Angiotensin II Increases Oxidative Stress and Inflammation in Female, But Not Male, Endothelial Cells

Springer Science and Business Media LLC - Tập 16 - Trang 127-141 - 2023
Callie M. Weber1, Mikayla N. Harris2, Sophia M. Zic1, Gurneet S. Sangha1, Nicole S. Arnold2, Douglas F. Dluzen2, Alisa Morss Clyne1
1Fischell Department of Bioengineering, University of Maryland, College Park, USA
2Department of Biology, Morgan State University, Baltimore, USA

Tóm tắt

Women are at elevated risk for certain cardiovascular diseases, including pulmonary arterial hypertension, Alzheimer’s disease, and vascular complications of diabetes. Angiotensin II (AngII), a circulating stress hormone, is elevated in cardiovascular disease; however, our knowledge of sex differences in the vascular effects of AngII are limited. We therefore analyzed sex differences in human endothelial cell response to AngII treatment. Male and female endothelial cells were treated with AngII for 24 h and analyzed by RNA sequencing. We then used endothelial and mesenchymal markers, inflammation assays, and oxidative stress indicators to measure female and male endothelial cell functional changes in response to AngII. Our data show that female and male endothelial cells are transcriptomically distinct. Female endothelial cells treated with AngII had widespread gene expression changes related to inflammatory and oxidative stress pathways, while male endothelial cells had few gene expression changes. While both female and male endothelial cells maintained their endothelial phenotype with AngII treatment, female endothelial cells showed increased release of the inflammatory cytokine interleukin-6 and increased white blood cell adhesion following AngII treatment concurrent with a second inflammatory cytokine. Additionally, female endothelial cells had elevated reactive oxygen species production compared to male endothelial cells after AngII treatment, which may be partially due to nicotinamide adenine dinucleotide phosphate oxidase-2 (NOX2) escape from X-chromosome inactivation. These data suggest that endothelial cells have sexually dimorphic responses to AngII, which could contribute to increased prevalence of some cardiovascular diseases in women.

Tài liệu tham khảo

Hadi, H. A. R., C. S. Carr, and J. AlSuwaidi. Endothelial dysfunction: cardiovascular risk factors, therapy, and outcome. Vasc. Health Risk Manag. 1:183–198, 2005.

McGoon, M. D., R. L. Benza, P. Escribano-Subias, X. Jiang, D. P. Miller, A. J. Peacock, J. Pepke-Zaba, T. Pulido, S. Rich, S. Rosenkranz, S. Suissa, and M. Humbert. Pulmonary arterial hypertension: Epidemiology and registries. J. Am. Coll. Cardiol. 62:D51–D59, 2013.

Alzheimer’s Association. Alzheimer’s disease facts and figures. Alzheimer’s Dementia. 15(3):321–387, 2022.

de Ritter, R., M. de Jong, R. C. Vos, C. J. H. van der Kallen, S. J. S. Sep, M. Woodward, C. D. A. Stehouwer, M. Lp, and S. A. E. Bots. Sex differences in the risk of vascular disease associated with diabetes. Biol. Sex Differ. 11:1–11, 2020.

Hartman, R. J. G., D. M. C. Kapteijn, S. Haitjema, M. N. Bekker, M. Mokry, G. Pasterkamp, M. Civelek, and H. M. den Ruijter. Intrinsic transcriptomic sex differences in human endothelial cells at birth and in adults are associated with coronary artery disease targets. Sci. Rep. 10:1–12, 2020.

Carrel, L., and H. F. Willard. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature. 434:400–404, 2005.

Zhang, Y., A. Castillo-Morales, M. Jiang, Y. Zhu, L. Hu, A. O. Urrutia, X. Kong, and L. D. Hurst. Genes that escape X-inactivation in humans have high intraspecific variability in expression, are associated with mental impairment but are not slow evolving. Mol. Biol. Evol. 30:2588–2601, 2013.

Lorenz, M., J. Koschate, K. Kaufmann, C. Kreye, M. Mertens, W. M. Kuebler, G. Baumann, G. Gossing, A. Marki, A. Zakrzewicz, C. Miéville, A. Benn, D. Horbelt, P. R. Wratil, K. Stangl, and V. Stangl. Does cellular sex matter? Dimorphic transcriptional differences between female and male endothelial cells. Atherosclerosis. 240:61–72, 2015.

