Leonardo Rodríguez‐Sosa

Universidad Nacional Autónoma de México

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Hugo Aréchigá

Universidad Nacional Autónoma de México

Gabina Calderón‐Rosete

Universidad Nacional Autónoma de México

Juan Antonio González-Barrios

Instituto Politécnico Nacional

Gonzalo Flores

Benemérita Universidad Autónoma de Puebla

Celia Piña-Leyva

Institute for Social Security and Services for State Workers

Manuel Lara-Lozano

Center for Research and Advanced Studies of the National Polytechnic Institute

Hayde Nallely Moreno-Sandoval

Institute for Social Security and Services for State Workers

Edgar Villagran‐Vargas

Universidad de La Salle Bajío

Rodolfo Delgado‐Lezama

Center for Research and Advanced Studies of the National Polytechnic Institute

Mercedes Graciela Porras Villalobos

Universidad Nacional Autónoma de México

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Instituto Politécnico Nacional

Center for Research and Advanced Studies of the National Polytechnic Institute

Universidad Nacional Autónoma de México

Centro de Investigación en Materiales Avanzados

Benemérita Universidad Autónoma de Puebla

University of Copenhagen

Instituto de Estudios Avanzados

Institute for Social Security and Services for State Workers

Instituto Nacional de Cardiología

Universidad Autónoma del Estado de México

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Supplementary material 1 from: Calderón-Rosete G, González-Barrios JA, Piña-Leyva C, Moreno-Sandoval HN, Lara-Lozano M, Rodríguez-Sosa L (2021) Transcriptional identification of genes light-interacting in the extraretinal photoreceptors of the crayfish Procambarus clarkii. ZooKeys 1072: 107-127. https://doi.org/10.3897/zookeys.1072.73075

Gabina Calderón‐Rosete Juan Antonio González-Barrios Celia Piña-Leyva Hayde Nallely Moreno-Sandoval Manuel Lara-Lozano

Crayfish serve as a model for studying the effect of environmental lighting on locomotor activity and neuroendocrine functions. The effects of light on this organism are mediated differentially by retinal and extraretinal photoreceptors located in the cerebroid ganglion and the pleonal nerve cord. However, some molecular aspects of the phototransduction cascade in the pleonal extraretinal photoreceptors remain unknown. In this study, transcriptome data from the pleonal nerve cord of the crayfish Procambarus clarkii (Girard,1852) were analyzed to identify transcripts that potentially interact with phototransduction process. The Illumina MiSeq System and the pipeline Phylogenetically Informed Annotation (PIA) were employed, which places uncharacterized genes into pre-calculated phylogenies of gene families. Here, for the first time 62 transcripts identified from the pleonal nerve cord that are related to light-interacting pathways are reported; they can be classified into the following 11 sets: 1) retinoid pathway in vertebrates and invertebrates, 2) photoreceptor specification, 3) rhabdomeric phototransduction, 4) opsins 5) ciliary phototransduction, 6) melanin synthesis, 7) pterin synthesis, 8) ommochrome synthesis, 9) heme synthesis, 10) diurnal clock, and 11) crystallins. Moreover, this analysis comparing the sequences located on the pleonal nerve cord to eyestalk sequences reported in other studies reveals 94–100% similarity between the 55 common proteins identified. These results show that both retinal and pleonal non-visual photoreceptors in the crayfish equally expressed the transcripts involved in light detection. Moreover, they suggest that the genes related to ocular and extraocular light perception in the crayfish P. clarkii use biosynthesis pathways and phototransduction cascades commons.

