Stereological analysis of Ca2+/calmodulin-dependent protein kinase IIα-containing dorsal root ganglion neurons in the rat: Colocalization with isolectin Griffonia Simplicifolia, calcitonin gene-related peptide, or vanilloid receptor 1

Susan M. Carlton, Gregory L. Hargett

    Research output: Contribution to journalArticle

    52 Citations (Scopus)

    Abstract

    The enzyme Ca2+/calmodulin-dependent protein kinase II (CaMKII) is widely distributed in the nervous system. A previous report describes immunostaining for CaMKIIα in dorsal root ganglion (DRG) neurons. In this study, CaMKIIα is colocalized in the rat with three putative markers of nociceptive DRG neurons, isolectin Griffonia simplicifolia (I-B4), identifying small-diameter, "peptide-poor" neurons; calcitonin gene-related peptide (CGRP), identifying "peptide-rich" neurons; or the vanilloid receptor 1 (VR1), identifying neurons activated by heat, acid, and capsaicin. Lumbar 4 and 5 DRG sections were labeled using immunofluorescence or lectin binding histochemistry, and percentages of single and double-labeled CaMKIIα neurons were determined. Stereological estimates of total neuron number in the L4 DRG were 13,815 ± 2,798 and in the L5 DRG were 14,111 ± 4,043. Percentages of single-labeled L4 DRG neurons were 41% ± 2% CaMKIIα 38% ± 3% I-B4, 44% ± 3% CGRP, and 32% ± 6% VR1. Percentages of single-labeled L5 DRG neurons were 44% ± 5% CaMKIIα, 48% ± 2% I-B4, 41% ± 7% CGRP, and 39% ± 14% VR1. For L4 and L5, respectively, estimates of double-labeled CaMKIIα neurons showed 34% ± 2% and 38% ± 17% labeled for I-B4, 25% ± 14% and 19% ± 10% labeled for CGRP, and 37% ± 7% and 38% ± 5% labeled for VR1. Conversely, for L4 and L5, respectively, 39% ± 14% and 38% ± 7% I-B4 binding neurons, 24% ± 12% and 23% ± 10% CGRP neurons, and 42% ± 7% and 35% ± 7% VR1 neurons labeled for CaMKIIα. The mean diameter of CaMKIIα-labeled neurons was approximately 27 μm, confirming that this enzyme was preferentially localized in small DRG neurons. The results indicate that subpopulations of DRG neurons containing CaMKIIα are likely to be involved in the processing of nociceptive information. Thus, this enzyme may play a critical role in the modulation of nociceptor activity and plasticity of primary sensory neurons.

    Original languageEnglish (US)
    Pages (from-to)102-110
    Number of pages9
    JournalJournal of Comparative Neurology
    Volume448
    Issue number1
    DOIs
    StatePublished - Jun 17 2002

    Fingerprint

    Griffonia
    Calcitonin Gene-Related Peptide Receptors
    TRPV Cation Channels
    Calcium-Calmodulin-Dependent Protein Kinase Type 2
    Spinal Ganglia
    Lectins
    Neurons
    Calcitonin Gene-Related Peptide
    Enzymes
    Nociceptors
    Peptides

    Keywords

    • Calcium
    • Calmodulin
    • Capsaicin
    • Lectin
    • Nociception
    • Primary sensory neuron

