Discovery and functional study of a novel crustacean tachykinin neuropeptide

ACS Chemical Neuroscience

Volumn 2, Issue 12, 2011, Pages 711-722

  Hui, Limei ^a   Zhang, Yuzhuo ^a   Wang, Junhua ^b   Cook, Aaron ^c   Ye, Hui ^b   Nusbaum, Michael P ^c   Li, Lingjun ^a,b  

^a Department of Chemistry ^*  (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Callinectes sapidus; CalsTRP; feeding; mass spectrometry; Neuropeptide; stomatogastric nervous system; tachykinin related peptide

Indexed keywords

TACHYKININ; TACHYKININ RELATED PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BLUE CRAB; ELECTROPHYSIOLOGY; FOOD INTAKE; MALE; MASS SPECTROMETRY; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UPREGULATION;

CALLINECTES; CALLINECTES SAPIDUS; CANCER BOREALIS; CRUSTACEA; DECAPODA (CRUSTACEA); INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 84555220651     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn200042p     Document Type: Article

References (67)

1. Nässel, D. R. (1999) Tachykinin-related peptides in invertebrates: a review Peptides 20, 141-158 (Pubitemid 29158806)
2. Severini, C., Improta, G., Falconieri-Erspamer, G., Salvadori, S., and Erspamer, V. (2002) The tachykinin peptide family Pharmacol. Rev. 54, 285-322 (Pubitemid 34575718)
3. Vanden Broeck, J., Torfs, H., Poels, J., Van Poyer, W., Swinnen, E., Ferket, K., and De Loof, A. (1999) Tachykinin-like peptides and their receptors-A review Ann. N.Y. Acad. Sci. 897, 374-387 (Pubitemid 30040348)
4. Johansson, K. U. I., Lundquist, C. T., Hallberg, E., and Nässel, D. R. (1999) Tachykinin-related neuropeptide in the crayfish olfactory midbrain Cell Tissue Res 296, 405-415 (Pubitemid 29219190)
5. Lundquist, C. T., Clottens, F. L., Holman, G. M., Nichols, R., Nachman, R. J., and Nässel, D. R. (1994) Callitachykinin-I and Callitachykinin-Iii, 2 Novel Myotropic Peptides Isolated from the Blowfly, Calliphora-Vomitoria, That Have Resemblances to Tachykinins Peptides 15, 761-768 (Pubitemid 24248393)
6. Lundquist, C. T., Clottens, F. L., Holman, G. M., Riehm, J. P., Bonkale, W., and Nässel, D. R. (1994) Locustatachykinin immunoreactivity in the blowfly central nervous system and intestine J. Comp. Neurol. 341, 225-240 (Pubitemid 24058721)
7. Muren, J. E. and Nässel, D. R. (1996) Isolation of five tachykinin-related peptides from the midgut of the cockroach Leucophaea maderae: Existence of N-terminally extended isoforms Regul. Pept. 65, 185-196 (Pubitemid 26325605)
8. Muren, J. E. and Nässel, D. R. (1997) Seven tachykinin-related peptides isolated from the brain of the madeira cockroach: Evidence for tissue-specific expression of isoforms Peptides 18, 7-15 (Pubitemid 27192017)
9. Meola, S. M., Clottens, F. L., Holman, G. M., Nachman, R. J., Nichols, R., Schoofs, L., Wright, M. S., Olson, J. K., Hayes, T. K., and Pendleton, M. W. (1998) Isolation and immunocytochemical characterization of three tachykinin-related peptides from the mosquito, Culex salinarius Neurochem. Res. 23, 189-202 (Pubitemid 28130624)
10. Christie, A. E., Lundquist, C. T., Nässel, D. R., and Nusbaum, M. P. (1997) Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis J. Exp. Biol. 200, 2279-2294 (Pubitemid 27422665)
11. Blitz, D. M., Christie, A. E., Marder, E., and Nusbaum, M. P. (1995) Distribution and effects of tachykinin-like peptides in the stomatogastric nervous system of the crab, Cancer borealis J. Comp. Neurol. 354, 282-294
12. Evans, P. D. (1994) The effects of myomodulin and structurally related neuropeptides on skeletal neuromuscular-transmission in the locust J. Exp. Biol. 190, 253-264 (Pubitemid 2076419)
13. Nässel, D. R., Eckert, M., Muren, J. E., and Penzlin, H. (1998) Species-specific action and distribution of tachykinin-related peptides in the foregut of the cockroaches Leucophaea maderae and Periplaneta americana J. Exp. Biol. 201, 1615-1626 (Pubitemid 28320154)
