January 2004 22, 157–166 (2004).

[10]

Legedz, L. et al. Induction of tissue kallikrein in human carotid atheroma does not lead to kallikrein-kinins pathway activation. J. Hypertens. 23, 359–366 (2005). 10.1097/00004872-200502000-00018

[11]

Ayari, H. et al. Mutual amplification of corticosteroids and angiotensin systems in human vascular smooth muscle cells and carotid atheroma. J. Mol. Med. Berl. Ger. (2014). doi: 10.1007/s00109-014-1193-7 10.1007/s00109-014-1193-7

[12]

The renin&ndash;angiotensin system and diabetes: An update

Ana Simoes-e-Silva

Vascular Health and Risk Management 2008 10.2147/vhrm.s1905

[13]

Schwacke, J. H. et al. Network Modeling Reveals Steps in Angiotensin Peptide Processing. Hypertension 61, 690–700 (2013). 10.1161/hypertensionaha.111.00318

[14]

Hodroj, W. et al. Increased Insulin-Stimulated Expression of Arterial Angiotensinogen and Angiotensin Type 1 Receptor in Patients With Type 2 Diabetes Mellitus and Atheroma. Arterioscler. Thromb. Vasc. Biol. 27, 525–531 (2007). 10.1161/01.atv.0000254814.63768.3b

[15]

Speth, R. C. & Giese, M. J. Update on the Renin-Angiotensin System (2013). J. Pharmacol. Clin. Toxicol. Available at: <http://www.jscimedcentral.com/Pharmacology/Articles/pharmacology-1-1004.php>. (Accessed: 10th February 2015).

[16]

Suski, M. et al. The influence of angiotensin-(1–7) Mas receptor agonist (AVE 0991) on mitochondrial proteome in kidneys of apoE knockout mice. Biochim. Biophys. Acta. 1834, 2463–2469 (2013). 10.1016/j.bbapap.2013.08.008

[17]

Irizarry, R. A. et al. Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostat. Oxf. Engl. 4, 249–264 (2003). 10.1093/biostatistics/4.2.249

[18]

Cluster analysis and display of genome-wide expression patterns

Michael B. Eisen, Paul T. Spellman, Patrick O. Brown et al.

Proceedings of the National Academy of Sciences 1998 10.1073/pnas.95.25.14863

[19]

What is principal component analysis?

Markus Ringnér

Nature Biotechnology 2008 10.1038/nbt0308-303

[20]

Finding Groups in Data

Leonard Kaufman, Peter J. Rousseeuw

Wiley Series in Probability and Statistics 10.1002/9780470316801

[21]

Campbell, D. J. & Habener, J. F. Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat. J. Clin. Invest. 78, 31–39 (1986). 10.1172/jci112566

[22]

Jeunemaitre, X. et al. Molecular basis of human hypertension: role of angiotensinogen. Cell 71, 169–180 (1992). 10.1016/0092-8674(92)90275-h

[23]

Smithies, O. & Kim, H. S. Targeted gene duplication and disruption for analyzing quantitative genetic traits in mice. Proc. Natl. Acad. Sci. USA . 91, 3612–3615 (1994). 10.1073/pnas.91.9.3612

[24]

Lutterotti, N. von, Catanzaro, D. F., Sealey, J. E. & Laragh, J. H. Renin is not synthesized by cardiac and extrarenal vascular tissues. A review of experimental evidence. Circulation 89, 458–470 (1994). 10.1161/01.cir.89.1.458

[25]

Itskovitz, J. & Sealey, J. E. Ovarian prorenin-renin-angiotensin system. Obstet. Gynecol. Surv. 42, 545–551 (1987). 10.1097/00006254-198709000-00003

[26]

Shrikrishna, D., Astin, R., Kemp, P. R. & Hopkinson, N. S. Renin-angiotensin system blockade: a novel therapeutic approach in chronic obstructive pulmonary disease. Clin. Sci. Lond. Engl. 1979 123, 487–498 (2012).

[27]

Giacchetti, G. et al. Gene expression of angiotensinogen in adipose tissue of obese patients. Int. J. Obes. Relat. Metab. Disord. J. Int. Assoc. Study Obes . 24 Suppl 2 S142–143 (2000). 10.1038/sj.ijo.0801305

[28]

Ayari, H. et al. Mutual amplification of corticosteroids and angiotensin systems in human vascular smooth muscle cells and carotid atheroma. J. Mol. Med. 1–8 (2014). doi: 10.1007/s00109-014-1193-7 10.1007/s00109-014-1193-7

[29]

Rautureau, Y., Paradis, P. & Schiffrin, E. L. Cross-talk between aldosterone and angiotensin signaling in vascular smooth muscle cells. Steroids 76, 834–839 (2011).

