TY - JOUR
AU - Funk, K.
AU - Woitecki, A.
AU - Franjic-Würtz, C.
AU - Gensch, T.
AU - Möhrlen, F.
AU - Frings, S.
TI - Modulation of chloride homeostasis by inflammatory mediators in dorsal root ganglion neurons
JO - Molecular pain
VL - 4
SN - 1744-8069
CY - London
PB - BioMed Central
M1 - PreJuSER-238
SP - 32 - 43
PY - 2008
N1 - This work was supported by the Deutsche Forschungsgemeinschaft (Fr 937/6).
AB - Chloride currents in peripheral nociceptive neurons have been implicated in the generation of afferent nociceptive signals, as Cl- accumulation in sensory endings establishes the driving force for depolarizing, and even excitatory, Cl- currents. The intracellular Cl- concentration can, however, vary considerably between individual DRG neurons. This raises the question, whether the contribution of Cl- currents to signal generation differs between individual afferent neurons, and whether the specific Cl- levels in these neurons are subject to modulation. Based on the hypothesis that modulation of the peripheral Cl- homeostasis is involved in the generation of inflammatory hyperalgesia, we examined the effects of inflammatory mediators on intracellular Cl- concentrations and on the expression levels of Cl- transporters in rat DRG neurons.We developed an in vitro assay for testing how inflammatory mediators influence Cl- concentration and the expression of Cl- transporters. Intact DRGs were treated with 100 ng/ml NGF, 1.8 microM ATP, 0.9 microM bradykinin, and 1.4 microM PGE2 for 1-3 hours. Two-photon fluorescence lifetime imaging with the Cl--sensitive dye MQAE revealed an increase of the intracellular Cl- concentration within 2 hours of treatment. This effect coincided with enhanced phosphorylation of the Na+-K+-2Cl- cotransporter NKCC1, suggesting that an increased activity of that transporter caused the early rise of intracellular Cl- levels. Immunohistochemistry of NKCC1 and KCC2, the main neuronal Cl- importer and exporter, respectively, exposed an inverse regulation by the inflammatory mediators. While the NKCC1 immunosignal increased, that of KCC2 declined after 3 hours of treatment. In contrast, the mRNA levels of the two transporters did not change markedly during this time. These data demonstrate a fundamental transition in Cl- homeostasis toward a state of augmented Cl- accumulation, which is induced by a 1-3 hour treatment with inflammatory mediators.Our findings indicate that inflammatory mediators impact on Cl- homeostasis in DRG neurons. Inflammatory mediators raise intracellular Cl- levels and, hence, the driving force for depolarizing Cl- efflux. These findings corroborate current concepts for the role of Cl- regulation in the generation of inflammatory hyperalgesia and allodynia. As the intracellular Cl- concentration rises in DRG neurons, afferent signals can be boosted by excitatory Cl- currents in the presynaptic terminals. Moreover, excitatory Cl- currents in peripheral sensory endings may also contribute to the generation or modulation of afferent signals, especially in inflamed tissue.
KW - Adenosine Triphosphate: pharmacology
KW - Animals
KW - Bradykinin: pharmacology
KW - Chlorides: metabolism
KW - Dinoprostone: pharmacology
KW - Ganglia, Spinal: cytology
KW - Ganglia, Spinal: drug effects
KW - Ganglia, Spinal: metabolism
KW - Homeostasis: drug effects
KW - Homeostasis: physiology
KW - Inflammation Mediators: pharmacology
KW - Nerve Growth Factors: pharmacology
KW - Neurons: drug effects
KW - Neurons: metabolism
KW - Organ Culture Techniques
KW - Rats
KW - Chlorides (NLM Chemicals)
KW - Inflammation Mediators (NLM Chemicals)
KW - Nerve Growth Factors (NLM Chemicals)
KW - Dinoprostone (NLM Chemicals)
KW - Adenosine Triphosphate (NLM Chemicals)
KW - Bradykinin (NLM Chemicals)
KW - J (WoSType)
LB - PUB:(DE-HGF)16
C6 - pmid:18700020
C2 - pmc:PMC2526990
UR - <Go to ISI:>//WOS:000258959400001
DO - DOI:10.1186/1744-8069-4-32
UR - https://juser.fz-juelich.de/record/238
ER -