Visual phototransduction

Procambarus clarkii

Opsin

10.3897/zookeys.1072.73075.suppl1

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Serotonin‐caused phase shift of circadian rhythmicity in a photosensitive neuron

Synapse (2007)

Leonardo Rodrı́guez-Sosa Gabina Calderón‐Rosete Gonzalo Flores Mercedes G. Porras

Abstract In the sixth abdominal ganglion (sixth AG) of the crayfish, two photosensitive neurons are located and have been identified as caudal photoreceptors (CPRs). We have expanded our investigation on the role of 5‐Hydroxytryptamine (5‐HT) as a modulator of the spontaneous and light‐induced activity of the CPR. We located, by using immunocytochemistry, neurons in the sixth AG that contain the 5HT 1A receptor. The expression of these receptors was examined by binding assays with [ 3 H] 8‐hydroxy‐2 (di‐ n ‐propylamino) tetralin ([ 3 H(8‐OH‐DPAT). We examined the exogenous action of both 5HT and its agonist 8‐OH‐DPAT on the phase of circadian rhythms of the spontaneous electrical activity and the photoresponse of the CPR in the isolated sixth AG by conventional extracellular recording methods. Experiments were made on the adult crayfish Procambarus clarkii and Cherax quadricarinatus . Thirteen immunopositive neurons were located, principally near the ventral and dorsal surface of the sixth AG, with the mean diameter of their somata 20 ± 3 μm. The specific binding data showed the presence of 5‐HT 1A receptors with a mean level of 22.4 ± 6.6 fmol/mg of wet tissue. Spontaneous and light‐induced electrical activity of the CPR showed circadian variations with their activity more intense at night than in the day. Exogenous application of 5‐HT or 8‐OH‐DPAT causes a circadian phase‐shift in electrical activity of the CPR. Taken together, these results lead us to believe the 5‐HT acts as a modulator of circadian electrical activity of the CPR in the isolated sixth AG of crayfish. Moreover, it suggests that the 5‐HT 1A receptor participates in this modulation. Synapse 61:801–808, 2007. © 2007 Wiley‐Liss, Inc.

Procambarus clarkii

10.1002/syn.20425

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Plataforma económica para cirugía estereotáxica en rata neonata

Revista de Neurología (2009)

Arturo Sierra Israel Camacho Abrego Carlos Escamilla José V. Negrete Díaz Leonardo Rodrı́guez-Sosa

Usually, most commercial platforms that adapt to the stereotaxic apparatus in neonatal rats or small animals, to carry out surgery are very expensive. Moreover, the operator must have certain experience in its handling.The present work presents two platforms, one of them made in acrylic and the other of expanded polystyrene. These adapt perfectly to conventional stereotaxic apparatus, while operator does not require a great entrainment to carry out the surgical procedure. Histological slides of the prefrontal cortex, ventral hippocampus and basolateral amygdala from adult rats (postnatal day 70), staining with cresyl violet are shown. The neonatal lesions were made at postnatal day 7 with ibotenic acid applied in the prefrontal cortex, ventral hippocampus or basolateral amygdala.The present data suggest that it is possible to carry out lesions or to apply drugs in neonatal rats, by using an acrylic or expanded polystyrene adaptor for the stereotaxic apparatus. These have the advantage of being economic and having a simple design. Also, the type of anesthesia used in neonatal lesion rats, is discussed.

Basolateral amygdala

Ibotenic acid

Sensorimotor cortex

10.33588/rn.4803.2008571

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Citations (18)

Range of modulation of light sensitivity by accessory pigments in the crayfish compound eye

Vision Research (1982)

Leonardo Rodrı́guez-Sosa Hugo Aréchigá

Darkness

Light sensitivity

Modulation (music)

10.1016/0042-6989(82)90218-8

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Citations (20)

Review of: "Behavioral effects of ethanol in the Red Swamp Crayfish (Procambarus clarkii)"

Leonardo Rodrı́guez-Sosa

Procambarus clarkii

Swamp

10.32388/b1x6rk

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Transcriptional identification of genes light-interacting in the extraretinal photoreceptors of the crayfish Procambarus clarkii

ZooKeys (2021)

