Abstract
Amines function as neuromodulators throughout the animal kingdom. In decapod crustaceans, the amines serving neuromodulatory roles include dopamine, octopamine, serotonin and histamine. While much work has focused on examining the physiological effects of amines on decapod nervous systems, the identity of the native enzymes involved in their biosynthesis remains largely unknown. In an attempt to help fill this void, a transcriptome generated from multiple portions of the crab, Cancer borealis, nervous system, a species that has long served as a model species for investigating the neuromodulatory control of rhythmically active neural networks, was used to identify putative amine biosynthetic enzyme-encoding transcripts, and by proxy, proteins. Transcripts encoding full complements of the enzymes involved in the production of dopamine, octopamine, serotonin, and histamine were deduced from the C. borealis assembly, i.e., tryptophan–phenylalanine hydroxylase, tyrosine hydroxylase, DOPA decarboxylase, tyrosine decarboxylase, tyramine β-hydroxylase, tryptophan hydroxylase, and histidine decarboxylase. All proteins deduced from the C. borealis transcripts appear to be full-length sequences, with reciprocal BLAST and structural domain analyses supporting the protein family annotations ascribed to them. These data provide the first descriptions of the native amine biosynthetic enzymes of C. borealis, and as such, serve as a resource for initiating gene-based studies of aminergic control of physiology and behavior at the level of biosynthesis in this important biomedical model.
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, WoodageT WK, 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
Blitz DM, Nusbaum MP (2011) Neural circuit flexibility in a small sensorimotor system. Curr Opin Neurobiol 21:544–552
Christie AE (2011) Crustacean neuroendocrine systems and their signaling agents. Cell Tissue Res 345:41–67
Christie AE, Pascual MG (2016) Peptidergic signaling in the crab Cancer borealis: tapping the power of transcriptomics for neuropeptidome expansion. Gen Comp Endocrinol 237:53–67
Christie AE, Stemmler EA, Dickinson PS (2010) Crustacean neuropeptides. Cell Mol Life Sci 67:4135–4169
Christie AE, Stanhope ME, Gandler HI, Lameyer TJ, Pascual MG, Shea DN, Yu A, Dickinson PS, Hull JJ (2018) Molecular characterization of putative neuropeptide, amine, diffusible gas and small molecule transmitter biosynthetic enzymes in the eyestalk ganglia of the American lobster, Homarus americanus. Invertebr Neurosci 18:12
Coleman CM, Neckameyer WS (2004) Substrate regulation of serotonin and dopamine synthesis in Drosophila. Invertebr Neurosci 5:85–96
Coleman CM, Neckameyer WS (2005) Serotonin synthesis by two distinct enzymes in Drosophila melanogaster. Arch Insect Biochem Physiol 59:12–31
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
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
Fénelon V, Le Feuvre Y, Bem T, Meyrand P (2003) Maturation of rhythmic neural network: role of central modulatory inputs. J Physiol Paris 97:59–68
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
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
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. Invertebr Neurosci 1:105–112
Monastirioti M (1999) Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc Res Tech 45:106–121
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
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 N Y 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
Stein W (2009) Modulation of stomatogastric rhythms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:989–1009
Stuart AE (1999) From fruit flies to barnacles, histamine is the neurotransmitter of arthropod photoreceptors. Neuron 22:431–433
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
Acknowledgements
Lisa Baldwin is thanked for reading and editing 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 biosynthetic enzymes in the nervous system of the crab, Cancer borealis. Invert Neurosci 19, 6 (2019). https://doi.org/10.1007/s10158-019-0226-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10158-019-0226-x