Mass spectral charting of neuropeptidomic expression in the stomatogastric ganglion at multiple developmental stages of the lobster Homarus americanus

ACS Chemical Neuroscience

Volumn 3, Issue 6, 2012, Pages 439-450

  Jiang, Xiaoyue ^a   Chen, Ruibing ^a,c   Wang, Junhua ^a   Metzler, Anita ^b   Tlusty, Michael ^b   Li, Lingjun ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Edgerton Research Laboratory   (United States)

^c TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

capillary electrophoresis (CE); development; Homarus americanus; matrix assisted laser desorption ionization time of flight time of flight mass spectrometry (MALDI TOF TOF MS); neuropeptide; stomatogastric ganglion (STG); stomatogastric nervous system (STNS)

Indexed keywords

ALLATOSTATIN; NEUROPEPTIDE; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE; PROCTOLIN; TACHYKININ;

ANIMAL TISSUE; ARTICLE; CAPILLARY ELECTROPHORESIS; GANGLION; HOMARUS AMERICANUS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NERVOUS SYSTEM; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMATOGASTRIC GANGLION; STOMATOGASTRIC NERVOUS SYSTEM;

ANIMALS; GANGLIA, INVERTEBRATE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NEPHROPIDAE; NEUROPEPTIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ANIMALIA; CRUSTACEA; HOMARUS AMERICANUS;

EID: 84862839009     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn200107v     Document Type: Article

References (54)

