The interruption of thyroid and interrenal and the inter-hormonal interference in fish: Does it promote physiologic adaptation or maladaptation?

General and Comparative Endocrinology 174 (2011) 249–258

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Review

The interruption of thyroid and interrenal and the inter-hormonal interference in fish: Does it promote physiologic adaptation or maladaptation? Valsa S. Peter, M.C. Subhash Peter ⇑ Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram 695 581, Kerala, India

a r t i c l e

i n f o

Article history: Received 20 September 2011 Revised 27 September 2011 Accepted 29 September 2011 Available online 5 October 2011 Keywords: Fish Endocrine disruption Thyroid hormones Interrenal Cortisol Thyroid interruption

a b s t r a c t Endocrines, the chief components of chemical centers which produce hormones in tune with intrinsic and extrinsic clues, create a chemical bridge between the organism and the environment. In fishes also hormones integrate and modulate many physiologic functions and its synthesis, release, biological actions and metabolic clearance are well regulated. Consequently, thyroid hormones (THs) and cortisol, the products of thyroid and interrenal axes, have been identified for their common integrative actions on metabolic and osmotic functions in fish. On the other hand, many anthropogenic chemical substances, popularly known as endocrine disrupting chemicals, have been shown to disrupt the hormone–receptor signaling pathways in a number fish species. These chemicals which are known for their ability to induce endocrine disruption particularly on thyroid and interrenals can cause malfunction or maladaptation of many vital processes which are involved in the development, growth and reproduction in fish. On the contrary, evidence is presented that the endocrine interrupting agents (EIAs) can cause interruption of thyroid and interrenals, resulting in physiologic compensatory mechanisms which can be adaptive, though such hormonal interactions are less recognized in fishes. The EIAs of physical, chemical and biological origins can specifically interrupt and modify the hormonal interactions between THs and cortisol, resulting in specific patterns of inter-hormonal interference. The physiologic analysis of these interhormonal interruptions during acclimation and post-acclimation to intrinsic or extrinsic EIAs reveals that combinations of anti-hormonal, pro-hormonal or stati-hormonal interference may help the fish to finetune their metabolic and osmotic performances as part of physiologic adaptation. This novel hypothesis on the phenomenon of inter-hormonal interference and its consequent physiologic interference during thyroid and interrenal interruption thus forms the basis of physiologic acclimation. This interfering action of TH and cortisol during hormonal interruption may subsequently promote ecological adaptation in fish as these physiologic processes ultimately favor them to survive in their hostile environment. Ó 2011 Elsevier Inc. All rights reserved.

1. Introduction Fishes have evolved complex and multistep physiologic mechanisms by which they maintain their physiologic homeostasis in challenging environment. The sensitivity of these physiologic systems to environmental oscillations implies that this state of physiologic steadiness is due to the plasticity of physiologic systems coordinated by neuroendocrine circuitries. Fishes respond to environmental challenges or stressor by triggering a series of physiologic modifications evoking integrated stress responses which are either compensatory or adaptive or both but enable them to overcome the disturbance of physiologic homeostasis due to the state of stress [100,35,61]. Consequently, many environmental stressors have been identified for its effects on the rate of energy utilization, osmotic and metabolic functions and ultimately the growth ⇑ Corresponding author. Fax: +91 471 2597514. E-mail address: [email protected] (M.C.S. Peter). 0016-6480/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2011.09.018

functions of fish [5,65,41,61]. The effects of toxicants on metabolic pattern have been extensively studied in fishes [28,29,43,73] and many of them can affect its energy balance [65,100,70]. Likewise, many chemical stressors have been frequently shown to disrupt mineral and water balance in fishes [85,73,43]. A wide array of synthetic chemicals released into the environment may disrupt hormone/receptor signaling pathways and may be regarded as endocrine disrupting chemicals or EDCs [9,11,101,23]. Convincing evidences suggest that many EDCs can interact with TH receptor [15,36] and sex steroids receptors [1,97]. Furthermore, compelling evidences for the effects of EDCs on many expression and regulatory pathways are available in addition to its effects on cross-talks between the components of an endocrine axis [33,50,105]. Similarly, a negative impact of EDCs on wild population and communities of fishes of rivers of United Kingdom have also been studied [93]. A reduction in the fertility in fishes which can upset the progression of community structure has been found in fishes. Indeed, a long-term availability of many

