Research Article

Expression of vesicular glutamate transporters type 1 and 2 in sensory and autonomic neurons innervating the mouse colorectum

  1. Pablo R. Brumovsky1,2,†,*,
  2. David R. Robinson1,‡,
  3. Jun-Ho La1,
  4. Kim B. Seroogy3,
  5. Kerstin H. Lundgren3,
  6. Kathryn M. Albers1,
  7. Michael E. Kiyatkin1,
  8. Rebecca P. Seal4,
  9. Robert H. Edwards4,
  10. Masahiko Watanabe5,
  11. Tomas Hökfelt6,
  12. G.F. Gebhart1

Article first published online: 14 SEP 2011

DOI: 10.1002/cne.22730

Issue

Journal of Comparative Neurology

Journal of Comparative Neurology

Volume 519, Issue 16, pages 3346–3366, 1 November 2011

Additional Information

How to Cite

Brumovsky, P. R., Robinson, D. R., La, J.-H., Seroogy, K. B., Lundgren, K. H., Albers, K. M., Kiyatkin, M. E., Seal, R. P., Edwards, R. H., Watanabe, M., Hökfelt, T. and Gebhart, G.F. (2011), Expression of vesicular glutamate transporters type 1 and 2 in sensory and autonomic neurons innervating the mouse colorectum. J. Comp. Neurol., 519: 3346–3366. doi: 10.1002/cne.22730

Author Information

  1. 1

    Pittsburgh Center for Pain Research, Department of Anesthesiology, University of Pittsburgh, Pittsburgh, Pennsylvania 15213

  2. 2

    CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), Buenos Aires, Argentina

  3. 3

    Department of Neurology, University of Cincinnati, College of Medicine, Cincinnati, Ohio 45267-0536

  4. 4

    Program in Neurosciences, University of California, School of Medicine, San Francisco, California 94143

  5. 5

    Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan

  6. 6

    Department of Neuroscience, Karolinska Institutet, Stockholm, SE 17177, Sweden

  1. †

    Faculty of Biomedical Sciences, Austral University, Av. Juan D. Perón 1500, B1629AHJ, Pilar, Buenos Aires, Argentina

  2. ‡

    Swanson School of Engineering, University of Pittsburgh, Pittsburgh, PA 15213

*Faculty of Biomedical Sciences, Austral University, Av. Juan D. Perón 1500, B1629AHJ, Pilar, Buenos Aires, Argentina

Publication History

  1. Issue published online: 14 SEP 2011
  2. Article first published online: 14 SEP 2011
  3. Accepted manuscript online: 28 JUL 2011 10:43AM EST
  4. Manuscript Accepted: 7 JUL 2011
  5. Manuscript Revised: 12 APR 2011
  6. Manuscript Received: 8 JUN 2010

Funded by

  • National Institutes of Health (NIH). Grant Number: NS19912 (to G.G.)
  • IASP Early Career Research Award (to P.B.)

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Keywords:

  • colon;
  • DRG;
  • glutamate;
  • neuropeptides;
  • pain;
  • pelvic nerve

Abstract

Vesicular glutamate transporters (VGLUTs) have been extensively studied in various neuronal systems, but their expression in visceral sensory and autonomic neurons remains to be analyzed in detail. Here we studied VGLUTs type 1 and 2 (VGLUT1 and VGLUT2, respectively) in neurons innervating the mouse colorectum. Lumbosacral and thoracolumbar dorsal root ganglion (DRG), lumbar sympathetic chain (LSC), and major pelvic ganglion (MPG) neurons innervating the colorectum of BALB/C mice were retrogradely traced with Fast Blue, dissected, and processed for immunohistochemistry. Tissue from additional naïve mice was included. Previously characterized antibodies against VGLUT1, VGLUT2, and calcitonin gene-related peptide (CGRP) were used. Riboprobe in situ hybridization, using probes against VGLUT1 and VGLUT2, was also performed. Most colorectal DRG neurons expressed VGLUT2 and often colocalized with CGRP. A smaller percentage of neurons expressed VGLUT1. VGLUT2-immunoreactive (IR) neurons in the MPG were rare. Abundant VGLUT2-IR nerves were detected in all layers of the colorectum; VGLUT1-IR nerves were sparse. A subpopulation of myenteric plexus neurons expressed VGLUT2 protein and mRNA, but VGLUT1 mRNA was undetectable. In conclusion, we show 1) that most colorectal DRG neurons express VGLUT2, and to a lesser extent, VGLUT1; 2) abundance of VGLUT2-IR fibers innervating colorectum; and 3) a subpopulation of myenteric plexus neurons expressing VGLUT2. Altogether, our data suggests a role for VGLUT2 in colorectal glutamatergic neurotransmission, potentially influencing colorectal sensitivity and motility. J. Comp. Neurol. 519:3346–3366, 2011. © 2011 Wiley-Liss, Inc.

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