Lorenz, M., B. Blaschke, A. Benn, E. Hammer, E. Witt, J. Kirwan, R. Fritsche-Guenther, Y. Gloaguen, C. Bartsch, A. Vietzke, F. Kramer, K. Kappert, P. Brunner, H. G. Nguyen, H. Dreger, K. Stangl, P. Knaus, and V. Stangl. Sex-specific metabolic and functional differences in human umbilical vein endothelial cells from twin pairs. Atherosclerosis. 291:99–106, 2019.

Addis, R., I. Campesi, M. Fois, G. Capobianco, S. Dessole, G. Fenu, A. Montella, M. G. Cattaneo, L. M. Vicentini, and F. Franconi. Human umbilical endothelial cells (HUVECs) have a sex: Characterisation of the phenotype of male and female cells. Biol. Sex Differ. 5:1–12, 2014.

James, B. D., and J. B. Allen. Sex-specific response to combinations of shear stress and substrate stiffness by endothelial cells in vitro. Adv. Healthc. Mater. 10:2100735, 2021.

AbdAlla, S., A. el Hakim, A. Abdelbaset, Y. Elfaramawy, and U. Quitterer. Inhibition of ACE retards tau hyperphosphorylation and signs of neuronal degeneration in aged rats subjected to chronic mild stress. Biomed. Res. Int. 2015:917156, 2015.

Choi, H., T. L. Leto, L. Hunyady, K. J. Catt, S. B. Yun, and G. R. Sue. Mechanism of angiotensin II-induced superoxide production in cells reconstituted with angiotensin type 1 receptor and the components of NADPH oxidase. J. Biol. Chem. 283:255–267, 2008.

Romero, J. C., and J. F. Reckelhoff. Role of angiotensin and oxidative stress in essential hypertension. Hypertension. 34:943–949, 1999.

Bruner, C. A., J. M. Weaver, and G. D. Fink. Sodium-dependent hypertension produced by chronic central angiotensin II infusion. Am. J. Physiol. Heart Circ. Physiol. 18:H321, 1985.

Heeneman, S., J. F. M. Smits, P. J. A. Leenders, P. M. H. Schiffers, and M. J. A. P. Daemen. Effects of angiotensin II on cardiac function and peripheral vascular structure during compensated heart failure in the rat. Arterioscler. Thromb. Vasc. Biol. 17:1985–1994, 1997.

Landmesser, U., H. Cai, S. Dikalov, L. McCann, J. Hwang, H. Jo, S. M. Holland, and D. G. Harrison. Role of p47phox in vascular oxidative stress and hypertension caused by angiotensin II. Hypertension. 40:511–515, 2002.

Madhur, M. S., S. A. Funt, L. Li, A. Vinh, W. Chen, H. E. Lob, Y. Iwakura, Y. Blinder, A. Rahman, A. A. Quyyumi, and D. G. Harrison. Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein e-deficient mice. Arterioscler. Thromb. Vasc. Biol. 31:1565–1572, 2011.

Li, W. J., Y. Liu, J. J. Wang, Y. L. Zhang, S. Lai, Y. L. Xia, H. X. Wang, and H. H. Li. “angiotensin II memory” contributes to the development of hypertension and vascular injury via activation of NADPH oxidase. Life Sci. 149:18–24, 2016.

Ryan, M. J., S. P. Didion, S. Mathur, F. M. Faraci, and C. D. Sigmund. Angiotensin II-induced vascular dysfunction is mediated by the AT 1A receptor in mice. Hypertension. 43:1074–1079, 2004.

Rio, D. C., M. Ares, G. J. Hannon, and T. W. Nilsen. Purification of RNA using TRIzol (TRI Reagent). Cold Spring Harb. Protoc. 5:5439, 2010.

Tarca, A. L., S. Draghici, P. Khatri, S. S. Hassan, P. Mittal, J.-S. Kim, C. J. Kim, J. P. Kusanovic, and R. Romero. A novel signaling pathway impact analysis. Bioinformatics. 25:75–82, 2009.

Ahsan, S., and S. Drăghici. Identifying significantly impacted pathways and putative mechanisms with iPathwayGuide. Curr. Protoc. Bioinform. 2017:7.15.1-7.15.30, 2017.

de Man, F. S., L. Tu, M. L. Handoko, S. Rain, G. Ruiter, C. François, I. Schalij, P. Dorfmüller, G. Simonneau, E. Fadel, and F. Perros. Dysregulated renin–angiotensin–aldosterone system contributes to pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 186(8):780–789, 2012.