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EDCs in aquatic ecosystem can induce specific endocrine disruption phenotypes. Unlike many EDCs that are chiefly the byproducts, the availability of pharmaceuticals in aquatic ecosystem produces greater threat to many non-target organisms including fish [48,81]. As a chemical link between the organism and its environment, endocrines work in conjunction with the physiologic demand that comes either from a biologic or environmental clue. Among the key endocrine axes that integrate and modulate the network of physiologic processes, thyroid and interrenal axes enjoy supreme positions in the chemical signaling scenario in fish physiology. Mounting evidences have clearly documented that thyroxine (T4) and triiodothyronine (T3) as thyroid hormones (THs) of thyroid axes and cortisol as the product of interrenal axis, direct and modulate many physiologic processes in the development, growth and reproduction in fish [31,39,40,47,20,21,77,61]. Consequently, the synthesis, release, biologic actions and metabolic clearence of these hormones have been well documented in fishes. The presence of anthropogenic chemicals in many contaminated aquatic bodies imposes variations in the THs production in many fish species. For example, fishes collected from San Francisco Bay which is known for high levels of contaminant showed reduced plasma T4 with varied levels of T3 [10]. The thyroid disruption in these fishes has shown significant correlation with hepatic concentration of environmental contaminants including PCB, PAH and pesticides [10]. A varied pattern of thyroid response found in shiner surf perch and Pacific staghorn sculpin indicates the differential sensitivity of the thyroid gland to different contaminants [10]. Extensive studies on climbing perch have also shown similar sensitivity of thyroid to both toxic and non-toxic stressors [73,71,74,72,60,61]. Like thyroid, fish interrenals have also shown a higher sensitivity to many biologic and environmental stimuli. The distruption of interrenals due to environmental chemicals has also been well documented in many fish species [88–91,53]. Interruption of thyroid and interrenals occur in many fish species due to the action of endocrine interrupting agents (EIAs) which comprise biological, physical and chemical agents. Physiologic analyses on the effects of EIAs on thyroid and interrenal axes have indicated that the interactive property of these axes can become adaptive during the processes of acclimation in many fish species. In this review we attempt to illustrate this property of hormones of thyroid and interrenal in fish during its acclimation to varied toxic and non-toxic EIAs. Consequently, we have recognized specific patterns of inter-hormonal interference as an adaptive mechanism that operates during the interruption of thyroid and interrenals. The physiologic and ecological implications of this inter-hormonal interruption and its subsequent physiologic interference in some fish models have been discussed in this review. As key endocrine axes of fish, thyroid and interrenal show a great degree of integrated and coupled interaction and many instances, the components of these axes integrate and modulate each other and modify its common hormonal actions [61].

2. Endocrine interrupting agents (EIAs) and physiologic acclimation Fishes rely on their physiologic and biochemical machineries to cope up with a physiologic threat that may be of either extrinsic or intrinsic orgins. The process of acclimation lies on the physiologic competence of an organism to perceive and accommodate specific stimuli which arise either from within the body or from the environment. In general, fishes are equipped well to perceive stress stimuli and they respond to the stimuli by exhibiting a series by physiologic modifications including stress response. This biologic or physiologic response of fish to accommodate a threat allows

