Autoimmunity in the pathogenesis of hypertension

Nature Reviews Nephrology

Volumn 10, Issue 1, 2014, Pages 56-62

  Rodríguez Iturbe, Bernardo ^a   Pons, Héctor ^b   Quiroz, Yasmir ^a   Lanaspa, Miguel A ^c,d   Johnson, Richard J ^c,d  

^a INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

^b UNIVERSIDAD DEL ZULIA   (Venezuela)

^c HOSPITAL UNIVERSITARIO DE MARACAIBO   (Venezuela)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70;

AUTOIMMUNITY; ESSENTIAL HYPERTENSION; HUMAN; HYPERTENSION; IMMUNOPATHOGENESIS; INFLAMMATION; NATRIURESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW;

AUTOIMMUNITY; BLOOD PRESSURE; HUMANS; HYPERTENSION; T-LYMPHOCYTES;

EID: 84890789703     PISSN: 17595061     EISSN: 1759507X     Source Type: Journal    
DOI: 10.1038/nrneph.2013.248     Document Type: Review

References (83)

1. Ryan, M. J. An update on immune system activation in the pathogenesis of hypertension. Hypertension 62, 226-230 (2013).
2. Marvar, P. J. & Harrison, D. G. Stress-dependent hypertension and the role of T lymphocytes. Exp. Physiol. 97, 1161-1167 (2012).
3. Harrison, D. G., Marvar, P. J. & Titze, J. M. Vascular inflammatory cells in hypertension. Front. Physiol. 3, 128 http://dx.doi.org/10.3389/fphys. 2012.00128.
4. Leibowitz, A. & Schiffrin, E. L. Immune mechanisms in hypertension. Curr. Hypertens. Rep. 13, 465-472 (2011).
5. Muller, D. N., Kvakan, H. & Luft, F. C. Immune-related effects in hypertension and target-organ damage. Curr. Opin. Nephrol. Hypertens. 20, 113-117 (2011).
6. Harrison, D. G. et al. Inflammation, immunity, and hypertension. Hypertension 57, 132-140 (2011).
7. Rodríguez-Iturbe, B., Franco, M., Tapia, E., Quiroz, Y. & Johnson, R. J. Renal inflammation, autoimmunity and salt-sensitive hypertension. Clin. Exp. Pharmacol. Physiol. 39, 96-103 (2012).
8. Rodríguez-Iturbe, B. & Johnson, R. J. The role of microvascular disease and interstitial inflammation in salt-sensitive hypertension. Hypertens. Res. 33, 975-980 (2010).
9. Bendich, A., Belisle, E. H. & Strausser, H. R. Immune system modulation and its effects on blood pressure of the spontaneously hypertensive male and female rat. Biochem. Biophys. Res. Commun. 99, 600-607 (1981).
10. Olsen, F. Transfer of arterial hypertension by splenic cells from DOCA-salt hypertensive and renal hypertensive rats to normotensive recipients. Acta Pathol. Microbiol. Scand. C 88, 1-5 (1980).
11. Svendsen, U. G. Evidence for an initial, thymus independent and a chronic, thymus dependent phase of DOCA and salt hypertension in mice. Acta Pathol. Microbiol. Scand. A 84, 523-528 (1976).
12. Ba, D., Takeichi, N., Kodama, T. & Kobayashi, H. Restoration of T cell depression and suppression of blood pressure in spontaneously hypertensive rats (SHR) by thymus grafts or thymus extracts. J. Immunol. 128, 1211-1216 (1982).
13. Tuttle, R. S. & Boppana, D. P. Antihypertensive effect of interleukin-2. Hypertension 15, 89-94 (1990).
14. Dzielak, D. J. AIDS, lupus, rheumatoid arthritis-hypertension? Hypertension 15, 95-96 (1990).
15. Guzik, T. J. et al. Role of T cell in the genesis of angiotensin II-induced hypertension and vascular dysfunction. J. Exp. Med. 204, 2449-2460 (2007).
16. Kasal, D. A. et al. T regulatory lymphocytes prevent aldosterone-induced vascular injury. Hypertension 59, 324-330 (2012).
17. 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).
18. Zimmerman, M. C. et al. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ. Res. 91, 1038-1045 (2002).
19. Lob, H. E. et al. Induction of hypertension and peripheral inflammation by reduction of extracellular superoxide dismutase in the central nervous system. Hypertension 55, 277-283 (2010).
20. Shi, P. et al. Microglial cytokines in neurogenic hypertension. Hypertension 56, 297-303 (2010).
