Stress induces substance P in vagal sensory neurons innervating the mouse airways
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Stress induces substance P in vagal sensory neurons innervating the mouse airways. / Joachim, R A; Cifuentes, L B; Sagach, V; Quarcoo, D; Hagen, E; Arck, P C; Fischer, A; Klapp, B F; Dinh, Q T.
in: CLIN EXP ALLERGY, Jahrgang 36, Nr. 8, 08.2006, S. 1001-10.Publikationen: SCORING: Beitrag in Fachzeitschrift/Zeitung › SCORING: Zeitschriftenaufsatz › Forschung › Begutachtung
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TY - JOUR
T1 - Stress induces substance P in vagal sensory neurons innervating the mouse airways
AU - Joachim, R A
AU - Cifuentes, L B
AU - Sagach, V
AU - Quarcoo, D
AU - Hagen, E
AU - Arck, P C
AU - Fischer, A
AU - Klapp, B F
AU - Dinh, Q T
PY - 2006/8
Y1 - 2006/8
N2 - BACKGROUND: Tachykinins-like substance P (SP) have been shown to play an important role in initiating and perpetuating airway inflammation. Furthermore, they are supposed to be released into tissues in response to stress.OBJECTIVE: The aim of this study was to investigate the effects of stress alone or in combination with allergic airway inflammation on SP expression in sensory neurons innervating the mouse airways.METHODS: Balb/c mice were systemically sensitized to ovalbumin (OVA), followed by allergen aerosol exposure, and compared with non-sensitized controls. Additionally, OVA-sensitized and -challenged and non-sensitized mice were exposed to sound stress. SP expression in airway-specific and overall vagal sensory neurons of the jugular and nodose ganglion complex was analysed using retrograde neuronal tracing in combination with immunohistochemistry. Preprotachykinin A (PPT-A) mRNA, the precursor for SP, was quantified in lung tissue by real-time PCR. Bronchoalveolar lavage (BAL) fluid was obtained, and cell numbers and differentiation were determined.RESULTS: Stress and/or allergic airway inflammation significantly increased SP expression in retrograde-labelled vagal sensory neurons from the mouse lower airways compared with controls [stress: 15.7+/-0.8% (% of retrograde-labelled neurons, mean+/-SEM); allergen: 17.9+/-0.4%; allergen/stress: 13.1+/-0.7% vs. controls: 6.3+/-0.3%]. Similarly, SP expression increased in overall vagal sensory neurons identified by the neuronal marker protein gene product (PGP) 9.5 [stress: 9.3+/-0.6% (% of PGP 9.5-positive neurons, means+/-SEM); allergen: 12.5+/-0.4%; allergen/stress: 10.2+/-0.4% vs. controls: 5.1+/-0.3%]. Furthermore, stress significantly increased PPT-A mRNA expression in lung tissue from OVA-sensitized and -challenged animals, and immune cells were identified as an additional source of SP in the lung by immunohistochemistry. Associated with enhanced neuronal SP expression, a significantly higher number of leucocytes were found in the BAL following allergen exposure. Further, stress significantly increased allergen-induced airway inflammation identified by increased leucocyte numbers in BAL fluids.CONCLUSION: The central event of sound stress leads to the stimulation of SP expression in airway-specific neurons. However, in sensitized stressed mice an additional local source of SP (probably inflammatory cells) might enhance allergic airway inflammation.
AB - BACKGROUND: Tachykinins-like substance P (SP) have been shown to play an important role in initiating and perpetuating airway inflammation. Furthermore, they are supposed to be released into tissues in response to stress.OBJECTIVE: The aim of this study was to investigate the effects of stress alone or in combination with allergic airway inflammation on SP expression in sensory neurons innervating the mouse airways.METHODS: Balb/c mice were systemically sensitized to ovalbumin (OVA), followed by allergen aerosol exposure, and compared with non-sensitized controls. Additionally, OVA-sensitized and -challenged and non-sensitized mice were exposed to sound stress. SP expression in airway-specific and overall vagal sensory neurons of the jugular and nodose ganglion complex was analysed using retrograde neuronal tracing in combination with immunohistochemistry. Preprotachykinin A (PPT-A) mRNA, the precursor for SP, was quantified in lung tissue by real-time PCR. Bronchoalveolar lavage (BAL) fluid was obtained, and cell numbers and differentiation were determined.RESULTS: Stress and/or allergic airway inflammation significantly increased SP expression in retrograde-labelled vagal sensory neurons from the mouse lower airways compared with controls [stress: 15.7+/-0.8% (% of retrograde-labelled neurons, mean+/-SEM); allergen: 17.9+/-0.4%; allergen/stress: 13.1+/-0.7% vs. controls: 6.3+/-0.3%]. Similarly, SP expression increased in overall vagal sensory neurons identified by the neuronal marker protein gene product (PGP) 9.5 [stress: 9.3+/-0.6% (% of PGP 9.5-positive neurons, means+/-SEM); allergen: 12.5+/-0.4%; allergen/stress: 10.2+/-0.4% vs. controls: 5.1+/-0.3%]. Furthermore, stress significantly increased PPT-A mRNA expression in lung tissue from OVA-sensitized and -challenged animals, and immune cells were identified as an additional source of SP in the lung by immunohistochemistry. Associated with enhanced neuronal SP expression, a significantly higher number of leucocytes were found in the BAL following allergen exposure. Further, stress significantly increased allergen-induced airway inflammation identified by increased leucocyte numbers in BAL fluids.CONCLUSION: The central event of sound stress leads to the stimulation of SP expression in airway-specific neurons. However, in sensitized stressed mice an additional local source of SP (probably inflammatory cells) might enhance allergic airway inflammation.
KW - Allergens
KW - Animals
KW - Biomarkers/analysis
KW - Bronchial Hyperreactivity
KW - Bronchoalveolar Lavage Fluid/immunology
KW - Immunohistochemistry/methods
KW - Lung/chemistry
KW - Mice
KW - Mice, Inbred BALB C
KW - Models, Animal
KW - Neural Pathways
KW - Neurons, Afferent/chemistry
KW - Nodose Ganglion/chemistry
KW - Ovalbumin
KW - Protein Precursors/analysis
KW - Respiratory Hypersensitivity/metabolism
KW - Reverse Transcriptase Polymerase Chain Reaction
KW - Stress, Psychological/metabolism
KW - Substance P/analysis
KW - Tachykinins/analysis
KW - Ubiquitin Thiolesterase/analysis
U2 - 10.1111/j.1365-2222.2006.02533.x
DO - 10.1111/j.1365-2222.2006.02533.x
M3 - SCORING: Journal article
C2 - 16911356
VL - 36
SP - 1001
EP - 1010
JO - CLIN EXP ALLERGY
JF - CLIN EXP ALLERGY
SN - 0954-7894
IS - 8
ER -