them to rely on the process of physiologic acclimation [67]. In this phase, the fish shows classic physiologic response which is often coupled with a stabilizing phase where they depend on compensatory or an adaptive modification of physiologic processes. The process of acclimation can be seen in fish models during or after exposure to EIAs which is more evident during their physiologic recovery after a challenge [67]. For example, when fishes are kept out of water for a few minutes they become hypoxic and that induces classic physiologic response. Similarly, keeping the challenged fish back into water help them to recover from this EIA exposure. During this phase of post-EIA acclimation, the fish again relies on their own physiologic processes to return to normal conditions [67]. The processes of physiologic acclimation can easily be identified in fish with these approaches. The involvement of endocrine signals including thyroid and interrenal hormones in the process of physiologic acclimation has been extensively studied in an air-breathing fish (Anabas testudineus), commonly known as climbing perch. This fish when kept at different environmental conditions respond differentially with its more adaptive physiologic modifications [61,71,72]. 2.1. Non-toxic EIAs Limited studies have addressed the sensitivity of thyroid to non-toxic EIAs like net confinement, air exposure, and high stocking density [40,96,12,100,70,59,61] compared to the studies which address the toxic challenges. Induction of stress by net confinement produces substantial rise in plasma cortisol in tilapia and climbing perch [59,61,71]. The involvement of thyroid in stress acclimation as a modulator of stress response has also been demonstrated in fish species [67,59,61]. For example, net confinement and air exposure of perch and tilapia decline plasma T3 [59,61]. On the contrary, many toxic stressors either promote or produce neutral thyroid responses [62]. Similarly, interrenal axis shows a greater sensitivity to many environmental contaminants. These pollutants interfere and act through many sites including receptor levels, transporters, cellular uptake and metabolism [7,82]. Similar to thyroid, many extrinsic and intrinsic factors have been identified as agents that could induce cortisol release in fishes. For example, age, sex and maturity of the fish [86], the environmental temperature [87], the species and strain of fish [76] and the chemical composition of the water [75] control the actions of cortisol in fish. 2.2. Toxic EIAs Many chemical stressors including EDCs have been shown to affect the physiologic and biochemical machineries of fish tissues [For e.g., 26–29,70,73]. There is evidence of modification of energy status in fish due to the involvement of THs which may enable them to accommodate the direct effects of stressors [71]. Similar involvement of THs can also be found in fish challenged with nimbicidine or rotenone [65,71,74]. Evidences are also available which support the hypothesis on the role of THs in the compensatory and adaptive mechanisms in fish during its recovery phase to combat the disturbed homeostasis [61]. Rotenone, a naturally occurring plant product appears to interrupt thyroid activity in our fish model as it declined its serum concentration of T3 and T4 [60]. This interruption of thyroid due to the declined T3 and T4 levels has also been found in the TH-pretreated and rotenone-exposed fish [60]. This further supports the notion that like many synthetic chemicals, this plant product can also act as an EIA. A number of potent synthetic chemicals which are present in the environment produce thyroid disruption in many vertebrates including fishes [16]. Exposure of catfishes to malathion and endosulfan caused disturbances in circulating THs

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Table 1 The specific patterns of inter-hormonal interference observed between the interaction of thyroid hormone (TH) and cortisol during acclimation or post-acclimation of fish to varied endocrine interrupting agents (EIAs) of extrinsic and intrinsic origins. The phenomenon of inter-hormonal interference occurs during the interaction of TH and cortisol which produces antagonistic, permissive or synergestic interactions in general but it produces a pattern of specific TH-cortisol interferences as listed below. Type

TH status

Cortisol status

Interaction status

Specific inter-hormonal interference status

EIA acclimation

Post EIA-acclimation or (Recovery)

1

"

;

Antagonistic

Not found

Air exposure, phenol (Fig. 5C and D; T4)

2

"



Permissive

"

"

Synergistic

4

;

"

Antagonistic

5

;



Permissive

Salinity acclimation Ref. [80] Hypoxia (Fig. 2A and B; T3, T4) Kerosine (Fig 5A and B; T4) Phenol (Fig. 5C, D; T3) Net confinement Ref. [74], Net confinement (Fig. 1A and B) Bromide (Fig. 4A and B; T3)

Not found

3

6

;

;

Synergistic

7





Neutral

8



"

Permissive

9



;

Permissive

Pro-TH anti-cortisol interference Pro-TH stati-cortisol interference Pro-TH pro-cortisol interference Anti-TH pro-cortisol interference Anti-TH stati-cortisol interference Anti-TH anti-cortisol interference Stati-TH stati-cortisol interference Pro-cortisol stati-TH interference Anti-cortisol stati-TH interference

Air exposure (Fig. 1C and D; T4) Kerosine (Fig. 5A and B; T4), Phenol (Fig. 5C and D; T3)

Not found

Fe II iron (Fig 3A and B; T3), Al (Fig. 3C and D; T3), Hypoxia (Fig. 2A and B; T3,T4) Nitrate (Fig. 4C and D; T4)

