Sodium-induced inflammation-an invisible player in resistant hypertension.
Factor XII
Glycocalyx
Inflammation
RAAS
Salt sensitivity
Journal
Hypertension research : official journal of the Japanese Society of Hypertension
ISSN: 1348-4214
Titre abrégé: Hypertens Res
Pays: England
ID NLM: 9307690
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
28
12
2019
accepted:
18
01
2020
revised:
18
01
2020
pubmed:
24
3
2020
medline:
18
8
2021
entrez:
24
3
2020
Statut:
ppublish
Résumé
The purpose of this review was to discuss the role of sodium and inflammation in the pathophysiology of hypertension and the observed different hemodynamic effects of drugs. The Pathway-2 study revealed that similar reductions in vascular resistance after spironolactone and doxazosin resulted in opposite effects on sodium balance, water retention, and hemodynamic parameters. These and other clinical findings were bridged to recent experimental and physiological data. Tissue sodium accumulation in salt-sensitive individuals due to endothelial glycocalyx dysfunction causes macrophage infiltration, vascular inflammation, and local changes in angiotensin-2 and aldosterone concentrations. This inflammatory cascade leads to factor XII-related coagulation disorders with neutrophil extracellular trap formation (NETosis). This model of sodium-induced microcirculation impairment was used to explain the differences in central hemodynamic parameters after spironolactone or doxazosin treatment in resistant hypertension. Hypertension treatment by induced sodium removal or reduced sodium intake should reduce endothelial glycocalyx dysfunction, inflammation, NETosis, and coagulation disorders, leading to improved vascular health and cardiac diastolic function.
Identifiants
pubmed: 32203452
doi: 10.1038/s41440-020-0428-y
pii: 10.1038/s41440-020-0428-y
doi:
Substances chimiques
Sodium Chloride, Dietary
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
629-633Références
Williams B, MacDonald TM, Morant S, Webb DJ, Sever P, McInnes G, et al. Spironolactone versus placebo, bisoprolol, and doxazosin to determine the optimal treatment for drug-resistant hypertension (PATHWAY-2): a randomised, double-blind, crossover trial. Lancet. 2015;386:2059–68.
doi: 10.1016/S0140-6736(15)00257-3
Williams B, MacDonald TM, Morant SV, Webb DJ, Sever P, McInnes GT, et al. Endocrine and haemodynamic changes in resistant hypertension, and blood pressure responses to spironolactone or amiloride: the PATHWAY-2 mechanisms substudies. Lancet Diabetes Endocrinol.2018;6:464–75. [b] This study presents key data on the renin and aldosterone balance in patients treated for resistant hypertension with various standard medications. It also describes hemodynamic changes observed with the selected drugs.
doi: 10.1016/S2213-8587(18)30071-8
Kurtz TW, DiCarlo SE, Pravenec M, Morris RC. Changing views on the common physiologic abnormality that mediates salt sensitivity and initiation of salt-induced hypertension: Japanese research underpinning the vasodysfunction theory of salt sensitivity. Hypertens Res. 2019;42:6–18. https://doi.org/10.1038/s41440-018-0122-5 .
doi: 10.1038/s41440-018-0122-5
pubmed: 30390036
Forouzanfar MH, Alexander L, Anderson HR, Bachman VF, Biryukov S, Brauer M, et al. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;386:2287–323.
doi: 10.1016/S0140-6736(15)00128-2
Morimoto A, Uzu T, Fujii T, Nishimura M, Kuroda S, Nakamura S, et al. Sodium sensitivity and cardiovascular events in patients with essential hypertension. Lancet. 1997;350:1734–7.
doi: 10.1016/S0140-6736(97)05189-1
Wiig H, Swartz MA. Interstitial fluid and lymph formation and transport: physiological regulation and roles in inflammation and cancer. Physiol Rev. 2012;92:1005–60.
doi: 10.1152/physrev.00037.2011
Oberleithner H, Sodium selective erythrocyte glycocalyx and salt sensitivity in man. Pflugers Arch. 2015;467:1319–25. https://www.ncbi.nlm.nih.gov/pubmed/25027385 .
doi: 10.1007/s00424-014-1577-0
Olde Engberink RHG, Selvarajah V, Vogt L. Clinical impact of tissue sodium storage. Pediatr Nephrol. 2019. https://doi.org/10.1007/s00467-019-04305-8 .
