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

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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.

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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

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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.

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  1. Department of Functional Biology, Edificio CIBUS, Campus Vida, Faculty of Biology, Universidade de Santiago de Compostela, 15782, Santiago de Compostela, A Coruña, Spain

    D. Sobrido-Cameán, E. López-Varela, M. C. Rodicio, R. Anadón & Antón Barreiro-Iglesias

  2. School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK

    L. A. Yáñez-Guerra & M. R. Elphick

  3. The Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, EH25 9RG, UK

    D. Robledo

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  1. D. Sobrido-Cameán
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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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Sobrido-Cameán, D., Yáñez-Guerra, L.A., Robledo, D. et al. Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems. Brain Struct Funct 225, 249–284 (2020). https://doi.org/10.1007/s00429-019-01999-2

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