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Identification of putative neuropeptidergic signaling systems in the spiny lobster, Panulirus argus

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Invertebrate Neuroscience

Abstract

Members of the decapod infraorder Achelata, specifically species from the genus Panulirus, have storied histories as models for investigating the basic principles governing the generation, maintenance, and modulation of rhythmic motor behavior, including modulation by locally released and circulating peptides. Despite their contributions to our understanding of peptidergic neuromodulation, little is known about the identity of the native neuropeptides and neuronal peptide receptors present in these crustaceans. Here, a Panulirus argus nervous system-specific transcriptome was used to help fill this void, providing insight into the neuropeptidome and neuronal peptide receptome of this species. A neuropeptidome consisting of 266 distinct peptides was predicted using the P. argus assembly, 128 having structures placing them into a generally recognized arthropod peptide family: agatoxin-like peptide, allatostatin A (AST-A), allatostatin B, allatostatin C, bursicon, CCHamide, crustacean cardioactive peptide, crustacean hyperglycemic hormone/molt-inhibiting hormone, diuretic hormone 31 (DH31), ecdysis-triggering hormone (ETH), FMRFamide-like peptide (FLP), glycoprotein hormone (GPH), GSEFLamide, inotocin, leucokinin, myosuppressin, natalisin, neuroparsin, neuropeptide F, orcokinin, orcomyotropin, periviscerokinin, pigment-dispersing hormone, pyrokinin, red pigment-concentrating hormone, RYamide, short neuropeptide F (sNPF), SIFamide, sulfakinin, tachykinin-related peptide (TRP), and trissin. Twenty-five putative neuronal receptors, encompassing 15 peptide groups, were also identified from the P. argus transcriptome: AST-A, bursicon, CCHamide, DH31, diuretic hormone 44, ETH, FLP, GPH, inotocin, insulin-like peptide, myosuppressin, natalisin, periviscerokinin, sNPF, and TRP. Collectively, the reported data provide a powerful resource for expanding studies of neuropeptidergic control of physiology and behavior in members of the genus Panulirus specifically, and decapods generally.

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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

    PubMed  Google Scholar 

  • Alexander J, Oliphant A, Wilcockson DC, Webster SG (2018) Functional identification and characterization of the diuretic hormone 31 (DH31) signaling system in the green shore crab, Carcinus maenas. Front Neurosci 12:454

    PubMed  PubMed Central  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    PubMed  Google Scholar 

  • Blitz DM, Nusbaum MP (2011) Neural circuit flexibility in a small sensorimotor system. Curr Opin Neurobiol 21:544–552

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cape SS, Rehm KJ, Ma M, Marder E, Li L (2008) Mass spectral comparison of the neuropeptide complement of the stomatogastric ganglion and brain in the adult and embryonic lobster, Homarus americanus. J Neurochem 105:690–702

    PubMed  CAS  Google Scholar 

  • Chen R, Jiang X, Conaway MC, Mohtashemi I, Hui L, Viner R, Li L (2010) Mass spectral analysis of neuropeptide expression and distribution in the nervous system of the lobster Homarus americanus. J Proteome Res 9:818–832

    PubMed  PubMed Central  CAS  Google Scholar 

  • Christie AE (2011) Crustacean neuroendocrine systems and their signaling agents. Cell Tissue Res 345:41–67

    PubMed  CAS  Google Scholar 

  • Christie AE, Hull JJ (2019) What can transcriptomics reveal about the phylogenetic/structural conservation, tissue localization, and possible functions of CNMamide peptides in decapod crustaceans? Gen Comp Endocrinol 282:113217

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Christie AE, Cashman CR, Stevens JS, Smith CM, Beale KM, Stemmler EA, Greenwood SJ, Towle DW, Dickinson PS (2008) Identification and cardiotropic actions of brain/gut-derived tachykinin-related peptides (TRPs) from the American lobster Homarus americanus. Peptides 29:1909–1918

    PubMed  CAS  Google Scholar 

  • Christie AE, Stemmler EA, Dickinson PS (2010a) Crustacean neuropeptides. Cell Mol Life Sci 67:4135–4169