Laffer CL, Scott RC 3rd, Titze JM, Luft FC, Elijovich F. Hemodynamics and salt-and-water balance link sodium storage and vascular dysfunction in salt-sensitive subjects. Hypertension. 2016;68:195–203. [a] This reveals the effect of salt loading and depletion in salt-sensitive and salt-resistant human subjects for the first time.
doi: 10.1161/HYPERTENSIONAHA.116.07289
Olde Engberink RHG, Rorije NMG, Lambers Heerspink HJ, De Zeeuw D, van den Born B-JH, Vogt L. The blood pressure lowering potential of sulodexide-a systematic review and meta-analysis. Br J Clin Pharmacol Engl. 2015;80:1245–53.
doi: 10.1111/bcp.12722
Schierke F, Wyrwoll MJ, Wisdorf M, Niedzielski L, Maase M, Ruck T, et al. Nanomechanics of the endothelial glycocalyx contribute to Na+-induced vascular inflammation. Sci Rep. 2017;7:46476. https://doi.org/10.1038/srep46476 .
doi: 10.1038/srep46476
pubmed: 28406245
pmcid: 5390251
Muller DN, Wilck N, Haase S, Kleinewietfeld M, Linker RA. Sodium in the microenvironment regulates immune responses and tissue homeostasis. Nat Rev Immunol Engl. 2019;19:243–54. [a] This review offers insight into the precise mechanisms of immune regulation via tissue sodium concentrations. It also describes the role of such regulation in cardiovascular and other diseases.
doi: 10.1038/s41577-018-0113-4
Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. England. 2013;496:518–22.
Chadwick JA, Swager SA, Lowe J, Welc SS, Tidball JG, Gomez-Sanchez CE, et al. Myeloid cells are capable of synthesizing aldosterone to exacerbate damage in muscular dystrophy. Hum Mol Genet Engl. 2016;25:5167–77.
Natarajan R, Stern N, Hsueh W, Do Y, Nadler J. Role of the lipoxygenase pathway in angiotensin II-mediated aldosterone biosynthesis in human adrenal glomerulosa cells. J Clin Endocrinol Metab. 1988;67:584–91.
doi: 10.1210/jcem-67-3-584
Kirabo A. A new paradigm of sodium regulation in inflammation and hypertension. Am J Physiol Regul Integr Comp Physiol. 2017;313:R706–10. [b] This is a comprehensive review of earlier studies on the role of sodium in inflammation and hypertension and highlights the gaps, some of which our article attempts to bridge using recent data. The authors conclude that “understanding mechanisms of salt and body fluid regulation is the sine qua non of research efforts to identify therapeutic targets for hypertension and cardiovascular disease.”
doi: 10.1152/ajpregu.00250.2017
Stavrou EX, Fang C, Bane KL, Long AT, Naudin C, Kucukal E, et al. Factor XII and uPAR upregulate neutrophil functions to influence wound healing. J Clin Investig.2018;128:944–59.
doi: 10.1172/JCI92880
Wang Y, Luo L, Braun OO, Westman J, Madhi R, Herwald H, et al. Neutrophil extracellular trap-microparticle complexes enhance thrombin generation via the intrinsic pathway of coagulation in mice. Sci Rep. 2018;8:4020.
doi: 10.1038/s41598-018-22156-5
Kamat NV, Thabet SR, Xiao L, Saleh MA, Kirabo A, Madhur MS, et al. Renal transporter activation during angiotensin-II hypertension is blunted in interferon-gamma-/- and interleukin-17A-/- mice. Hypertension. 2015;65:569–76.
doi: 10.1161/HYPERTENSIONAHA.114.04975
Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol Engl. 2013;13:34–45.
