Direct anti-inflammatory effects of angiotensin-(1-7) on microglia

Journal of Neurochemistry

Volumn 136, Issue 1, 2016, Pages 163-171

  Liu, Meng ^a   Shi, Peng ^b   Sumners, Colin ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

(pro)renin; hypothalamus; microglia; pro inflammatory cytokine; renin angiotensin system

Indexed keywords

ANGIOTENSIN RECEPTOR; ANGIOTENSIN[1-7]; ANGIOTENSIN[1-7][7 DEXTRO ALANINE]; CD11B ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; MESSENGER RNA; PRORENIN; PROTEIN MAS; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ANTIINFLAMMATORY AGENT; AUTACOID; PEPTIDE FRAGMENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CD11B GENE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; HYPOTHALAMUS; IL 10 GENE; IL 1B GENE; MICROGLIA; MICROGLIAL CELL CULTURE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; TNFA GENE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; FEMALE; METABOLISM; PREGNANCY; SPRAGUE DAWLEY RAT;

ANGIOTENSIN I; ANIMALS; ANIMALS, NEWBORN; ANTI-INFLAMMATORY AGENTS; CELLS, CULTURED; FEMALE; INFLAMMATION MEDIATORS; MICROGLIA; PEPTIDE FRAGMENTS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84951906004     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13386     Document Type: Article

References (37)