1. 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)
2. Maynard, D. M. (1972) Simpler networks. Ann. N.Y. Acad. Sci. 193, 59-72.
3. Marder, E. (1976) Cholinergic motor neurones in the stomatogastric system of the lobster. J. Physiol. 257, 63-86.
4. Marder, E., and Eisen, J. S. (1984) Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. J. Neurophysiol. 51, 1345-1361. (Pubitemid 14076776)
5. Katz, P. S., Eigg, M. H., and Harris-Warrick, R. M. (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells. J. Neurophysiol. 62, 558-570. (Pubitemid 19208083)
6. Nusbaum, M. P., and Beenhakker, M. P. (2002) A small-systems approach to motor pattern generation. Nature 417, 343-350. (Pubitemid 34534722)
7. Skiebe, P. (2001) Neuropeptides are ubiquitous chemical mediators: Using the stomatogastric nervous system as a model system. J. Exp. Biol. 204, 2035-2048.
8. Casasnovas, B., and Meyrand, P. (1995) Functional differentiation of adult neural circuits from a single embryonic network. J. Neurosci. 15, 5703-5718.
9. Richards, K. S., Miller, W. L., and Marder, E. (1999) Maturation of lobster stomatogastric ganglion rhythmic activity. J. Neurophysiol. 82, 2006-2009. (Pubitemid 29471290)
10. Bucher, D., Taylor, A. L., and Marder, E. (2006) Central pattern generating neurons simultaneously express fast and slow rhythmic activities in the stomatogastric ganglion. J. Neurophysiol. 95, 3617-3632. (Pubitemid 43846169)
11. Fenelon, V. S., Le Feuvre, Y., and Meyrand, P. (2004) Phylogenetic, ontogenetic and adult adaptive plasticity of rhythmic neural networks: a common neuromodulatory mechanism? J. Comp. Physiol., A 190, 691-705. (Pubitemid 40876354)
12. Le Feuvre, Y., Fenelon, V. S., and Meyrand, P. (2001) Ontogeny of modulatory inputs to motor networks: early established projection and progressive neurotransmitter acquisition. J. Neurosci. 21, 1313-1326. (Pubitemid 32128776)
13. Le Feuvre, Y., Fenelon, V. S., and Meyrand, P. (1999) Central inputs mask multiple adult neural networks within a single embryonic network. Nature 402, 660-664. (Pubitemid 129516335)
14. Pulver, S. R., Thirumalai, V., Richards, K. S., and Marder, E. (2003) Dopamine and histamine in the developing stomatogastric system of the lobster Homarus americanus. J. Comp. Neurol. 462, 400-414. (Pubitemid 36775902)
15. Kilman, V., Fenelon, V. S., Richards, K. S., Thirumalai, V., Meyrand, P., and Marder, E. (1999) Sequential developmental acquisition of cotransmitters in identified sensory neurons of the stomatogastric nervous system of the lobsters, Homarus americanus and Homarus gammarus. J. Comp. Neurol. 408, 318-334. (Pubitemid 29211186)
16. Fenelon, V. S., Kilman, V., Meyrand, P., and Marder, E. (1999) Sequential developmental acquisition of neuromodulatory inputs to a central pattern-generating network. J. Comp. Neurol. 408, 335-351. (Pubitemid 29211187)
17. Li, L., Pulver, S. R., Kelley, W. P., Thirumalai, V., Sweedler, J. V., and Marder, E. (2002) Orcokinin peptides in developing and adult crustacean stomatogastric nervous systems and pericardial organs. J. Comp. Neurol. 444, 227-244. (Pubitemid 34117088)
18. Richards, K. S., and Marder, E. (2000) The actions of crustacean cardioactive peptide on adult and developing stomatogastric ganglion motor patterns. J. Neurobiol. 44, 31-44. (Pubitemid 30451666)
19. Rehm, K. J., Deeg, K. E., and Marder, E. (2008) Developmental regulation of neuromodulator function in the stomatogastric ganglion of the lobster Homarus americanus. J. Neurosci. 28, 9828-9839.
20. Baggerman, G., Verleyen, P., Clynen, E., Huybrechts, J., De Loof, A., and Schoofs, L. (2004) Peptidomics. J. Chromatogr., B 803, 3-16. (Pubitemid 38340634)
21. Bulau, P., Meisen, I., Schmitz, T., Keller, R., and Peter-Katalinic, J. (2004) Identification of neuropeptides from the sinus gland of the crayfish Orconectes limosus using nanoscale on-line liquid chromatography tandem mass spectrometry. Mol. Cell Proteomics 3, 558-564. (Pubitemid 38878515)
22. Fu, Q., Christie, A. E., and Li, L. (2005) Mass spectrometric characterization of crustacean hyperglycemic hormone precursor-related peptides (CPRPs) from the sinus gland of the crab Cancer productus. Peptides 26, 2137-2150. (Pubitemid 41584077)
23. Fu, Q., Kutz, K. K., Schmidt, J. J., Hsu, Y. W., Messinger, D. I., Cain, S. D., de la Iglesia, H. O., Christie, A. E., and 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. (Pubitemid 41780631)
24. Huybrechts, J., Nusbaum, M. P., Bosch, L. V., Baggerman, G., De Loof, A., and Schoofs, L. (2003) Neuropeptidomic analysis of the brain and thoracic ganglion from the Jonah crab Cancer borealis. Biochem. Biophys. Res. Commun. 308, 535-544. (Pubitemid 36945526)
25. Li, L., Kelley, W. P., Billimoria, C. P., Christie, A. E., Pulver, S. R., Sweedler, J. V., and 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. (Pubitemid 37310630)
26. Messinger, D. I., Kutz, K. K., Le, T., Verley, D. R., Hsu, Y. W., Ngo, C. T., Cain, S. D., Birmingham, J. T., Li, L., 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)
27. Behrens, H. L., Chen, R., and Li, L. (2008) Combining microdialysis, NanoLC-MS, and MALDI-TOF/TOF to detect neuropeptides secreted in the crab Cancer borealis. Anal. Chem. 80, 6949-6958.
28. Skiebe, P., Dreger, M., Meseke, M., Evers, J. F., and Hucho, F. (2002) Identification of orcokinins in single neurons in the stomatogastric nervous system of the crayfish Cherax destructor. J. Comp. Neurol. 444, 245-259. (Pubitemid 34117089)