21. Franco, M. et al. Impaired pressure natriuresis resulting in salt-sensitive hypertension is caused by tubulointerstitial immune cell infiltration in the kidney. Am. J. Physiol. Renal Physiol. 304, F982-F990 (2013).
22. Franco, M. et al. Renal angiotensin II concentration and interstitial infiltration of immune cells are correlated with blood pressure levels in salt-sensitive hypertension. Am. J. Physiol. Reg. Integr. Comp. Physiol. 293, R251-R256 (2007).
23. Rodríguez-Iturbe, B., Quiroz, Y., Ferrebuz, A., Parra, G. & Vaziri, N. D. Evolution of renal interstitial inflammation and NF-kB activation in spontaneously hypertensive rats. Am. J. Nephrol. 24, 587-594 (2004).
24. Rodríguez-Iturbe, B. et al. Reduction of renal immune cell infiltration results in blood pressure control in genetically hypertensive rats. Am. J. Physiol. Renal Physiol. 282, F191-F201 (2002).
25. De Miguel, C., Guo, C., Lund, H., Feng, D. & Mattson, D. L. Infiltrating T lymphocytes in the kidney increase oxidative stress and participate in the development of hypertension and renal disease. Am. J. Physiol. Renal Physiol. 300, F734-F742 (2011).
26. Alvarez, V., Quiroz, Y., Nava, M., Pons, H. & Rodríguez- Iturbe, B. Overload proteinuria is followed by salt-sensitive hypertension caused by renal infiltration of immune cells. Am. J. Physiol. Renal Physiol. 283, F1132-F1141 (2002).
27. Vanegas, V., Ferrebuz, A., Quiroz, Y. & Rodríguez-Iturbe, B. Hypertension in Page (cellophane wrapped) kidney is due to interstitial nephritis. Kidney Int. 68, 1161-1170 (2005).
28. Madhur, M. S. et al. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 55, 500-507 (2010).
29. Mattson, D. L. et al. Genetic mutation of recombination activating gene 1 in Dahl salt-sensitive rats attenuates hypertension and renal damage. Am. J. Physiol. Regul. Integr.Comp. Physiol. 304, R407-R414 (2013).
30. Basu, R., Hatton, R. D. & Weaver, C. T. The Th17 family: flexibility follows function. Immunol. Rev. 252, 89-103 (2013).
31. Gratze, P. et al. Novel role for inhibitor of differentiation 2 in the genesis of angiotensin II-induced hypertension. Circulation 117, 2645-2656 (2008).
32. Viel, E. C., Lemarié, C. A., Benkirane, K., Paradis, P. & Schiffrin, E. L. Immune regulation and vascular inflammation in genetic hypertension. Am. J. Physiol. Heart Circ. Physiol. 298, H938-H944 (2010).
33. Barhoumi, T. et al. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 57, 469-476 (2011).
34. Chiasson, V. L. et al. FK506 binding protein 12 deficiency in endothelial and hematopoietic cells decreases regulatory T cells and causes hypertension. Hypertension 57, 1167-1175 (2011).
35. Rodríguez-Iturbe, B., Zhan, C.-D., Quiroz, Y., Sindhu, R., K & Vaziri, N. D. Antioxidant-rich diet improves hypertension and reduces renal immune infiltration in spontaneously hypertensive rats. Hypertension 41, 341-346 (2003).
36. Herrada, A. A. et al. Aldosterone as a modulator of immunity: implications in the organ damage. J. Hypertens. 29, 1684-1692 (2011).
37. Gonzalez-Villalobos, R. A. et al. The absence of intrarenal ACE protects against hypertension. J. Clin. Invest. 123, 2011-2023 (2013).
38. Crowley, S. D. et al. A role for angiotensin II type 1 receptors on bone marrow-derived cells in the pathogenesis of angiotenin II-dependent hypertension. Hypertension 55, 99-108 (2010).
39. Guyton, A. C. et al. Arterial pressure regulation. Overriding dominance of the kidneys in long-term regulation and in hypertension. Am. J. Med. 52, 584-594 (1972).
40. Titze, J. & Matchnik, A. Sodium sensing in the interstitium and relationship to hypertension. Curr. Opin. Nephrol. Hypertens. 19, 385-392 (2010).
41. Machnik, A. et al. Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C dependent buffering mechanism. Nat. Med. 15, 545-552 (2009).