Bromide (Fig. 4A and B; T4) Fe II (Fig. 3A and B; T4) Al (Fig 3C and D; T4)

Nitrate (Fig 4A and B; T3), Fe II (Fig. 3A and B; T4), Bromide (Fig. 4A and B; T3), Hypoxia (Fig. 2C and D; T3, T4) Kerosine (Fig. 5A and B; T3)

Hypoxia (Fig. 2C and D; T3, T4)

Nitrate (Fig 4C and D; T3)

[102,84]. Similarly, a decrease in T3 has been reported in rainbow trout exposed to acidic water [14] and to starvation [54]. On the contrary, an activated thyroid axes as evident in the rise of TH release has been demonstrated during acidic exposure of airbreathing fish [67]. The disruptive effect of rotenone on thyroid activity of climbing perch [71] however, contradicts the role of THs in metabolic adaptation in this fish during nimbicidine exposure [71]. There is evidence that chemical stressors like kerosene [73] and the effluent of coconut husk retting [41,68] promote thyroid activity in this

fish. These varied TH responses in fish indicate that both TH homeostasis and its functions are sensitive to the chemical nature and the toxicity of the tested stressor [74]. 3. Inter-hormonal interruption and interference The phenomenon of inter-hormonal interference can be identified in fish models, where it produces specific patterns of THcortisol interference. For example, a decrease in T3 in FW tilapia after a prolonged net-confinement has yielded evidence for a lead

Fig. 1. Pattern of inter-hormonal interference as evident in the plasma T3 and T4 and cortisol levels of fish exposed to EIAs. Columns are means ± SEM for six fish. In (A and B), ⁄⁄ P < 0.01 and ⁄⁄⁄P < 0.001 denote significant difference in the net-confined (NC) fish from the FW control fish, @@P < 0.01 shows significant difference in the air-exposed (AE) and recovery fish from the air-exposed fish.

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Fig. 2. Pattern of inter-hormonal interference as evident in the plasma T3 and T4 and cortisol levels of fish exposed to non-toxic EIAs like hypoxia for 20 min and kept for 1 or 4 days recovery (d R). Columns are means ± SEM for six fish. In (A) ⁄⁄P < 0.01 and ⁄⁄⁄P < 0.001 represent significant difference from SA control fish. @P < 0.05 and @@P < 0.01 denote significant difference from hypoxic fish. In (D) ⁄P < 0.05 shows significant difference from FW control fish.

role of cortisol in regulating the metabolic and hydromineral actions in this fish in the absence of a T3 action [59]. The pattern of metabolic and osmotic responses of this fish further support the specificity of cortisol actions during stress conditions [62]. The altered deiodination activity in the peripheral tissues has been shown to modulate the TH activity in mammals [38] and fishes [20,22,94,98]. A declined plasma T3 and not plasma T4, has been found during confinement of tilapia which indicates a possibility of a modification of T3 metabolism and its availability. The rapid clearance of T3 by cortisol in this fish to combat stress could be one of the adaptive strategies as evident in the earlier studies [96]. Similar decline of plasma T3 has also been reported in physically-disturbed rainbow trout [32] and in kerosene-treated climbing perch [73]. The differential thyroid responses resulting in its interaction with cortisol and its subsequent inter-hormonal interference can also influence the role of deiodinases in directing the specific interference status of these hormones in fish. In other words, peripheral deiodination appears to be a target for EIAs as it critically regulates this system which could determines the hormonal interaction status in fish. The varied pattern of plasma T3 and T4 in fish in response to EIAs exposure also points to a decisive role and the sensitivity of iodothyronine deiodinase system in the regulation of thyroid status in fish. 3.1. TH-cortisol interference and its specific patterns during acclimation and post-acclimation The status of THs and cortisol in the plasma, the important clues on its availability for actions, are in tune with the body’s physiologic demand. Upon analysis, the plasma levels of T3, T4 and corti-

