Mass spectral comparison of the neuropeptide complement of the stomatogastric ganglion and brain in the adult and embryonic lobster, Homarus americanus

Journal of Neurochemistry

Volumn 105, Issue 3, 2008, Pages 690-702

  Cape, Stephanie S ^a   Rehm, Kristina J ^b   Ma, Mingming ^a   Marder, Eve ^b   Li, Lingjun ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

Central pattern generator; Crustacean; ESI QTOF MS MS; MALDI FTMS; Neuromodulation; Neuronal development

Indexed keywords

ALANYLPROLYLSERYLGLYCYLPHENYLALANYLLEUCYLGLYCYLMETHIONYLARGINYLGLYCINE; ALLATOSTATIN; ARGINYLPHENYLANALYLAMIDE; ASPARAGINYLPHENYLALANYLASPARTYLGLUTAMYLISOLEUCYLASPARTYLARGINYLSERYLGLYCYLPHENYLALANYLGLYCYLPHENYLALANINE; ASPARAGINYLPHENYLALANYLASPARTYLGLUTAMYLISOLEUCYLASPARTYLARGINYLSERYLGLYCYLPHENYLALANYLGLYCYLPHENYLALANYLASPARAGINE; ASPARAGINYLPHENYLALANYLASPARTYLGLUTAMYLISOLEUCYLASPARTYLARGINYLSERYLGLYCYLPHENYLALANYLGLYCYLPHENYLALANYLVALINE; ASPARTYLTHREONYLSERYLTHREONYLPROLYLALANYLLEUCYLARGINYLLEUCYLARGINYLPHENYLALANINE; GLUTAMINYLASPARTYLLEUCYLASPARTYLHISTIDYLVALYLPHENYLALANYLLEUCYLARGINYLPHENYLALANINE; GLYCYLPROLYLPROLYLSERYLLEUCYLARGINYLLEUCYLARGINYLPHENYLALANINE; NEUROPEPTIDE; PHENYLALANYLASPARTYLALANYLPHENYLALANYLTHREONYLTHREONYLGLYCYLPHENYLALANYLGLYCYLHISTIDYLSERINE; SERYLTHREONYLASPARAGINYLTRYPTOPHANYLSERYLSERYLLEUCYLARGINYLSERYLALANYLTRYPTOPHAN; TACHYKININ; UNCLASSIFIED DRUG; VALYLTYROSYLGLYCYLPROLYLARGINYLASPARTYLISOLEUCYLALANYLASPARAGINYLLEUCYLTYROSINE;

ABDOMINAL GANGLION; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN GANGLION; CONTROLLED STUDY; EMBRYO; FEMALE; LOBSTER; MALE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL;

AGING; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CELL DIFFERENTIATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EMBRYO, NONMAMMALIAN; GANGLIA, INVERTEBRATE; GASTROINTESTINAL TRACT; MASS SPECTROMETRY; NEPHROPIDAE; NEURONS; NEUROPEPTIDES; PHYLOGENY;

CANCER BOREALIS; CRUSTACEA; HOMARUS AMERICANUS;

EID: 42349117573     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05154.x     Document Type: Article

References (61)