42. Wiig, H. et al. Immune cells control skin lymphatic electrolyte homeostasis and blood pressure. J. Clin. Invest. 123, 2803-2815 (2013).
43. Rodríguez-Iturbe, B., Vaziri, N. D., Herrera-Acosta, J. & Johnson, R. J. Oxidative stress, renal infiltration of immune cells and salt-sensitive hypertension: all for one and one for all. Am. J. Physiol. Renal Physiol. 286, F606-F616 (2004).
44. Bravo, J. et al. Vimentin and heat shock protein expression are induced in the kidney by angiotensin and by nitric oxide inhibition. Kidney Int. 64 (Suppl. 86), S46-S51 (2003).
45. Ishizaka, N. et al. Regulation and localization of HSP70 and HSP25 in the kidney of rats undergoing long-term administration of angiotensin II. Hypertension 39, 122-128 (2002).
46. Udelsman, R. et al. Vascular heat shock protein expression response to stress. J. Clin. Invest. 91, 465-473 (1993).
47. Mazurek, B., Haupt, H., Klapp, B. F., Szczepek, A. J. & Olze, H. Exposure of Wistar rats to 24-h psycho-social stress alters gene expression in the inferior colliculus. Neurosci. Lett. 527, 40-45 (2012).
48. Todryk, S. M., Gough, M. J. & Pockley, A. G. Facets of heat shock protein 70 show immunotherapeutic potential. Immunology 110, 1-9 (2003).
49. Parra, G. et al. Experimental induction of salt-sensitive hypertension is associated with lymphocyte proliferative response to HSP70. Kidney Int. Suppl. 111, S55-S59 (2008).
50. Quiroz, Y. et al. Mycophenolate mofetil prevents the salt-sensitive hypertension resulting from short-term nitric oxide synthesis inhibition. Am. J. Physiol. Renal Physiol. 281, F38-F47 (2001).
51. Kleinewietfeld, M. et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496, 518-522 (2013).
52. Wu, C. et al. Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 496, 513-517 (2013).
53. Wendling, U. et al. A conserved mycobacterial heat shock protein (hsp) 70 sequence prevents adjuvant arthritis upon nasal administration and induces IL-10-producing T cells that cross-react with the mammalian self-hsp70 homologue. J. Immunol. 164, 2711-2717 (2000).
54. Prakken, B. J. et al. Induction of IL-10 and inhibition of experimental arthritis are specific features of microbial heat shock proteins that are absent for other evolutionary conserved immunodominant proteins. J. Immunol. 167, 4147-4153 (2001).
55. Pons, H. et al. Immune reactivity to heat shock protein 70 expressed in the kidney is cause of salt sensitive hypertension. Am. J. Physiol. Renal Physiol. 304, F289-F299 (2013).
56. Boursier, G., Siri, A. & de Boysson, H. Utilisation des lymphocytes T régulateurs en thérapies cellulaires dans les maladies auto-immunes [French]. Med. Sci. (Paris) 28, 757-763 (2012).
57. Vinh, A. et al. Inhibition and genetic ablation of the B7/CD28 T-cell costimulation axis prevents experimental hypertension. Circulation 122, 2529-2537 (2010).
58. Gareau, R. J. & Cartier, G. E. Étude histologique de 55 biopsies rénales prélevées chez maladies hypertendus [French]. Union Med. Can. 84, 1134-1142 (1955).
59. Heptinstall, R. H. Renal biopsies in hypertension. Br. Heart J. 16, 133-141 (1954).
60. Sommers, S. C., Relman, A. S. & Smithwick, R. H. Histologic studies of kidney biopsy specimens from patients with hypertension. Am. J. Pathol. 34, 685-715 (1954).
61. Hughson, M. D. et al. Associations of glomerular number and birth weight with clinicopathological features of African Americans and whites. Am. J. Kidney Dis. 52, 18-28 (2008).
62. Lefkos, N. et al. Immunopathogenic mechanisms in hypertension. Am. J. Hypertens. 8, 1141-1145 (1995).
63. Stumpf, C. et al. Serum levels of the Th1 chemoattractant interferon-gamma-inducible protein (IP) 10 are elevated in patients with essential hypertension. Hypertens. Res. 34, 484-488 (2011).