Gabina Calderón‐Rosete Juan Antonio González-Barrios Celia Piña-Leyva Hayde Nallely Moreno-Sandoval Manuel Lara-Lozano

Visual phototransduction

Procambarus clarkii

Eyestalk

Phototaxis

Opsin

10.3897/zookeys.1072.73075

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Citations (1)

Serotonin modulation of caudal photoreceptor in crayfish

Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology (2005)

Leonardo Rodrı́guez-Sosa Gabina Calderón‐Rosete Mercedes Graciela Porras Villalobos Elena Mendoza Zamora Víctor Anaya González

Modulation (music)

10.1016/j.cbpc.2005.10.006

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Citations (13)

Hypothalamic A11 Nuclei Regulate the Circadian Rhythm of Spinal Mechanonociception through Dopamine Receptors and Clock Gene Expression

Life (2022)

Celia Piña-Leyva Manuel Lara-Lozano Marina Rodríguez-Sánchez Guadalupe C. Vidal‐Cantú Ericka Barrientos Zavalza

Several types of sensory perception have circadian rhythms. The spinal cord can be considered a center for controlling circadian rhythms by changing clock gene expression. However, to date, it is not known if mechanonociception itself has a circadian rhythm. The hypothalamic A11 area represents the primary source of dopamine (DA) in the spinal cord and has been found to be involved in clock gene expression and circadian rhythmicity. Here, we investigate if the paw withdrawal threshold (PWT) has a circadian rhythm, as well as the role of the dopaminergic A11 nucleus, DA, and DA receptors (DR) in the PWT circadian rhythm and if they modify clock gene expression in the lumbar spinal cord. Naïve rats showed a circadian rhythm of the PWT of almost 24 h, beginning during the night-day interphase and peaking at 14.63 h. Similarly, DA and DOPAC's spinal contents increased at dusk and reached their maximum contents at noon. The injection of 6-hydroxydopamine (6-OHDA) into the A11 nucleus completely abolished the circadian rhythm of the PWT, reduced DA tissue content in the lumbar spinal cord, and induced tactile allodynia. Likewise, the repeated intrathecal administration of D1-like and D2-like DA receptor antagonists blunted the circadian rhythm of PWT. 6-OHDA reduced the expression of Clock and Per1 and increased Per2 gene expression during the day. In contrast, 6-OHDA diminished Clock, Bmal, Per1, Per2, Per3, Cry1, and Cry2 at night. The repeated intrathecal administration of the D1-like antagonist (SCH-23390) reduced clock genes throughout the day (Clock and Per2) and throughout the night (Clock, Per2 and Cry1), whereas it increased Bmal and Per1 throughout the day. In contrast, the intrathecal injection of the D2 receptor antagonists (L-741,626) increased the clock genes Bmal, Per2, and Per3 and decreased Per1 throughout the day. This study provides evidence that the circadian rhythm of the PWT results from the descending dopaminergic modulation of spinal clock genes induced by the differential activation of spinal DR.

PER2

PER1

10.3390/life12091411

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Localization and Release of 5-Hydroxytryptamine in the Crayfish Eyestalk

Journal of Experimental Biology (1997)

Leonardo Rodrı́guez-Sosa Arturo Picones Gabina Calderón Rosete Socorro Islas Hugo Aréchigá