Ranchoux, B., F. Antigny, C. Rucker-Martin, A. Hautefort, C. Péchoux, H. J. Bogaard, P. Dorfmüller, S. Remy, F. Lecerf, S. Planté, S. Chat, E. Fadel, A. Houssaini, I. Anegon, S. Adnot, G. Simonneau, M. Humbert, S. Cohen-Kaminsky, and F. Perros. Endothelial-to-mesenchymal transition in pulmonary hypertension. Circulation. 131:1006–1018, 2015.

Kehoe, P. G., S. Miners, and S. Love. Angiotensins in Alzheimer’s disease-friend or foe? Trends Neurosci. 32:619–628, 2009.

Birk, M., E. Baum, J. K. Zadeh, C. Manicam, N. Pfeiffer, A. Patzak, J. Helmstädter, S. Steven, M. Kuntic, A. Daiber, and A. Gericke. Angiotensin II induces oxidative stress and endothelial dysfunction in mouse ophthalmic arteries via involvement of AT1 receptors and NOX2. Antioxidants. 10:1238, 2021.

Khramtsova, E. A., L. K. Davis, and B. E. Stranger. The role of sex in the genomics of human complex traits. Nat. Rev. Genet. 20:494, 2019.

Oliva, M., et al. The impact of sex on gene expression across human tissues. Science. 369(eaba3066):2020, 1979.

Xiao, L., D. J. Kim, C. L. Davis, J. V. McCann, J. M. Dunleavey, A. K. Vanderlinden, N. Xu, S. G. Pattenden, S. V. Frye, X. Xu, and M. Onaitis. Tumor endothelial cells with distinct patterns of TGFβ-driven endothelial-to-mesenchymal transition endothelial-to-mesenchymal transition. Cancer Res. 75(7):1244–1254, 2015.

Robertson, I. B., and D. B. Rifkin. Regulation of the bioavailability of TGF-β and TGF-β-related proteins. Cold Spring Harb. Perspect. Biol.8:a021907, 2016.

Walton, K. L., Y. Makanji, J. Chen, M. C. Wilce, K. L. Chan, D. M. Robertson, and C. A. Harrison. Two distinct regions of latency-associated peptide coordinate stability of the latent transforming growth factor-Î21 complex*. J. Biol. Chem. 285:17029–17037, 2010.

Miyazono, K., A. Olofsson, P. Colosetti, and C. H. Heldin. A role of the latent TGF-β1-binding protein in the assembly and secretion of TGF-β1. EMBO J. 10:1091–1101, 1991.

Maleszewska, M., J. R. A. J. Moonen, N. Huijkman, B. van de Sluis, G. Krenning, and M. C. Harmsen. IL-1β and TGFβ2 synergistically induce endothelial to mesenchymal transition in an NFκB-dependent manner. Immunobiology. 218:443–454, 2013.

Yoshimatsu, Y., I. Wakabayashi, S. Kimuro, N. Takahashi, K. Takahashi, M. Kobayashi, N. Maishi, K. A. Podyma-Inoue, K. Hida, K. Miyazono, and T. Watabe. TNF-α enhances TGF-β-induced endothelial-to-mesenchymal transition via TGF-β signal augmentation. Cancer Sci. 111:2385–2399, 2020.

Evrard, S. M., L. Lecce, K. C. Michelis, A. Nomura-Kitabayashi, G. Pandey, K. R. Purushothaman, V. D’Escamard, J. R. Li, L. Hadri, K. Fujitani, P. R. Moreno, L. Benard, P. Rimmele, A. Cohain, B. Mecham, G. J. Randolph, E. G. Nabel, R. Hajjar, V. Fuster, M. Boehm, and J. C. Kovacic. Endothelial to mesenchymal transition is common in atherosclerotic lesions and is associated with plaque instability. Nat. Commun. 7:11853, 2016.

Aguado, B. A., C. J. Walker, J. C. Grim, M. E. Schroeder, D. Batan, B. J. Vogt, A. G. Rodriguez, J. A. Schwisow, K. S. Moulton, R. M. Weiss, D. D. Heistad, L. A. Leinwand, and K. S. Anseth. Genes that escape X chromosome inactivation modulate sex differences in valve myofibroblasts. Circulation. 145:513–530, 2022.

