Dorsal and Ventral Medullary Catecholamine Cell Groups Contribute Differentially to Systemic Interleukin-1β-Induced Hypothalamic Pituitary Adrenal Axis Responses

Buller, Kathryn M.; Xu, Yangyang; Dayas, Christopher V.; Day, Trevor A.

doi:10.1159/000054629

Cited by 87 publications

(80 citation statements)

References 41 publications

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“…Data from the present study demonstrate that endogenous glucocorticoids act at DHB GR to inhibit baseline corticosterone secretion, but to enhance the corticosterone response to stress. These results are consistent with other studies demonstrating that the NTS both tonically inhibits baseline HPA axis function (24) and can mediate stimulation of the HPA axis (4,40). The finding that corticosterone can act at DHB GR to maintain the corticosterone response to repeated psychological stress is also in agreement with a study by Laugero et al (34) reporting positive feedback Fig.…”

Section: Effects Of Dhb Mif On Plasma Corticosteronesupporting

confidence: 93%

Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress

Bechtold

Patel²,

Hochhaus³

et al. 2009

American Journal of Physiology-Regulatory, Integrative and Comp

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Exogenous glucocorticoids act within the hindbrain to enhance the arterial pressure response to acute novel stress. Here we tested the hypothesis that endogenous glucocorticoids act at hindbrain glucocorticoid receptors (GR) to augment cardiovascular responses to restraint stress in a model of stress hyperreactivity, the borderline hypertensive rat (BHR). A 3-to 4-mg pellet of the GR antagonist mifepristone (Mif) was implanted over the dorsal hindbrain (DHB) in WistarKyoto (WKY) and BHRs. Control pellets consisted of either sham DHB or subcutaneous Mif pellets. Rats were either subjected to repeated restraint stress (chronic stress) or only handled (acute stress) for 3-4 wk, then all rats were stressed on the final day of the experiment. BHR showed limited adaptation of the arterial pressure response to restraint, and DHB Mif significantly (P Յ 0.05) attenuated the arterial pressure response to restraint in both acutely and chronically stressed BHR. In contrast, WKY exhibited a substantial adaptation of the pressure response to repeated restraint that was significantly reversed by DHB Mif. DHB Mif and chronic stress each significantly increased baseline plasma corticosterone concentration and adrenal weight and reduced the corticosterone response to stress in all rats. We conclude that endogenous corticosterone acts via hindbrain GR to enhance the arterial pressure response to stress in BHR, but to promote the adaptation of the arterial pressure response to stress in normotensive rats. Endogenous corticosterone also acts in the hindbrain to restrain corticosterone at rest but to maintain the corticosterone response to stress in both BHR and WKY rats. corticosterone; brain; nucleus of the solitary tract; hypothalamicpituitary-adrenal axis; chronic stress EXAGGERATED CARDIOVASCULAR responses to acute stress and chronic stress increase the risk for hypertension and cardiovascular disease (1,3,13,15,31,38,42,58,68). Acute stress rapidly increases blood pressure, heart rate, plasma glucocorticoid concentration, and blood glucose levels (8), while chronic or repeated stress is associated with increases in baseline blood pressure and glucocorticoids (17). Chronically elevated glucocorticoids increase morbidity and mortality from cardiovascular disease and alterations in the glucocorticoid receptor (GR), and in glucocorticoid metabolizing enzymes are associated with hypertension and cardiovascular disease in humans (28,30,35,36,39,48,49,61, 65,67,70,71). Thus, chronic stress-induced elevations in glucocorticoids likely contribute to the adverse effects of stress on cardiovascular health.The mechanisms by which glucocorticoids modulate cardiovascular stress responses are not fully understood. A review by Sapolsky et al. (52) concluded that glucocorticoids act permissively to enhance the arterial pressure response to many physical stressors, in part by supporting the peripheral effects of catecholamines. Other studies indicate that chronic, systemic elevations in glucocorticoids enhance cardiovascular and catecholamine re...

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Section: Effects Of Dhb Mif On Plasma Corticosteronesupporting

confidence: 93%

Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress

Bechtold

Patel²,

Hochhaus³

et al. 2009

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Aside from the CeA, in animals that received IL-1␤, the amygdala was virtually devoid of Fospositive cells, except for a very small number of cells in the medial amygdala. We have reported and illustrated these patterns in several recent publications (Buller et al, 1998, Buller et al, 2001Xu et al, 1999).…”

Section: Control Animals and Distribution Of Fos Immunolabeling In Thsupporting

confidence: 56%

“…The next day, each animal received recombinant human IL-1␤ (1 g/kg, i.a., R & D Systems Inc., Minneapolis, MN). This dose of IL-1␤ was chosen because it has been shown to be just sufficient to produce reliable HPA axis activation and associated c-fos expression in the brain regions of interest (Ericsson et al, 1994;Buller et al, 1998, Buller et al, 2001Xu et al, 1999). Two hours after IL-1␤ injection, animals were deeply anesthetized with sodium pentobarbitone (80 mg/ kg, i.p.)…”