The content and regional distribution of 5-hydroxytryptamine (5-HT) in the crayfish eyestalk was determined by high-performance liquid chromatography. Levels of the 5-HT precursors l-tryptophan (L-TRP) and 5-hydroxytryptophan (5-OH-TRP), and of three metabolites, 5-hydroxytryptophol (5-HTPH), N-acetylserotonin (NA-5-HT) and 5-hydroxy-indole-3-acetic acid (5-HIAA), were also determined. The total content of 5-HT in the eyestalk was 95.4+/-49.3 pg mg-1 wet mass (mean +/- s.d., N=55) while the specific content was 9.6+/-4.9 fmol microg-1 protein (mean +/- s.d. N=5). 5-HT was present in all four ganglia of the eyestalk. The highest proportion was found in the medulla terminalis (40.2 %) and the lowest in the retina lamina ganglionaris (9.9 %), which also had the lowest specific content. Conversely, the highest specific content of L-TRP was in the retina lamina ganglionaris. 5-HT biosynthesis and metabolism were explored in isolated eyestalks. The monoamine oxidase blocker pargyline, at concentrations between 0.8 and 10 mmol l-1, elicited a dose-dependent increase in 5-HT content. The biosynthesis of 5-HT in the crayfish eyestalk is suggested by the presence of its immediate precursor (5-OH-TRP) and by the suppression of 5-HT synthesis induced by m-hydroxybenzyl-hydrazine (m-HBH), a blocker of 5-OH-TRP decarboxylase. The presence of immunopositive cell bodies and axons was demonstrated using an anti-5-HT antiserum. 5-HT-like immunopositivity was detected in various regions of the eyestalk. Efferent immunopositive axons were also identified in the optic nerve, and these may have originated in the protocerebral lobe of the supraoesophageal ganglion. The branchings of these axons were profusely distributed in the neuropile of the medulla terminalis. A basal level release of 5-HT was detected in isolated eyestalks. The amount recovered was increased two-to threefold after blocking 5-HT uptake with fluoxetine (1 micromol l-1). Incubation of eyestalks in solutions containing a high K+ concentration (80 mmol l-1) released 5-HT. Electrical stimulation of the optic nerve released 5-HT as a function of the intensity of stimulation. Both the basal and evoked release were suppressed by lowering the Ca2+ concentration in the medium. These observations support a role for 5-HT as a neurotransmitter or neuromodulator in the crayfish eyestalk.

Eyestalk

Pargyline

Tryptophan hydroxylase

10.1242/jeb.200.23.3067

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Citations (37)

Dopaminergic modulation of the caudal photoreceptor in crayfish

Synapse (2010)

Leonardo Rodrı́guez-Sosa Gabina Calderón‐Rosete Minerva E. Calvillo Jorge Guevara Gonzalo Flores

Abstract In our study we investigated the influence of dopamine (DA) on the caudal photoreceptor (CPR) in crayfish. Here we report the following: (a) the chromatographic determination of DA in the sixth abdominal ganglion (6th AG) shows a variation in the content during a 24‐h cycle with the maximum value at dawn. (b) There are possibly dopaminergic neurons in the 6th AG with antityrosine hydroxylase antibodies. Immunopositive neurons (164) were located in the anterior and posterior regions of the 6th AG with the mean (± SE) diameter of their somata 23 ± 1 μm. In addition, there is immunopositive staining in axons, neuropilar fibers, and varicosities. (c) We also identified, using immunohistochemistry, 108 neurons in the sixth AG that contain dopamine D1‐like receptors, with the mean (±SE) diameter of their somata 18 ± 1 μm. (d) We examined the exogenous action of DA on the electrical activity of the CPR in the isolated sixth AG by conventional extracellular‐recording methods. This CPR displays spontaneous activity and phasic‐tonic responses to light pulses. Topical application of dopamine to ganglia kept in the dark increased the spontaneous firing rate of the CPR, whereas the photoresponse of the CPR remained unchanged. The effect on the spontaneous activity is dose‐dependent with an ED 50 of 33 μM, and is blocked by the dopamine D1‐like antagonist SCH23390. These observations suggested that the DA is playing the role of a neurotransmitter or a neuromodulator of the CPR in the 6th AG in both species of crayfish, Procambarus clarkii and Cherax quadricarinatus . Synapse, 2011. © 2010 Wiley‐Liss, Inc.

Procambarus clarkii

Tonic (physiology)

Cherax quadricarinatus

Dopamine antagonist

Bursting

10.1002/syn.20866

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Citations (8)