Ma, J., G. van der Zon, M. A. F. V. Gonçalves, M. van Dinther, M. Thorikay, G. Sanchez-Duffhues, and P. ten Dijke. TGF-β-induced endothelial to mesenchymal transition is determined by a balance between SNAIL and ID factors. Front. Cell Dev. Biol. 9:182, 2021.

Paschoud, S., A. M. Dogar, C. Kuntz, B. Grisoni-Neupert, L. Richman, and L. C. Kühn. Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNA-binding protein AUF1. Mol. Cell Biol. 26:8228–8241, 2006.

Masuda, K., B. Ripley, R. Nishimura, T. Mino, O. Takeuchi, G. Shioi, H. Kiyonari, and T. Kishimoto. Arid5a controls IL-6 mRNA stability, which contributes to elevation of IL-6 level in vivo. Proc. Natl. Acad. Sci. USA. 110:9409–9414, 2013.

Matsushita, K., O. Takeuchi, D. M. Standley, Y. Kumagai, T. Kawagoe, T. Miyake, T. Satoh, H. Kato, T. Tsujimura, H. Nakamura, and S. Akira. Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature. 458:1185–1190, 2009.

Elias, J. A., and V. Lentz. IL-1 and tumor necrosis factor synergistically stimulate fibroblast IL-6 production and stabilize IL-6 messenger RNA. J. Immunol. 145:161–166, 1990.

Simonneau, G., D. Montani, D. S. Celermajer, C. P. Denton, M. A. Gatzoulis, M. Krowka, P. G. Williams, and R. Souza. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur. Respir. J. 53:1801913, 2019.

Kostyunina, D. S., and P. McLoughlin. Sex dimorphism in pulmonary hypertension: the role of the sex chromosomes. Antioxidants. 10:779, 2021.

Mitchell, S. M., S. Lange, and H. Brus. Gendered citation patterns in international relations journals. Int. Stud. Perspect. 14:485–492, 2013.

Dion, M. L., J. L. Sumner, and S. M. Mitchell. Gendered citation patterns across political science and social science methodology fields. Polit. Anal. 26:312–327, 2018.

Caplar, N., S. Tacchella, and S. Birrer. Quantitative evaluation of gender bias in astronomical publications from citation counts. Nat. Astron. 1:141, 2017.

Maliniak, D., R. Powers, and B. F. Walter. The gender citation gap in international relations. Int. Organ. 67:889–922, 2013.

Dworkin, J. D., K. A. Linn, E. G. Teich, P. Zurn, R. T. Shinohara, and D. S. Bassett. The extent and drivers of gender imbalance in neuroscience reference lists. bioRxiv. 2020. https://doi.org/10.1101/2020.01.03.894378.

Bertolero, M. A., J. D. Dworkin, S. U. David, C. L. Lloreda, P. Srivastava, J. Stiso, D. Zhou, K. Dzirasa, D. A. Fair, A. N. Kaczkurkin, B. J. Marlin, D. Shohamy, L. Q. Uddin, P. Zurn, and D. S. Bassett. Racial and ethnic imbalance in neuroscience reference lists and intersections with gender. bioRxiv. 64:583, 2020.

Wang, X., J. D. Dworkin, D. Zhou, J. Stiso, E. B. Falk, D. S. Bassett, P. Zurn, and D. M. Lydon-Staley. Gendered citation practices in the field of communication. Ann. Int. Commun. Assoc. 2021. https://doi.org/10.1080/23808985.2021.1960180.

Chatterjee, P., and R. M. Werner. Gender disparity in citations in high-impact journal articles. JAMA Netw. Open.4:e2114509, 2021.

Fulvio, J. M., I. Akinnola, and B. R. Postle. Gender (im)balance in citation practices in cognitive neuroscience. J. Cogn. Neurosci. 33:3–7, 2021.

Zhou, D., E. J. Cornblath, J. Stiso, E. G. Teich, J. D. Dworkin, A. S. Blevins, and D. S. Bassett. Gender Diversity Statement and Code Notebook v1.0. 2020. https://doi.org/10.5281/zenodo.3672110

Ambekar, A., C. Ward, J. Mohammed, S. Male, and S. Skiena. Name-ethnicity classification from open sources. 2009.

Sood, G., and S. Laohaprapanon. Predicting race and ethnicity from the sequence of characters in a name. arXiv:1805.02109, 2018.

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