Abstract
In decapod crustaceans, the amines dopamine, octopamine, serotonin, and histamine are known to serve as locally released and/or circulating neuromodulators. While many studies have focused on determining the modulatory actions of amines on decapod nervous systems, comparatively little is known about the identity of the receptors through which they exert their actions. Here, a crayfish, Procambarus clarkii, tissue-specific transcriptome was used to identify putative amine receptors in the eyestalk, a structure composed largely of the eyestalk ganglia, including the neuroendocrine X-organ-sinus gland system, and retina. Transcripts encoding 17 distinct putative amine receptors, three dopamine (one dopamine 1-like, one dopamine 2-like, and one dopamine/ecdysteroid-like), five octopamine (one alpha-like, three beta-like, and one octopamine/tyramine-like), three serotonin (two type-1-like and one type-7-like), and six histamine (five histamine-gated chloride channel A-like and one histamine-gated chloride channel B-like) were identified in the assembly. Comparison of the nucleotide sequence of the transcript encoding one predicted type-1-like serotonin receptor with that cloned previously from the P. clarkii nervous system shows the two sequences to be essentially identical, providing increased support for the validity of the transcripts used to deduce the proteins reported here. Reciprocal BLAST and structural/functional domain analyses support the protein family annotations ascribed to the putative P. clarkii receptors. These data represent the first large-scale description of amine receptors from P. clarkii, and as such provide a new resource for initiating gene-based studies of aminergic control of physiology/behavior at the level of receptors in this species.
References
Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke Z, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky AA, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RD, Scheeler F, Shen H, Shue BC, Sidén-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, Worley KC, Woodage T, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang G, Zhao Q, Zheng L, Zheng XH, Zhong FN, Zhong W, Zhou X, Zhu S, Zhu X, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195
Alvarez-Alvarado R, Porras Villalobos MG, Calderón-Rosete G, Rodríguez-Sosa L, Aréchiga H (2005) Dopaminergic modulation of neurosecretory cells in the crayfish. Cell Mol Neurobiol 25:345–370
Bauknecht P, Jékely G (2017) Ancient coexistence of norepinephrine, tyramine, and octopamine signaling in bilaterians. BMC Biol 15:6
Beltz BS (1999) Distribution and functional anatomy of amine-containing neurons in decapod crustaceans. Microsc Res Tech 44:105–120
Blitz DM, Nusbaum MP (2011) Neural circuit flexibility in a small sensorimotor system. Curr Opin Neurobiol 21:544–552
Cebada J, García U (2007) Histamine operates Cl-gated channels in crayfish neurosecretory cells. J Exp Biol 210:3962–3969
Christie AE (2011) Crustacean neuroendocrine systems and their signaling agents. Cell Tissue Res 345:41–67
Christie AE, Yu A (2019) Identification of peptide hormones and their cognate receptors in Jasus edwardsii—a potential resource for the development of new aquaculture management strategies for rock/spiny lobsters. Aquaculture 503:636–662
Christie AE, Stemmler EA, Dickinson PS (2010) Crustacean neuropeptides. Cell Mol Life Sci 67:4135–4169
Christie AE, Roncalli V, Wu LS, Ganote CL, Doak T, Lenz PH (2013) Peptidergic signaling in Calanus finmarchicus (Crustacea, Copepoda): in silico identification of putative peptide hormones and their receptors using a de novo assembled transcriptome. Gen Comp Endocrinol 187:117–135
Christie AE, Chi M, Lameyer TJ, Pascual MG, Shea DN, Stanhope ME, Schulz DJ, Dickinson PS (2015) Neuropeptidergic signaling in the American lobster Homarus americanus: new insights from high-throughput nucleotide sequencing. PLoS ONE 10:e0145964
Christie AE, Roncalli V, Lenz PH (2016) Diversity of insulin-like peptide signaling system proteins in Calanus finmarchicus (Crustacea; Copepoda)—possible contributors to seasonal pre-adult diapause. Gen Comp Endocrinol 236:157–173
Christie AE, Pascual MG, Yu A (2018) Peptidergic signaling in the tadpole shrimp Triops newberryi: a potential model for investigating the roles played by peptide paracrines/hormones in adaptation to environmental change. Mar Genom 39:45–63
