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Genomic discovery of ion channel genes in the central nervous system of the lamprey Petromyzon marinus.

ABSTRACT: The lamprey is a popular animal model for a number of types of neurobiology studies, including organization and operation of locomotor and respiratory systems, behavioral recovery following spinal cord injury (SCI), cellular and synaptic neurophysiology, comparative neuroanatomy, neuropharmacology, and neurodevelopment. Yet relatively little work has been done on the molecular underpinnings of nervous system function in lamprey. This is due in part to a paucity of gene information for some of the most fundamental proteins involved in neural activity: ion channels. We report here 47 putative ion channel sequences in the central nervous system (CNS) of larval lampreys from the predicted coding sequences (CDS) discovered in the P. marinus genome. These include 32 potassium (K+) channels, six sodium (Na+) channels, and nine calcium (Ca2+) channels. Through RT-PCR, we examined the distribution of these ion channels in the anterior (ARRN), middle (MRRN), and posterior (PRRN) rhombencephalic reticular nuclei, as well as the spinal cord (SC). This study lays the foundation for incorporating more advanced molecular techniques to investigate the role of ion channels in the neural networks of the lamprey.

SUBMITTER: Northcutt AJ

PROVIDER: S-EPMC6579644 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Genomic discovery of ion channel genes in the central nervous system of the lamprey Petromyzon marinus.

Northcutt Adam J AJ Hough Ryan A RA Frese Alexander N AN McClellan Andrew D AD Schulz David J DJ

Marine genomics 20190314

The lamprey is a popular animal model for a number of types of neurobiology studies, including organization and operation of locomotor and respiratory systems, behavioral recovery following spinal cord injury (SCI), cellular and synaptic neurophysiology, comparative neuroanatomy, neuropharmacology, and neurodevelopment. Yet relatively little work has been done on the molecular underpinnings of nervous system function in lamprey. This is due in part to a paucity of gene information for some of th ...[more]

PMID: 30878501

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Project description:The sea lamprey, Petromyzon marinus, is an anadromous, semelparous species that is vulnerable to endangered in parts of its native range due in part to loss of spawning habitat because of man-made barriers. The ability of lampreys to return to the ocean or estuary and search out alternative spawning river systems would be limited by their osmoregulatory ability in seawater. A reduction in tolerance to salinity has been documented in migrants, although the underlying mechanisms have not been characterized. We examined the capacity for marine osmoregulation in upstream spawning migrants by characterizing the physiological effects of salinity challenge from a molecular perspective. Estuarine-captured migrants held in freshwater (FW) for ∼1 week (short-term acclimation) or 2 months (long-term acclimation) underwent an incremental salinity challenge until loss of equilibrium occurred and upper thresholds of 25 and 17.5, respectively, occurred. Regardless of salinity tolerance, all lamprey downregulated FW ion-uptake mechanisms [gill transcripts of Na(+):Cl(-) cotransporter (NCC/slc12a3) and epithelial Na(+) channel (ENaC/scnn1) and kidney Na(+)/K(+)-ATPase (NKA) protein and activity but not transcript]. At their respective salinity limits, lamprey displayed a clear osmoregulatory failure and were unable to regulate [Na(+)] and [Cl(-)] in plasma and intestinal fluid within physiological limits, becoming osmocompromised. A >90% drop in haematocrit indicated haemolysis, and higher plasma concentrations of the cytosolic enzymes alanine aminotransferase, aspartate aminotransferase and lactate dehydrogenase indicated damage to other tissues, including liver. However, >80% of short-term FW-acclimated fish were able to osmoregulate efficiently, with less haemolysis and tissue damage. This osmoregulatory ability was correlated with significant upregulation of the secretory form of Na(+):K(+):2Cl(-) cotransporter (NKCC1/slc12a2) transcript levels and the re-emergence of seawater-type ionocytes detected through immunohistochemical NKA immunoreactivity in the gill, the central ionoregulatory organ. This work sheds light on the molecular and physiological limits to the potential return to seawater for lampreys searching for alternative FW systems in which to spawn.

Dataset Information

Genomic discovery of ion channel genes in the central nervous system of the lamprey Petromyzon marinus.

Publications

Genomic discovery of ion channel genes in the central nervous system of the lamprey Petromyzon marinus.

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