Stress Neurohormones & Psychiatric Populations
As noted in section 1.44 psychiatric populations, such as those with DSM-IV diagnoses of post-traumatic stress disorder (PTSD) and major depression present different adrenocortical responses to stress, e.g. hypocortisolemia and hypercortisolemia, respectively. The former is reflective of negative-feedback sensitivity, the later, negative-feedback inhibition. Hypocortisolism is a state of chronic low levels of circulating steroid (Tsigos & Chrousos, 2002). During exogenous challenge of CRH and ACTH endogenous cortisol synthesis and secretion is reduced (Heim et al., 2000a; Raison & Miller, 2003). Low cortisol levels are one of two very important criteria that meet Th1 dominance for immune response, the other being lack of sensitivity for mast cell activation (Webster et al., 1998; Elekov and Chrousos, 2002). Th1 dominance can heighten immunity due to low levels of the immunosuppressing secreting steroid (Elenkov et al., 2000). Due to chronic low levels of circulating steroid the hypocortisolemic patient may demonstrate greater propensity for developing later site-specific and inflammatory diseases, such as irritable bowel disorder (Fass et al., 1995; Irwin et al., 1996) and rheumatoid arthritis (Boscarino, unpublished findings). Fibromyalgia has been associated with chronic psychological stress noted in section 1.33 of this web site and also stress related condition, PTSD (Culclasure et al., 1993; Amir et al., 1997).
In hypercortisolism the adrenal gland has been hyperresponsive to stress, cumulatively synthesizing and secreting cortisol in response to chronic stress-induced HPA activity (McAllister-Williams et al., 1998; Pariante & Miller, 2001). This has resulted in chronic high levels of circulating endogenous steroid that with negative feedback inhibition suppresses further HPA activity and the cascade for neurohormonal secretion, e.g. pituitary CRH and ACTH. Hypercortisolism is one of two criteria that is associated with anti-inflammatory Th2 dominance for humoral immunity (Elenkov et al., 1999), the other being mast cell production and secretion (Elenkov and Chrousos, 2002). Hypercortisolism suppresses immunity due to heightened levels of immunosuppressing secreting steroid (Elenkov et al., 2000) in response to its relationship in mediating the secretion of anti-inflammatory cytokines, like IL-10 (Elenkov and Chrousos, 2002).
The remainder of this document will examine the nature of stress-induced neurohormone responses in certain psychiatric populations. Because the nature of neurohormone response may be linked with the degree and intensity of chronic stress, this document will also introduce research findings that examine both the stress response and its association with stress-related histories.
One way to monitor cortisol levels is to examine the number of glucocorticoid receptors (GRs) which often suggests a reduction in circulating cortisol levels. Conversely higher levels of circulating cortisol suggest reduced GRs. Patients with PTSD (with and without comorbid depression) have substantially greater numbers of plasma (Yehuda et al., 1991b) and urinary (Yehuda et al., 1993a) lymphocyte GR levels when compared with controls and patients with major depression, respectively. Depressed patients present comparable (Rupprecht et al., 1991a) and significantly decreased plasma lymphocyte GR levels (Gormley et al., 1985) and GR levels in peripheral blood mononuclear cells in response to dexamethasone treatment (Calfa et al., 2003) when compared with healthy controls. GR levels are increased and corrected to control levels in response to the onset of mood stabilizing psychopharmacological treatments with tricyclic antidepressants, selective 5-HT reuptake inhibitiors (SSRIs), and MAO inhibitors (Calfa et al., 2003).
Administration of oral metyrapone, an 11-β-hydroxylase inhibitor, serves to block cortisol synthesis (Lisansky et al., 1989). In high doses it is capable of almost completely suppressing the secretion and circulation of cortisol and dramatically increasing ACTH and 11-deoxycortisol levels in both PTSD and healthy controls (Yehuda et al., 1996). Lower doses of the drug suppress circulating cortisol and induce ACTH and 11-deoxycortisol decreases in symptomatic versus asymptomatic combat vets (Kanter et al., 2001). Administration of lower doses of the drug followed by dexamethasone treatment completely suppress ACTH secretion in depressed patients when compared with healthy controls (Rupprecht et al., 1991b).