1. Aguilar R., Maestro J. L., Vilaplana L., Chiva C., Andreu D. Belles X. (2004) Identification of leucomyosuppressin in the German cockroach, Blattella germanica, as an inhibitor of food intake. Regul. Pept. 119, 105 112.
2. Bardoni R., Ghirri A., Salio C., Prandini M. Merighi A. (2007) BDNF-mediated modulation of GABA and glycine release in dorsal horn lamina II from postnatal rats. Dev. Neurobiol. 67, 960 975.
3. Beltz B. S. Burd G. D. (1989) Immunocytochemical techniques: principles and practice. Blackwell Scientific Publications, Cambridge, Massachusetts, USA.
4. A receptor surface expression. Eur. J. Neurosci. 13, 1320 1328.
5. Bucher D., Johnson C. D. Marder E. (2007) Neuronal morphology and neuropil structure in the stomatogastric ganglion of the lobster, Homarus americanus. J. Comp. Neurol. 501, 185 205.
6. Casasnovas B. Meyrand P. (1995) Functional differentiation of adult neural circuits from a single embryonic network. J. Neurosci. 15, 5703 5718.
7. Christie A. E., Stemmler E. A., Peguero B. et al. (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.
8. DeKeyser S. S. Li L. (2007) Mass spectrometric charting of neuropeptides in arthropod neurons. Anal Bioanal Chem. 387, 29 35.
9. DeKeyser S. S., Kutz-Naber K. K., Schmidt J. J., Barrett-Wilt G. A. Li L. (2007) Imaging mass spectrometry of neuropeptides in decapod crustacean neuronal tissues. J. Proteome Res. 6, 1782 1791.
10. Dierick H. A. Greenspan R. J. (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat. Genet. 39, 678 682.
11. Ducret E., Le Feuvre Y., Meyrand P. Fénelon V. S. (2007) Removal of GABA within adult modulatory systems alters electrical coupling and allows expression of an embryonic-like network. J. Neurosci. 27, 3626 3638.
12. Fénelon V. S., Casasnovas B., Faumont S. Meyrand P. (1998) Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system. J. Comp. Neurol. 399, 289 305.
13. Fénelon V. S., Kilman V., Meyrand P. Marder E. (1999) Sequential developmental acquisition of neuromodulatory inputs to a central pattern-generating network. J. Comp. Neurol. 408, 335 351.
14. Frerking M., Malenka R. C. Nicoll R. A. (1998) Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J. Neurophysiol. 80, 3383 3386.
15. Fu Q., Goy M. F. Li L. (2005a) Identification of neuropeptides from the decapod crustacean sinus glands using nanoscale liquid chromatography tandem mass spectrometry. Biochem. Biophys. Res. Commun. 337, 765 778.
16. 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. Li L. (2005b) Hormone complement of the Cancer productus sinus gland and pericardial organ: an anatomical and mass spectrometric investigation. J. Comp. Neurol. 493, 607 626.
17. Goldberg D., Nusbaum M. P. 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.
18. Helluy S. M. 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.
19. Hummon A. B., Amare A. Sweedler J. V. (2006) Discovering new invertebrate neuropeptides using mass spectrometry. Mass Spectrom. Rev. 25, 77 98.
20. Kapuscinski M. Shulkes A. (1995) Peptide amidating activity and gastrin processing in the developing sheep pancreas. J. Endocrinol. 145, 137 142.
21. Kilman V., Fénelon V. S., Richards K. S., Thirumalai V., Meyrand P. 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.
22. Le Feuvre Y., Fénelon V. S. Meyrand P. (1999) Central inputs mask multiple adult neural networks within a single embryonic network. Nature 402, 660 664.
23. Lee K. S., You K. H., Choo J. K., Han Y. M. Yu K. (2004) Drosophila short neuropeptide F regulates food intake and body size. J. Biol. Chem. 279, 50781 50789.
24. Levine E. S., Dreyfus C. F., Black I. B. Plummer M. R. (1995) Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl Acad. Sci. USA, 92, 8074 8077.
25. Li L., Garden R. W. Sweedler J. V. (2000) Single-cell MALDI: a new tool for direct peptide profiling. Trends Biotechnol. 18, 151 160.
26. Li L., Pulver S. R., Kelley W. P., Thirumalai V., Sweedler J. V. Marder E. (2002) Orcokinin peptides in developing and adult crustacean stomatogastric nervous systems and pericardial organs. J. Comp. Neurol. 444, 227 244.
27. Ma M., Kutz-Naber K. K. Li L. (2007) Methyl esterification assisted MALDI FTMS characterization of the orcokinin neuropeptide family. Anal. Chem. 79, 673 681.
28. Manent J. B. Represa A. (2007) Neurotransmitters and brain maturation: early paracrine actions of GABA and glutamate modulate neuronal migration. Neuroscientist 13, 268 279.
29. Marchand J. E., Shimonaka H. Kream R. M. (1991) Biochemical characterization and anatomical distribution of a major form of unamidated precursor of substance P in rat brain. Brain Res. 567, 290 305.
30. Marder E. Bucher D. (2001) Central pattern generators and the control of rhythmic movements. Curr. Biol. 11, R986 R996.