14. Bartho, L. and Holzer, P. (1985) Search for a physiological-role of substance-P in gastrointestinal motility Neuroscience 16, 1-32 (Pubitemid 16233310)
15. Pernow, B. (1983) Substance-P Pharmacol. Rev. 35, 85-141
16. Kulkarni, S. K. and Dhir, A. (2009) Current investigational drugs for major depression Expert Opin. Invest. Drugs 18, 767-788
17. Poulsen, A., Liljefors, T., Gundertofte, K., and Bjornholm, B. (2002) A pharmacophore model for NK2 antagonist comprising compounds from several structurally diverse classes J. Comput-Aided. Mol. Des. 16, 273-286 (Pubitemid 35174568)
18. Satake, H., Kawada, T., Nomoto, K., and Minakata, H. (2003) Insight into tachykinin-related peptides, their receptors, and invertebrate tachykinins: A review Zool. Sci. 20, 533-549 (Pubitemid 36844319)
19. Otsuka, M. and Yoshioka, K. (1993) Neurotransmitter functions of mammalian tachykinins Physiol. Rev. 73, 229-308 (Pubitemid 23119035)
20. Chen, R. B., Hui, L. M., Cape, S. S., Wang, J. H., and Li, L. J. (2010) Comparative neuropeptidomic analysis of food intake via a multifaceted mass spectrometric approach ACS Chem. Neurosci. 1, 204-214
21. Chen, R. B., Ma, M. M., Hui, L. M., Zhang, J., and Li, L. J. (2009) Measurement of neuropeptides in crustacean hemolymph via MALDI mass spectrometry J. Am. Soc. Mass Spectrom. 20, 708-718
22. Dickinson, P. S., Stemmler, E. A., and Christie, A. E. (2008) The pyloric neural circuit of the herbivorous crab Pugettia producta shows limited sensitivity to several neuromodulators that elicit robust effects in more opportunistically feeding decapods J. Exp. Biol. 211, 1434-1447 (Pubitemid 351954826)
23. Wood, D. E., Stein, W., and Nusbaum, M. P. (2000) Projection neurons with shared cotransmitters elicit different motor patterns from the same neural circuit J. Neurosci. 20, 8943-8953
24. Stein, W., DeLong, N. D., Wood, D. E., and Nusbaum, M. P. (2007) Divergent co-transmitter actions underlie motor pattern activation by a modulatory projection neuron Eur. J. Neurosci. 26, 1148-1165 (Pubitemid 47346762)
25. Nusbaum, M. P. and Beenhakker, M. P. (2002) A small-systems approach to motor pattern generation Nature 417, 343-350 (Pubitemid 34534722)
26. Nusbaum, M. P. (2002) Regulating peptidergic modulation of rhythmically active neural circuits Brain Behav. Evol. 60, 378-387 (Pubitemid 36160303)
27. Marder, E. and Bucher, D. (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs Annu. Rev. Physiol. 69, 291-316 (Pubitemid 46457645)
28. Stein, W. (2009) Modulation of stomatogastric rhythms J. Comp. Physiol., A 195, 989-1009
29. Sousa, G. L., Lenz, P. H., Hartline, D. K., and Christie, A. E. (2008) Distribution of pigment dispersing hormone- and tachykinin-related peptides in the central nervous system of the copepod crustacean Calanus finmarchicus Gen. Comp. Endrocrinol. 156, 454-459
30. Blitz, D. M., White, R. S., Saideman, S. R., Cook, A., Christie, A. E., Nadim, F., and Nusbaum, M. P. (2008) A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons J. Exp. Biol. 211, 1000-1011 (Pubitemid 351580068)
31. Blitz, D. M., Christie, A. E., Coleman, M. J., Norris, B. J., Marder, E., and Nusbaum, M. P. (1999) Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network J. Neurosci. 19, 5449-5463 (Pubitemid 29300210)
32. Kirby, M. S. and Nusbaum, M. P. (2007) Central nervous system projections to and from the commissural ganglion of the crab Cancer borealis Cell Tissue Res. 328, 625-637 (Pubitemid 46684512)
33. Messinger, D. I., Kutz, K. K., Le, T., Verley, D. R., Hsu, Y. W. A., Ngo, C. T., Cain, S. D., Birmingham, J. T., Li, L. J., and Christie, A. E. (2005) Identification and characterization of a tachykinin-containing neuroendocrine organ in the commissural ganglion of the crab Cancer productus J. Exp. Biol. 208, 3303-3319 (Pubitemid 41399778)
