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Brain Structure and Function

, Volume 225, Issue 1, pp 249–284 | Cite as

Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems

  • D. Sobrido-Cameán
  • L. A. Yáñez-Guerra
  • D. Robledo
  • E. López-Varela
  • M. C. Rodicio
  • M. R. Elphick
  • R. Anadón
  • Antón Barreiro-IglesiasEmail author
Original Article

Abstract

Cholecystokinin (CCK) is a neuropeptide that modulates processes such as digestion, satiety, and anxiety. CCK-type peptides have been characterized in jawed vertebrates and invertebrates, but little is known about CCK-type signalling in the most ancient group of vertebrates, the agnathans. Here, we have cloned and sequenced a cDNA encoding a sea lamprey (Petromyzon marinus L.) CCK-type precursor (PmCCK), which contains a CCK-type octapeptide sequence (PmCCK-8) that is highly similar to gnathostome CCKs. Using mRNA in situ hybridization, the distribution of PmCCK-expressing neurons was mapped in the CNS of P. marinus. This revealed PmCCK-expressing neurons in the hypothalamus, posterior tubercle, prethalamus, nucleus of the medial longitudinal fasciculus, midbrain tegmentum, isthmus, rhombencephalic reticular formation, and the putative nucleus of the solitary tract. Some PmCCK-expressing neuronal populations were only observed in adults, revealing important differences with larvae. We generated an antiserum to PmCCK-8 to enable immunohistochemical analysis of CCK expression, which revealed that GABA or glutamate, but not serotonin, tyrosine hydroxylase or neuropeptide Y, is co-expressed in some PmCCK-8-immunoreactive (ir) neurons. Importantly, this is the first demonstration of co-localization of GABA and CCK in neurons of a non-mammalian vertebrate. We also characterized extensive cholecystokinergic fibre systems of the CNS, including innervation of habenular subnuclei. A conspicuous PmCCK-8-ir tract ascending in the lateral rhombencephalon selectively innervates a glutamatergic population in the dorsal isthmic grey. Interestingly, this tract is reminiscent of the secondary gustatory/visceral tract of teleosts. In conclusion, this study provides important new information on the evolution of the cholecystokinergic system in vertebrates.