Administration of dexamethasone (DEX) induces exaggerated plasma super-suppression of the steroid in adult trauma survivors (e.g. combat veterans and Holocaust survivors) with PTSD when compared with weaker suppression levels in survivors with PTSD symptoms in the presence of comorbid major depression, survivors without PTSD symptoms and healthy controls (Yehuda et al., 1993b, 1995a, 2002; Grossman et al., 2003). In addition exaggerated cortisol suppression is accompanied by significant reductions in GR concentrations in response to increasing circulating steroid. PTSD with comorbidity for major depression weakens this suppression and slows and lowers reductions in GR concentrations (Yehuda et al., 2002). Adults who report dissociative symptoms along with histories of childhood PTS are more likely to suppress administered cortisol than asymptomatic adults with similar histories (Stein et al., 1997). Exaggerated cortisol suppression is probably due in part to receptor influences on ligand (that fuels receptor transcription and then reduces it in response to circulating steroid) and HPA responsivity to circulating ligand. Moderate amounts of dexamethasone suppress stress-induced HPA activity at the pituitary level by blocking the secretion of endogenous corticosterone secretion from the adrenal cortex to the brain and in particular to GRs. Dexamethasone binds with high affinity to the GRs, corticosterone prefers the MR (de Kloet, 2003).
Another trauma-related psychiatric condition, borderline personality disorder (BPD) presents less uniform DEX findings. One study (Grossman et al., 1997) individualized its findings, reflecting that 4 of 5 subjects diagnosed with BPD suppress cortisol, 2 of 5 downregulate GRs, and 1 of 5 presents a history of childhood abuse with comorbid PTSD symptoms. Despite that fact that 13 of 19 BPD subjects report histories of PTS, the entire sample of 28 (without comorbid depression) presents tendencies for suppressing cortisol and ACTH in response to DEX administration (Rinne et al., 2002). Those BPD patients with PTSD symptoms are more apt to significantly suppress exogenous cortisol (Grossman et al., 2003) then those without symptoms.
Patients with major depression (melancholic-type) demonstrate lower baseline cytoplasmic receptor content than control subjects and higher baseline serum cortisol values (Lowy et al., 1984). They fail to suppress cortisol in response to DEX administration and exhibit reduced GR responsivity in their downregulation (Gormley et al., 1985; Grossman et al., 2003). On the other hand all patients with drug resistant depression have normal levels of circulating cortisol and the majority suppress exogenous cortisol in a similar manner as patients diagnosed with atypical depression (Levitan et al., 2002). These neurohormonal characteristics along with lymphocyte steroid resistance underlie their resistance to antidepressant therapies (Bauer et al., 2002). This may also suggest that the sense of depression associated with drug resistant depression and atypical depression may be differentially linked with proinflammatory cytokine activation of IFN-α and IL-6 as noted in section 1.43 and 1.46b.
Women symptomatic for PTSD and with histories of childhood sexual abuse in response to CRH challenge present blunted ACTH response and lower levels of cortisol when compared with asymptomatic abuse survivors (Bremner et al., 2003). On the other hand in response to CRH challenge (with ovine CRH-οCRH) women without depression and with histories of child abuse present higher mean stimulated ACTH concentrations when compared with other groups (depressed women without prior child abuse history, depressed women with prior child abuse history, and nondepressed women without prior child abuse history). Depressed women (with concurrent PTSD symptoms) with and depressed women without histories of child abuse exhibit lower ACTH concentrations in response of οCRH than comparison subjects. In response to exogenous stimulation by either οCRH or ACTH1-24 depressed women (with concurrent PTSD symptoms) with histories of child abuse and abused women without depression demonstrate lower basal and stimulated cortisol concentrations (Heim et al., 2001). In addition, in response to CRH challenge depressed individuals present significant increases in plasma cortisol and cerebrospinal fluid (CSF) cortisol and norepinephrine (NE) levels (Wong et al., 2000) when compared with controls. Although depressives share similar plasma values for ACTH when compared with healthy controls or even blunted levels; the plasma cortisol-to-ACTH ratio is significantly higher in individuals with melancholic depression (Dinan et al., 1999; Wong et al., 2000).
Serum and salivary cortisol levels for symptomatic combat veterans for PTSD exposed to heavy combat and children with history exposure to trauma and PTSD symptoms are lower than when compared to those for asymptomatic controls respectively (Boscarino, 1996; Carrion et al., 2002). Low urinary cortisol levels in adult offspring of holocaust survivors (Yehuda et al., 2000) are significantly associated with PTSD symptoms and low urinary cortisol levels in their parents who are holocaust survivors (Yehuda et al., 1995b). Elevated salivary cortisol secretion is linked with disorganized thought and greater positive symptom severity in a group of schizophrenic subjects (Walder et al., 2000).
