Zymosan-induced immune challenge modifies the stress response of hypoxic air-breathing fish ( Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transporter functions and non-specific immune response

Simi, S.; Peter, Valsa S.; Peter, M. C. Subhash

doi:10.1016/j.ygcen.2016.11.009

Cited by 17 publications

(21 citation statements)

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“…An ouabain-sensitive ATPase system that is activated by NH 4 + , could direct the transport of NH 4 + against Na + because hydrated NH 4 + and K + ions can compete each other because of the same ionic radius. 93 Our recent study provided evidence that a NNA system exists in the osmoregulatory tissues of our air-breathing fish, 5 and it is likely that it may have a functional role in the fish brain segments that transport NH 4 + in exchange of Na + . However, traditionally, in brain, excess NH 4 + has been converted to glutamine by glutamine synthetase via an ATP-dependent reaction of NH 4 + and glutamate.…”

Section: Discussionmentioning

confidence: 94%

“…Consistent observation has also been found in the osmoregulatory epithelia of air-breathing fish where NKA responded differentially to both immune challenge and hypoxia stress. 5…”

Section: Discussionmentioning

confidence: 99%

“…4 For example, zymosan treatment that evokes nonspecific immune response can activate phagocytic and lysozomal functions in air-breathing fish, providing evidence for a direct association of ion transporter functions with phagocytic and lysozomal activities in this fish. 5…”

Section: Introductionmentioning

confidence: 99%

“…9 In contrast, a lowered plasma cortisol level after zymosan treatment has been found in this fish and that indicates suppression of a cortisol-driven stress response during immune challenge. 5…”

Section: Introductionmentioning

confidence: 99%

“…Recently, we have found evidence for the presence of a Na + / NH 4 + - ATPase (NNA) transporter system in the osmoregulatory epithelia of air-breathing fish. 5 Ammonia rapidly compromises astrocyte K + buffering, increasing its extracellular concentration and over activating the Na + -K + -2Cl − cotransporter isoform 1 (NKCC1) in neurons. 52 NH 4 + increases Na + uptake into all areas of the brain which indicates that NH 4 + could stimulate NKA function and increases extracellular Na + concentrations and possibly intracellular concentrations with a concomitant decrease in K + concentrations.…”

Section: Introductionmentioning

confidence: 99%

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Hypoxia Stress Modifies Na⁺/K⁺-ATPase, H⁺/K⁺-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Peter

Simi

2017

J Exp Neurosci

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Fishes are equipped to sense stressful stimuli and are able to respond to environmental stressor such as hypoxia with varying pattern of stress response. The functional attributes of brain to hypoxia stress in relation to ion transport and its interaction during immune challenge have not yet delineated in fish. We, therefore, explored the pattern of ion transporter functions and messenger RNA (mRNA) expression of α1-subunit isoforms of Na+/K+-ATPase (NKA) in the brain segments, namely, prosencephalon (PC), mesencephalon (MC), and metencephalon (MeC) in an obligate air-breathing fish exposed either to hypoxia stress (30 minutes forced immersion in water) or challenged with zymosan treatment (25-200 ng g−1 for 24 hours) or both. Zymosan that produced nonspecific immune responses evoked differential regulation of NKA, H+/K+-ATPase (HKA), and Na+/NH4+-ATPase (NNA) in the varied brain segments. On the contrary, hypoxia stress that demanded activation of NKA in PC and MeC showed a reversed NKA activity pattern in MeC of immune-challenged fish. A compromised HKA and NNA regulation during hypoxia stress was found in immune-challenged fish, indicating the role of these brain ion transporters to hypoxia stress and immune challenges. The differential mRNA expression of α1-subunit isoforms of NKA, nkaα1a, nkaα1b, and nkaα1c, in hypoxia-stressed brain showed a shift in its expression pattern during hypoxia stress-immune interaction in PC and MC. Evidence is thus presented for the first time that ion transporters such as HKA and NNA along with NKA act as functional brain markers which respond differentially to both hypoxia stress and immune challenges. Taken together, the data further provide evidence for a differential Na+, K+, H+, and NH4+ ion signaling that exists in brain neuronal clusters during hypoxia stress-immune interaction as a result of modified regulations of NKA, HKA, and NNA transporter functions and nkaα1 isoform regulation.