64. Herrera, J., Ferrebuz, A., García-Macgregor, E. & Rodríguez-Iturbe, B. Mycophenolate mofetil treatment improves hypertension in patients with psoriasis and rheumatoid arthritis. J. Am. Soc. Nephrol. 17, S218-S225 (2006).
65. Seaberg, E. C. et al. Multicenter AIDS Cohort Study. Association between highly active antiretroviral therapy and hypertension in a large cohort of men followed from 1984 to 2003. AIDS 19, 953-960 (2005).
66. Pockley, A. G., Georgiades, A., Thulin, T., de Faire, U. & Frostegård, J. Serum heat shock protein 70 levels predict the development of atherosclerosis in subjects with established hypertension. Hypertension 42, 235-238 (2003).
67. Pockley, A. G. et al. Circulating heat shock protein and heat shock protein antibody levels in established hypertension. J. Hypertens. 20, 1815-1829 (2002).
68. Kunes, J., Poirier, M., Tremblay, J. & Hamet, P. Expression of HSP70 gene in lymphocytes from normotensive and hypertensive humans. Acta Physiol. Scand. 146, 307-311 (1992).
69. Li, J. X. et al. Interacting contribution of the five polymorphisms in three genes of Hsp70 family to essential hypertension in Uygur ethnicity. Cell Stress Chaperones 14, 355-362 (2009).
70. Marketou, M. E. et al. TLR2 and TLR4 gene expression in peripheral monocytes in nondiabetic hypertensive patients: the effect of intensive blood pressure-lowering. J. Clin. Hypertens. (Greenwich) 14, 330-335 (2012).
71. Mattson, D. L., James. L., Berdan. E. A. & Meister, C, J. Immune suppression attenuates hypertension and renal disease in Dahl salt hypertensive rats. Hypertension 48, 149-156 (2006).
72. Tian, N. et al. Immune suppression prevents renal damage and dysfunction and reduces arterial pressure in salt-sensitive hypertension. Am. J. Physiol. Heart Circ. Physiol. 292, H1018-H1022 (2007).
73. Stewart, T., Jung, F. F., Manning, J. & Vehaskari, V. M. Kidney immune cell infiltration and oxidative stress contribute to prenatally programmed hypertension. Kidney Int. 68, 2180-2188 (2005).
74. Rodríguez-Iturbe, B. et al. Early and sustained inhibition of nuclear factor-κB prevents hypertension in spontaneously hypertensive rats. J. Pharmacol. Exp. Ther. 315, 51-57 (2005).
75. Müller, D. N. et al. NF-κB inhibition ameliorates angiotensin II-induced inflammatory damage in rats. Hypertension 35 (Part 2), 193-201 (2000).
76. Müller, D. N. et al. Immunosuppressive treatment protects against angiotensin-II induced renal damage. Am. J. Pathol. 161, 1679-1690 (2002).
77. Khraibi, A. A., Norman, R. A. Jr & Dzielak, D. J. Chronic immunosuppression attenuates hypertension in Okamoto spontaneously hypertensive rats. Am. J. Physiol. 247, H722-H726 (1984).
78. Norman, R. A. Jr, Galloway, P. G., Dzielak, D. J. & Huang, M. Mechanisms of partial renal infarct hypertension. J. Hypertens. 6, 397-403 (1988).
79. Svendsen, J. G. Spontaneous hypertension and hypertensive vascular disease in the NZB strain of mice. Acta Pathol. Microbiol. Scand. A 85, 261-268 (1977).
80. Svendsen, U. G. The importance of thymus in the pathogenesis of the chronic phase of hypertension in mice following partial infarction of the kidney. Acta Pathol. Microbiol. Scand. A 85, 539-547 (1977).
81. Bataillard, P., Freiche, J.-C., Vincent, M., Touraine, J.-L. & Sassard, J. U. Effects of neonatal thymectomy on blood pressure and immunological characteristics of the genetically hypertensive rats of the Lyon strain. J. Hypertens. 4 (Suppl. 3), 5455-5467 (1986).
82. Bomfim, G. F. et al. Toll-like receptor 4 contributes to blood pressure regulation and vascular contraction in spontaneously hypertensive rats. Clin. Sci. (Lond.) 122, 535-543 (2012).
83. Delves, P. J. in Essential Immunology 12th edn (ed. Roitt, P. J.) 475-510 (Wiley-Blackwell, 2011).