Both NE and CRH cerebrospinal fluid (CSF) levels are elevated in combat vets with PTSD symptoms (Bremner et al., 1997; Baker et al., 1999; Geracioti et al., 2001) and patients with obsessive-compulsive and panic disorder (Fossey et al., 1996) suggesting some degree of HPA dysregulation in these populations. Postmortem tissue analysis reveals that CRH and AVP expressing neurons are four and three times higher in depressed individuals when compared with controls (Raadsheer et al. 1994). Increases in mean plasma norepinephrine levels in depressed subjects are positively associated with symptom severity and degree (Yehuda et al., 1998).
The psychological stress (Heim et al., 2000b) of anticipated public speaking induces increases in mean ACTH, cortisol and heart rate levels across all experimental groups (e.g. women with and without depression with histories of childhood sexual abuse and women with and without depression without histories of childhood sexual abuse). Depressed and non-depressed women with histories of childhood sexual abuse exhibit greater ACTH concentrations than the other groups reporting no histories of childhood sexual abuse. Depressed women with abuse histories also exhibit higher reactive (Heim et al., 2000b) and resting plasma cortisol levels. Depressed individuals not only present resting increases in cortisol levels but also increases in heart rate (Lehofer et al., 1997; Moser et al., 1998) and in skin conductance and decreases in respiration (Guinjoan et al., 1995). Depressed individuals also present resting diurnal alterations in morning and evening salivary cortisol concentrations (Strickland et al., 2002), and sustained elevations in plasma cortisol (Depue & Keiman, 1979). Experimentally induced stress in response to role playing a previously anger-filled event increases both diastolic and systolic blood pressure and greater plasma NE responses in bioassay analysis (Light et al., 1998).
Neurohormonal and HPA alterations have been reported for many psychiatric disorders. These alterations seem to be associated with chronic neurobiological maladaptations to cumulative responses to stressors.
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Neurohormone Stress Challenges
According to the animal research acute immobilization stress produces significant increases in CRH mRNA expression in the hypothalamic paraventricular nucleus parvocellular neurons (PVNpc) and plasma ACTH and corticosterone levels (Makino et al., 1995) when compared to basal conditions (Ma et al., 1997a). Newly formed transcripts for both CRH and AVP mRNA in the PVN are expressed in the cytoplasm several hours after stress onset (Ma et al., 1997). A single immobilization session is capable of inducing prolonged expression of median PVNpc CRH and AVP mRNA levels that persist (without additional transcription and peptide release) for as long as one and four days respectively (Aubry et al., 1999). Repeated immobilization stress produces elevations in plasma corticosterone and even greater AVP mRNA expression when compared to CRH mRNA levels (Makino et al., 1995). Laboratory animals who have been repeatedly and chronically immobilized for as many as sixteen days produce concurrent significant increases in AVP mRNA and insignificant changes or decreases in PVNpc CRH mRNA levels and labeling when compared with basal states (Bartanusz et al., 1993; Ma et al., 1997b). These findings are fairly consistent across strains (Gomez et al., 1996). The slowing of CRH secretion suggests that AVP may take over as the major stimulator of ACTH as well as the HPA axis in response to repeated and chronic stress (Harbuz, 2002). Removal of the adrenal gland, adrenalectomy, induces immediate CRH mRNA gene transcription that is followed by decreases in the rate of CRH mRNA degradation (Ma et al., 2001) and decreases in pituitary CRH mRNA levels (Rabadan-Diehl et al., 1997). The former is suggestive of corticosterone/glucocorticoid’s role in regulating CRH mRNA by inhibiting its transcription and decreasing its nuclear mRNA stability. CRH receptor 1 knock out (CRHR1 KO) rats are unable to mount HPA activity in response to ACTH challenge, suggesting that this receptor specifically plays a significant role in the eventual release of corticosterone (Muller et al., 2001). Reductions in CRH and/or ACTH secretion on post-training day 28 in previously stressed rats in response to repeated immobilization stress may be suggestive of desensitization of HPA responsivity (Valles et al., 2003). Psychological stress produces neurohormonal alterations in stress-induced neurohormonal response.