sol in climbing perch clearly illustrate that depending on the type of EIAs, these hormone profiles show varied pattern of specific THcortisol interferences which are listed in Table 1. An inter-hormonal interference between TH and cortisol has been seen during acclimation of fish to net confinement, a nontoxic EIA (Fig. 1). A temporal and inverse yet functional relationship has been found between these hormones in tilapia during net confinement (Fig. 1A and B), suggesting a lead role of cortisol in acclimation processes in this fish. This antagonistic interaction of TH with cortisol is one of the examples of a specific pro-cortisol anti-TH interference that clearly points to a cortisol-driven acclimation processes during a non-toxic EIA exposure (Table 1). Similar negative interaction of thyroid with interrenal axes has been reported earlier for salmonids [104,96], though no correlation between thyroid activity and cortisol has been observed in rainbow trout [44,30] and mummichog [45]. In some studies the possibility of a rapid clearance of THs after cortisol treatment has been proposed [95,13]. For example, in brook trout, cortisol increased the hepatic conversion of T4 to T3 [95]. The rise in plasma cortisol after net-confinement has also been reported in many fishes including striped bass [52], paddlefish [6], gilthead sea bream [2], rainbow trout [92,56] and in the olive flounder [34]. Although a timedependent and stressor-sensitive rise in plasma cortisol has been reported in many fish species [96,19], its relationship between thyroid axes has not been examined in many studies. Acclimation of fish to attend environmental condition thus demands hormonal interaction particularly TH-cortisol interference. A time-dependent increase in plasma cortisol has been found in tilapia after net-confinement with a maximum increase at 12 h, indicating an induction of stress acclimation in this fish [63]. Confinement of this fish to net for 6 and 12 h do not require plasma T3

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but its level decreased at 24 h, without affecting the plasma T4 levels. The anti-TH pro-cortisol interference observed in this fish clearly indicates a cortisol-driven mechanism during a non-toxic EIA acclimation. On the other hand, salinity acclimation of climbing perch produced a rise in T3 with no change in plasma cortisol. This permissive action of TH gives a specific pro-TH stati-cortisol interference that activates TH release to promote salinity acclimation in this fish (Table 1). In tilapia, however, a rise in T4 and not T3 was found during salinity acclimation [59]. Thus, a species-specific hormonal involvement and subsequent changes in the pattern of inter-hormonal interference could be observed during salinity acclimation in these fish. Post-acclimation of climbing perch to 4 day recovery after 2 h air-exposure yielded rises in plasma T4 and cortisol, indicating active roles of both T4 and cortisol in the process of post-EIA acclimation (Fig. 1C and D). This pattern is a classic pro-TH pro-cortisol interference as described in Table 1. Acclimation of climbing perch to kerosine (Fig. 5A and B) or phenol (Fig. 5C and D) rich freshwater produces anti-TH procortisol interference. This inter-hormonal interference indicates a lead role of cortisol in this fish during a toxic EIA acclimation. This is consistent with the earlier report on the protective role of cortisol in metal-exposed tilapia [17]. A specific permissive action of T3 and cortisol can be seen in climbing perch when acclimated to short-term waterborne bromide where it produced anti-TH staticortisol interference (Fig. 4A and B; T3). Similar inter-hormonal interference could also be found in this fish when kept for postEIA acclimation after placing them for short-term Al or Fe(II) iron exposure. Acclimation of fish to these EIAs does not demand TH-driven physiologic machinery instead they manage with the

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existing basal endogenous cortisol or with some unidentified hormonal systems. On the contrary, anti-TH anti-cortisol interference could be found in post-EIA acclimated climbing perch particularly during the acclimation to water-borne nitrate (Fig. 4C and D; T4), though no experimental data on this inter-hormonal interference is available (Table 1). A classic neutral hormonal interaction could be found in fish during acclimation and post-acclimation phases. For example, when climbing perch acclimated to waterborne Fe(II) iron (Fig. 3A and B) its T4 and cortisol levels remained unaffected showing a classic stati-TH stati-cortisol interference status (Table 1). Similar type of inter-hormonal interference could be found in this fish when kept for post-EIA acclimation i.e., keeping the fish for 4 day recovery after 20 min hypoxic condition (Fig. 2C and D) or placing the fish for recovery after acclimating them to Al-rich water (Fig. 3C and D) or recovery after acclimation to water-born bromide (Fig. 4A and B). In contrast, a pattern of anti-cortisol stati-TH interference could be seen when climbing perch were held in hypoxic condition for 20 min (Fig. 2C and D). During this type of inter-hormonal interruption, cortisol has little role in the acclimation process whereas TH shows a permissive role (Table 1). Similar inter-hormonal interference between cortisol and T3 has been found in climbing perch when held for recovery for 4 days after nitrate exposure (Fig. 4C and D; T3). An example of pro-cortisol stati-TH interference could be found in climbing perch when held for acclimation to waterborne Al (Fig. 3C and D; T4). Similar type of inter-hormonal interference could be seen in climbing perch held for post-EIA acclimation of kerosine (Fig. 5A and B; T3), where a rise in plasma

