A cholinergic-sympathetic pathway primes immunity in hypertension and mediates brain-to-spleen communication

Nature Communications

Volumn 7, Issue , 2016, Pages

  Carnevale, Daniela ^a,b   Perrotta, Marialuisa ^a   Pallante, Fabio ^a   Fardella, Valentina ^a   Iacobucci, Roberta ^a   Fardella, Stefania ^a   Carnevale, Lorenzo ^a   Carnevale, Raimondo ^a   De Lucia, Massimiliano ^a   Cifelli, Giuseppe ^a   Lembo, Giuseppe ^a,b  

^a IRCCS NEUROMED   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINIC RECEPTOR; NITROPRUSSIDE SODIUM; PHENYLEPHRINE;

BRAIN; EXPERIMENTAL STUDY; GENE EXPRESSION; HYPERTENSION; IMMUNITY; MOLECULAR ANALYSIS; NERVOUS SYSTEM; PHYSIOLOGICAL RESPONSE; RODENT;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC INNERVATION; BLOOD PRESSURE REGULATION; BRAIN; CHOLINERGIC NERVE; CONTROLLED STUDY; GANGLION BLOCK; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MALE; MOUSE; NONHUMAN; PARASYMPATHETIC INNERVATION; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RESISTANT HYPERTENSION; SPLANCHNIC BLOOD FLOW; SPLEEN; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE; SYMPATHETIC TONE; T LYMPHOCYTE ACTIVATION; VAGOTOMY;

MUS;

EID: 84989323271     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13035     Document Type: Article

References (41)