34. Stemmler, E. A., Cashman, C. R., Messinger, D. I., Gardner, N. P., Dickinson, P. S., and Christie, A. E. (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 (Pubitemid 47600414)
35. Ma, M. M., Bors, E. K., Dickinson, E. S., Kwiatkowski, M. A., Sousa, G. L., Henry, R. P., Smith, C. M., Towle, D. W., Christie, A. E., and Li, L. J. (2009) Characterization of the Carcinus maenas neuropeptidome by mass spectrometry and functional genomics Gen. Comp. Endrocrinol. 161, 320-334
36. Ma, M. M., Wang, J. H., Chen, R. B., and Li, L. J. (2009) Expanding the crustacean neuropeptidome using a multifaceted mass spectrometric approach J. Proteome Res. 8, 2426-2437
37. Stemmler, E. A., Peguero, B., Bruns, E. A., Dickinson, P. S., and Christie, A. E. (2007) Identification, physiological actions, and distribution of TPSGFLGMRamide: a novel tachykinin-related peptide from the midgut and stomatogastric nervous system of Cancer crabs J. Neurochem. 101, 1351-1366 (Pubitemid 46718825)
38. Christie, A. E., Cashman, C. R., Stevens, J. S., Smith, C. M., Beale, K. M., Stemmler, E. A., Greenwood, S. J., Towle, D. W., and Dickinson, P. S. (2008) Identification and cardiotropic actions of brain/gut-derived tachykinin-related peptides (TRPs) from the American lobster Homarus americanus Peptides 29, 1909-1918
39. Ma, M. M., Gard, A. L., Xiang, F., Wang, J. H., Davoodian, N., Lenz, P. H., Malecha, S. R., Christie, A. E., and Li, L. J. (2010) Combining in silico transcriptome mining and biological mass spectrometry for neuropeptide discovery in the Pacific white shrimp Litopenaeus vannamei Peptides 31, 27-43
40. Christie, A. E., Stemmler, E. A., and Dickinson, P. S. (2010) Crustacean neuropeptides Cell. Mol. Life Sci. 67, 4135-4169
41. Yasuda-Kamatani, Y. and Yasuda, A. (2004) APSGFLGMRamide is a unique tachykinin-related peptide in crustaceans Eur. J. Biochem. 271, 1546-1556 (Pubitemid 38553560)
42. Wang, J. H., Ma, M., Chen, R., and Li, L. (2008) Enhanced neuropeptide profiling via capillary electrophoresis off-line coupled with MALDI FTMS Anal. Chem. 80, 6168-6177
43. Wang, J. H., Zhang, Y. Z., Xiang, F., Zhang, Z. C., and Li, L. J. (2010) Combining capillary electrophoresis matrix-assisted laser desorption/ionization mass spectrometry and stable isotopic labeling techniques for comparative crustacean peptidomics J. Chromatogr., A 1217, 4463-4470
44. Hsu, J. L., Huang, S. Y., Chow, N. H., and Chen, S. H. (2003) Stable-isotope dimethyl labeling for quantitative proteomics Anal. Chem. 75, 6843-6852
45. DeKeyser, S. S. and Li, L. J. (2006) Matrix-assisted laser desorption/ionization Fourier transform mass spectrometry quantitation via in cell combination Analyst 131, 281-290
46. Ji, C. J. and Li, L. (2005) Quantitative proteome analysis using differential stable isotopic labeling and microbore LC-MALDI MS and MS/MS J. Proteome Res. 4, 734-742 (Pubitemid 40863262)
47. Tachibana, T., Khan, M. S. I., Matsuda, K., Ueda, H., and Cline, M. A. (2010) Central administration of substance P inhibits feeding behavior in chicks Horm. Behav. 57, 203-208
48. Audsley, N. and Weaver, R. J. (2009) Neuropeptides associated with the regulation of feeding in insects Gen. Comp. Endocr. 162, 93-104
49. Chen, R. B., Hui, L. M., Sturm, R. M., and Li, L. J. (2009) Three dimensional mapping of neuropeptides and lipids in crustacean brain by mass spectral imaging J. Am. Soc. Mass Spectrom. 20, 1068-1077
50. DeKeyser, S. S., Kutz-Naber, K. K., Schmidt, J. J., Barrett-Wilt, G. A., and Li, L. J. (2007) Imaging mass spectrometry of neuropeptides in decapod crustacean neuronal tissues J. Proteome Res. 6, 1782-1791 (Pubitemid 46814502)