[30]

Jaffe, I. Z. & Mendelsohn, M. E. Angiotensin II and aldosterone regulate gene transcription via functional mineralocortocoid receptors in human coronary artery smooth muscle cells. Circ. Res. 96, 643–650 (2005). 10.1161/01.res.0000159937.05502.d1

[31]

Ayari, H. et al. Auto-amplification of cortisol actions in human carotid atheroma is linked to arterial remodeling and stroke. Fundam. Clin. Pharmacol. 28, 53–64 (2014). 10.1111/j.1472-8206.2012.01064.x

[32]

Briones, A. M. et al. Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension 59, 1069–1078 (2012). 10.1161/hypertensionaha.111.190223

[33]

Chapman, K., Holmes, M. & Seckl, J. 11β-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol. Rev. 93, 1139–1206 (2013). 10.1152/physrev.00020.2012

[34]

Dhaouadi, N. et al. Computational identification of potential transcriptional regulators of TGF-ß1 in human atherosclerotic arteries. Genomics 103, 357–370 (2014). 10.1016/j.ygeno.2014.05.001

[35]

Zhou, L. et al. Multiple Genes of the Renin-Angiotensin System Are Novel Targets of Wnt/β-Catenin Signaling. J. Am. Soc. Nephrol. JASN (2014). doi: 10.1681/ASN.2014010085 10.1681/asn.2014010085

[36]

Williams, C., Rezgui, D., Prince, S. N., Zaccheo, O. J., Foulstone, E. J., Forbes, B.E., Norton, R.S., Crosby, J., Hassan, A.B. & Crump, M.P. Structural Insights into the Interaction of Insulin-like Growth Factor 2 with IGF2R Domain 11. Structure 15, 1065 (2007). PDBe ID: 2CNJ (doi: 10.2210/pdb2cnj/pdb). 10.2210/pdb2cnj/pdb

[37]

Zhang, Y., Gao, X. & Michael Garavito, R. Structural analysis of the intracellular domain of (pro)renin receptor fused to maltose-binding protein. Biochem.Biophys.Res.Commun. 407 674–679 (2011). PDBe ID: 3LBS (doi: 10.2210/pdb3lbs/pdb). 10.2210/pdb3lbs/pdb

[38]

Bledsoe, R. K., Madauss, K. P., Holt, J. A., Apolito, C. J., Lambert, M. H., Pearce, K. H., Stanley, T. B., Stewart, E. L., Trump, R. P., Willson, T. M., Williams, S. P. A Ligand-mediated Hydrogen Bond Network Required for the Activation of the Mineralocorticoid Receptor. J.Biol.Chem. 280 31283–31293 (2005). PDBe ID: 2AA2 (doi: 10.2210/pdb2aa2/pdb). 10.2210/pdb2aa2/pdb

[39]

Kauppi, B., Jakob, C., Farnegardh, M., Yang, J., Ahola, H., Alarcon, M., Calles, K., Engstrom, O., Harlan, J., Muchmore, S., Ramqvist, A.-K., Thorell, S., Ohman, L., Greer, J., Gustafsson, J.-A., Carlstedt-Duke, J. & Carlquist, M. The three-dimensional structures of antagonistic and agonistic forms of the glucocorticoid receptor ligand-binding domain: RU-486 induces a transconformation that leads to active antagonism. J.Biol.Chem. 278 22748–22754 (2003). PDBe ID: 1P93 (doi: 10.2210/pdb1p93/pdb). 10.2210/pdb1p93/pdb

[40]

Lebon, G., Warne, T., Edwards, P. C., Bennett, K., Langmead, C. J., Leslie, A. G. W. & Tate, C. G. Agonist-Bound Adenosine A(2A) Receptor Structures Reveal Common Features of Gpcr Activation. Nature 474 521 (2011). PDBe ID: 2YDO (doi: 10.2210/pdb2ydo/pdb). 10.1038/nature10136

[41]

Hermans, S. J., Ascher, D. B., Hancock, N. C., Holien, J. K., Michell, B. J., Yeen Chai, S., Morton, C. J. & Parker, M. W. Crystal structure of human insulin-regulated aminopeptidase with specificity for cyclic peptides. Protein Sci. 24 190–199 (2015). PDBe ID: 4P8Q (doi: 10.2210/pdb4p8q/pdb). 10.2210/pdb4p8q/pdb

[42]

Epidermal Growth Factor. June 2010 Molecule of the Month by David Goodsell. (doi: 10.2210/rcsb_pdb/mom_2010_6).

Cited By

64

Emerging importance of ACE2 in external stratified epithelial tissues

Nihal Kaplan, Elena Gonzalez · 2021

Molecular and Cellular Endocrinolog...

Metrics

64

Citations

42

References

Details

Published: May 20, 2015
Vol/Issue: 5(1)
License: View

Authors

6Hospices Civils de Lyon, Service de cardiologie, IMMUCARE, Hôpital de la Croix-Rousse et Hôpital Lyon Sud, Lyon, France; Université de Lyon, CREATIS UMR INSERM U1044, INSA, Lyon France.

Cite This Article

Ali Nehme, Catherine Cerutti, Nedra Dhaouadi, et al. (2015). Atlas of tissue renin-angiotensin-aldosterone system in human: A transcriptomic meta-analysis. Scientific Reports, 5(1). https://doi.org/10.1038/srep10035

Atlas of tissue renin-angiotensin-aldosterone system in human: A transcriptomic meta-analysis

You May Also Like