Fig. 3. Pattern of inter-hormonal interference as evident in the plasma T3 and T4 and cortisol levels of fish exposed to toxic EIAs. Columns are means ± SEM for six fish. In (A, C and D) ⁄P < 0.05 and ⁄⁄P < 0.01 indicate significant difference from FW control fish. In (A) @P < 0.05 denotes significant difference from Fe(II)-treated fish. In (C) @P < 0.05 shows significant difference from Al-treated fish.

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Fig. 4. Pattern of inter-hormonal interference as evident in the plasma T3 and T4 and cortisol levels of fish exposed to toxic EIAs. Columns are means ± SEM for six fish. In (A and C) ⁄P < 0.05 and ⁄⁄P < 0.01 represent significant difference from FW control fish. In (C and D) @P < 0.05 indicates significant difference from nitrate-treated fish.

cortisol occurred whereas plasma T3 remained unaffected (Table 1). There is evidence in fish that TH exert some permissive action with cortisol. For example, an upregulation of the number of gill cortisol receptors by T3 alone and its administration together with growth hormone has been reported in Atlantic salmon [83]. Notwithstanding these evidences that document the involvement of TH and cortisol in osmotic regulations in fishes, the role of these hormones during acclimation and post-stress acclimation is less understood [67]. At the same time, the relationship between T3 and T4 that determines its availability in both plasma and tissue corresponds to deiodination status. During salinity acclimation, a decline of T3 occurs in climbing perch which may be due to an inhibition of outer ring deiodination of T4, the key pathway in T4 metabolism. Here, the elevated plasma T4 also points to an increased T4 synthesis which is required for the fish to cope with the salinity challenge. There are instances where plasma T3 increases and plasma T4 decreases as evident in climbing perch during their exposure to phenol (Fig. 5C). In this fish along with the rise in plasma T3, plasma cortisol also shoots up. This synergetic interaction of T3 and cortisol gives a specific pro-TH pro-cortisol interference that occurs during phenol-acclimation (Fig. 5C and D; T3) (Table 1). Salinity-acclimated climbing perch when kept at hypoxic condition for 20 min and placed for 4 day recovery in clean water show a remarkable permissive interaction with TH and cortisol (Fig. 2A and B). A specific anti-TH stati-cortisol interference could be found in this state of post-EIA acclimation (Table 1). 3.2. Physiologic implications of TH-cortisol interference The functional significance of hormonal and physiologic interferences in the process of acclimation and adaptation is worth con-

sidering in animals particularly in fishes. For example, the phenomenon of inter-hormonal interference could be seen in fish when kept at varied biological and environmental conditions. The reciprocal relationship between cortisol and T3 found in the netconfined tilapia [59,61] could further account for their modifications of osmotic and metabolic performances. In climbing perch a tight regulation of plasma cortisol was found during dilute seawater acclimation. This shows a specific interference status in this fish that drives salinity acclimation [80]. On the contrary, an increased plasma cortisol and a decreased plasma free T4 were obtained in Senegalese sole during salinity exposure, suggesting an interaction between these hormones in this fish [3]. The diversity of actions of THs and cortisol on many organs and the metabolic processes in fish make these hormones vital for the development, growth and reproduction [31,61]. For example, in vivo and in vitro studies have clearly shown that THs exert profound influence on many metabolites and indices of intermediary and oxidative metabolism in fishes [64,55,58,70,73]. Likewise, cortisol has been known for its osmotic and metabolic functions in fish [100,18,4]. In many instances, both THs and cortisol ultimately fine-tune the physiologic homeostasis as many physiologic processes work optimally at this state of equilibrium [4,72,61]. A detailed account on the fine-tune mechanism of these processes by TH and cortisol has been reported elsewhere [61]. It is known that many pesticides as endocrine disrupting chemicals influence the metabolic and osmotic machineries in fish [51,37]. On the other hand, the EIAs are equally demanding and can induce compensatory/adaptive modifications of metabolic and osmotic functions in fish. A biphasic nature of the thyroid function particularly on metabolic regulation has been reported in fish and this further suggest the possibility of hormones like cortisol in this processes [58,59,61]. For example, a proteogenic action of THs is most likely

