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Research ArticleNegative Results, Sensory and Motor Systems

Metabotropic Glutamate Receptor 2/3 (mGluR2/3) Activation Suppresses TRPV1 Sensitization in Mouse, But Not Human, Sensory Neurons

Tayler D. Sheahan, Manouela V. Valtcheva, Lisa A. McIlvried, Melanie Y. Pullen, David A.A. Baranger and Robert W. Gereau IV
eNeuro 5 March 2018, 5 (2) ENEURO.0412-17.2018; https://doi.org/10.1523/ENEURO.0412-17.2018
Tayler D. Sheahan
1Washington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri 63110
2Washington University Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri 63110
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  • ORCID record for Tayler D. Sheahan
Manouela V. Valtcheva
1Washington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri 63110
2Washington University Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri 63110
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Lisa A. McIlvried
1Washington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri 63110
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Melanie Y. Pullen
1Washington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri 63110
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David A.A. Baranger
2Washington University Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri 63110
3BRAIN Laboratory, Department of Psychological and Brain Sciences, Washington University in St. Louis, St. Louis, Missouri 63130
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Robert W. Gereau IV
1Washington University Pain Center and Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri 63110
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  • Figure 1.
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    Figure 1.

    mGlu2/3 receptor activation blocks PGE2-induced TRPV1 sensitization in mouse, but not human, sensory neurons. Representative traces of 100 nm capsaicin (Cap)-induced calcium responses in mouse (A) and human (B) DRG neurons in response to vehicle (left), 1 μm PGE2 (middle), or 1 μm PGE2 + 10 μm APDC (right). Experiments concluded with a pulse of 50 mm KCl to determine cell viability. The degree of TRPV1 sensitization is expressed as a response ratio calculated by dividing the peak amplitude of Cap 2 by the peak amplitude of Cap 1 (A, dashed lines). C, In mouse DRG neurons, PGE2 significantly increased the capsaicin response ratio compared with vehicle (**** p = 2.1 × 10–5; n = 143–150 neurons, n = 4 preps/condition). Coapplication of APDC with PGE2 blocked this effect and significantly reduced the response ratio compared to PGE2 alone (** p = 0.0081; n = 89–150 neurons, n = 3–4 preps/condition). D, PGE2 also significantly increased the capsaicin response ratio of human DRG neurons compared with vehicle (**** p = 3.0 × 10–6; n = 59–71 neurons, n = 5–6 donors/condition); whereas coapplication of APDC did not suppress PGE2-induced increases in the capsaicin response ratio (p = 1, n = 59–64 neurons, n = 6 donors/condition), which remained significantly greater than vehicle (** p = 0.0053, n = 64–71 neurons, n = 5–6 donors/condition). Capsaicin response ratios were compared using unpaired t tests and a Bonferroni correction for multiple comparisons. Data are presented as mean ± SEM. E, Compared with those of mice, a greater percentage of human DRG neurons responded to 100 nm capsaicin (χ2 = 15.45, **** p = 8.5 × 10–5, mouse: 405/1761 neurons, n = 4 preps, human: 223/731 neurons, n = 8 donors). F, LMM regression correction for impact of individual donor, as well as donor age and sex, did not alter human capsaicin response ratio analysis statistical outcomes compared with t tests alone.

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    Figure 2.

    Expression of Trpv1, Grm2, and Grm3 mRNA transcripts in dissociated mouse and human sensory neurons. A, Size distribution of total and Trpv1 + mouse DRG neuron populations; mean diameter of total neurons: 17.7 ± 0.2 μm (n = 395 neurons, n = 4 preps), mean diameter of Trpv1+ neurons: 20.3 ± 0.4 μm (n = 147 neurons). B, Size distribution of total and TRPV1+ human DRG neuron populations; mean diameter of total neurons: 31.9 ± 0.5 μm (n = 258 neurons, n = 5 donors), mean diameter of TRPV1+ neurons: 33.9 ± 0.9 μm (n = 83 neurons). Data are reported as mean ± SEM. C, The mean diameter of total human DRG neurons was significantly larger than that of total mouse DRG neurons (unpaired t test, **** p = 1.0 × 10–14). Data are presented as mean ± SD. Percentage of total mouse (D) and human (E) DRG neurons that expressed Trpv1, Grm2, and Grm3, as well as the percentage of neurons that coexpressed one mRNA transcript with another. Pie charts showing the percentage of Trpv1 + mouse (F) and human (G) DRG neurons that coexpressed Grm2, Grm3, or both transcripts. No significant differences in gene transcript expression of total neurons or Trpv1 + neuron subpopulations were observed between species.