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    @article{19f12401507c4221a5e02c1e70cc9d6c,
    title = "Stereological analysis of Ca2+/calmodulin-dependent protein kinase IIα-containing dorsal root ganglion neurons in the rat: Colocalization with isolectin Griffonia Simplicifolia, calcitonin gene-related peptide, or vanilloid receptor 1",
    abstract = "The enzyme Ca2+/calmodulin-dependent protein kinase II (CaMKII) is widely distributed in the nervous system. A previous report describes immunostaining for CaMKIIα in dorsal root ganglion (DRG) neurons. In this study, CaMKIIα is colocalized in the rat with three putative markers of nociceptive DRG neurons, isolectin Griffonia simplicifolia (I-B4), identifying small-diameter, {"}peptide-poor{"} neurons; calcitonin gene-related peptide (CGRP), identifying {"}peptide-rich{"} neurons; or the vanilloid receptor 1 (VR1), identifying neurons activated by heat, acid, and capsaicin. Lumbar 4 and 5 DRG sections were labeled using immunofluorescence or lectin binding histochemistry, and percentages of single and double-labeled CaMKIIα neurons were determined. Stereological estimates of total neuron number in the L4 DRG were 13,815 ± 2,798 and in the L5 DRG were 14,111 ± 4,043. Percentages of single-labeled L4 DRG neurons were 41{\%} ± 2{\%} CaMKIIα 38{\%} ± 3{\%} I-B4, 44{\%} ± 3{\%} CGRP, and 32{\%} ± 6{\%} VR1. Percentages of single-labeled L5 DRG neurons were 44{\%} ± 5{\%} CaMKIIα, 48{\%} ± 2{\%} I-B4, 41{\%} ± 7{\%} CGRP, and 39{\%} ± 14{\%} VR1. For L4 and L5, respectively, estimates of double-labeled CaMKIIα neurons showed 34{\%} ± 2{\%} and 38{\%} ± 17{\%} labeled for I-B4, 25{\%} ± 14{\%} and 19{\%} ± 10{\%} labeled for CGRP, and 37{\%} ± 7{\%} and 38{\%} ± 5{\%} labeled for VR1. Conversely, for L4 and L5, respectively, 39{\%} ± 14{\%} and 38{\%} ± 7{\%} I-B4 binding neurons, 24{\%} ± 12{\%} and 23{\%} ± 10{\%} CGRP neurons, and 42{\%} ± 7{\%} and 35{\%} ± 7{\%} VR1 neurons labeled for CaMKIIα. The mean diameter of CaMKIIα-labeled neurons was approximately 27 μm, confirming that this enzyme was preferentially localized in small DRG neurons. The results indicate that subpopulations of DRG neurons containing CaMKIIα are likely to be involved in the processing of nociceptive information. Thus, this enzyme may play a critical role in the modulation of nociceptor activity and plasticity of primary sensory neurons.",
    keywords = "Calcium, Calmodulin, Capsaicin, Lectin, Nociception, Primary sensory neuron",
    author = "Carlton, {Susan M.} and Hargett, {Gregory L.}",
    year = "2002",
    month = "6",
    day = "17",
    doi = "10.1002/cne.10250",
    language = "English (US)",
    volume = "448",
    pages = "102--110",
    journal = "Journal of Comparative Neurology",
    issn = "0021-9967",
    publisher = "Wiley-Liss Inc.",
    number = "1",

    }

    TY - JOUR

    T1 - Stereological analysis of Ca2+/calmodulin-dependent protein kinase IIα-containing dorsal root ganglion neurons in the rat

    T2 - Colocalization with isolectin Griffonia Simplicifolia, calcitonin gene-related peptide, or vanilloid receptor 1

    AU - Carlton, Susan M.

    AU - Hargett, Gregory L.