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Fig. 5. Pattern of inter-hormonal interference as evident in the plasma T3 and T4 and cortisol levels of fish exposed to toxic EIAs. Columns are means ± SEM for six fish. In (A– D) ⁄P < 0.05, ⁄⁄P < 0.01 and ⁄⁄⁄P < 0.001 denote significant difference from FW control fish. In (A and B) @P < 0.05 shows significant difference from kerosene-treated fish. In (C and D) @P < 0.05 and @@@P < 0.001 indicate significant difference from phenol-treated fish.

permissive and would facilitate the actions of other hormones [40,55,65,59,61]. A large body of evidence confirm the interaction of thyroid axis with interrenal axis in fish. For example, experimental hypothyroidism due to propylthiouracil feeding has produced little effect on interrenal activity [66]. However, an activated interrenal axis in this hypothyroid tilapia by exogenous T3 shows a direct action of T3 on the interrenal axis which becomes apparent only in hypothyroidic state, though in euthyroid state exogenous T3 has no effect on cortisol release [59]. It is likely that a sort of central interaction between thyroid and interrenal axis might occur in this fish. A central regulation of peripheral interaction between TH and cortisol has been reported in common carp [25] though a release of cortisol from carp head kidney fragment does not occur after T4 treatment [24]. But the release of T4 from kidney of carp occurs after cortisol and ACTH additions [25]. Similarly, an interaction of thyroid and interrenal axis occur at the central level as a decreased plasma cortisol has been found in carp after T4 injection [24]. A stimulatory effect of THs on the interrenal axis has been demonstrated in coho salmon [103], probably because of the need of an increased clearance of T3 by cortisol in this fish as reported in European eels [79] and coho salmon [78]. The results of other studies also indicate a rapid clearance of T3 after cortisol treatment. For instance, an increased hepatic conversion of T4 to T3 by cortisol has been found in brook trout [95]. However, a reduction in plasma T3 by its rapid clearance, without changing the hepatic conversion of T4 to T3, occurs in rainbow trout [13]. The specific actions of THs and cortisol on osmolite regulation are well documented in fishes [66,72,8,18,4,25,40,49]. Stimulation of osmotic competence of osmoregulatory organs [49,45,4] including mitochondria-rich cell function has been demonstrated in a

number fish species [42,57,61,69,72,100]. In many instances, modification of osmotic and metabolic functions correlate with altered thyroid and interrenal functions [61]. The physiologic implication of inter-hormonal interference between TH and cortisol during acclimation are, therefore, vital for the osmotic and metabolic homeostasis in many fish species.

3.3. Ecological implications of TH-cortisol interference The inter-hormonal interference during the disruption of thyroid and interrenal has tremendous impact on the survival of fish particularly during the process of acclimation to a variety of EIAs. In fact, the fish rely on its hormonal and physiologic systems to correct its disturbed homeostasis. Euryhaline fishes thus possess multiple endocrine mechanisms to combat osmotic challenges [46,99]. In these fish, salinity acclimation demands a complex process involving a set of physiologic responses to varied environments with differing ionoregulatory requirements. For example, transfer of climbing perch to 20 ppt salinity on day 1 after transient salinity changes, showed a rise in plasma T4 but declined plasma T3 with an unaffected plasma cortisol [80]. The levels of these hormones, however, returned to basal levels when these fish were kept for a prolonged acclimation of 3 weeks. The salinity acclimation in this fish reveals that they demand TH secretion and its action and not the co-ordinating action of cortisol during the early phase of salinity acclimation. This hormonal interaction, however, fades when the fish becomes fully adaptive to brackish water salinity of 20 ppt after 3 weeks [80]. This mode of interaction falls under pro-TH stati-cortisol interference (Table 1), where T4 leads the acclimation process and not cortisol. The successful salinity