    PubMed  CAS  Google Scholar 

  • Christie AE, Durkin CS, Hartline N, Ohno P, Lenz PH (2010b) Bioinformatic analyses of the publicly accessible crustacean expressed sequence tags (ESTs) reveal numerous novel neuropeptide-encoding precursor proteins, including ones from members of several little studied taxa. Gen Comp Endocrinol 167:164–178

    PubMed  CAS  Google Scholar 

  • Christie AE, Stevens JS, Bowers MR, Chapline MC, Jensen DA, Schegg KM, Goldwaser J, Kwiatkowski MA, Pleasant TK Jr, Shoenfeld L, Tempest LK, Williams CR, Wiwatpanit T, Smith CM, Beale KM, Towle DW, Schooley DA, Dickinson PS (2010c) Identification of a calcitonin-like diuretic hormone that functions as an intrinsic modulator of the American lobster, Homarus americanus, cardiac neuromuscular system. J Exp Biol 213:118–127

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Christie AE, Roncalli V, Cieslak MC, Pascual MG, Yu A, Lameyer TJ, Stanhope ME, Dickinson PS (2017) Prediction of a neuropeptidome for the eyestalk ganglia of the lobster Homarus americanus using a tissue-specific de novo assembled transcriptome. Gen Comp Endocrinol 243:96–119

    PubMed  PubMed Central  CAS  Google Scholar 

  • Christie AE, Cieslak MC, Roncalli V, Lenz PH, Major KM, Poynton HC (2018a) Prediction of a peptidome for the ecotoxicological model Hyalella azteca (Crustacea; Amphipoda) using a de novo assembled transcriptome. Mar Gen 38:67–88

    Google Scholar 

  • Christie AE, Pascual MG, Yu A (2018b) 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 Genomics 39:45–63

    PubMed  Google Scholar 

  • Christie AE, Yu A, Pascual MG, Roncalli V, Cieslak MC, Warner AN, Lameyer TJ, Stanhope ME, Dickinson PS, Hull JJ (2018c) Circadian signaling in Homarus americanus: region-specific de novo assembled transcriptomes show that both the brain and eyestalk ganglia possess the molecular components of a putative clock system. Mar Genomics 40:25–44

    PubMed  PubMed Central  Google Scholar 

  • Christie AE, Rivera CD, Call CM, Dickinson PS, Stemmler EA, Hull JJ (2019) In silico transcriptome mining, molecular cloning, and mass spectrometry reveal clues to the phylogenetic and structural conservation, tissue localization, and possible functions of agatoxin-like peptides in decapod crustaceans. Gen Comp Endocrinol Submitted

  • Cooke IM (2002) Reliable, responsive pacemaking and pattern generation with minimal cell numbers: the crustacean cardiac ganglion. Biol Bull 202:108–136

    PubMed  Google Scholar 

  • de Kleijn DP, Sleutels FJ, Martens GJ, Van Herp F (1994) Cloning and expression of mRNA encoding prepro-gonad-inhibiting hormone (GIH) in the lobster Homarus americanus. FEBS Lett 353:255–258

    PubMed  Google Scholar 

  • Dickinson PS, Stevens JS, Rus S, Brennan HR, Goiney CC, Smith CM, Li L, Towle DW, Christie AE (2007) Identification and cardiotropic actions of sulfakinin peptides in the American lobster Homarus americanus. J Exp Biol 210:2278–2289

    PubMed  CAS  Google Scholar 

  • Dickinson PS, Stemmler EA, Cashman CR, Brennan HR, Dennison B, Huber KE, Peguero B, Rabacal W, Goiney CC, Smith CM, Towle DW, Christie AE (2008) SIFamide peptides in clawed lobsters and freshwater crayfish (Crustacea, Decapoda, Astacidea): a combined molecular, mass spectrometric and electrophysiological investigation. Gen Comp Endocrinol 156:347–360

    PubMed  CAS  Google Scholar 

  • Dickinson PS, Stemmler EA, Barton EE, Cashman CR, Gardner NP, Rus S, Brennan HR, McClintock TS, Christie AE (2009a) Molecular, mass spectral, and physiological analyses of orcokinins and orcokinin precursor-related peptides in the lobster Homarus americanus and the crayfish Procambarus clarkii. Peptides 30:297–317

