Skip to main content
SpringerLink
Log in

Immunocytochemical study of parvalbumin, calbindin D-28k, and calretinin in the superficial dorsal horn of the rat spinal cord following unilateral hindpaw inflammation

  • Original Articles
  • Published:
Journal of Anesthesia Aims and scope Submit manuscript

Abstract

The effect of noxious stimulation on the immunore-activity of the calcium-binding proteins parvalbumin (PV), calbindin-D-28k (CB) and calretinin (CR) was investigated in the superficial dorsal horn of lumbar levels L5-L3 of the rat spinal cord. Freund's adjuvant was injected unilaterally into the hindpaw to induce inflammation. Immunohistochemical techniques were utilized to investigate changes in the calcium-binding proteins 2h and 1, 2, 4, and 7 days after injection. At 24h after injection, a decrease in the intensity of fluorescence of PV-immunoreactive (IR) fibers was observed in the superficial layer (substantia gelatinosa) of the ipsilateral dorsal horn (L5-L3) in most animals. Comparatively fewer animals exhibited changes in the CB- and CR-IR fibers, except at the L3 level 2 days after, and at the L4 level 7 days after the hindpaw injection. After the peak response, at 24h in most animals, there was a decline in the number of responders at 2 days and no differences were noted at 4 days. However, at 7 days, there was again an increase in the number of animals revealing diminished fluorescence intensity in the ipsilateral substantia gelatinosa. Changes in immunoreactivity of calcium binding proteins in the interneurons of the superficial lumbar dorsal horn may reflect hyperactivity within these neurons following noxious stimulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Heizmann CW (1993) Calcium signaling in the brain. Acta Neurobiol Exp 53:15–23

    CAS  Google Scholar 

  2. Neher E (1992) Controls on calcium influx. Nature 355:298–299

    Article  PubMed  CAS  Google Scholar 

  3. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. TINS 15:303–308

    PubMed  CAS  Google Scholar 

  4. Antal M, Freund TF, Polgár E (1990) Calcium-binding proteins, parvalbumin and calbindin-D28k immunoreactive neurons in the rat spinal cord and dorsal root ganglia: A light and electron microscopic study. J Comp Neurol 295:467–484

    Article  PubMed  CAS  Google Scholar 

  5. Fournet N, Garcia-Segura LM, Norman AW, Orci L (1986) Selective localization of calcium-binding protein in human brainstem, cerebellum and spinal cord. Brain Res 399:310–316

    Article  PubMed  CAS  Google Scholar 

  6. Ren K, Ruda MA (1995) A comparative study of the calcium binding proteins calbindin-D28k, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Res Rev 19:163–179

    Article  Google Scholar 

  7. Ren K, Ruda MA, Jacobowitz DM (1993) Immunohistochemical localization of calretinin in the dorsal root ganglion and spinal cord of the rat. Brain Res Bull 31:13–22

    Article  PubMed  CAS  Google Scholar 

  8. Yamamoto T, Carr PA, Baimbridge KG, Nagy JI (1989) Parvalbumin and calbindin-D28k immunoreactive neurons in the superficial layers of the spinal cord dorsal horn of the rat. Brain Res Bull 23:493–508

    Article  PubMed  CAS  Google Scholar 

  9. Yoshida S, Senba E, Kubota Y, Hagihira S, Yoshiya I, Emson PC, Tohyama M (1990) Calcium-binding proteins calbindin and parvalbumin in the superficial dorsal horn of the rat spinal cord. Neuroscience 37:839–848

    Article  PubMed  CAS  Google Scholar 

  10. Grant G (1993) Projection patterns of primary sensory neurons studies by transganglionic methods: Somatotopy and targetrelated organization. Brain Res Bull 30:199–208

    Article  PubMed  CAS  Google Scholar 

  11. Molander C, Grant G (1985) Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA-HRP conjugate. J Comp Neurol 237:476–484

    Article  PubMed  CAS  Google Scholar 

  12. Zimmerman M (1983) Ethical guidelines for investigation of experimental pain in conscious animals. Pain 16:109–110

    Article  Google Scholar 

  13. Molander C, Xu Q, Grant G (1984) The cytoarchitectonic organization of the spinal cord in the rat. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133–141

    Article  PubMed  CAS  Google Scholar 

  14. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic, New York

    Google Scholar 

  15. Winsky L, Nakata H, Martin BM, Jacobowitz DM (1989) Isolation, partial amino acid sequence and immunohistochemical localization of a brain-specific calcium-binding protein. Proc Natl Acad Sci USA 86:139–10143.

    Article  Google Scholar 

  16. Fitzgerald M, Sweet JE (1983) The termination pattern of sciatic afferents in the substantia gelatinosa of neonatal rats. Neurosci Lett 43:149–154

    Article  PubMed  CAS  Google Scholar 

  17. Robertson B, Grant G (1985) A comparison between wheat germ agglutinin and choleragenoid-horseradish peroxidase as anterograde transport markers in central branches of primary sensory neurons in the rat with some observations in the cat. Neuroscience 14:895–905

    Article  PubMed  CAS  Google Scholar 

  18. Smith CL (1983) The development and postnatal organization of primary afferent projections to the thoracic spinal cord. J Comp Neurol 220:29–43

    Article  PubMed  CAS  Google Scholar 

  19. Molander C, Grant G (1986) Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat. Neuroscience 19:297–312

    Article  PubMed  CAS  Google Scholar 

  20. Rivero-Melian C, Grant G (1991) Choleragenoid horseradish peroxidase used for studying projections of some hindlimb cutaneous nerves and plantar foot afferent to the dorsal horn and Clark's column in the rat. Exp Brain Res 84:125–132