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Fig. 6. The schematic chart representing the phenomenon of inter-hormonal interference that operates between thyroid and interrenal axes of a fish model in response to varied extrinsic and intrinsic stmuli. Upon acclimation, endocrine interrupting agents (EIAs) induce hormonal responses which clearly show interference of thyroid hormone (T3, T4) and cortisol due to the disruption of thyroid and interrenal axes. These interfering actions of TH and cortisol in response to intrinsic and extrinsic EIAs induce hormonal and physiologic interferences which promote physiologic acclimation and adaptation. In contrast, lethal EIAs produce malfunctions of physiologic processes and subsequently maladaptation.

tolerance in this freshwater fish is due to its TH-driven physiologic mechanism which they develop during salinity acclimation. Likewise, there are ample evidences to suggest that the compensatory physiologic modifications in fishes occurs due to the integrated function of osmotic and metabolic organs duly coordinated by hormones like TH and cortisol [4,72,67,61] with an appropriate intervention called inter-hormonal interference. For example, cortisol, along with T3, has been reported to promote the hypo-osmoregulatory ability of coho salmon during smoltification and seawater adaptation [104]. T4 treatment in tilapia had been shown to exert an additive effect on the stimulatory action of cortisol on osmotic regulation activity, though T4 alone failed to elicit such a response in this fish [59]. These results demonstrate the sensitivity of interrenal axis to TH availability, besides indicating a positive correlation between the exogenous TH and interrenal activity in this fish. It is likely that the inter-hormonal interruption and subsequent interference that may occur at hormonal and physiologic levels favor the fish to accommodate the challenge that they perceive during the processes of acclimation to EIAs. Fishes, therefore, rely on thyroid and interrenal axes for accommodating their physiologic demands and the phenomenon of inter-hormonal interference particularly TH-cortisol interference during the process of acclimation thus makes its profound influence on the ecological adaptations of fish. A schematic model illustrating the TH-cortisol interference is presented in Fig. 6. During the controlled conditions, hypothal-

amo–pituitary–thyroid (HPT) axis and the hypothalamo– pituitary–interrenal (HPI) axis shows sensitivity to both intrinsic and extrinsic stimuli. Once the brain and these axes perceive the stimuli which come from endocrine interrupting agents (EIAs) they respond to it with an appropriate pattern of specific TH-cortisol interference. This inter-hormonal interference supports the fish to combat with the challenges with the help of physiologic processes and consequently accomplishes physiologic adaptation. On the other hand, EIAs at its high magnitude and with lethal effects can cause maladaptation in fish due to the malfunction of physiologic processes. 4. Conclusions The varied patterns of thyroid and interrenal responses to EIAs in fish species clearly point to the plasticity of the hormone-driven mechanisms during the processes of acclimation and post-acclimation. There is no doubt that this physiologic plasticity of fish is due to the specific pattern of TH-cortisol interference. This mechanism of physiologic competence thus establishes an error-free physiologic machinery during the course of homeostatic regulation. In this context, it is reasonable that the inter-hormonal interference observed during TH-cortisol interaction has both genetic and adaptive basis which would ensure the continuity of physiologic processes in the event of an EIA challenge. The phenomenon of TH-cortisol interference, as an example of inter-hormonal

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interference due to the thyroid-interrenal interruption during the processes of acclimation, thus forms a physiologic basis of adaptive mechanism favours the fish to survive in the demanding environment. Acknowledgments We thank our students for their involvement in some of the research mentioned in this review. We also thank Rejitha, Manish, Nimta and Sujitha for their technical support. V.S.P. acknowledges UGC, New Delhi for a Research Award (F.30-1/2009/SA-II). We acknowledge UGC for financial support (MRP No. F-39-609/2010/ SR) and the UGC-SAP facility in the Department of Zoology of the University of Kerala for some infrastructural support. References

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