Keywords

Lamprey Cholecystokinin GABA Glutamate Brain Spinal cord 

Abbreviations

5-HT

Serotonin

ALL

Anterior lateral line nerve

ARRN

Anterior rhombencephalic reticular nucleus

B3

Rhombencephalic Müller cell 3

Ch

Optic chiasm

dc

Dorsal cell

DC

Dorsal column

DCN

Dorsal column nucleus

DHyp

Dorsal hypothalamus

dic

Dorsal isthmic commissure

DIG

Dorsal isthmic grey

DN

Dorsal nucleus of the octavolateralis area

dV

Descending trigeminal root

Em

Prethalamic eminence

fr

Fasciculus retroflexus

GABA

Gamma-aminobutyric acid

Gl

Glomerular layer of olfactory bulb

Ha

Habenula

NH

Neurohypophysis

Hyp

Hypothalamus

I1

Giant isthmic neuron

IIId

Oculomotor nucleus, dorsal subnucleus

III-l

Oculomotor nucleus, lateral subnucleus

IP

Interpeduncular nucleus

IS

Isthmus

ISd

Dorsal isthmus region

ISv

Ventral isthmus region

IV

Trochlear nucleus

IXm

Glossopharyngeal motor nucleus

lHa

Left habenula

LHyp

Lateral hypothalamus

LP

Lateral pallium

LPd

Lateral pallium, dorsal part

LPv

Lateral pallium, ventral part

LT

Lamina terminalis

M

Mesencephalon

M1–3

Giant Müller cells 1–3

M5

Nucleus M5 of Schober

Ma

Mammillary nucleus

mlf

Medial longitudinal fasciculus

MN

Medial nucleus of the octavolateralis area

MP

Medial pallium

Mr

Mammillary recess

MRRN

Medial rhombencephalic reticular nucleus

Mth

Mauthner neuron

NH

Neurohypophysis

Nmlf

Nucleus of the medial longitudinal fasciculus

OB

Olfactory bulb

OLA

Octavolateralis area

OMa

Octavomotor anterior nucleus

ON

Optic nerve

OT

Optic tectum

ot

Optic tract

P

Pineal organ

PC

Posterior commissure

pl

Choroid plexus

PLL

Posterior lateral line nerve

Pm

Petromyzon marinus

PO

Preoptic nucleus

PoC

Nucleus of the postoptic commissure

PoR

Postoptic recess

prIII

Perioculomotor region

PRRN

Posterior rhombencephalic reticular nucleus

PT

Pretectum

PTh

Prethalamus

PTN

Posterior tubercle nucleus

Rh

Rhombencephalon

rHa

Right habenula

N-SC

Neurobiotin labelling from the spinal cord

NPY

Neuropeptide Y

SC

Spinal cord

ShL

Subhippocampal lobe

sl

Sulcus limitans

So

Nucleus of the solitary tract

SOC

Spino‐occipital motor column

Sp

Septum

Str

Striatum

TH

Tyrosine hydroxylase

Th

Thalamus

TS

Torus semicircularis

v

Ventricle

VIIm

Facial motor nucleus

VIII

Octaval nerve

VHyp

Ventral hypothalamus

Vm

Trigeminal motor nucleus

VN

Ventral nucleus of the octavolateralis area

Vs

Trigeminal spinal nucleus

Xm

Vagal motor nucleus

zl

Zona limitans intrathalamica

Notes

Acknowledgements

Grant sponsors: Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund 2007–2013 (Grant number: BFU-2017-87079-P). L.A.Y.G was supported by a PhD studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship no. 418612) and Queen Mary University of London. D.R. is supported by Institute Strategic Funding Grants to The Roslin Institute (BBS/E/D/20002172, BBS/E/D/30002275 and BBS/E/D/10002070). The authors thank the staff of Ximonde Biological Station for providing the lampreys used in this study, and the Microscopy Service (University of Santiago de Compostela) and Dr. Mercedes Rivas Cascallar for confocal microscope facilities and help.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest (financial or non-financial).

Ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

429_2019_1999_MOESM1_ESM.pdf (74 kb)
Supplementary Figure 1. Alignment of selected CCK precursors from chordates used for construction of the phylogenetic tree in figure 1. Conserved residues are highlighted. Conservation in more than 70% of sequences is highlighted in black, conservative substitutions are highlighted in grey. Species names and accession numbers are as follows: Hsap (Homo sapiens; P06307), Rnor (Rattus norvegicus; P01355), Sscr (Sus scrofa; P01356), Ggal (Gallus gallus; Q9PU41), Cpic (Chrysemys picta belli; XP_005278641.1, XP_005278642.1), Amis (Alligator mississippiensis; KYO43311.1), Lcha (Latimeria chalumnae; XP_006013099.1), Ipun (Ictalurus punctatus; XM_017484277.1), Amex (Astyanax mexicanus; XP_022531953.1), Drer (Danio rerio; XP_002665661.2), Saca (Squalus acanthias; CAB10585.1), Cmil (Callorhinchus milii; XP_007895078.1), Pmar (P. marinus; ADJ57604.1), Lcam (Lethenteron camtschaticum; APJL01044986.1), Cint (Ciona intestinalis; NP_001027711.1) (PDF 74 kb)

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Functional Biology, Edificio CIBUS, Campus Vida, Faculty of BiologyUniversidade de Santiago de CompostelaSantiago de CompostelaSpain
  2. 2.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK
  3. 3.The Roslin Institute and Royal (Dick) School of Veterinary StudiesThe University of EdinburghMidlothianUK

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