Abstract
The identification of three somatostatin (SST) genes (SSTa, SSTb, and SSTc) in lampreys (Tostivint et al. Gen Comp Endocrinol 237:89–97 https://doi.org/10.1016/j.ygcen.2016.08.006, 2016) prompted us to study their expression in the brain and spinal cord of the sea lamprey by in situ hybridization. These three genes were only expressed in equivalent neuronal populations in the hypothalamus. In other regions, SST transcripts showed clear differential expression. In the telencephalon, SSTc-positive cells were observed in the medial pallium, ventral part of the lateral pallium, striatum, subhippocampal lobe, and preoptic region. In the diencephalon, SSTa-positive cells were observed in the thalamus and SSTc-positive cells in the prethalamus, posterior tubercle, pretectal area, and nucleus of the medial longitudinal fascicle. In the midbrain, SSTc-positive cells were observed in the torus semicircularis, lateral reticular area, and perioculomotor tegmentum. Different SSTa- and SSTc-positive populations were observed in the isthmus. SSTc neurons were also observed in the rostral octavolateralis area and caudal rhombencephalon. In the spinal cord, SSTa was expressed in cerebrospinal-fluid-contacting (CSF-c) neurons and SSTc in non-CSF-c interneurons. Comparison with previous immunohistochemical studies using anti-SST-14 antibodies strongly suggests that SST-14-like neurons correspond with the SSTa populations. Thus, the SSTc populations were not reported previously in immunohistochemical studies. Cluster-based analyses and alignments of mature peptides suggested that SSTa is an ortholog of SST1 and that SSTb is closely related to SST2 and SST6. These results provide important new insights into the evolution of the somatostatinergic system in vertebrates.
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Availability of data and materials
Histological material and raw images are available from the authors upon reasonable request. Sequences have been deposited in GenBank (NCBI).
Abbreviations
- ARRN:
-
Anterior rhombencephalic reticular nucleus
- Cc:
-
Central canal of spinal cord
- Ch:
-
Optic chiasm
- DC:
-
Dorsal column
- DCN:
-
Dorsal column nucleus
- DIG:
-
Dorsal isthmic gray
- dNpoc:
-
Dorsal part of the nucleus of the tract of the postoptic commissure
- fr:
-
Fasciculus retroflexus
- Ha:
-
Habenula
- Hy:
-
Hypothalamus
- Hyp:
-
Hypophysis
- I1:
-
I1 isthmic giant reticulospinal neuron
- III:
-
Oculomotor nucleus
- IP:
-
Interpeduncular nucleus
- Is:
-
Isthmus
- IXm:
-
Glossopharyngeal motor nucleus
- j:
-
Juvenile (post-metamorphic adult)
- l:
-
Larva
- lHa:
-
Left habenula
- LP:
-
Lateral pallium
- LPv:
-
Ventral region of the lateral pallium
- m:
-
Mature adult (upstream migrating)
- M:
-
Mesencephalon
- MAR:
-
Mammillary recess
- M2:
-
M2 giant Müller reticulospinal cell
- M3:
-
M3 giant Müller reticulospinal cell
- M5:
-
Schober’s M5 nucleus of the mesencephalon
- mlf:
-
Medial longitudinal fascicle
- MP:
-
Medial pallium (prethalamic eminence of Pombal et al. 2009)
- Mpl:
-
Mesencephalic choroid plexus
- MRA:
-
Mesencephalic reticular area
- Nmlf:
-
Nucleus of the medial longitudinal fascicle
- Npoc:
-
Nucleus of the tract of the postoptic commissure
- OB:
-
Olfactory bulbs
- OLA:
-
Octavolateralis area
- OT:
-
Optic tectum
- ot:
-
Optic tract
- P:
-
Pineal organ
- Pa:
-
Parapineal organ
- pc:
-
Posterior commissure
- PO:
-
Preoptic nucleus
- pOc:
-
Perioculomotor region (griseum centrale of Olson et al. 2017)
- poc:
-
Postoptic commissure
- pOMN:
-
Posterior octavomotor nucleus
- Pr:
-
Preoptic recess
- Prn:
-
Preoptic recess nucleus
- PRRN:
-
Posterior rhombencephalic reticular nucleus
- PT:
-
Pretectum
- Pth:
-
Prethalamus (ventral thalamus)
- PTN:
-
Posterior tubercle nucleus
- PTu:
-
Paratubercular region
- rHa:
-
Right habenula
- Rho:
-
Rhombencephalon
- Rpl:
-
Rhombencephalic choroid plexus
- SC:
-
Spinal cord
- sco:
-
Subcomissural organ
- SHL:
-
Subhippocampal lobe
- SO:
-
Spinooccipital motor nucleus
- St:
-
Striatum
- T:
-
Telencephalon
- Th:
-
Thalamus (dorsal thalamus)
- TS:
-
Torus semicircularis
- Vd:
-
Descending trigeminal tract
- Vm:
-
Trigeminal motor nucleus
- vNpoc:
-
Ventral part of the nucleus of the tract of the postoptic commissure
- Xm:
-
Vagal motor nucleus
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Acknowledgements
This work was funded by FEDER/Ministerio de Ciencia, Innovación y Universidades—Agencia Estatal de Investigación (Grant number: BFU-2017-87079-P). We would also like to thank the members of the biological station of Ximonde for help capturing the lamprey samples.
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FEDER/Ministerio de Ciencia, Innovación y Universidades–Agencia Estatal de Investigación (Grant Number: BFU-2017–87079-P).
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429_2021_2224_MOESM1_ESM.fasta
Supplementary file 1. Sequences used for the cluster analysis and alignments performed and shown in figure 1 (FASTA 23 KB)
429_2021_2224_MOESM2_ESM.tif
Supplementary Fig. 1. Raw figure of the cluster analysis presented in Figure 9A. BLOSUM62 cluster map of somatostatin precursors. Nodes correspond to the precursors and are colored according to the key. Edges correspond to BLAST connections of P value >1e-20. The names of the sequences are included in the figure (TIF 1542 KB)
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Sobrido-Cameán, D., Yáñez-Guerra, L.A., Deber, A. et al. Differential expression of somatostatin genes in the central nervous system of the sea lamprey. Brain Struct Funct 226, 1031–1052 (2021). https://doi.org/10.1007/s00429-021-02224-9
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DOI: https://doi.org/10.1007/s00429-021-02224-9