Clark MC, Baro DJ (2006) Molecular cloning and characterization of crustacean type-one dopamine receptors: D1alphaPan and D1betaPan. Comp Biochem Physiol B Biochem Mol Biol 143:294–301
Clark MC, Baro DJ (2007) Arthropod D2 receptors positively couple with cAMP through the Gi/o protein family. Comp Biochem Physiol B Biochem Mol Biol 146:9–19
Cooke IM (2002) Reliable, responsive pacemaking and pattern generation with minimal cell numbers: the crustacean cardiac ganglion. Biol Bull 202:108–136
Dickinson PS, Qu X, Stanhope ME (2016) Neuropeptide modulation of pattern-generating systems in crustaceans: comparative studies and approaches. Curr Opin Neurobiol 41:149–157
Dickinson PS, Hull JJ, Miller A, Oleisky ER, Christie AE (2019) To what extent may peptide receptor gene diversity/complement contribute to functional flexibility in a simple pattern-generating neural network? Comp Biochem Physiol Part D Genom Proteom 30:262–282
Edwards DH, Yeh SR, Musolf BE, Antonsen BL, Krasne FB (2002) Metamodulation of the crayfish escape circuit. Brain Behav Evol 60:360–369
El Manira A, Clarac F (1994) Presynaptic inhibition is mediated by histamine and GABA in the crustacean escape reaction. J Neurophysiol 71:1088–1095
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A, Sonnhammer ELL, Hirsh L, Paladin L, Piovesan D, Tosatto SCE, Finn RD (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432
Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Cattaert D, Delbecque JP (2015) Serotonin, but not dopamine, controls the stress response and anxiety-like behavior in the crayfish Procambarus clarkii. J Exp Biol 218:2745–2752
Glanzman DL, Krasne FB (1983) Serotonin and octopamine have opposite modulatory effects on the crayfish’s lateral giant escape reaction. J Neurosci 3:2263–2269
Harris-Warrick RM, Marder E, Selverston AI, Moulins M (1992) Dynamic biological networks: the stomatogastric nervous system. MIT press, Cambridge
Hooper SL, DiCaprio RA (2004) Crustacean motor pattern generator networks. Neurosignals 13:50–69
Huber R (2005) Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:231–239
Issa FA, Drummond J, Cattaert D, Edwards DH (2012) Neural circuit reconfiguration by social status. J Neurosci 32:5638–5645
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Manfrin C, Tom M, De Moro G, Gerdol M, Giulianini PG, Pallavicini A (2015) The eyestalk transcriptome of red swamp crayfish Procambarus clarkii. Gene 557:28–34
Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291–316
Marder E, Christie AE, Kilman VL (1995) Functional organization of cotransmission systems: lessons from small nervous systems. Invert Neurosci 1:105–112
McCoole MD, Atkinson NJ, Graham DI, Grasser EB, Joselow AL, McCall NM, Welker AM, Wilsterman EJ Jr, Baer KN, Tilden AR, Christie AE (2012a) Genomic analyses of aminergic signaling systems (dopamine, octopamine and serotonin) in Daphnia pulex. Comp Biochem Physiol Part D Genom Proteom 7:35–58
McCoole MD, D’Andrea BT, Baer KN, Christie AE (2012b) Genomic analyses of gas (nitric oxide and carbon monoxide) and small molecule transmitter (acetylcholine, glutamate and GABA) signaling systems in Daphnia pulex. Comp Biochem Physiol Part D Genom Proteom 7:124–160
Momohara Y, Kanai A, Nagayama T (2013) Aminergic control of social status in crayfish agonistic encounters. PLoS ONE 8:e74489
Mulloney B, Hall WM (1991) Neurons with histaminelike immunoreactivity in the segmental and stomatogastric nervous systems of the crayfish Pacifastacus leniusculus and the lobster Homarus americanus. Cell Tissue Res 266:197–207
Mulloney B, Acevedo LD, Bradbury AG (1987) Modulation of the crayfish swimmeret rhythm by octopamine and the neuropeptide proctolin. J Neurophysiol 58:584–597
Northcutt AJ, Lett KM, Garcia VB, Diester CM, Lane BJ, Marder E, Schulz DJ (2016) Deep sequencing of transcriptomes from the nervous systems of two decapod crustaceans to characterize genes important for neural circuit function and modulation. BMC Genom 17:868
Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E (2001) The roles of co-transmission in neural network modulation. Trends Neurosci 24:146–154
Ongvarrasopone C, Roshorm Y, Somyong S, Pothiratana C, Petchdee S, Tangkhabuanbutra J, Sophasan S, Panyim S (2006) Molecular cloning and functional expression of the Penaeus monodon 5-HT receptor. Biochim Biophys Acta 1759:328–339
Reyes-Colón D, Vázquez-Acevedo N, Rivera NM, Jezzini SH, Rosenthal J, Ruiz-Rodríguez EA, Baro DJ, Kohn AB, Moroz LL, Sosa MA (2010) Cloning and distribution of a putative octopamine/tyramine receptor in the central nervous system of the freshwater prawn Macrobrachium rosenbergii. Brain Res 1348:42–54
