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The Journal of Neuroscience, January 11, 2006, 26(2):518-529; doi:10.1523/JNEUROSCI.2566-05.2006

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Cellular/Molecular
Peptidomics of a Single Identified Neuron Reveals Diversity of Multiple Neuropeptides with Convergent Actions on Cellular Excitability

Connie R. Jiménez,¹ Sabine Spijker,¹ Simone de Schipper,¹ Johannes C. Lodder,² Cornelis Kees Janse,³ Wijnand P. M. Geraerts,¹ Jan van Minnen,¹ Naweed I. Syed,⁴ Alma L. Burlingame,⁵ August B. Smit,¹ and KaWan Li¹

Departments of ¹Molecular and Cellular Neurobiology, ²Experimental Neurophysiology, and ³Developmental Neurobiology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, The Netherlands, ⁴Neuroscience Research Group, Departments of Anatomy and Cell Biology, Physiology, and Biophysics, Health Sciences Centre, Calgary, Alberta, Canada T2N 4N1, and ⁵Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, California 94143-0446

In contrast to classical transmitters, the detailed structures and cellular and synaptic actions of neuropeptides are less well described. Peptide mass profiling of single identified neurons of the mollusc Lymnaea stagnalis indicated the presence of 17 abundant neuropeptides in the cardiorespiratory neuron, visceral dorsal 1 (VD1), and a subset of 14 peptides in its electrically coupled counterpart, right parietal dorsal 2. Altogether, based on this and previous work, we showed that the high number of peptides arises from the expression and processing of four distinct peptide precursor proteins, including a novel one. Second, we established a variety of posttranslational modifications of the generated peptides, including phosphorylation, disulphide linkage, glycosylation, hydroxylation, N-terminal pyroglutamylation, and C-terminal amidation. Specific synapses between VD1 and its muscle targets were formed, and their synaptic physiology was investigated. Whole-cell voltage-clamp analysis of dissociated heart muscle cells revealed, as tested for a selection of representative family members and their modifications, that the peptides of VD1 exhibit convergent activation of a high-voltage-activated Ca current. Moreover, the differentially glycosylated and hydroxylated 2 peptides were more potent than the unmodified 2 peptide in enhancing these currents. Together, this study is the first to demonstrate that single neurons exhibit such a complex pattern of peptide gene expression, precursor processing, and differential peptide modifications along with a remarkable degree of convergence of neuromodulatory actions. This study thus underscores the importance of a detailed mass spectrometric analysis of neuronal peptide content and peptide modifications related to neuromodulatory function.

Key words: mollusk; MALDI-TOF mass spectrometry; glycopeptide; posttranslational modification; HVA calcium channel; neuromodulation

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Received June 22, 2005; revised November 9, 2005; accepted November 9, 2005.

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