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Clinical & Experimental Allergy

Trigeminal nasal-specific neurons respond to nerve growth factor with substance-P biosynthesis

Authors

  • E. Mingomataj,

    1. Department of Pneumology and Immunology, Allergy-Centre-Charité, Otto-Heubner-Centre, Clinical Research Unit of Allergy, Berlin, Germany,
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    • 1These authors contributed equally to this work.

  • Q. T. Dinh,

    1. Department of Pneumology and Immunology, Allergy-Centre-Charité, Otto-Heubner-Centre, Clinical Research Unit of Allergy, Berlin, Germany,
    2. Department of Internal Medicine, Berlin, Germany,
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    • 1These authors contributed equally to this work.

  • D. Groneberg,

    1. Department of Pneumology and Immunology, Allergy-Centre-Charité, Otto-Heubner-Centre, Clinical Research Unit of Allergy, Berlin, Germany,
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  • W. Feleszko,

    1. Department of Pneumology and Immunology, Allergy-Centre-Charité, Otto-Heubner-Centre, Clinical Research Unit of Allergy, Berlin, Germany,
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  • B. Schmeck,

    1. Department of Medicine Infectious and Respiratory Diseases, Allergy and Asthma Clinic, Berlin, Germany
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  • R. Joachim,

    1. Department of Internal Medicine, Berlin, Germany,
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  • O. Noga,

    1. Department of Medicine Infectious and Respiratory Diseases, Allergy and Asthma Clinic, Berlin, Germany
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  • S. Nagel,

    1. Department of Comparative Medicine and Experimental Animal Sciences, Charité-Universitätsmedizin Berlin, Berlin, Germany
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  • B. F. Klapp,

    1. Department of Internal Medicine, Berlin, Germany,
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    • 1These authors contributed equally to this work.

  • A. Fischer

    1. Department of Pneumology and Immunology, Allergy-Centre-Charité, Otto-Heubner-Centre, Clinical Research Unit of Allergy, Berlin, Germany,
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    • 1These authors contributed equally to this work.


Correspondence:
Q. T. Dinh, Department of Internal Medicine/Psychosomatics, Charité-Universitätsmedizin Berlin, Augustenburger Platz 1, D-13353 Berlin, Germany.
E-mail: q-thai.dinh@charite.de

Summary

Background Nerve growth factor (NGF) has been found to induce substance-P biosynthesis in large-diameter A-fibres vagal airway neurons. However, the effect of NGF on trigeminal neurons innervating the nasal mucosa of the mouse has not been investigated so far.

Objective NGF has been implicated in allergic diseases by modulating sensory nerves. Therefore, the present study investigated the effect of NGF on neuropeptides expression such as substance-P and glutamate in nasal trigeminal neurons.

Methods Using neuronal tracing in combination with double labelling immunohistochemistry the expression of substance-P, glutamate and neurofilament protein 68-kDa expression was examined in nasal-specific trigeminal neurons of BALB/c-mice.

Results The numbers of Fast blue-labelled trigeminal neurons expressing substance-P were significantly increased after NGF exposure (NGF-treated ganglia: 16.4 ± 0.6% vs. control: 7.0 ± 0.4%, Pleqslant R: less-than-or-eq, slant0.001). NGF treatment-induced substance-P biosynthesis in neurofilament-positive (NGF-treated ganglia: 8.6 ± 0.2% vs. control: 1.1 ± 0.2%, Pleqslant R: less-than-or-eq, slant0.001) as well as neurofilament-negative (NGF-treated ganglia: 7.8 ± 0.6% vs. control: 5.9 ± 0.4%, P=0.05) and non-glutamatergic neurons (NGF-treated ganglia: 11.8 ± 1.9% vs. control 1.1 ± 1.0%, Pleqslant R: less-than-or-eq, slant0.001) 24 h after NGF exposure.

Conclusion Under normal conditions, substance-P was expressed in nasal-specific neurofilament-negative, glutamatergic and C-fibre neurons. Nasal-specific trigeminal neurons respond to NGF treatment with substance-P biosynthesis in non-glutamatergic, neurofilament-positive as well as -negative neurons. These findings suggest that nasal-specific trigeminal neurons are composed of heterogenous subpopulations in relation to their peptide profiles and therefore may have different functions in neurogenic airway inflammation.

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