51. Poels, J., Birse, R. T., Nachman, R. J., Fichna, J., Janecka, A., Broeck, J. V., and Nassel, D. R. (2009) Characterization and distribution of NKD, a receptor for Drosophila tachykinin-related peptide 6 Peptides 30, 545-556
52. Poels, J., Nachman, R. J., Akerman, K. E., Oonk, H. B., Guerrero, F., De Loof, A., Janecka, A. E., Torfs, H., and Vanden Broeck, J. (2005) Pharmacology of stomoxytachykinin receptor depends on second messenger system Peptides 26, 109-114 (Pubitemid 40038883)
53. Poels, J., Verlinden, H., Fichna, J., Van Loy, T., Franssens, V., Studzian, K., Janecka, A., Nachman, R. J., and Broeck, J. V. (2007) Functional comparison of two evolutionary conserved insect neurokinin-like receptors Peptides 28, 103-108 (Pubitemid 44959198)
54. Turner, A. J., Isaac, R. E., and Coates, D. (2001) The neprilysin (NEP) family of zinc metalloendopeptidases: genomics and function Bioessays 23, 261-269 (Pubitemid 32192145)
55. Isaac, R. E., Bland, N. D., and Shirras, A. D. (2009) Neuropeptidases and the metabolic inactivation of insect neuropeptides Gen. Comp. Endrocrinol. 162, 8-17
56. Coleman, M. J., Konstant, P. H., Rothman, B. S., and Nusbaum, M. P. (1994) Neuropeptide degradation produces functional inactivation in the crustacean nervous system J. Neurosci. 14, 6205-6216 (Pubitemid 24307811)
57. Wood, D. E. and Nusbaum, M. P. (2002) Extracellular peptidase activity tunes motor pattern modulation J. Neurosci. 22, 4185-4195 (Pubitemid 37465725)
58. Isaac, R. E., Parkin, E. T., Keen, J. N., Nässel, D. R., Siviter, R. J., and Shirras, A. D. (2002) Inactivation of a tachykinin-related peptide: identification of four neuropeptide-degrading enzymes in neuronal membranes of insects from four different orders Peptides 23, 725-733 (Pubitemid 34233817)
59. Goldberg, D., Nusbaum, M. P., and Marder, E. (1988) Substance-P-like immunoreactivity in the stomatogastric nervous systems of the crab Cancer borealis and the lobsters Panulirus interruptus and Homarus americanus Cell Tissue Res. 252, 515-522
60. Monnier, D., Colas, J. F., Rosay, P., Hen, R., Borrelli, E., and Maroteaux, L. (1992) Nkd, a developmentally regulated tachykinin receptor in Drosophila J. Biol. Chem. 267, 1298-1302
61. Li, X. J., Wolfgang, W., Wu, Y. N., North, R. A., and Forte, M. (1991) Cloning, heterologous expression and developmental regulation of a Drosophila receptor for tachykinin-like peptides EMBO J. 10, 3221-3229 (Pubitemid 21905346)
62. Kalra, S. P., Dube, M. G., and Kalra, P. S. (1991) Neuropeptide-K (Npk) suppresses copulatory behavior in male rats Physiol. Behav. 49, 1297-1300
63. Kalra, S. P., Sahu, A., Dube, M. G., and Kalra, P. S. (1991) Effects of various tachykinins on pituitary LH-Secretion, feeding, and sexual-behavior in the rat Ann. N.Y. Acad. Sci. 632, 332-338
64. Christie, A. E., Kutz-Naber, K. K., Stemmler, E. A., Klein, A., Messinger, D. I., Goiney, C. C., Conterato, A. J., Bruns, E. A., Hsu, Y. W. A., and Dickinson, P. S. (2007) Midgut epithelial endocrine cells are a rich source of the neuropeptides APSGFLGMRamide (Cancer borealis tachykinin-related peptide Ia) and GYRKPPFNGSIFamide (Gly(1)-SIFamide) in the crabs Cancer borealis, Cancer magister and Cancer productus J. Exp. Biol. 210, 699-714 (Pubitemid 46450816)
65. Thirumalai, V. and Marder, E. (2002) Colocalized neuropeptides activate a central pattern generator by acting on different circuit targets J. Neurosci. 22, 1874-1882 (Pubitemid 35386306)
66. Kutz, K. K., Schmidt, J. J., and Li, L. J. (2004) In situ tissue analysis of neuropeptides by MALDI FTMS in-cell accumulation Anal. Chem. 76, 5630-5640 (Pubitemid 39313308)
67. Weimann, J. M., Meyrand, P., and Marder, E. (1991) Neurons that form multiple pattern generators-identification and multiple activity patterns of gastric pyloric neurons in the crab stomatogastric system J. Neurophysiol. 65, 111-122