Dietary salt promotes neurovascular and cognitive dysfunction through a gut-initiated TH17 response

Nature Neuroscience

Volumn 21, Issue 2, 2018, Pages 240-249

  Faraco, Giuseppe ^a   Brea, David ^a   Garcia Bonilla, Lidia ^a   Wang, Gang ^a   Racchumi, Gianfranco ^a   Chang, Haejoo ^a   Buendia, Izaskun ^a   Santisteban, Monica M ^a   Segarra, Steven G ^a   Koizumi, Kenzo ^a   Sugiyama, Yukio ^a   Murphy, Michelle ^a   Voss, Henning ^b   Anrather, Joseph ^a   Iadecola, Costantino ^a  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; NITRIC OXIDE SYNTHASE; RHO KINASE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACETYLCHOLINE; AMIDE; ANTIHYPERTENSIVE AGENT; ENZYME INHIBITOR; HOMEODOMAIN PROTEIN; PYRIDINE DERIVATIVE; RAG-1 PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN BLOOD FLOW; BRAIN FUNCTION; BRAIN MICROCIRCULATION; CELL EXPANSION; CELL MEMBRANE DEPOLARIZATION; CEREBROVASCULAR DISEASE; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; ENVIRONMENTAL FACTOR; HBEC CELL LINE (BRAIN); MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SALT INTAKE; SMALL INTESTINE; TH17 CELL; ANIMAL; BLOOD; BRAIN CIRCULATION; C57BL MOUSE; CELL DIFFERENTIATION; CELL POLARITY; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEUROVASCULAR COUPLING; PATHOLOGY; PHOSPHORYLATION; TOXICITY; TRANSGENIC MOUSE;

ACETYLCHOLINE; AMIDES; ANIMALS; ANTIHYPERTENSIVE AGENTS; CELL DIFFERENTIATION; CELL POLARITY; CEREBROVASCULAR CIRCULATION; CEREBROVASCULAR DISORDERS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; INTERLEUKIN-17; INTESTINE, SMALL; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROVASCULAR COUPLING; PHOSPHORYLATION; PYRIDINES; SODIUM CHLORIDE, DIETARY; TH17 CELLS;

EID: 85040646955     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/s41593-017-0059-z     Document Type: Article

References (50)