Rieger V, Harzsch S (2008) Embryonic development of the histaminergic system in the ventral nerve cord of the Marbled Crayfish (Marmorkrebs). Tissue Cell 40:113–126
Rodríguez-Sosa L, Calderón-Rosete G, Porras Villalobos MG, Mendoza Zamora E, Anaya González V (2006) Serotonin modulation of caudal photoreceptor in crayfish. Comp Biochem Physiol C Toxicol Pharmacol 142:220–230
Rodríguez-Sosa L, Calderón-Rosete G, Calvillo ME, Guevara J, Flores G (2011) Dopaminergic modulation of the caudal photoreceptor in crayfish. Synapse 65:497–504
Rodríguez-Sosa L, Calderón-Rosete G, Ortega-Cambranis A, De-Miguel FF (2017) Octopamine cyclic release and its modulation of visual sensitivity in crayfish. Comp Biochem Physiol A Mol Integr Physiol 203:83–90
Sandeman RE, Sandeman DC (1987) Serotonin-like immunoreactivity of giant olfactory interneurons in the crayfish brain. Brain Res 403:371–374
Sandeman DC, Benton JL, Beltz BS (2009) An identified serotonergic neuron regulates adult neurogenesis in the crustacean brain. Dev Neurobiol 69:530–545
Selverston AI (2005) A neural infrastructure for rhythmic motor patterns. Cell Mol Neurobiol 25:223–244
Selverston AI, Ayers J (2006) Oscillations and oscillatory behavior in small neural circuits. Biol Cybern 95:537–554
Selverston AI, Moulins M (1987) The crustacean stomatogastric system. Springer, Berlin
Selverston A, Elson R, Rabinovich M, Huerta R, Abarbanel H (1998) Basic principles for generating motor output in the stomatogastric ganglion. Ann NY Acad Sci 860:35–50
Skiebe P (2001) Neuropeptides are ubiquitous chemical mediators: using the stomatogastric nervous system as a model system. J Exp Biol 204:2035–2048
Sosa MA, Spitzer N, Edwards DH, Baro DJ (2004) A crustacean serotonin receptor: cloning and distribution in the thoracic ganglia of crayfish and freshwater prawn. J Comp Neurol 473:526–537
Spitzer N, Edwards DH, Baro DJ (2008) Conservation of structure, signaling and pharmacology between two serotonin receptor subtypes from decapod crustaceans, Panulirus interruptus and Procambarus clarkii. J Exp Biol 211:92–105
Stein W (2009) Modulation of stomatogastric rhythms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:989–1009
Sukthaworn S, Panyim S, Udomkit A (2013) Molecular and functional characterization of a dopamine receptor type1 from Penaeus monodon. Aquaculture 380–383:99–105
Sullivan JM, Genco MC, Marlow ED, Benton JL, Beltz BS, Sandeman DC (2009) Brain photoreceptor pathways contributing to circadian rhythmicity in crayfish. Chronobiol Int 26:1136–1168
Thurmond J, Goodman JL, Strelets VB, Attrill H, Gramates LS, Marygold SJ, Matthews BB, Millburn M, Antonazzo G, Trovisco V, Kaufman TC, Calvi BR, the FlyBase Consortium (2019) FlyBase 2.0: the next generation. Nucleic Acids Res 47:D759–D765
Tierney AJ, Godleski MS, Rattananont P (1999) Serotonin-like immunoreactivity in the stomatogastric nervous systems of crayfishes from four genera. Cell Tissue Res 295:537–551
Tierney AJ, Kim T, Abrams R (2003) Dopamine in crayfish and other crustaceans: distribution in the central nervous system and physiological functions. Microsc Res Tech 60:325–335
Tierney AJ, Greenlaw MA, Dams-O’Connor K, Aig SD, Perna AM (2004) Behavioral effects of serotonin and serotonin agonists in two crayfish species, Procambarus clarkii and Orconectes rusticus. Comp Biochem Physiol A Mol Integr Physiol 139:495–502
Tiu SH, He JG, Chan SM (2005) Organization and expression study of the shrimp (Metapenaeus ensis) putative 5-HT receptor: up-regulation in the brain by 5-HT. Gene 353:41–52
Yang X, Huang G, Xu M, Zhang C, Cheng Y (2018) Molecular cloning and functional expression of the 5-HT7 receptor in Chinese mitten crab (Eriocheir sinensis). Comp Biochem Physiol B Biochem Mol Biol 226:10–17
Zhang Y, Benton JL, Beltz BS (2011) HT receptors mediate lineage-dependent effects of serotonin on adult neurogenesis in Procambarus clarkii. Neural Dev 6:2
Acknowledgements
Lisa Baldwin is thanked for reading and editing an earlier version of this article. The Cades Foundation (Honolulu, Hawaii) provided funding for this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Christie, A.E. Identification of putative amine receptor complement in the eyestalk of the crayfish, Procambarus clarkii. Invert Neurosci 19, 12 (2019). https://doi.org/10.1007/s10158-019-0232-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10158-019-0232-z