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Section: Discussionmentioning

confidence: 94%

“…Consistent observation has also been found in the osmoregulatory epithelia of air-breathing fish where NKA responded differentially to both immune challenge and hypoxia stress. 5…”

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Hypoxia Stress Modifies Na⁺/K⁺-ATPase, H⁺/K⁺-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Peter

Simi

2017

J Exp Neurosci

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Nitric oxide synthase (NOS) inhibitor L‐NAME activates inducible NOS/NO system and drives multidimensional regulation of Na⁺/K⁺‐ATPase in ionocyte epithelia of immersion‐stressed air‐breathing fish (Anabas testudineus Bloch)

Peter

Gayathry

2021

J Exp Zool Pt A

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Nitric oxide (NO) has been implicated in Na+ homeostatic control in water‐breathing fishes. It is, however, uncertain whether air‐breathing fish relies on NO to coordinate Na+/K+‐ATPase (NKA)‐driven Na+ transport during acute hypoxemia. We, thus, examined the action of nitric oxide synthase (NOS) inhibitor, L‐NAME on NO availability, inducible NOS (iNOS) protein abundance and the regulatory dynamics of NKA in osmoregulatory epithelia of Anabas testudineus kept at induced hypoxemia. As expected in nonstressed fish, in vivo L‐NAME (100 ng g−1) challenge for 30 min declined NO production in serum (40%) and osmoregulatory tissues (average 51.6%). Surprisingly, the magnitude of such reduction was less in hypoxemic fish after L‐NAME challenge due to the net gain of NO (average 23.7%) in these tissues. Concurrently, higher iNOS protein abundance was found in branchial and intestinal epithelia of these hypoxemic fish. In nonstressed fish, L‐NAME treatment inhibited the NKA activity in branchial and intestinal epithelia while stimulating its activity in renal epithelia. Interestingly in hypoxemic fish, L‐NAME challenge restored the hypoxemia‐inhibited NKA activity in branchial and renal epithelia. Similar recovery response was evident in the NKAα protein abundance in immunoblots and immunofluorescence images of branchial epithelia of these fish. Analysis of Nkaα1 isoform transcript abundance (Nkaα1a, α1b, α1c) also showed spatial and preferential regulation of Nkaα1 isoform switching. Collectively, the data indicate that L‐NAME challenge activates iNOS/NO system in the branchial ionocyte epithelia of hypoxemia‐stressed Anabas and demands multidimensional regulation of NKA to restore the Na+ transport rate probably to defend against acute hypoxemia.

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Thyroid axis participates in high-temperature-induced male sex reversal through its activation by the stress response

Castañeda-Cortés,

Rosa,

Boan

et al. 2023

Cell. Mol. Life Sci.

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Zymosan-induced immune challenge modifies the stress response of hypoxic air-breathing fish ( Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transporter functions and non-specific immune response

Cited by 17 publications

References 73 publications

Hypoxia Stress Modifies Na⁺/K⁺-ATPase, H⁺/K⁺-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Hypoxia Stress Modifies Na⁺/K⁺-ATPase, H⁺/K⁺-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Nitric oxide synthase (NOS) inhibitor L‐NAME activates inducible NOS/NO system and drives multidimensional regulation of Na⁺/K⁺‐ATPase in ionocyte epithelia of immersion‐stressed air‐breathing fish (Anabas testudineus Bloch)

Thyroid axis participates in high-temperature-induced male sex reversal through its activation by the stress response

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Zymosan-induced immune challenge modifies the stress response of hypoxic air-breathing fish ( Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transporter functions and non-specific immune response

Cited by 17 publications

References 73 publications

Hypoxia Stress Modifies Na+/K+-ATPase, H+/K+-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Hypoxia Stress Modifies Na+/K+-ATPase, H+/K+-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Nitric oxide synthase (NOS) inhibitor L‐NAME activates inducible NOS/NO system and drives multidimensional regulation of Na+/K+‐ATPase in ionocyte epithelia of immersion‐stressed air‐breathing fish (Anabas testudineus Bloch)

Thyroid axis participates in high-temperature-induced male sex reversal through its activation by the stress response

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Hypoxia Stress Modifies Na⁺/K⁺-ATPase, H⁺/K⁺-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Hypoxia Stress Modifies Na⁺/K⁺-ATPase, H⁺/K⁺-ATPase, Na+/NH4+-ATPase, and nkaα1 Isoform Expression in the Brain of Immune-Challenged Air-Breathing Fish

Nitric oxide synthase (NOS) inhibitor L‐NAME activates inducible NOS/NO system and drives multidimensional regulation of Na⁺/K⁺‐ATPase in ionocyte epithelia of immersion‐stressed air‐breathing fish (Anabas testudineus Bloch)