Blood-borne angiotensin II acts in the brain to influence behavioral and endocrine responses to psychogenic stress

Journal of Neuroscience

Volumn 31, Issue 42, 2011, Pages 15009-15015

  Krause, Eric G ^a   de Kloet, Annette D ^b   Scott, Karen A ^c   Flak, Jonathan N ^c   Jones, Kenneth ^c   Smeltzer, Michael D ^c   Ulrich Lai, Yvonne M ^c   Woods, Stephen C ^c   Wilson, Steven P ^d   Reagan, Lawrence P ^d   Herman, James P ^c   Sakai, Randall R ^c  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

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

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; LENTIVIRUS VECTOR; MESSENGER RNA; PROTEIN C FOS;

ANGIOTENSIN 1 RECEPTOR GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN NERVE CELL; CONTROLLED STUDY; CORTICOSTERONE RELEASE; ELEVATED PLUS MAZE; GENE; GENE EXPRESSION; GENE SILENCING; HORMONE RELEASE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMOBILIZATION STRESS; MALE; MAZE TEST; MENTAL STRESS; NERVE FIBER; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PSYCHOGENIC STRESS; RAT; RECEPTOR BLOCKING; SUBFORNICAL ORGAN; TRANQUILIZING ACTIVITY;

ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ENDOCRINE SYSTEM; GREEN FLUORESCENT PROTEINS; HORMONES; MALE; PHYTOHEMAGGLUTININS; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1; STRESS, PSYCHOLOGICAL; SUBFORNICAL ORGAN; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 80054734904     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0892-11.2011     Document Type: Article

References (48)

