The puzzle of acute stressinduced immunosuppression in animals

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When responding to danger, animals shift into a new physiological state: the acute stress response. Most of the resulting alterations in physiological function optimize the animal's ability to perform flight-or-fight behaviours (Figure 11.1; insects, Roeder, 2005; mammals, Charmandari et al., 2005). However, the effects of acute stress on immune function seem maladaptive. Acute stress is immunosuppressive in animals from three different phyla (Chordata, Mollusca, and Arthropoda) (Adamo, 2008b). It results in a transient decline in resistance to infection in insects (Figure 11.2), molluscs (Lacoste et al., 2001), and vertebrates (Davis et al., 1997). Some of the effects of acute stress on immune function are induced directly via neural/neuroendocrine/immune connections (Adamo, 2008b).

Some of these direct connections to the immune system appear to be conserved across phyla, suggesting that they serve an important function (Ottaviani and Franceschi, 1996). For example, vertebrates, molluscs, and insects use chemically similar derivatives of the amino acid tyrosine to implement their acute stress responses (Ottaviani and Franceschi, 1996). Vertebrates (Cooper et al., 2003) and molluscs (Lacoste et al., 2001) release noradrenaline (norepinephrine) during acute stress, whereas insects release noradrenaline's chemical cousin, octopamine (Orchard et al, 1993). The chemical similarity between octopamine

Figure 11.1 Fighting crickets (Gryllus texensis).

Figure 11.1 Fighting crickets (Gryllus texensis).

on a 30

Control

Flight

Fight

Running

Control

Flight

Fight

Running

Figure 11.2 Flying, fighting, and forced running result in a decline in resistance to the bacterium Serratia marcescens compared with resting control crickets (Gryllus texensis) (Z= 3.3, P<0.001; test for trends and contrasts for frequency data; Meddis, 1984). Data are normalized and taken from Adamo and Parsons (2006) and unpublished data. Sample sizes: control n = 225, flight n=94, fight n = 24, running n = 120.

and noradrenaline (Figure 11.3), the similarity between the enzymes involved in their synthesis, and the similarities between the sequences of their receptor and transporter molecules support the argument that octopamine and noradrenaline pathways arose from the same ancestral pathway (Evans and Maqueira, 2005; Roeder, 2005; Caveney et al., 2006).

Both octopamine (Table 11.1) and noradrenaline are involved in preparing the body for flight-or-fight behaviours (Roeder, 2005), suggesting that this is an ancient, conserved function of these compounds (Gerhardt et al., 1997; Roeder, 1999). In vertebrates, noradrenaline also mediates a connection between the nervous system and the immune system that is active during acute stress (Emeny et al., 2007; Nance and Sanders, 2007). In insects, the evidence suggests that octopamine performs a similar function (Table 11.2). Octopamine is released as a neurohormone in insects (e.g. orthopterans) by the dorsal unpaired medial cells (DUM neurones) during an acute stress response (Orchard et al., 1993; Pflüger and Stevenson, 2005; Roeder, 2005). DUM neurones also have extensive peripheral processes (Pflüger and Stevenson, 2005). Therefore, octopamine has the potential to reach both circulating immune cells (i.e. haemocytes) and immune organs such as the fat body.

Noradrenaline and octopamine can influence immune function because immune cells in vertebrates (e.g. Webster et al,, 2002; Madden, 2003), molluscs (Lacoste et al., 2002), and insects (Gole et al, 1982; Orr et al., 1985) have receptors for these compounds. In insects, octopamine may mediate some of the decline in disease resistance after acute stress. Injections of octopamine prior to a bacterial challenge result in increased mortality (Adamo and Parsons, 2006). However, octopamine also has immunoenhancing effects (Table 11.2; Brey, 1994). Octopamine can increase resistance to infection on a 30

when the pathogen is co-incubated with it (Baines et al., 1992; Baines and Downer, 1992; Dunphy and Downer, 1994). However, this effect may be non-specific. When bacteria were incubated with

Noradrenaline

Octopamine

Figure 11.3 The chemical structures of octopamine and noradrenaline (norepinephrine). Adapted from Cooper et al. (2003).

octopamine plus an octopamine antagonist, cockroaches still exhibited increased disease resistance (Baines and Downer, 1994). This is opposite to the result that would be expected if the effect were specific for octopamine. Dunphy and Downer (1994) suggest that octopamine may act as an opso-nin, due to the surface charge on the molecule. If octopamine could act as an opsonin, this would explain why co-incubating bacteria or other pathogens with octopamine prior to injection increases pathogen clearance from the haemocoel (Dunphy and Downer, 1994) and increases host survival (e.g. Baines et al, 1992). Other octopamine effects on the immune system, however, appear to be mediated by specific octopamine receptors (Baines and Downer, 1994).

Like octopamine in insects, noradrenaline in vertebrates produces a mix of immunosuppres-sive and immunoenhancing effects (Nance and Sanders, 2007). As in insects, the overall effect of noradrenaline in vertebrates is an increase in susceptibility to pathogens (e.g. Cao and Lawrence,

Table 11.1 Effects of octopamine in insects. Not all effects occur in all species (Orchard et al, 1993; Roeder, 1999, 2005).

Function

Direction of change

Respiratory rate Heart rate

Lipid release (direct and/or indirect effects) Responsiveness to sensory stimuli Muscle tension Energy metabolism Feeding

Increased Increased Increased Increased

Increased (some muscles) Increased glycolysis Decreased

Table 11.2 Effects of octopamine on

insect immune function.

Immune function

Change

Reference

Susceptibility to bacterial infection

Increased

Adamo and Parsons (2006)

Haemocyte phagocytic ability

Increased

Baines et al. (1992)

Haemocyte motility

Increased

Diehl-Jones et al. (1996)

Nodule formation

Increased

Baines et al. (1992)

Number of circulating haemocytes

Increased (pharmacological dose)

Dunphy and Downer (1994)

Decreased (physiological dose)

Phenoloxidase activity

No effect

Dunphy and Downer (1994)

S.A. Adamo (unpublished results)

2002). The complexity of the effects of noradren-aline and other stress hormones on vertebrate immune function has prevented a clear adaptive explanation for these changes (Sternberg, 2006). Madden (2003), Maestroni (2005), and Kin and Sanders (2006) suggest that these complex effects are a result of noradrenaline playing a role in maintaining immune homeostasis (i.e. normal immune function). Octopamine may play a similar role in invertebrates. Octopamine is present in the haemolymph of resting insects (e.g. Adamo et al., 1995). Although this may reflect the difficulty of taking blood from insects without stressing them, it may also indicate that octopamine is chronically present in the haemolymph. Octopamine has a half-life of 15 min or less in insect haemolymph (Goosey and Candy, 1982; Adamo, 2005). Therefore, it should be undetectable unless it is being released constantly. A background level of octopamine in non-stressed animals would be consistent with the hypothesis that octopamine helps to maintain normal immune function in invertebrates. However, if octopamine (in insects) and noradrenaline (in mammals) help to maintain immune homeostasis, why do the levels of both compounds increase dramatically during acute stress (e.g. Orchard et al., 1993; Kin and Sanders, 2006)? In other words, how does an increase in the octopamine or noradrenaline concentration help to maintain optimal immune function in animals during acute stress?

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