    PubMed  CAS  Google Scholar 

  21. Swett JE, Woolf CJ (1985) The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J Comp Neurol 231:66–77

    Article  PubMed  CAS  Google Scholar 

  22. Ueyama T, Arakawa H, Mizuno N (1987) Central distribution of efferent and afferent components of the pudendal nerve in the rat. Anat Embryo 177:37–49

    Article  CAS  Google Scholar 

  23. Woolf CJ, Fitzgerald M (1986) Somatotopic organization of cutaneous afferent terminals dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord. J Comp Neurol 251:517–531

    Article  PubMed  CAS  Google Scholar 

  24. Ygge J, Grant G (1983) The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglion transport of horseradish peroxidase. J Comp Neurol 216:1–9

    Article  PubMed  CAS  Google Scholar 

  25. Presley RW, Menétrey D, Levine JD, Basbaum AI (1990) Systemic morphine suppresses noxious stimulus-evoked fos protein-like immunoreactivity in the rat spinal cord. J Neurosci 10: 323–335

    PubMed  CAS  Google Scholar 

  26. Draisci G, Iadarola MJ (1989) Temporal analysis of increases in c-fos, preprodynorphin and preproenkephalin mRNAs in rat spinal cord. Mol Brain Res 6:31–37

    Article  PubMed  CAS  Google Scholar 

  27. Iadarola MJ, Brady LS, Draisci G, Dubner R (1988) Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: Stimulus specificity behavioral parameters and opioid receptor binding. Pain 35:13–326

    Article  Google Scholar 

  28. Iadarola MJ, Douglass, J, Civelli O, Naranjo JR (1988) Differential activation of spinal cord dynorphin and enkephalin neurons during hyperalgesia: Evidence using cDNA hybridization. Brain Res 455:205–212

    Article  PubMed  CAS  Google Scholar 

  29. Millan MJ, Millan MH, Czlonkowski A, Höllt V, Picher CWT, Hertz A, Colpaert FC (1986) A model of chronic pain in the rat: Response of opioid systems to adjuvant-induced arthritis. J Neurosci 6:899–906.

    PubMed  CAS  Google Scholar 

  30. Chavkin C, Goldstein A (1981) Dynorphin is a specific endogenous ligand of the k-opioid receptor. Science 215:413–415

    Google Scholar 

  31. Law PY, Hom DS, Loh HH (1982) Loss of opiate receptor activity in neuroblastoma X glioma NG 108-15 hybrid cells after chronic opiate treatment. Mol Pharmacol 22:1–4

    PubMed  CAS  Google Scholar 

  32. Strang PF, Potter JD (1992) A monoclonal antibody that recognizes different conformational status of skeletal muscle troponin C and other calcium binding proteins. J Muscle Res Cell Motil 13: 308–314

    Article  PubMed  CAS  Google Scholar 

  33. Winsky L, Kuznick J (1994) Evidence for calcium-dependent antibody recognition of calcium binding proteins. Soc Neurosci Abstract: 20

  34. Johansen FF, Tønder N, Zimmer J, Baimbridge KG, Diemer NH (1990) Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia. Neurosci Lett 120:171–174

    Article  PubMed  CAS  Google Scholar 

  35. Nitsch C, Scotti A, Sommacal A, Kalt G (1989) GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2+-binding protein parvalbumin. Neurosci Lett 105:263–268

    Article  PubMed  CAS  Google Scholar 

  36. Rami A, Rabie A, Thomasset M, Krieglstein J (1992) Calbindin-D28k and ischemic damage of pyramidal cells in rat hippocampus. J Neurosci Res 31:89–95

    Article  PubMed  CAS  Google Scholar 

  37. Freund TF, Maglóczky ZS (1993) Early degeneration of calretinin-containing neurons in the rat hippocampus after ischemia. Neurosci 56:581–596

    Article  CAS  Google Scholar 

  38. Sloviter RS (1989) Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: Localization in the hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280: 183–196

    Article  PubMed  CAS  Google Scholar 

  39. Freund TF, Ylinen A, Miettinen R, Pitkänen A, Lahtinen H, Baimbridge KG, Riekkinen PJ (1991) Pattern of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability. Brain Res Bull 28:27–38

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anesthesiology, Saga Medical School, 5-1-1 Nabeshima, 849, Saga, Japan

    Yoko Mineta, Hiroshi Koyanagi, Kiyoshi Harano & Tadahide Totoki

  2. Laboratory Animal Center, Saga Medical School, 5-1-1 Nabeshima, 849, Saga, Japan

    Masatoshi Morimoto

  3. Laboratory of Clinical Science, National Institute of Mental Health, Building 10, Room 3D-48, 10 Center Drive-MSC 1266, 20892-1266, Bethesda, MD, USA

    David M. Jacobowitz

Authors
  1. Yoko Mineta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroshi Koyanagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masatoshi Morimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiyoshi Harano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tadahide Totoki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David M. Jacobowitz
    View author publications

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Mineta, Y., Koyanagi, H., Morimoto, M. et al. Immunocytochemical study of parvalbumin, calbindin D-28k, and calretinin in the superficial dorsal horn of the rat spinal cord following unilateral hindpaw inflammation. J Anesth 10, 211–217 (1996). https://doi.org/10.1007/BF02471393

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02471393

Key words

Search

Navigation