    PubMed  CAS  Google Scholar 

  • Dickinson PS, Wiwatpanit T, Gabranski ER, Ackerman RJ, Stevens JS, Cashman CR, Stemmler EA, Christie AE (2009b) Identification of SYWKQCAFNAVSCFamide: a broadly conserved crustacean C-type allatostatin-like peptide with both neuromodulatory and cardioactive properties. J Exp Biol 212:1140–1152

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dickinson PS, Dickinson ES, Oleisky ER, Rivera CD, Stanhope ME, Stemmler EA, Hull JJ, Christie AE (2019a) AMGSEFLamide, a member of a broadly conserved peptide family, modulates multiple neural networks in Homarus americanus. J Exp Biol 222:jeb194092

    PubMed  PubMed Central  Google Scholar 

  • Dickinson PS, Hull JJ, Miller A, Oleisky ER, Christie AE (2019b) 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 Gen Proteomics 30:262–282

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ferrè F, Clote P (2005) DiANNA: a web server for disulfide connectivity prediction. Nucleic Acids Res 33:W230–W232

    PubMed  PubMed Central  Google Scholar 

  • Fu Q, Kutz KK, Schmidt JJ, Hsu YW, Messinger DI, Cain SD, de la Iglesia HO, Christie AE, Li L (2005) Hormone complement of the Cancer productus sinus gland and pericardial organ: an anatomical and mass spectrometric investigation. J Comp Neurol 493:607–626

    PubMed  CAS  Google Scholar 

  • Harris-Warrick RM, Marder E, Selverston AI, Moulins M (1992) Dynamic biological networks: the stomatogastric nervous system. MIT Press, Cambridge

    Google Scholar 

  • Hooper SL, DiCaprio RA (2004) Crustacean motor pattern generator networks. Neurosignals 13:50–69

    PubMed  CAS  Google Scholar 

  • Huybrechts J, Nusbaum MP, Bosch LV, Baggerman G, De Loof A, Schoofs L (2003) Neuropeptidomic analysis of the brain and thoracic ganglion from the Jonah crab, Cancer borealis. Biochem Biophys Res Commun 308:535–544

    PubMed  CAS  Google Scholar 

  • Jia C, Lietz CB, Ye H, Hui L, Yu Q, Yoo S, Li L (2013) A multi-scale strategy for discovery of novel endogenous neuropeptides in the crustacean nervous system. J Proteomics 91:1–12

    PubMed  CAS  Google Scholar 

  • Jiang X, Chen R, Wang J, Metzler A, Tlusty M, Li L (2012) Mass spectral charting of neuropeptidomic expression in the stomatogastric ganglion at multiple developmental stages of the lobster Homarus americanus. ACS Chem Neurosci 3:439–450

    PubMed  PubMed Central  CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li L, Kelley WP, Billimoria CP, Christie AE, Pulver SR, Sweedler JV, Marder E (2003) Mass spectrometric investigation of the neuropeptide complement and release in the pericardial organs of the crab, Cancer borealis. J Neurochem 87:642–656

    PubMed  CAS  Google Scholar 

  • Ma M, Chen R, Sousa GL, Bors EK, Kwiatkowski MA, Goiney CC, Goy MF, Christie AE, Li L (2008) Mass spectral characterization of peptide transmitters/hormones in the nervous system and neuroendocrine organs of the American lobster Homarus americanus. Gen Comp Endocrinol 156:395–409

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ma M, Wang J, Chen R, Li L (2009) Expanding the crustacean neuropeptidome using a multifaceted mass spectrometric approach. J Proteome Res 8:2426–2437

    PubMed  PubMed Central  CAS  Google Scholar 

  • Marder E, Bucher D (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Ann Rev Physiol 69:291–316

    CAS  Google Scholar 

  • Marder E, Christie AE, Kilman VL (1995) Functional organization of cotransmission systems: lessons from small nervous systems. Invert Neurosci 1:105–112

