PAIN
Volume 114, Issue 1 , Pages 7-18 , March 2005

Altered primary afferent anatomy and reduced thermal sensitivity in mice lacking galectin-1

  • J. McGraw

      Affiliations

    • ICORD (International Collaboration on Repair Discoveries), Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver V6T 1Z4, Canada
    • These authors contributed equally to this work.
  • ,
  • A.D. Gaudet

      Affiliations

    • ICORD (International Collaboration on Repair Discoveries), Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver V6T 1Z4, Canada
    • These authors contributed equally to this work.
  • ,
  • L.W. Oschipok

      Affiliations

    • ICORD (International Collaboration on Repair Discoveries), Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver V6T 1Z4, Canada
  • ,
  • J.D. Steeves

      Affiliations

    • ICORD (International Collaboration on Repair Discoveries), Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver V6T 1Z4, Canada
  • ,
  • F. Poirier

      Affiliations

    • Departement de Biologie du Developpement, Institut Jacques Monod, Paris, France
  • ,
  • W. Tetzlaff

      Affiliations

    • ICORD (International Collaboration on Repair Discoveries), Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver V6T 1Z4, Canada
  • ,
  • M.S. Ramer

      Affiliations

    • ICORD (International Collaboration on Repair Discoveries), Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver V6T 1Z4, Canada
    • Corresponding Author InformationCorresponding author. Tel.: +604 822 4956; fax: +604 827 5169.

Received 3 September 2004 ,Revised 6 October 2004 ,Accepted 18 October 2004.