1. Mozaffarian, D. et al. Global sodium consumption and death from cardiovascular causes. N. Engl. J. Med. 371, 624-634 (2014).
2. Zemel, M. B. & Sowers, J. R. Salt sensitivity and systemic hypertension in the elderly. Am. J. Cardiol. 61, 7H-12H (1988).
3. Farquhar, W. B., Edwards, D. G., Jurkovitz, C. T. & Weintraub, W. S. Dietary sodium and health: more than just blood pressure. J. Am. Coll. Cardiol. 65, 1042-1050 (2015).
4. Appel, L. J. et al. The importance of population-wide sodium reduction as a means to prevent cardiovascular disease and stroke: a call to action from the American Heart Association. Circulation 123, 1138-1143 (2011).
5. Institute of Medicine (US) Committee on Strategies to Reduce Sodium Intake. Strategies to Reduce Sodium Intake in the United States. (Henney, J.E., Taylor, C.L. & Boon, C.S. eds.) (National Academies Press, Washington DC, 2010).
6. Kotchen, T. A., Cowley, A. W. Jr. & Frohlich, E. D. Salt in health and disease-a delicate balance. N. Engl. J. Med. 368, 1229-1237 (2013).
7. Nicholls, M. G. Population-wide dietary sodium restriction: a cautious view. Curr. Hypertens. Rep. 13, 325-327 (2011).
8. Oh, Y. S. et al. National Heart, Lung, and Blood Institute Working Group report on salt in human health and sickness: building on the current scientific evidence. Hypertension 68, 281-288 (2016).
9. Heye, A. K. et al. Blood pressure and sodium: association with MRI markers in cerebral small vessel disease. J. Cereb. Blood Flow. Metab. 36, 264-274 (2016).
10. Strazzullo, P., D'Elia, L., Kandala, N.-B. & Cappuccio, F. P. Salt intake, stroke, and cardiovascular disease: meta-analysis of prospective studies. Br. Med. J. 339, b4567 (2009).
11. Boegehold, M. A. The effect of high salt intake on endothelial function: reduced vascular nitric oxide in the absence of hypertension. J. Vasc. Res. 50, 458-467 (2013).
12. Cosic, A. et al. Attenuated flow-induced dilatation of middle cerebral arteries is related to increased vascular oxidative stress in rats on a short-term high salt diet. J. Physiol. (Lond.) 594, 4917-4931 (2016).
13. Iadecola, C. The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron 96, 17-42 (2017).
14. Iadecola, C. The pathobiology of vascular dementia. Neuron 80, 844-866 (2013).
15. Kleinewietfeld, M. et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496, 518-522 (2013).
16. Wu, C. et al. Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 496, 513-517 (2013).
17. Kebir, H. et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13, 1173-1175 (2007).
18. Nguyen, H. et al. Interleukin-17 causes Rho-kinase-mediated endothelial dysfunction and hypertension. Cardiovasc. Res. 97, 696-704 (2013).
19. Powles, J. et al. Global, regional and national sodium intakes in 1990 and 2010: a systematic analysis of 24 h urinary sodium excretion and dietary surveys worldwide. BMJ Open. 3, e003733 (2013).
20. Cochet, H. et al. Comprehensive phenotyping of salt-induced hypertensive heart disease in living mice using cardiac magnetic resonance. Eur. Radiol. 23, 332-338 (2013).
21. Schlote, J. et al. Cardiovascular and renal effects of high salt diet in GDNF+ /- mice with low nephron number. Kidney Blood Press. Res. 37, 379-391 (2013).
22. Jackman, K. A. et al. Dichotomous effects of chronic intermittent hypoxia on focal cerebral ischemic injury. Stroke 45, 1460-1467 (2014).
23. Toda, N., Ayajiki, K. & Okamura, T. Cerebral blood flow regulation by nitric oxide: recent advances. Pharmacol. Rev. 61, 62-97 (2009).
24. Wang, G. et al. Angiotensin II slow-pressor hypertension enhances NMDA currents and NOX2-dependent superoxide production in hypothalamic paraventricular neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R1096-R1106 (2013).
25. Chen, B. R., Kozberg, M. G., Bouchard, M. B., Shaik, M. A. & Hillman, E. M. C. A critical role for the vascular endothelium in functional neurovascular coupling in the brain. J. Am. Heart Assoc. 3, e000787 (2014).
26. Poggesi, A., Pasi, M., Pescini, F., Pantoni, L. & Inzitari, D. Circulating biologic markers of endothelial dysfunction in cerebral small vessel disease: a review. J. Cereb. Blood Flow. Metab. 36, 72-94 (2016).
27. Cohen, S. J. et al. The rodent hippocampus is essential for nonspatial object memory. Curr. Biol. 23, 1685-1690 (2013).
28. Barnes, C. A. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93, 74-104 (1979).
29. Deacon, R. M. Assessing nest building in mice. Nat. Protoc. 1, 1117-1119 (2006).
30. Rosenblum, W. I., Nelson, G. H. & Shimizu, T. L-Arginine suffusion restores response to acetylcholine in brain arterioles with damaged endothelium. Am. J. Physiol. 262, H961-H964 (1992).
31. Harris, M. B. et al. Reciprocal phosphorylation and regulation of endothelial nitric-oxide synthase in response to bradykinin stimulation. J. Biol. Chem. 276, 16587-16591 (2001).
32. Smith, L., Payne, J. A., Sedeek, M. H., Granger, J. P. & Khalil, R. A. Endothelin-induced increases in Ca2+ entry mechanisms of vascular contraction are enhanced during high-salt diet. Hypertension 41, 787-793 (2003).
33. Faraco, G. et al. Circulating endothelin-1 alters critical mechanisms regulating cerebral microcirculation. Hypertension 62, 759-766 (2013).
34. Benakis, C. et al. Commensal microbiota affects ischemic stroke outcome by regulating intestinal γ δ T cells. Nat. Med. 22, 516-523 (2016).
35. Hernandez, A. L. et al. Sodium chloride inhibits the suppressive function of FOXP3+ regulatory T cells. J. Clin. Invest. 125, 4212-4222 (2015).
36. Kipnis, J. Multifaceted interactions between adaptive immunity and the central nervous system. Science 353, 766-771 (2016).
37. Faraco, G. et al. Perivascular macrophages mediate the neurovascular and cognitive dysfunction associated with hypertension. J. Clin. Invest. 126, 4674-4689 (2016).
38. Binger, K. J. et al. High salt reduces the activation of IL-4- and IL-13- stimulated macrophages. J. Clin. Invest. 125, 4223-4238 (2015).
39. Mandala, S. et al. Alteration of lymphocyte trafficking by sphingosine-1- phosphate receptor agonists. Science 296, 346-349 (2002).
40. Sugimoto, M. et al. Rho-kinase phosphorylates eNOS at threonine 495 in endothelial cells. Biochem. Biophys. Res. Commun. 361, 462-467 (2007).
41. Guterbaum, T. J. et al. Endothelial nitric oxide synthase phosphorylation at Threonine 495 and mitochondrial reactive oxygen species formation in response to a high H2O2 concentration. J. Vasc. Res. 50, 410-420 (2013).
42. Katusic, Z. S. & Austin, S. A. Endothelial nitric oxide: protector of a healthy mind. Eur. Heart J. 35, 888-894 (2014).
43. Love, S. & Miners, J. S. Cerebral hypoperfusion and the energy deficit in Alzheimer's disease. Brain Pathol. 26, 607-617 (2016).
44. Garthwaite, J. Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 27, 2783-2802 (2008).
45. Gu, C., Wu, L. & Li, X. IL-17 family: cytokines, receptors and signaling. Cytokine 64, 477-485 (2013).
46. Tablazon, I. L. D., Al-Dabagh, A., Davis, S. A. & Feldman, S. R. Risk of cardiovascular disorders in psoriasis patients: current and future. Am. J. Clin. Dermatol. 14, 1-7 (2013).
47. Liou, T.-H. et al. Risk of stroke in patients with rheumatism: a nationwide longitudinal population-based study. Sci. Rep. 4, 5110 (2014).
48. Ferro, J. M., Oliveira, S. N. & Correia, L. Neurologic manifestations of inflammatory bowel diseases. Handb. Clin. Neurol. 120, 595-605 (2014).
49. Marshall, O. et al. Impaired cerebrovascular reactivity in multiple sclerosis. JAMA Neurol. 71, 1275-1281 (2014).
50. Park, L. et al. Scavenger receptor CD36 is essential for the cerebrovascular oxidative stress and neurovascular dysfunction induced by amyloid-beta. Proc. Natl. Acad. Sci. USA 108, 5063-5068 (2011).