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The Role of δ-Opioid Receptors in Brain Ionic Homeostasis Under Physiological Condition

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Neural Functions of the Delta-Opioid Receptor

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Abstract

Homeostasis is one of the most fundamental concepts in understanding the physiological functions of bodies as well as the pathophysiology of diseases, and in a global view of system biology, is also a vital guiding principle for medicine. Because of the particular importance of ionic environment in neuronal functions, ion homeostasis is the most fundamental mechanism among all the brain homeostasis regulations, and most of the functional activities of the brain are highly dependent on the dynamic and relatively steady state of ionic environment. The concentrations of ions are in dynamic balance under physiological conditions, which depend on the complicated, but elaborate, regulatory mechanisms. The δ-opioid receptor (DOR) regulates a diverse array of physiological functions. DOR and its cognate endogenous opioids are widely expressed throughout the central nervous system and have an extensive interaction with ion channels, receptors, and transporters. DOR can regulate the release of many neurotransmitters, modify neuronal electrical activities and synaptic plasticity, and thereby tightly regulates ion homeostasis in neural activities. In this chapter, we will focus on the regulation of homeostasis of the key cations such as Na+, K+, Ca2+ in the brain under physiological conditions and the role of DOR in such homeostatic regulation. Almost all the previous studies regarding DOR-mediated regulation of ionic homeostasis under normoxic condition focused on intracellular Ca2+ activity. Few studies highlighted the regulation of K+ and Na+ homeostasis despite the functional coupling of DOR with K+ channels and Na+ channels. Overall, the predominant effect of DOR activation on Ca2+ entry is inhibitory. However, some studies show either mobilization of intracellular Ca2+ or stimulation of Ca2+ entry with opioid activation. In general, DOR signaling is inhibitory to Na+ influx and K+ efflux. In regard to this issue, we have recently made the first finding that DOR activation and expression reduces Na+ currents by targeting voltage-sensitive Na+ channels. The DOR effects have been demonstrated to occur through activation of different kind of G proteins, including Gi, Go, and even Gs classes.

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Abbreviations

[Ca2+]i:

Cytosolic free Ca2+ concentrations

[Ca2+]o:

Extracellular Ca2+ concentrations

[K+]e:

Extracellular K+ concentrations

[K+]i:

Intracellular K+ concentrations

[Na+]i:

Intracellular Na+ concentrations

[Na+]o:

Extracellular Na+ concentrations

ACSF:

Artificial cerebrospinal fluid

AMPARs:

AMPA receptors

BBB:

Blood-brain barrier

CCCP:

Carbonyl cyanide m-chlorophenyl hydrazone

CNS:

Central nervous system

CSF:

Cerebrospinal fluid

DA:

Dopamine

DAG:

Diacylglycerol

DAT:

Dopamine transporter

DOR:

δ-Opioid receptor

DRG:

Dorsal root ganglion

EAAT:

Excitatory amino acid transporter (glutamate transporter, also as GluT in Table 5.3)

eGFP:

Enhanced green fluorescent protein

EPSPs/EPSCs:

Excitatory postsynaptic potentials/currents

ER:

Endoplasmic reticulum

GAT:

GABA transporter

GIRK channels:

G-protein-activated inwardly rectifying K+ channels

GPCRs:

G protein-coupled receptors

i.c.v:

Intracerebroventricular

iGluRs:

Ionotropic glutamate receptors

IKir :

Inwardly rectifying K+ currents

IMM:

Inner mitochondrial membrane

IP3 :

Inositol triphosphate

IP3Rs:

IP3 receptors

IPSCs:

Inhibitory postsynaptic currents

ISEs:

Ion-selective electrodes

KOR:

κ-Opioid receptor

LTD:

Long-term depression

LTP:

Long-term potentiation

MAM:

Mitochondria-associated membrane

MAPK:

Mitogen-activated kinase

MCU:

Mitochondrial Ca2+ uniporter

mNCX:

Mitochondrial Na+/Ca2+ exchanger

MOR:

μ-Opioid receptor

nAChRs:

Nicotinic acetylcholine receptors

NCX:

Na+/Ca2+ exchanger

NKCC:

Na+-K+-2Cl− cotransporter

NMDARs:

NMDA receptors

NMDG+ :

N-methyl-D-glucamine

NMR:

Nuclear magnetic resonance

OMM:

Outer mitochondrial membrane

PAG:

Midbrain periaqueductal gray

PBFI:

Potassium-binding benzofuran isophtalate

PIP2 :

Phosphatidylinositol 4,5-bisphosphate

PLC:

Phospholipase C

PMCA:

Plasma membrane Ca2+-ATPase

PTP:

Permeability transition pores

ROCs:

Receptor-operated channels

RYRs:

Ryanodine receptors

SBFI:

Sodium-binding benzofuran isophtalate

SERCA:

Sarco-endoplasmic reticular Ca2+ ATPase

SNAP:

Soluble N-ethylmaleimide sensitive factor Attachment Protein

SNARE:

SNAP REceptor

SOCs:

Store-operated Ca2+ entry channels

STIM:

Stromal interaction molecules

TEA:

Tetraethylammonium

TMA+ :

Tetramethylammonium

TRPCs:

Transient receptor potential channels

TTX:

Tetrodotoxin

VGCCs:

Voltage-gated Ca2+ channels

VGSCs:

Voltage-gated sodium channels

WT:

Wild type

ΔΨm:

Mitochondrial potential

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Acknowledgements

This work was supported by NIH (AT-004422, and HD-034852) and Vivian L Smith Neurologic Foundation.

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  1. Department of Neurosurgery, The University of Texas Medical School at Houston, Houston, TX, 77030, USA

    Dongman Chao Ph.D.

  2. University of Texas Medical School, Houston, TX, USA

    Ying Xia M.D., Ph.D.

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    Ying Xia

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Chao, D., Xia, Y. (2015). The Role of δ-Opioid Receptors in Brain Ionic Homeostasis Under Physiological Condition. In: Xia, Y. (eds) Neural Functions of the Delta-Opioid Receptor. Springer, Cham. https://doi.org/10.1007/978-3-319-25495-1_5

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