References 

  1. Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci. 1995;7:1484–1494
  2. Bradbury EJ, Burnstock G, McMahon SB. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci. 1998;12:256–268
  3. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN. A P2X purinoceptor expressed by a subset of sensory neurons. Nature. 1995;377:428–431
  4. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell. 1994;76:1001–1011
  5. Dai Y, Iwata K, Kondo E, Morimoto T, Noguchi K. A selective increase in Fos expression in spinal dorsal horn neurons following graded thermal stimulation in rats with experimental mononeuropathy. Pain. 2001;90:287–296
  6. Dodd J, Jessell TM. Cell surface glycoconjugates and carbohydrate-binding proteins: possible recognition signals in sensory neurone development. J Exp Neurol. 1986;124:225–238
  7. Fukaya K, Hasegawa M, Mashitani T, Kadoya T, Horie H, Hayashi Y, et al. Oxidized galectin-1 stimulates the migration of Schwann cells from both proximal and distal stumps of transected nerves and promotes axonal regeneration after peripheral nerve injury. J Neuropathol Exp Neurol. 2003;62:162–172
  8. Garcia-Martinez C, Humet M, Planells-Cases R, Gomis A, Caprini M, Viana F, et al. Attenuation of thermal nociception and hyperalgesia by VR1 blockers. Proc Natl Acad Sci USA. 2002;99:2374–2379
  9. Gaudet AD, Williams SJ, Hwi LP, Ramer MS. Regulation of TRPV2 by axotomy in sympathetic, but not sensory neurons. Brain Res. 2004;1017:155–162
  10. Horie H, Kadoya T. Identification of oxidized galectin-1 as an initial repair regulatory factor after axotomy in peripheral nerves. Neurosci Res. 2000;38:131–137
  11. Horie H, Inagaki Y, Sohma Y, Nozawa R, Okawa K, Hasegawa M, et al. Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. J Neurosci. 1999;19:9964–9974
  12. Horie H, Kadoya T, Hikawa N, Sango K, Inoue H, Takeshita K, et al. Oxidized galectin-1 stimulates macrophages to promote axonal regeneration in peripheral nerves after axotomy. J Neurosci. 2004;24:1873–1880
  13. Hunt SP, Pini A, Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 1987;328:632–634
  14. Hynes MA, Gitt M, Barondes SH, Jessell TM, Buck LB. Selective expression of an endogenous lactose-binding lectin gene in subsets of central and peripheral neurons. J Neurosci. 1990;10:1004–1013
  15. Imbe H, Okamoto K, Kadoya T, Horie H, Senba E. Galectin-1 is involved in the potentiation of neuropathic pain in the dorsal horn. Brain Res. 2003;993:72–83
  16. Jarvis MF, Burgard EC, McGaraughty S, Honore P, Lynch K, Brennan TJ, et al. A-317491, a novel potent and selective non-nucleotide antagonist of P2X3 and P2X2/3 receptors, reduces chronic inflammatory and neuropathic pain in the rat. Proc Natl Acad Sci USA. 2002;99:17179–17184
  17. John JA, Key B. Expression of galectin-1 in the olfactory nerve pathway of rat. Brain Res Dev Brain Res. 1999;117:171–178
  18. Kobayashi NR, Bedard AM, Hincke MT, Tetzlaff W. Increased expression of BDNF and trkB mRNA in rat facial motoneurons after axotomy. Eur J Neurosci. 1996;8:1018–1029
  19. Lawson SN, Harper AA, Harper EI, Garson JA, Anderton BH. A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones. J Comp Neurol. 1984;228:263–272
  20. Mahanthappa NK, Cooper DN, Barondes SH, Schwarting GA. Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism, Development. 1994;120:1373–1384
  21. McGraw J, Oschipok L, Liu J, Hiebert GW, Mak CFW, Horie H, et al. Galectin-1 expression correlates with the regenerative potential of rubrospinal and spinal motoneurons. Neuroscience. 2004;128:713–719
  22. McKemy DD, Neuhausser WM, Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature. 2002;416:52–58
  23. McMahon SB, Moore CE. Plasticity of primary afferent acid phosphatase expression following rerouting of afferents from muscle to skin in the adult rat. J Comp Neurol. 1988;274:1–8
  24. McPhail LT, McBride CB, McGraw J, Steeves JD, Tetzlaff W. Axotomy abolishes NeuN expression in facial but not rubrospinal neurons. Exp Neurol. 2004;185:182–190
  25. Molliver DC, Snider WD. Nerve growth factor receptor TrkA is down-regulated during postnatal development by a subset of dorsal root ganglion neurons. J Comp Neurol. 1997;381:428–438
  26. Molliver DC, Radeke MJ, Feinstein SC, Snider WD. Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J Comp Neurol. 1995;361:404–416
  27. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, et al. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron. 1997;19:849–861
  28. Outenreath RL, Jones AL. Influence of an endogenous lectin substrate on cultured dorsal root ganglion cells. J Neurocytol. 1992;21:788–795
  29. Ozaki S, Snider WD. Initial trajectories of sensory axons toward laminar targets in the developing mouse spinal cord. J Comp Neurol. 1997;380:215–229
  30. Poirier F, Robertson EJ. Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development. 1993;119:1229–1236
  31. Puche AC, Poirier F, Hair M, Bartlett PF, Key B. Role of galectin-1 in the developing mouse olfactory system. Dev Biol. 1996;179:274–287
  32. Ramer MS, Bradbury EJ, McMahon SB. Nerve growth factor induces P2X(3) expression in sensory neurons. J Neurochem. 2001;77:864–875
  33. Ramer MS, Duraisingam I, Priestley JV, McMahon SB. Two-tiered inhibition of axon regeneration at the dorsal root entry zone. J Neurosci. 2001;21:2651–2660
  34. Ramer MS, Bradbury EJ, Michael GJ, Lever IJ, McMahon SB. Glial cell line-derived neurotrophic factor increases calcitonin gene-related peptide immunoreactivity in sensory and motoneurons in vivo. Eur J Neurosci. 2003;18:2713–2721
  35. Regan LJ, Dodd J, Barondes SH, Jessell TM. Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons. PNAS. 1986;83:2248–2252
  36. Rose RD, Rohrlich D. Counting sectioned cells via mathematical reconstruction. J Comp Neurol. 1988;272:365–386
  37. Sango K, Tokashiki A, Horie M, Kawano H, Watabe K, Horie H, et al. Synthesis, localization and externalization of galectin-1 in mature dorsal root ganglion neurons and Schwann cells. Eur J Neurosci. 2004;19:55–64
  38. Silos-Santiago I, Molliver DC, Ozaki S, Smeyne RJ, Fagan AM, Barbacid M, et al. Non-TrkA-expressing small DRG neurons are lost in TrkA deficient mice. J Neurosci. 1995;15:5929–5942
  39. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, et al. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature. 1994;368:246–249[see comments]
  40. Snider WD, McMahon SB. Tackling pain at the source: new ideas about nociceptors. Neuron. 1998;20:629–632
  41. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell. 2003;112:819–829
  42. Stucky CL, Lewin GR. Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J Neurosci. 1999;19:6497–6505
  43. Vulchanova L, Riedl MS, Shuster SJ, Stone LS, Hargreaves KM, Buell G, et al. P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci. 1998;10:3470–3478
  44. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, et al. Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci. 2004;24:6410–6415
  45. Zwick M, Davis BM, Woodbury CJ, Burkett JN, Koerber HR, Simpson JF, et al. Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci. 2002;22:4057–4065

PII: S0304-3959(04)00497-X

doi: 10.1016/j.pain.2004.10.009

PAIN
Volume 114, Issue 1 , Pages 7-18 , March 2005