doi: 10.1038/nri3345
Arai Y, Yamashita K, Mizugishi K, Watanabe T, Sakamoto S, Kitano T, et al. Serum neutrophil extracellular trap levels predict thrombotic microangiopathy after allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2013;19:1683–9.
doi: 10.1016/j.bbmt.2013.09.005
Matam V-K, Piu S, San YB, Rachel G, Cameron M, Adam S, et al. Abstract P1126: Neutrophil Extracellular Traps: New Players in Hypertension. Hypertension. 2019;74:AP1126–AP1126. https://doi.org/10.1161/hyp.74.suppl_1.P1126 . [a] This abstract briefly describes the results of experimental research on the role of neutrophils and certain inflammatory signaling molecules in the development of hypertension. The authors demonstrated that NETs are an important feature directly linked to elevated BP in a strain-independent manner
doi: 10.1161/hyp.74.suppl_1.P1126
Shefer G, Marcus Y, Knoll E, Dolkart O, Foichtwanger S, Nevo N, et al. Angiotensin 1-7 is a negative modulator of aldosterone secretion in vitro and in vivo. Hypertension. 2016;68:378–84.
doi: 10.1161/HYPERTENSIONAHA.116.07088
Schmaier AH. The contact activation and kallikrein/kinin systems: pathophysiologic and physiologic activities. J Thromb Haemost. 2016;14:28–39.
doi: 10.1111/jth.13194
Hood SJ, Taylor KP, Ashby MJ, Brown MJ.The spironolactone, amiloride, losartan, and thiazide (SALT) double-blind crossover trial in patients with low-renin hypertension and elevated aldosterone-renin ratio. Circulation. 2007;116:268–75.
doi: 10.1161/CIRCULATIONAHA.107.690396
Brown MJ, Williams B, Morant SV, Webb DJ, Caulfield MJ, Cruickshank JK, et al. Effect of amiloride, or amiloride plus hydrochlorothiazide, versus hydrochlorothiazide on glucose tolerance and blood pressure (PATHWAY-3): a parallel-group, double-blind randomised phase 4 trial. Lancet Diabetes Endocrinol. 2016;4:136–47. https://doi.org/10.1016/S2213-8587(15)00377-0 .
doi: 10.1016/S2213-8587(15)00377-0
pubmed: 26489809
pmcid: 4728199
Navar LG, Kobori H, Prieto MC, Gonzalez-Villalobos RA. Intratubular renin-angiotensin system in hypertension. Hypertension. 2011;57:355–62. https://www.ncbi.nlm.nih.gov/pubmed/21282552
doi: 10.1161/HYPERTENSIONAHA.110.163519
Drumm K, Kress TR, Gassner B, Krug AW, Gekle M. Aldosterone stimulates activity and surface expression of NHE3 in human primary proximal tubule epithelial cells (RPTEC). Cell Physiol Biochem. 2006;17:21–8.
doi: 10.1159/000091456
Dahlmann A, Dorfelt K, Eicher F, Linz P, Kopp C, Mossinger I, et al. Magnetic resonance-determined sodium removal from tissue stores in hemodialysis patients. Kidney Int. 2015;87:434–41.
doi: 10.1038/ki.2014.269
Chamarthi B, Williams JS, Williams GH. A mechanism for salt-sensitive hypertension: abnormal dietary sodium-mediated vascular response to angiotensin-II. J Hypertens Engl. 2010;28:1020–6.
doi: 10.1097/HJH.0b013e3283375974
Markou A, Sertedaki A, Kaltsas G, Androulakis II, Marakaki C, Pappa T, et al. Stress-induced aldosterone hyper-secretion in a substantial subset of patients with essential hypertension. J Clin Endocrinol Metab. 2015;100:2857–64.
doi: 10.1210/jc.2015-1268
Pabel S, Wagner S, Bollenberg H, Bengel P, Kovacs A, Schach C, et al. Empagliflozin directly improves diastolic function in human heart failure. Eur J Heart Fail. 2018;20:1690–700. [a] This study demonstrates that sodium balance modified by empagliflozin plays an important role in hemodynamics, improving diastolic function.
doi: 10.1002/ejhf.1328