29. Skiebe, P., Dreger, M., Borner, J., Meseke, M., and Weckwerth, W. (2003) Immunocytochemical and molecular data guide peptide identification by mass spectrometry: orcokinin and orcomyotropin-related peptides in the stomatogastric nervous system of several crustacean species. Cell. Mol. Biol. 49, 851-871.
30. Torfs, P., Baggerman, G., Meeusen, T., Nieto, J., Nachman, R. J., Calderon, J., De Loof, A., and Schoofs, L. (2002) Isolation, identification, and synthesis of a disulfated sulfakinin from the central nervous system of an arthropods the white shrimp Litopenaeus vannamei. Biochem. Biophys. Res. Commun. 299, 312-320. (Pubitemid 35373716)
31. Yasuda, A., Yasuda-Kamatani, Y., Nozaki, M., and Nakajima, T. (2004) Identification of GYRKPPFNGSIFamide (crustacean-SIFamide) in the crayfish Procambarus clarkii by topological mass spectrometry analysis. Gen. Comp. Endrocrinol. 135, 391-400. (Pubitemid 38064253)
32. Yasuda-Kamatani, Y., and Yasuda, A. (2000) Identification of orcokinin gene-related peptides in the brain of the crayfish Procambarus clarkii by the combination of MALDI-TOF and on-line capillary HPLC/Q-Tof mass spectrometries and molecular cloning. Gen. Comp. Endrocrinol. 118, 161-172. (Pubitemid 30217774)
33. Li, L., Garden, R. W., and Sweedler, J. V. (2000) Single-cell MALDI: a new tool for direct peptide profiling. Trends Biotechnol. 18, 151-160. (Pubitemid 30171333)
34. Li, L., Romanova, E. V., Rubakhin, S. S., Alexeeva, V., Weiss, K. R., Vilim, F. S., and Sweedler, J. V. (2000) Peptide profiling of cells with multiple gene products: combining immunochemistry and MALDI mass spectrometry with on-plate microextraction. Anal. Chem. 72, 3867-3874. (Pubitemid 30646527)
35. Kutz, K. K., Schmidt, J. J., and Li, L. (2004) In situ tissue analysis of neuropeptides by MALDI FTMS in-cell accumulation. Anal. Chem. 76, 5630-5640. (Pubitemid 39313308)
36. Ma, M., Chen, R., Sousa, G. L., Bors, E. K., Kwiatkowski, M. A., Goiney, C. C., Goy, M. F., Christie, A. E., and 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. Endrocrinol. 156, 395-409.
37. Chen, R., Jiang, X., Conaway, M. C., Mohtashemi, I., Hui, L., Viner, R., and 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.
38. Cape, S. S., Rehm, K. J., Ma, M., Marder, E., and 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. (Pubitemid 351562713)
39. Wang, J., 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.
40. Wang, J., Jiang, X., Sturm, R. M., and Li, L. (2009) Combining tissue extraction and off-line capillary electrophoresis matrix-assisted laser desorption/ionization Fourier transform mass spectrometry for neuropeptide analysis in individual neuronal organs using 2,5- dihydroxybenzoic acid as a multi-functional agent. J. Chromatogr., A 1216, 8283-8288.
41. Christie, A. E., Stemmler, E. A., Peguero, B., Messinger, D. I., Provencher, H. L., Scheerlinck, P., Hsu, Y. W., Guiney, M. E., de la Iglesia, H. O., and Dickinson, P. S. (2006) Identification, physiological actions, and distribution of VYRKPPFNGSIFamide (Val1)-SIFamide) in the stomatogastric nervous system of the American lobster Homarus americanus. J. Comp. Neurol. 496, 406-421.
42. Verleyen, P., Huybrechts, J., and Schoofs, L. (2009) SIFamide illustrates the rapid evolution in Arthropod neuropeptide research. Gen. Comp. Endrocrinol. 162, 27-35.
43. Dickinson, P. S., Stemmler, E. A., Barton, E. E., Cashman, C. R., Gardner, N. P., Rus, S., Brennan, H. R., McClintock, T. S., and Christie, A. E. (2009) 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.
44. 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.
45. Christie, A. E., Cashman, C. R., Brennan, H. R., Ma, M., Sousa, G. L., Li, L., Stemmler, E. A., and Dickinson, P. S. (2008) Identification of putative crustacean neuropeptides using in silico analyses of publicly accessible expressed sequence tags. Gen. Comp. Endrocrinol. 156, 246-264.
46. Bucknall, M., Fung, K. Y., and Duncan, M. W. (2002) Practical quantitative biomedical applications of MALDI-TOF mass spectrometry. J. Am. Soc. Mass Spectrom. 13, 1015-1027. (Pubitemid 36871597)
47. Rubakhin, S. S., and Sweedler, J. V. (2008) Quantitative measurements of cell-cell signaling peptides with single-cell MALDI MS. Anal. Chem. 80, 7128-7136.
48. Wang, M. Z., and Fitzgerald, M. C. (2001) A solid sample preparation method that reduces signal suppression effects in the MALDI analysis of peptides. Anal. Chem. 73, 625-631.
49. Rehm, K. J., Taylor, A. L., Pulver, S. R., and Marder, E. (2008) Spectral analyses reveal the presence of adult-like activity in the embryonic stomatogastric motor patterns of the lobster Homarus americanus. J. Neurophysiol. 99, 3104-3122.
50. Stangier, J., Hilbich, C., Burdzik, S., and Keller, R. (1992) Orcokinin: a novel myotropic peptide from the nervous system of the crayfish Orconectes limosus. Peptides 13, 859-864.
51. Zajac, J. M., and Mollereau, C. (2006) RFamide peptides. Introduction. Peptides 27, 941-942.
52. Helluy, S. M., and Beltz, B. S. (1991) Embryonic development of the American lobster (Homarus americanus): Quantitative staging and characterization of an embryonic molt cycle. Biol. Bull. 180, 355-371.
53. 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)
54. Ma, M., Gard, A. L., Xiang, F., Wang, J., Davoodian, N., Lenz, P. H., Malecha, S. R., Christie, A. E., and Li, L. (2010) Combining in silico transcriptome mining and biological mass spectrometry for neuropeptide discovery in the Pacific white shrimp Litopenaeus vannamei. Peptides 31, 27-43.