These neurohormonal alterations can also be simulated by injection of respective neurohormones. Single injection of corticosterone immediately reduces pituitary CRH receptor mRNA, increases plasma corticosterone that persists for as long as six days (Ochedalski et al., 1998), and significantly decreases pituitary GR binding 30-90 minutes after injection (Cole et al., 2000). Single injection of ovine CRH (οCRH) decreases circulating CRH receptor expression (Ochedalski et al., 1998) by stimulating corticosterone release, which is comparable to typical stress response levels (Cole et al., 2000). Laboratory animals, 7 and 21 days after having experienced two sessions of chronic social defeat, respond to CRH injection with significant increases in ACTH levels immediately after injection (Buwalda et al., 1999).
Repeated daily restraint for 10 minutes over 3 days diminishes ACTH response. Corticosterone pretreatment similarly reduces adrenocorticotropin (ACTH) levels even further (Gadek-Michalska & Bugajski, 2003) reflecting this secretagogue’s vulnerability to steroid-influenced inhibition with furthering stimulation of HPA negative feedback inhibition (Dallman et al., 1987). Two weeks of chronic immobilization stress produces ACTH increases that are strain specific, i.e. Brown-Norway (BN), Spontaneous Hypertensive (SHR), Fisher (FIS), and Wistar-Kyoto(WKY) rats. Corticosterone increases have also been noted in Lewis, SHR, and WKY strains (Gomez et al., 1996). Reexposure to a previous acute stressor tends to reduce ACTH reactivity in adrenalectomized (ADX) or intact animals in the presence or absence of exogenous corticosterone respectively (Marti et al., 1999). But when a new stressor is introduced ACTH levels exceed levels achieved with the initial or preceding stressor (Johnson et al., 2002).
In summary CRH (intensified by subsequent vasopressin (AVP)) secretion in the medial PVN and median eminence induces CRH secretion of ACTH in the anterior pituitary. CRH-induced ACTH then sets off the cascade for adrenocortical steroid secretion (GCs). According to section 1.41 of this web site circulating GCs in vitro stimulate the expression of GR and MR transcription factors, which result in their nuclear transactivation and binding with steroid responsive DNA sequences. According to section 1.43 of this web site steroid transcription provides anti-inflammatory negative feedback by allowing transcription and expression of anti-inflammatory markers, like IL-10. Steroid transcription according to section 1.43 also interferes in proinflammatory transcription factor’s NF-κB expression (by allowing expression of inhibitory IκB) which contains NF-κB to the cell’s cytoplasm.
There are many ways neuroscientists and neuroendocrinologists can monitor neurohormone responses in certain patient populations. One way is to monitor human subject’s plasma neurohormone response to psychological stressors during an experimental paradigm or exposing a subject to script driven imagery or sensory cues and reminders of a previously stressful, traumatic event to which one has since adapted. Another way is to measure the course of a patient’s neurohormone response evidenced in secreted body fluids, i.e. resting cerebral spinal fluid, saliva, and urine over a sustained period of time. A third way is to monitor and document a patient’s response to neurohormonal injection and challenge relating to the stress-related neurohormonal cascade. As noted above the addition of or reduction of any component of the HPA neurohormonal cascade can alter its nature. Additionally these alterations are able to simulate the nature of the stress-induced neurohormonal cascade.
Different psychiatric and autoimmune populations present alterations in the nature of their neurohormonal cascade. This is typically monitored by methods noted above. For example post-traumatic stress disorder (PTSD) or certain inflammatory diseases (such as chronic fatigue syndrome and fibromyalgia) are associated with a hyposecretion of cortisol called hypocortisolemia (Yehuda et al., 1991; Heim et al., 2000; Raison & Miller, 2003). As noted earlier animal research demonstrates rather vividly that acute stress stimulates the secretion of stress-related neurohormones for HPA negative feedback inhibition; however, chronic stress induces alterations in CRH and ACTH secretion, likely at the level of the pituitary, regulating the nature of adrenocortical secretion (Tsigos & Chrousos, 2002). A state of hypersecretion of cortisol, hypercortisolemia, (McAllister-Williams et al., 1998; Pariante & Miller, 2001; Groenink et al., 2002) is characteristic of the neurohormone state that underlies major depression and obsessive-compulsive disorder as well as physical conditions, such as type 2 diabetes mellitus and central obesity (Tsigos & Chrousos, 2002). Changes associated with chronic stress may have the capacity to later induce changes in cortisol secretion.
Like animal models healthy individuals and patients in different diagnostic categories demonstrate particular neurohormonal and neuroimmune composites that are symptom-linked and predictable in their cascade. These concepts will be expanded on in subsequent sections.
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