    PubMed  CAS  Google Scholar 

  • Monigatti F, Gasteiger E, Bairoch A, Jung E (2002) The Sulfinator: predicting tyrosine sulfation sites in protein sequences. Bioinformatics 18:769–770

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Selverston AI (2005) A neural infrastructure for rhythmic motor patterns. Cell Mol Neurobiol 25:223–244

    PubMed  Google Scholar 

  • Selverston AI, Ayers J (2006) Oscillations and oscillatory behavior in small neural circuits. Biol Cybern 95:537–554

    PubMed  Google Scholar 

  • Selverston AI, Moulins M (1987) The crustacean stomatogastric system. Springer, Berlin

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Skiebe P (2001) Neuropeptides are ubiquitous chemical mediators: using the stomatogastric nervous system as a model system. J Exp Biol 204:2035–2048

    PubMed  CAS  Google Scholar 

  • Stafflinger E, Hansen KK, Hauser F, Schneider M, Cazzamali G, Williamson M, Grimmelikhuijzen CJ (2008) Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects. Proc Natl Acad Sci USA 105:3262–3267

    PubMed  CAS  Google Scholar 

  • Stein W (2009) Modulation of stomatogastric rhythms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195:989–1009

    PubMed  Google Scholar 

  • Stemmler EA, Provencher HL, Guiney ME, Gardner NP, Dickinson PS (2005) Matrix-assisted laser desorption/ionization fourier transform mass spectrometry for the identification of orcokinin neuropeptides in crustaceans using metastable decay and sustained off-resonance irradiation. Anal Chem 77:3594–3606

    PubMed  CAS  Google Scholar 

  • Stemmler EA, Cashman CR, Messinger DI, Gardner NP, Dickinson PS, Christie AE (2007) High-mass-resolution direct-tissue MALDI-FTMS reveals broad conservation of three neuropeptides (APSGFLGMRamide, GYRKPPFNGSIFamide and pQDLDHVFLRFamide) across members of seven decapod crustaean infraorders. Peptides 28:2104–2115

    PubMed  CAS  Google Scholar 

  • Stevens JS, Cashman CR, Smith CM, Beale KM, Towle DW, Christie AE, Dickinson PS (2009) The peptide hormone pQDLDHVFLRFamide (crustacean myosuppressin) modulates the Homarus americanus cardiac neuromuscular system at multiple sites. J Exp Biol 212:3961–3976

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tensen CP, De Kleijn DP, Van Herp F (1991) Cloning and sequence analysis of cDNA encoding two crustacean hyperglycemic hormones from the lobster Homarus americanus. Eur J Biochem 200:103–106

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Turrigiano GG, Van Wormhoudt A, Ogden L, Selverston AI (1994) Partial purification, tissue distribution and modulatory activity of a crustacean cholecystokinin-like peptide. J Exp Biol 187:181–200

    PubMed  CAS  Google Scholar 

  • Veenstra JA (2000) Mono- and dibasic proteolytic cleavage sites in insect neuroendocrine peptide precursors. Arch Insect Biochem Physiol 43:49–63

    PubMed  CAS  Google Scholar 

  • Yasuda-Kamatani Y, Yasuda A (2004) APSGFLGMRamide is a unique tachykinin-related peptide in crustaceans. Eur J Biochem 271:1546–1556

    PubMed  CAS  Google Scholar 

  • Ye H, Wang J, Zhang Z, Jia C, Schmerberg C, Catherman AD, Thomas PM, Kelleher NL, Li L (2015) Defining the neuropeptidome of the spiny lobster Panulirus interruptus brain using a multidimensional mass spectrometry-based platform. J Proteome Res 14:4776–4791

    PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

Lisa Baldwin is thanked for reading and editing an earlier version of this article. The National Science Foundation (IOS-1856307) and the Cades Foundation (Honolulu, Hawaii) provided funding for this study.

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Christie, A.E. Identification of putative neuropeptidergic signaling systems in the spiny lobster, Panulirus argus. Invert Neurosci 20, 2 (2020). https://doi.org/10.1007/s10158-020-0235-9

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