31. Marder E. Bucher D. (2007) Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu. Rev. Physiol. 69, 291 316.
32. Marder E. Calabrese R. L. (1996) Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687 717.
33. Marder E. Rehm K. J. (2005) Development of central pattern generating circuits. Curr. Opin. Neurobiol. 15, 86 93.
34. Marder E. Richards K. S. (1999) Development of the peptidergic modulation of a rhythmic pattern generating network. Brain Res. 848, 35 44.
35. Marder E., Hooper S. L. Siwicki K. K. (1986) Modulatory action and distribution of the neuropeptide proctolin in the crustacean stomatogastric nervous system. J. Comp. Neurol. 243, 454 467.
36. Marder E., Bucher D., Schulz D. J. Taylor A. L. (2005) Invertebrate central pattern generation moves along. Curr. Biol. 15, R685 R699.
37. Marino L., Muglia B. Dickinson C. J. (1994) Glycine-extended post-translational processing intermediates of gastrin and cholecystokinin in the gut. Regul. Pept. 50, 73 85.
38. McLean Bolton M., Pittman A. J. Lo D. C. (2000) Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J. Neurosci. 20, 3221 3232.
39. Nusbaum M. P. Beenhakker M. P. (2002) A small-systems approach to motor pattern generation. Nature 417, 343 350.
40. Pezet S. McMahon S. B. (2006) Neurotrophins: mediators and modulators of pain. Annu. Rev. Neurosci. 29, 507 538.
41. Pulver S. R., Thirumalai V., Richards K. S. Marder E. (2003) Dopamine and histamine in the developing stomatogastric system of the lobster Homarus americanus. J. Comp. Neurol. 462, 400 414.
42. Read M. Shulkes A. (1993) Developmental expression of pancreatic gastrin and somatostatin in the sheep. Mol. Cell. Endocrinol. 93, 31 38.
43. Represa A. Ben-Ari Y. (2005) Trophic actions of GABA on neuronal development. Trends Neurosci. 28, 278 283.
44. Richards K. S., Simon D. J., Pulver S. R., Beltz B. S. Marder E. (2003) Serotonin in the developing stomatogastric system of the lobster, Homarus americanus. J. Neurobiol. 54, 380 392.
45. Scholz N. L., Chang E. S., Graubard K. Truman J. W. (1998) The NO/cGMP pathway and the development of neural networks in postembryonic lobsters. J. Neurobiol. 34, 208 226.
46. Skiebe P. (1999) Allatostatin-like immunoreactivity in the stomatogastric nervous system and the pericardial organs of the crab Cancer pagurus, the lobster Homarus americanus, and the crayfish Cherax destructor and Procambarus clarkii. J. Comp. Neurol. 403, 85 105.
47. Skiebe P. (2001) Neuropeptides are ubiquitous chemical mediators: using the stomatogastric nervous system as a model system. J. Exp. Biol. 204, 2035 2048.
48. Skiebe P., Dreger M., Borner J., Meseke M. 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. (Noisy-le-grand). 49, 851 871.
49. Stemmler E. A., Provencher H. L., Guiney M. E., Gardner N. P. Dickinson P. S. (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.
50. + ion formation in dried droplet tissue preparations. J Mass Spectrom. 41, 295 311.
51. Stemmler E. A., Peguero B., Bruns E. A., Dickinson P. S. 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.
52. Stepan V. M., Krametter D. F., Matsushima M., Todisco A., Delvalle J. Dickinson C. J. (1999) Glycine-extended gastrin regulates HEK cell growth. Am. J. Physiol. 277, R572 R581.
53. Stepanyan R., Day K., Urban J., Hardin D. L., Shetty R. S., Derby C. D., Ache B. W. McClintock T. S. (2006) Gene expression and specificity in the mature zone of the lobster olfactory organ. Physiol. Genomics 25, 224 233.
54. Taghert P. H. (1999) FMRFamide neuropeptides and neuropeptide-associated enzymes in Drosophila. Microsc. Res. Tech. 45, 80 95.
55. A synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci. 17, 2959 2966.
56. Thirumalai V. Marder E. (2002) Colocalized neuropeptides activate a central pattern generator by acting on different circuit targets. J. Neurosci. 22, 1874 1882.
57. Turrigiano G. G. Selverston A. I. (1991) Distribution of cholecystokinin-like immunoreactivity within the stomatogastric nervous systems of four species of decapod crustacea. J. Comp. Neurol. 305, 164 176.
58. Velazquez-Marrero C., Beltz B. S. Marder E. (1999) Sequential developmental acquisition of cholecystokinin-like immunoreactivity in the stomatogastric nervous system of the lobster, Homarus americanus. Abstr. - Soc. Neurosci. 25, 1966.
59. Wen T., Parrish C. A., Xu D., Wu Q. Shen P. (2005) Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc. Natl Acad. Sci. USA 102, 2141 2146.
60. Xu B., Gottschalk W., Chow A. et al. (2000) The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J. Neurosci. 20, 6888 6897.
61. Yasuda-Kamatani Y. Yasuda A. (2006) Characteristic expression patterns of allatostatin-like peptide, FMRFamide-related peptide, orcokinin, tachykinin-related peptide, and SIFamide in the olfactory system of crayfish Procambarus clarkii. J. Comp. Neurol. 496, 135 147.