    PY - 2002/6/17

    Y1 - 2002/6/17

    N2 - The enzyme Ca2+/calmodulin-dependent protein kinase II (CaMKII) is widely distributed in the nervous system. A previous report describes immunostaining for CaMKIIα in dorsal root ganglion (DRG) neurons. In this study, CaMKIIα is colocalized in the rat with three putative markers of nociceptive DRG neurons, isolectin Griffonia simplicifolia (I-B4), identifying small-diameter, "peptide-poor" neurons; calcitonin gene-related peptide (CGRP), identifying "peptide-rich" neurons; or the vanilloid receptor 1 (VR1), identifying neurons activated by heat, acid, and capsaicin. Lumbar 4 and 5 DRG sections were labeled using immunofluorescence or lectin binding histochemistry, and percentages of single and double-labeled CaMKIIα neurons were determined. Stereological estimates of total neuron number in the L4 DRG were 13,815 ± 2,798 and in the L5 DRG were 14,111 ± 4,043. Percentages of single-labeled L4 DRG neurons were 41% ± 2% CaMKIIα 38% ± 3% I-B4, 44% ± 3% CGRP, and 32% ± 6% VR1. Percentages of single-labeled L5 DRG neurons were 44% ± 5% CaMKIIα, 48% ± 2% I-B4, 41% ± 7% CGRP, and 39% ± 14% VR1. For L4 and L5, respectively, estimates of double-labeled CaMKIIα neurons showed 34% ± 2% and 38% ± 17% labeled for I-B4, 25% ± 14% and 19% ± 10% labeled for CGRP, and 37% ± 7% and 38% ± 5% labeled for VR1. Conversely, for L4 and L5, respectively, 39% ± 14% and 38% ± 7% I-B4 binding neurons, 24% ± 12% and 23% ± 10% CGRP neurons, and 42% ± 7% and 35% ± 7% VR1 neurons labeled for CaMKIIα. The mean diameter of CaMKIIα-labeled neurons was approximately 27 μm, confirming that this enzyme was preferentially localized in small DRG neurons. The results indicate that subpopulations of DRG neurons containing CaMKIIα are likely to be involved in the processing of nociceptive information. Thus, this enzyme may play a critical role in the modulation of nociceptor activity and plasticity of primary sensory neurons.

    AB - The enzyme Ca2+/calmodulin-dependent protein kinase II (CaMKII) is widely distributed in the nervous system. A previous report describes immunostaining for CaMKIIα in dorsal root ganglion (DRG) neurons. In this study, CaMKIIα is colocalized in the rat with three putative markers of nociceptive DRG neurons, isolectin Griffonia simplicifolia (I-B4), identifying small-diameter, "peptide-poor" neurons; calcitonin gene-related peptide (CGRP), identifying "peptide-rich" neurons; or the vanilloid receptor 1 (VR1), identifying neurons activated by heat, acid, and capsaicin. Lumbar 4 and 5 DRG sections were labeled using immunofluorescence or lectin binding histochemistry, and percentages of single and double-labeled CaMKIIα neurons were determined. Stereological estimates of total neuron number in the L4 DRG were 13,815 ± 2,798 and in the L5 DRG were 14,111 ± 4,043. Percentages of single-labeled L4 DRG neurons were 41% ± 2% CaMKIIα 38% ± 3% I-B4, 44% ± 3% CGRP, and 32% ± 6% VR1. Percentages of single-labeled L5 DRG neurons were 44% ± 5% CaMKIIα, 48% ± 2% I-B4, 41% ± 7% CGRP, and 39% ± 14% VR1. For L4 and L5, respectively, estimates of double-labeled CaMKIIα neurons showed 34% ± 2% and 38% ± 17% labeled for I-B4, 25% ± 14% and 19% ± 10% labeled for CGRP, and 37% ± 7% and 38% ± 5% labeled for VR1. Conversely, for L4 and L5, respectively, 39% ± 14% and 38% ± 7% I-B4 binding neurons, 24% ± 12% and 23% ± 10% CGRP neurons, and 42% ± 7% and 35% ± 7% VR1 neurons labeled for CaMKIIα. The mean diameter of CaMKIIα-labeled neurons was approximately 27 μm, confirming that this enzyme was preferentially localized in small DRG neurons. The results indicate that subpopulations of DRG neurons containing CaMKIIα are likely to be involved in the processing of nociceptive information. Thus, this enzyme may play a critical role in the modulation of nociceptor activity and plasticity of primary sensory neurons.

    KW - Calcium

    KW - Calmodulin

    KW - Capsaicin

    KW - Lectin

    KW - Nociception

    KW - Primary sensory neuron

    UR - http://www.scopus.com/inward/record.url?scp=0037124381&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=0037124381&partnerID=8YFLogxK

    U2 - 10.1002/cne.10250

    DO - 10.1002/cne.10250

    M3 - Article

    C2 - 12012376

    AN - SCOPUS:0037124381

    VL - 448

    SP - 102

    EP - 110

    JO - Journal of Comparative Neurology

    JF - Journal of Comparative Neurology

    SN - 0021-9967

    IS - 1

    ER -