1. Chobanian, A. V. Time to reassess blood-pressure goals. N. Engl. J. Med. 373, 2093-2095 (2015).
2. Chobanian, A. V. Shattuck lecture. the hypertension paradox-more uncontrolled disease despite improved therapy. N. Engl. J. Med. 361, 878-887 (2009).
3. Coffman, T. M. Under pressure: the search for the essential mechanisms of hypertension. Nat. Med. 17, 1402-1409 (2011).
4. Harrison, D. G. The mosaic theory revisited: common molecular mechanisms coordinating diverse organ and cellular events in hypertension. J. Am. Soc. Hypertens. 7, 68-74 (2013).
5. 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).
6. Vinh, A. et al. Inhibition and genetic ablation of the B7/CD28 T-cell costimulation axis prevents experimental hypertension. Circulation 122, 2529-2537 (2010).
7. Carnevale, D. et al. The angiogenic factor PlGF mediates a neuroimmune interaction in the spleen to allow the onset of hypertension. Immunity 41, 737-752 (2014).
8. McMaster, W. G., Kirabo, A., Madhur, M. S. & Harrison, D. G. Inflammation, immunity, and hypertensive end-organ damage. Circ. Res. 116, 1022-1033 (2015).
9. Zhang, J. & Crowley, S. D. Role of T lymphocytes in hypertension. Curr. Opin. Pharmacol. 21, 14-19 (2015).
10. Malpas, S. C. Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol. Rev. 90, 513-557 (2010).
11. Symplicity HTN-2 Investigators et al. Renal sympathetic denervation in patients with treatment-resistant hypertension (the symplicity HTN-2 trial): a randomised controlled trial. Lancet 376, 1903-1909 (2010).
12. Esler, M. D. et al. Catheter-based renal denervation for treatment of patients with treatment-resistant hypertension: 36 month results from the SYMPLICITY HTN-2 randomized clinical trial. Eur. Heart. J. 35, 1752-1759 (2014).
13. Bhatt, D. L. et al. A controlled trial of renal denervation for resistant hypertension. N. Engl. J. Med. 370, 1393-1401 (2014).
14. Abboud, F. M., Harwani, S. C. & Chapleau, M. W. Autonomic neural regulation of the immune system: implications for hypertension and cardiovascular disease. Hypertension 59, 755-762 (2012).
15. Andersson, U. & Tracey, K. J. Neural reflexes in inflammation and immunity. J. Exp. Med. 209, 1057-1068 (2012).
16. Ordovas-Montanes, J. et al. The regulation of immunological processes by peripheral neurons in homeostasis and disease. Trends Immunol. 36, 578-604 (2015).
17. Nahrendorf, M. & Swirski, F. K. Innate immune cells in ischaemic heart disease: does myocardial infarction beget myocardial infarction? Eur. Heart. J. 37, 868-872 (2016).
18. King, A. J., Osborn, J. W. & Fink, G. D. Splanchnic circulation is a critical neural target in angiotensin II salt hypertension in rats. Hypertension 50, 547-556 (2007).
19. Marvar, P. J. et al. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ. Res. 107, 263-270 (2010).
20. Hamza, S. M. & Hall, J. E. Direct recording of renal sympathetic nerve activity in unrestrained, conscious mice. Hypertension 60, 856-864 (2012).
21. Stocker, S. D. & Muntzel, M. S. Recording sympathetic nerve activity chronically in rats: surgery techniques, assessment of nerve activity, and quantification. Am. J. Physiol. Heart. Circ. Physiol. 305, 1407-1416 (2013).
22. Guild, S. J. et al. Quantifying sympathetic nerve activity: problems, pitfalls and the need for standardization. Exp. Physiol. 95, 41-50 (2010).
23. Hilzendeger, A. M. et al. Angiotensin type 1a receptors in the subfornical organ are required for deoxycorticosterone acetate-salt hypertension. Hypertension 61, 716-722 (2013).
24. Huston, J. M. et al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J. Exp. Med. 7, 1623-1628 (2006).
25. Rosas-Ballina, M. et al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl Acad. Sci. USA 105, 11008-11013 (2008).
26. Vida, G., Pena, G., Deitch, E. A. & Ulloa, L. a7-cholinergic receptor mediates vagal induction of splenic norepinephrine. J. Immunol. 186, 4340-4346 (2011).
27. Borovikova, L. V. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405, 458-462 (2000).
28. Guo, G. B., Thames, M. D. & Abboud, F. M. Differential baroreflex control of heart rate and vascular resistance in rabbits. Relative role of carotid, aortic, and cardiopulmonary baroreceptors. Circ. Res. 50, 554-565 (1982).
29. Stokes, C., Treinin, M. & Papke, R. L. Looking below the surface of nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 36, 514-523 (2015).
30. Deck, J. et al. a7-Nicotinic acetylcholine receptor subunit is not required for parasympathetic control of the heart in the mouse. Physiol. Genomics 22, 86-92 (2005).
31. DiBona, G. F. & Kopp, U. C. Neural control of renal function. Physiol. Rev. 77, 75-197 (1997).
32. Rosas-Ballina, M. & Tracey, K. J. The neurology of the immune system: neural reflexes regulate immunity. Neuron 64, 28-32 (2009).
33. Pena, G. et al. Cholinergic regulatory lymphocytes re-establish neuromodulation of innate immune responses in sepsis. J. Immunol. 2, 718-725 (2011).
34. Rosas-Ballina, M. et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334, 98-101 (2011).
35. Nance, D. M. & Sanders, V. M. Autonomic innervation and regulation of the immune system. Brain Behav. Immun. 21, 736-745 (2007).
36. Ganta, C. K. et al. Central angiotensin II-enhanced splenic cytokine gene expression is mediated by the sympathetic nervous system. Am. J. Physiol. Heart. Circ. Physiol 289, 1683-1691 (2005).
37. Inoue, T. et al. Vagus nerve stimulation mediates protection from kidney ischemia-reperfusion injury through a7nAChR splenocytes. J. Clin. Invest. 126, 1939-1952 (2016).
38. Rahmouni, K., Haynes, W. G., Morgan, D. A. & Mark, A. L. Role of melanocortin-4 receptors in mediating renal sympathoactivation to leptin and insulin. J. Neurosci. 23, 5998-6004 (2003).
39. Brancaccio, M. et al. Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat. Med 9, 68-75 (2003).
40. Zacchigna, L. et al. Emilin1 links TGF-beta maturation to blood pressure homeostasis. Cell 124, 929-942 (2006).
41. Fedorov, A. et al. 3D Slicer as an Image Computing Platform for the Quantitative Imaging Network. Magn. Reson. Imaging 9, 1323-1341 (2012).