Tables

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    Table 1.

    Donor information and tissue uses

    DonorAge, ySexRaceCause of deathTissue uses
    121MaleWhiteStrokeCa2+ imaging
    255FemaleWhiteStrokeCa2+ imaging, FISH
    322MaleBlackAnoxiaCa2+ imaging
    444FemaleWhiteStrokeCa2+ imaging
    512FemaleWhiteAnoxiaCa2+ imaging, FISH
    626MaleWhiteHead traumaCa2+ imaging, FISH
    718FemaleWhiteHead traumaCa2+ imaging, FISH
    818MaleWhiteHead traumaCa2+ imaging, FISH
    • y, year; FISH, fluorescent in situ hybridization.

    • View popup
    Table 2.

    RNAscope probes used for FISH

    TargetCatalog no.
    Mm-Trpv1313331
    Mm-Grm2-C3317831-C3
    Mm-Grm3-C2317821-C2
    Positive Control Probe-Mm320881
    Hs-TRPV1415381
    Hs-GRM2-C3589771-C3
    Hs-GRM3-C2500181-C2
    Positive Control Probe-Hs320861
    Negative Control Probe320871
    • Mm, mus musculus; Hs, homo sapiens; C2, channel 2; C3, channel 3.

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    Table 3.

    Statistical analysis

    LocationData StructureType of TestComparison95% confidence interval
    aNon-normally distributedt testVehicle vs. PGE2–0.6862 to –0.2728
    bNon-normally distributedt testPGE2 vs. PGE2 + APDC0.1317 to 0.618
    Non-normally distributedt testVehicle vs. PGE2 + APDC–0.2736 to 0.06428
    cNon-normally distributedt testVehicle vs. PGE2–0.5774 to –0.2563
    dNon-normally distributedt testPGE2 vs. PGE2 + APDC–0.4204 to 0.2717
    Non-normally distributedVehicle vs. PGE2 + APDC–0.7953 to –0.1871
    eNon-normally distributedRegressionVehicle vs. PGE2 vs. PGE2 + APDC–0.1178 to 0.1284
    fCategoricalChi-squareda0.5621 to 0.8235
    gMouse: non-normally distributedt testMouse vs. human–15.17 to –13.08
    Human: normally distributed
    hCategoricalChi-squareda2.653 to 4.769
    iCategoricalChi-squareda1.846 to 3.855
    jCategoricalChi-squareda1.047 to 1.967
    • The D’Agnostino and Pearson normality test was performed, when applicable.

    • aOdds ratio confidence interval reported.

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Metabotropic Glutamate Receptor 2/3 (mGluR2/3) Activation Suppresses TRPV1 Sensitization in Mouse, But Not Human, Sensory Neurons
Tayler D. Sheahan, Manouela V. Valtcheva, Lisa A. McIlvried, Melanie Y. Pullen, David A.A. Baranger, Robert W. Gereau IV
eNeuro 5 March 2018, 5 (2) ENEURO.0412-17.2018; DOI: 10.1523/ENEURO.0412-17.2018

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Metabotropic Glutamate Receptor 2/3 (mGluR2/3) Activation Suppresses TRPV1 Sensitization in Mouse, But Not Human, Sensory Neurons
Tayler D. Sheahan, Manouela V. Valtcheva, Lisa A. McIlvried, Melanie Y. Pullen, David A.A. Baranger, Robert W. Gereau IV
eNeuro 5 March 2018, 5 (2) ENEURO.0412-17.2018; DOI: 10.1523/ENEURO.0412-17.2018
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Keywords

  • Dorsal root ganglia
  • glutamate
  • human neurons
  • Metabotropic
  • Nociceptors
  • pain

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