1. Batenburg W. W., Krop M., Garrelds I. M., de Vries R., de Bruin R. J., Burcklé C. A., Müller D. N., Bader M., Nguyen G., and, Danser A. H., (2007) Prorenin is the endogenous agonist of the (pro)renin receptor. Binding kinetics of renin and prorenin in rat vascular smooth muscle cells overexpressing the human (pro)renin receptor. J. Hypertens. 25, 2441-2453.
2. Becker L. K., Etelvino G. M., Walther T., Santos R. A., and, Campagnole-Santos M. J., (2007) Immunofluorescence localization of the receptor Mas in cardiovascular-related areas of the rat brain. Am. J. Physiol. Heart Circ. Physiol. 293, H1416-H1424.
3. Campagnole-Santos M. J., Diz D. I., Santos R. A., Khosla M. C., Brosnihan K. B., and, Ferrario C. M., (1989) Cardiovascular effects of angiotensin-(1-7) injected into the dorsal medulla of rats. Am. J. Physiol. 257, H324-H329.
4. Cardinale J. P., Sriramula S., Mariappan N., Agarwal D., and, Francis J., (2012) Angiotensin II-induced hypertension is modulated by nuclear factor-κB in the paraventricular nucleus. Hypertension 59, 113-121.
5. Coote J. H., (2005) A role for the paraventricular nucleus of the hypothalamus in the autonomic control of heart and kidney. Exp. Physiol. 90, 169-173.
6. Cuadra A. E., Shan Z., Sumners C., and, Raizada M. K., (2010) A current view of brain renin-angiotensin system: is the (pro)renin receptor the missing link? Pharmacol. Ther. 125, 27-38.
7. Dhawan P., and, Richmond A., (2002) A novel NF-kappa B-inducing kinase-MAPK signaling pathway up-regulates NF-kappa B activity in melanoma cells. J. Biol. Chem. 277, 7920-7928.
8. Esler M., (2011) The sympathetic nervous system through the ages: from Thomas Willis to resistant hypertension. Exp. Physiol. 96, 611-622.
9. Ferreira A. J., Santos R. A., Bradford C. N., Mecca A. P., Sumners C., Katovich M. J., and, Raizada M. K., (2010) Therapeutic implications of the vasoprotective axis of the renin-angiotensin system in cardiovascular diseases. Hypertension 55, 207-213.
10. Füchtbauer L., Groth-Rasmussen M., Holm T. H., Løbner M., Toft-Hansen H., Khorooshi R., and, Owens T., (2011) Angiotensin II Type 1 receptor (AT1) signaling in astrocytes regulates synaptic degeneration-induced leukocyte entry to the central nervous system. Brain Behav. Immun. 25, 897-904.
11. Garrido-Gil P., Valenzuela R., Villar-Cheda B., Lanciego J. L., and, Labandeira-Garcia J. L., (2013) Expression of angiotensinogen and receptors for angiotensin and prorenin in the monkey and human substantia nigra: an intracellular renin-angiotensin system in the nigra. Brain Struct. Funct. 218, 373-388.
12. Gironacci M. M., Cerniello F. M., Longo Carbajosa N. A., Goldstein J., and, Cerrato B. D., (2014) Protective axis of the renin-angiotensin system in the brain. Clin. Sci. (Lond.) 127, 295-306.
13. González-Scarano F., and, Baltuch G., (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci. 22, 219-240.
14. Guo F., Liu B., Tang F., Lane S., Souslova E. A., Chudakov D. M., Paton J. F., and, Kasparov S., (2010) Astroglia are a possible cellular substrate of angiotensin(1-7) effects in the rostral ventrolateral medulla. Cardiovasc. Res. 87, 578-584.
15. Guyenet P. G., (2006) The sympathetic control of blood pressure. Nat. Rev. Neurosci. 7, 335-346.
16. Iadecola C., and, Anrather J., (2011) The immunology of stroke: from mechanisms to translation. Nat. Med. 17, 796-808.
17. Jiang T., Gao L., Guo J., Lu J., Wang Y., and, Zhang Y., (2012) Suppressing inflammation by inhibiting the NF-κB pathway contributes to the neuroprotective effect of angiotensin-(1-7) in rats with permanent cerebral ischaemia. Br. J. Pharmacol. 167, 1520-1532.
18. Kandalam U., and, Clark M. A., (2010) Angiotensin II activates JAK2/STAT3 pathway and induces interleukin-6 production in cultured rat brainstem astrocytes. Regul. Pept. 159, 110-116.
19. de Kloet A. D., Krause E. G., Shi P. D., Zubcevic J., Raizada M. K., and, Sumners C., (2013) Neuroimmune communication in hypertension and obesity: a new therapeutic angle? Pharmacol. Ther. 138, 428-440.
20. Krause E. G., Melhorn S. J., Davis J. F., Scott K. A., Ma L. Y., de Kloet A. D., Benoit S. C., Woods S. C., and, Sakai R. R., (2008) Angiotensin type 1 receptors in the subfornical organ mediate the drinking and hypothalamic-pituitary-adrenal response to systemic isoproterenol. Endocrinology 149, 6416-6424.
21. Li W., Peng H., Cao T., Sato R., McDaniels S. J., Kobori H., Navar L. G., and, Feng Y., (2012) Brain-targeted (pro)renin receptor knockdown attenuates angiotensin II-dependent hypertension. Hypertension 59, 1188-1194.
22. Lind R. W., Swanson L. W., and, Ganten D., (1985) Organization of angiotensin II immunoreactive cells and fibers in the rat central nervous system. An immunohistochemical study. Neuroendocrinology 40, 2-24.
23. Mecca A. P., Regenhardt R. W., O'Connor T. E., Joseph J. P., Raizada M. K., Katovich M. J., and, Sumners C., (2011) Cerebroprotection by angiotensin-(1-7) in endothelin-1-induced ischaemic stroke. Exp. Physiol. 96, 1084-1096.
24. Miyoshi M., Miyano K., Moriyama N., Taniguchi M., and, Watanabe T., (2008) Angiotensin type 1 receptor antagonist inhibits lipopolysaccharide-induced stimulation of rat microglial cells by suppressing nuclear factor kappaB and activator protein-1 activation. Eur. J. Neurosci. 27, 343-351.
25. Nabi A. H., Kageshima A., Uddin M. N., Nakagawa T., Park E. Y., and, Suzuki F., (2006) Binding properties of rat prorenin and renin to the recombinant rat renin/prorenin receptor prepared by a baculovirus expression system. Int. J. Mol. Med. 18, 483-488.
26. Nguyen G., Delarue F., Burcklé C., Bouzhir L., Giller T., and, Sraer J. D., (2002) Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J. Clin. Invest. 109, 1417-1427.
27. Regenhardt R. W., Desland F., Mecca A. P., Pioquinto D. J., Afzal A., Mocco J., and, Sumners C., (2013) Anti-inflammatory effects of angiotensin-(1-7) in ischemic stroke. Neuropharmacology 71, 154-163.
28. Regenhardt R. W., Mecca A. P., Desland F., Ritucci-Chinni P. F., Ludin J. A., Greenstein D., Banuelos C., Bizon J. L., Reinhard M. K., and, Sumners C., (2014) Centrally administered angiotensin-(1-7) increases the survival of stroke-prone spontaneously hypertensive rats. Exp. Physiol. 99, 442-453.
29. Shi P., Diez-Freire C., Jun J. Y., Qi Y., Katovich M. J., Li Q., Sriramula S., Francis J., Sumners C., and, Raizada M. K., (2010) Brain microglial cytokines in neurogenic hypertension. Hypertension 56, 297-303.
30. Shi P., Grobe J. L., Desland F. A., Rodriguez V., Shan Z., Richards E. M., Raizada M. K., and, Sumners C., (2011) Stimulatory action of the renin-angiotensin-aldosterone system on the production of microglial derived cytokines. Hypertension 58, e37.
31. Shi P., Grobe J. L., Desland F. A., Zhou G., Shen X. Z., Shan Z., Liu M., Raizada M. K., and, Sumners C., (2014) Direct pro-inflammatory effects of prorenin on microglia. PLoS ONE 9, e92937.
32. Sriramula S., Cardinale J. P., Lazartigues E., and, Francis J., (2011) ACE2 overexpression in the paraventricular nucleus attenuates angiotensin II-induced hypertension. Cardiovasc. Res. 92, 401-408.
33. Sriramula S., Cardinale J. P., and, Francis J., (2013) Inhibition of TNF in the brain reverses alterations in RAS components and attenuates angiotensin II-induced hypertension. PLoS ONE 8, e63847.
34. Takahashi H., (2012) Upregulation of the Renin-Angiotensin-aldosterone-ouabain system in the brain is the core mechanism in the genesis of all types of hypertension. Int. J. Hypertens. 2012, 242786.
35. Tallant E. A., and, Clark M. A., (2003) Molecular mechanisms of inhibition of vascular growth by angiotensin-(1-7). Hypertension 42, 574-579.
36. Valenzuela R., Barroso-Chinea P., Villar-Cheda B., Joglar B., Muñoz A., Lanciego J. L., and, Labandeira-Garcia J. L., (2010) Location of prorenin receptors in primate substantia nigra: effects on dopaminergic cell death. J. Neuropathol. Exp. Neurol. 69, 1130-1142.
37. Zubcevic J., Waki H., Raizada M. K., and, Paton J. F., (2011) Autonomic-immune-vascular interaction: an emerging concept for neurogenic hypertension. Hypertension 57, 1026-1033.