1. Angunsri R, Sritharathikhun T, Suttirat S, Tencomnao T (2009) Association of angiotensin-converting enzyme gene promoter single nucleotide polymorphisms and haplotype with major depression in a northeastern Thai population. J Renin Angiotensin Aldosterone Syst 10:179-184.
2. Bader M, Ganten D (2008) Update on tissue renin-angiotensin systems. J Mol Med 86:615-621.
3. Baghai TC, Schule C, Zwanzger P, Minov C, Zill P, Ella R, Eser D, Oezer S, Bondy B, Rupprecht R (2002) Hypothalamic-pituitary-adrenocortical axis dysregulation in patients with major depression is influenced by the insertion/deletion polymorphism in the angiotensin I-converting enzyme gene. Neurosci Lett 328:299-303.
4. Baghai TC, Binder EB, Schule C, Salyakina D, Eser D, Lucae S, Zwanzger P, Haberger C, Zill P, Ising M, Deiml T, Uhr M, Illig T, Wichmann HE, Modell S, Nothdurfter C, Holsboer F, Müller-Myhsok B, Möller HJ, Rupprecht R, Bondy B (2006) Polymorphisms in the angiotensin-converting enzyme gene are associated with unipolar depression, ACE activity and hypercortisolism. Mol Psychiatry 11:1003-1015.
5. Bechtold AG, Patel G, Hochhaus G, Scheuer DA (2009) Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress. Am J Physiol Regul Integr Comp Physiol 296:R1445-R1454.
6. Bui JD, Kimura B, Phillips MI (1992) Losartan potassium, a nonpeptide antagonist of angiotensin II, chronically administered p.o. does not readily cross the blood-brain barrier. Eur J Pharmacol 219:147-151.
7. Carroll D, Phillips AC, Gale CR, Batty GD (2010) Generalized anxiety and major depressive disorders, their comorbidity and hypertension in middle-aged men. Psychosom Med 72:16-19.
8. Castren E, Saavedra JM (1988) Repeated stress increases the density of angiotensin II binding sites in rat paraventricular nucleus and subfornical organ. Endocrinology 122:370-372.
9. Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477-505.
10. Davern PJ, Chen D, Head GA, Chavez CA, Walther T, Mayorov DN (2009) Role of angiotensin II Type 1A receptors in cardiovascular reactivity and neuronal activation after aversive stress in mice. Hypertension 54:1262-1268.
11. Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261-265.
12. Ferguson AV (1988) Systemic angiotensin acts at the subfornical organ to control the activity of paraventricular nucleus neurons with identified projections to the median eminence. Neuroendocrinology 47:489-497.
13. Fink GD, Bruner CA, Mangiapane ML (1987) Area postrema is critical for angiotensin-induced hypertension in rats. Hypertension 9:355-361.
14. Garcia-Vera MP, Sanz J, Espinosa R, Fortún M, Magán I (2010) Differences in emotional personality traits and stress between sustained hypertension and normotension. Hypertens Res 33:203-208.
15. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151-180.
16. Holsboer F, Barden N (1996) Antidepressants and hypothalamic-pituitaryadrenocortical regulation. Endocr Rev 17:187-205.
17. Kanbar R, Oréa V, Barrès C, Julien C (2007) Baroreflex control of renal sympathetic nerve activity during air-jet stress in rats. Am J Physiol Regul Integr Comp Physiol 292:R362-R367.
18. Kawano H, Masuko S (2010) Region-specific projections from the subfornical organ to the paraventricular hypothalamic nucleus in the rat. Neuroscience 169:1227-1234.
19. Koob GF, Heinrichs SC, Pich EM, Menzaghi F, Baldwin H, Miczek K, Britton KT (1993) The role of corticotropin-releasing factor in behavioural responses to stress. Ciba Found Symp 172:277-295.
20. Kopp UC, DiBona GF (1993) Neural regulation of renin secretion. Semin Nephrol 13:543-551.
21. Krause EG, Sakai RR (2007) Richter and sodium appetite: from adrenalectomy to molecular biology. Appetite 49:353-367.
22. Krause EG, Curtis KS, Stincic TL, Markle JP, Contreras RJ (2006) Oestrogen and weight loss decrease isoproterenol-induced Fos immunoreactivity and angiotensin type 1 mRNA in the subfornical organ of female rats. J Physiol 573:251-262.
23. Krause EG, Melhorn SJ, Davis JF, Scott KA, Ma LY, de Kloet AD, Benoit SC, Woods SC, Sakai RR (2008) Angiotensin type 1 receptors in the subfornical organ mediate the drinking and hypothalamic-pituitary-adrenal response to systemic isoproterenol. Endocrinology 149:6416-6424.
24. Ku YH, Li YH (2003) Subfornical organ-angiotensin II pressor system takes part in pressor response of emotional circuit. Peptides 24:1063-1067.
25. Leong DS, Terrón JA, Falcón-Neri A, Armando I, Ito T, Jöhren O, Tonelli LH, Hoe KL, Saavedra JM (2002) Restraint stress modulates brain, pituitary and adrenal expression of angiotensin II AT(1A), AT(1B) and AT(2) receptors. Neuroendocrinology 75:227-240.
26. Li Z, Ferguson AV (1993) Subfornical organ efferents to paraventricular nucleus utilize angiotensin as a neurotransmitter. Am J Physiol 265: R302-R309.
27. Lind RW (1986) Bi-directional, chemically specified neural connections between the subfornical organ and the midbrain raphe system. Brain Res 384:250-261.
28. Lind RW, Ohman LE, Lansing MB, Johnson AK (1983) Transection of subfornical organ neural connections diminishes the pressor response to intravenously infused angiotensin II. Brain Res 275:361-364.
29. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, Gasser PJ, Shekhar A (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148:86-94.
30. Mangiapane ML, Simpson JB (1980) Subfornical organ: forebrain site of pressor and dipsogenic action of angiotensin II. Am J Physiol 239: R382-R389.
31. McKinley MJ, McAllen RM, Davern P, Giles ME, Penschow J, Sunn N, Uschakov A, Oldfield BJ (2003) The sensory circumventricular organs of the mammalian brain. Adv Anat Embryol Cell Biol 172:1-222.
32. Miselis RR (1981) The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance. Brain Res 230:1-23.
33. Oldfield BJ, McKinley MJ (1994) Distribution of Fos in rat brain resulting from endogenously-generated angiotensin II. Kidney Int 46:1567-1569.
34. Pavlatou MG, Mastorakos G, Lekakis I, Liatis S, Vamvakou G, Zoumakis E, Papassotiriou I, Rabavilas AD, Katsilambros N, Chrousos GP (2008) Chronic administration of an angiotensin II receptor antagonist resets the hypothalamic-pituitary-adrenal (HPA) axis and improves the affect of patients with diabetes mellitus type 2: preliminary results. Stress 11: 62-72.
35. Paxinos G, Watson C (1997) The rat brain in stereo-taxic coordinates. San Diego: Academic.
36. Plotsky PM, Sutton SW, Bruhn TO, Ferguson AV (1988) Analysis of the role of angiotensin II in mediation of adrenocorticotropin secretion. Endocrinology 122:538-545.
37. Randall DC, Brown DR, Brown LV, Kilgore JM (1994) Sympathetic nervous activity and arterial blood pressure control in conscious rat during rest and behavioral stress. Am J Physiol 267:R1241-R1249.
38. Rigat B, Hubert C, Alhenc-Gelas F, Cambien F, Corvol P, Soubrier F (1990) An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels. J Clin Invest 86:1343-1346.
39. Rowland NE, Morien A, Fregly MJ (1996) Losartan inhibition of angiotensin-related drinking and Fos immunoreactivity in hypertensive and hypotensive contexts. Brain Res 742:253-259.
40. Saavedra JM, Armando I, Bregonzio C, Juorio A, Macova M, Pavel J, Sanchez-Lemus E (2006) A centrally acting, anxiolytic angiotensin II AT1 receptor antagonist prevents the isolation stress-induced decrease in cortical CRF1 receptor and benzodiazepine binding. Neuropsychopharmacology 31:1123-1134.
41. Shafton AD, Ryan A, Badoer E (1998) Neurons in the hypothalamic paraventricular nucleus send collaterals to the spinal cord and to the rostral ventrolateral medulla in the rat. Brain Res 801:239-243.
42. Solomon MB, Jones K, Packard BA, Herman JP (2010) The medial amygdala modulates body weight but not neuroendocrine responses to chronic stress. J Neuroendocrinol 22:13-23.
43. Sowden GL, Huffman JC (2009) The impact of mental illness on cardiac outcomes: a review for the cardiologist. Int J Cardiol 132:30-37.
44. Stein DJ, Scott K, Haro Abad JM, Aguilar-Gaxiola S, Alonso J, Angermeyer M, Demytteneare K, de Girolamo G, Iwata N, Posada-Villa J, Kovess V, Lara C, Ormel J, Kessler RC, Von Korff M (2010) Early childhood adversity and later hypertension: data from the World Mental Health Survey. Ann Clin Psychiatry 22:19-28.
45. Swanson LW, Lind RW (1986) Neural projections subserving the initiation of a specific motivated behavior in the rat: new projections from the subfornical organ. Brain Res 379:399-403.
46. Tanaka J, Ushigome A, Hori K, Nomura M (1998) Responses of raphe nucleus projecting subfornical organ neurons to angiotensin II in rats. Brain Res Bull 45:315-318.
47. Tucker DC, Saper CB (1985) Specificity of spinal projections from hypothalamic and brainstem areas which innervate sympathetic preganglionic neurons. Brain Res 360:159-164.
48. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397-409.