Section: Systemic Administration Of Il-1␤mentioning

confidence: 99%

“…A 1-in-4 forebrain and 1-in-5 brainstem series of sections were then subjected to a well-documented dual immunoperoxidase technique Buller et al, 2001) for the combined visualization of nuclear Fos and cytoplasmic CTb.…”

Section: Immunohistochemistrymentioning

confidence: 99%

“…Also, unlike other brain regions recruited by IL-1␤ such as the PVN and brainstem catecholamine cell groups (Breder and Saper, 1996;Cao et al, 1996;Elmquist et al, 1997;Ericsson et al, 1997;Buller et al, 1998), CeA cell recruitment does not appear to depend on the production of secondary signaling molecules such as prostaglandins (Buller et al, 1998). In support of an immune activated afferent pathway to the CeA, we have demonstrated recently that chemical lesions of nucleus tractus solitarius (NTS) cells in the brainstem reduce the number of CeA cells recruited in response to systemic IL-1␤ (Buller et al, 2001). Furthermore, one study that examined the brainstem origins of afferent inputs to the CeA reported that systemic administration of lipopolysaccharide (LPS) activates CeA afferent inputs with cell bodies resident primarily in the parabrachial nucleus (PB) (Tkacs and Li, 1999).…”

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confidence: 95%

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Systemic administration of interleukin‐1β activates select populations of central amygdala afferents

Buller

Day

2002

J of Comparative Neurology

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The central nucleus of the amygdala (CeA) is activated robustly by an immune challenge such as the systemic administration of the proinflammatory cytokine interleukin-1␤ (IL-1␤). Because IL-1␤ is not believed to cross the blood-brain barrier in any significant amount, it is likely that IL-1␤ elicits CeA cell recruitment by means of activation of afferents to the CeA. However, although many studies have investigated the origins of afferent inputs to the CeA, we do not know which of these also respond to IL-1␤. Therefore, to identify candidate neurons responsible for the recruitment of CeA cells by an immune challenge, we iontophoretically deposited a retrograde tracer, cholera toxin b-subunit (CTb), into the CeA of rats 7 days before systemic delivery of IL-1␤ (1 g/kg, i.a.). By using combined immunohistochemistry, we then quantified the number of Fos-positive CTb cells in six major regions known to innervate the CeA. These included the medial prefrontal cortex, paraventricular thalamus (PVT), ventral tegmental area, parabrachial nucleus (PB), nucleus tractus solitarius, and ventrolateral medulla. Our results show that after deposit of CTb into the CeA, the majority of double-labeled cells were located in the PB and the PVT, suggesting that CeA cell activation by systemic IL-1␤ is likely to arise predominantly from cell bodies located in these regions. These findings may have significant implications in determining the central pathways involved in generating acute central responses to a systemic immune challenge.

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Evidence that the bed nucleus of the stria terminalis contributes to the modulation of hypophysiotropic corticotropin‐releasing factor cell responses to systemic interleukin‐1β

Crane

Buller

Day

2003

J of Comparative Neurology

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Systemic infection activates the hypothalamic-pituitary-adrenal (HPA) axis, and brainstem catecholamine cells have been shown to contribute to this response. However, recent work also suggests an important role for the central amygdala (CeA). Because direct connections between the CeA and the hypothalamic apex of the HPA axis are minimal, the present study investigated whether the bed nucleus of the stria terminalis (BNST) might act as a relay between them. This was done by using an animal model of acute systemic infection involving intravascular delivery of the proinflammatory cytokine interleukin-1beta (IL-1beta, 1 microg/kg). Unilateral ibotenic acid lesions encompassing the ventral BNST significantly reduced both IL-1beta-induced increases in Fos immunoreactivity in corticotropin-releasing factor (CRF) cells of the hypothalamic paraventricular nucleus (PVN) and corresponding increases in adrenocorticotropic hormone (ACTH) secretion. Similar lesions had no effect on CRF cell responses to physical restraint, suggesting that the effects of BNST lesions were not due to a nonspecific effect on stress responses. In further studies, we examined the functional connections between PVN, BNST, and CeA by combining retrograde tracing with mapping of IL-1beta-induced increases in Fos in BNST and CeA cells. In the case of the BNST, these studies showed that systemic IL-1beta administration recruits ventral BNST cells that project directly to the PVN. In the case of the CeA, the results obtained were consistent with an arrangement whereby lateral CeA cells recruited by systemic IL-1beta could regulate the activity of medial CeA cells projecting directly to the BNST. In conclusion, the present findings are consistent with the hypothesis that the BNST acts as a relay between the CeA and PVN, thereby contributing to CeA modulation of hypophysiotropic CRF cell responses to systemic administration of IL-1beta.

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Dorsal and Ventral Medullary Catecholamine Cell Groups Contribute Differentially to Systemic Interleukin-1β-Induced Hypothalamic Pituitary Adrenal Axis Responses

Cited by 87 publications

References 41 publications

Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress

Chronic blockade of hindbrain glucocorticoid receptors reduces blood pressure responses to novel stress and attenuates adaptation to repeated stress

Systemic administration of interleukin‐1β activates select populations of central amygdala afferents

Evidence that the bed nucleus of the stria terminalis contributes to the modulation of hypophysiotropic corticotropin‐releasing factor cell responses to systemic interleukin‐1β

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