Advertisement

Identification of putative amine biosynthetic enzymes in the nervous system of the crab, Cancer borealis

  • Andrew E. ChristieEmail author
Short Communication

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.

Keywords

Dopamine Histamine Octopamine Serotonin In silico transcriptome mining 

Notes

Acknowledgements

Lisa Baldwin is thanked for reading and editing earlier version of this article. The Cades Foundation (Honolulu, Hawaii) provided funding for this study.

Compliance with ethical standards

Conflict of interest

None.

Supplementary material

10158_2019_226_MOESM1_ESM.doc (36 kb)
Supplementary material 1 (DOC 36 kb)

References

  1. 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 287:2185–2195CrossRefGoogle Scholar
  2. Blitz DM, Nusbaum MP (2011) Neural circuit flexibility in a small sensorimotor system. Curr Opin Neurobiol 21:544–552CrossRefGoogle Scholar
  3. Christie AE (2011) Crustacean neuroendocrine systems and their signaling agents. Cell Tissue Res 345:41–67CrossRefGoogle Scholar
  4. Christie AE, Pascual MG (2016) Peptidergic signaling in the crab Cancer borealis: tapping the power of transcriptomics for neuropeptidome expansion. Gen Comp Endocrinol 237:53–67CrossRefGoogle Scholar
  5. Christie AE, Stemmler EA, Dickinson PS (2010) Crustacean neuropeptides. Cell Mol Life Sci 67:4135–4169CrossRefGoogle Scholar
  6. 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 18:12CrossRefGoogle Scholar
  7. Coleman CM, Neckameyer WS (2004) Substrate regulation of serotonin and dopamine synthesis in Drosophila. Invertebr Neurosci 5:85–96CrossRefGoogle Scholar
  8. Coleman CM, Neckameyer WS (2005) Serotonin synthesis by two distinct enzymes in Drosophila melanogaster. Arch Insect Biochem Physiol 59:12–31CrossRefGoogle Scholar
  9. Cooke IM (2002) Reliable, responsive pacemaking and pattern generation with minimal cell numbers: the crustacean cardiac ganglion. Biol Bull 202:108–136CrossRefGoogle Scholar
  10. Dickinson PS, Qu X, Stanhope ME (2016) Neuropeptide modulation of pattern-generating systems in crustaceans: comparative studies and approaches. Curr Opin Neurobiol 41:149–157CrossRefGoogle Scholar
  11. 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 30:262–282Google Scholar
  12. 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–D432CrossRefGoogle Scholar
  13. Fénelon V, Le Feuvre Y, Bem T, Meyrand P (2003) Maturation of rhythmic neural network: role of central modulatory inputs. J Physiol Paris 97:59–68CrossRefGoogle Scholar
  14. Harris-Warrick RM, Marder E, Selverston AI, Moulins M (1992) Dynamic biological networks: the stomatogastric nervous system. MIT Press, CambridgeGoogle Scholar
  15. Hooper SL, DiCaprio RA (2004) Crustacean motor pattern generator networks. Neurosignals 13:50–69CrossRefGoogle Scholar
  16. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefGoogle Scholar
  17. Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291–316CrossRefGoogle Scholar
  18. Marder E, Christie AE, Kilman VL (1995) Functional organization of cotransmission systems: lessons from small nervous systems. Invertebr Neurosci 1:105–112CrossRefGoogle Scholar
  19. Monastirioti M (1999) Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc Res Tech 45:106–121CrossRefGoogle Scholar
  20. 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 17:868CrossRefGoogle Scholar
  21. Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E (2001) The roles of co-transmission in neural network modulation. Trends Neurosci 24:146–154CrossRefGoogle Scholar
  22. Selverston AI (2005) A neural infrastructure for rhythmic motor patterns. Cell Mol Neurobiol 25:223–244CrossRefGoogle Scholar
  23. Selverston AI, Ayers J (2006) Oscillations and oscillatory behavior in small neural circuits. Biol Cybern 95:537–554CrossRefGoogle Scholar
  24. Selverston AI, Moulins M (1987) The crustacean stomatogastric system. Springer, BerlinCrossRefGoogle Scholar
  25. 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 860:35–50CrossRefGoogle Scholar
  26. Skiebe P (2001) Neuropeptides are ubiquitous chemical mediators: using the stomatogastric nervous system as a model system. J Exp Biol 204:2035–2048PubMedGoogle Scholar
  27. Stein W (2009) Modulation of stomatogastric rhythms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:989–1009CrossRefGoogle Scholar
  28. Stuart AE (1999) From fruit flies to barnacles, histamine is the neurotransmitter of arthropod photoreceptors. Neuron 22:431–433CrossRefGoogle Scholar
  29. 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–D765CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, School of Ocean and Earth Science and TechnologyUniversity of Hawaii at ManoaHonoluluUSA

Personalised recommendations