Long-term incubation with CXCL2, but not with CXCL1, alters the kinetics of TRPV1 receptors in cultured dorsal root ganglia neurons
Keywords:
CXCL1, CXCL2, TRPV1, dorsal root ganglia neuronsAbstract
CXCL1 and CXCL2 are homologous chemokines that can be upregulated in different pathological conditions, affecting among other targets, neuronal ionic channels or receptors. TRPV1 is a polymodal nociceptor expressed in both dorsal root and trigeminal ganglia neurons. According to existing data, short-term incubation with CXCL1 can reduce TRPV1 desensitization, however, the long-term modulatory effect of both CXCL1 and CXCL2 on this receptor is less known. In the present study we investigated the influence of overnight incubation with 1.5 nM CXCL1 or CXCL2 on the functioning of TRPV1 receptors expressed in cultured dorsal root ganglia neurons. Calcium imaging and patch-clamp recordings showed that under the same experimental conditions and at the same concentration, only CXCL2 significantly decreased the TRPV1 current and increased its desensitization rate, whereas CXCL1 had no effect. This study proposes a different contribution of CXCL1 and CXCL2 to the modulation of TRPV1-mediated processes, in spite of their highly homologous sequence.
Received: May 13, 2016; Revised: July 12, 2016; Accepted: July 25, 2016; Published online: August 17; 2016
How to cite this article: Deftu AT, Deftu AF, Ristoiu V. Long-term incubation with CXCL2, but not with CXCL1, alters the kinetics of TRPV1 receptors in cultured dorsal root ganglia neurons. Arch Biol Sci. 2017;69(1):53-9.
Downloads
References
Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med. 2006;354(6):610-21.
Semple BD, Kossmann T, Morganti-Kossmann MC. Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J Cereb Blood F Met. 2010;30(3):459-73.
Trettel F, Di Bartolomeo S, Lauro C, Catalano M, Ciotti MT, Limatola C. Ligand-independent CXCR2 dimerization. J Biol Chem. 2003;278(42):40980-8.
Acosta JC, O’Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, d’Adda di Fagagna F, Bernard D, Hernando E GJ. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell. 2008;133:1006-18.
Bolitho C, Hahn MA, Baxter RC, Marsh DJ. The chemokine CXCL1 induces proliferation in epithelial ovarian cancer cells by transactivation of the epidermal growth factor receptor. Endocr Relat Cancer. 2010;17(4):929-40.
Dhawan P, Richmond A. Role of CXCL1 in tumorigenesis of melanoma. J Leukoc Biol. 2002;72(1):9-18.
Kuo PL, Shen KH, Hung SH, Hsu YL. CXCL1/GROα increases cell migration and invasion of prostate cancer by decreasing fibulin-1 expression through NF-κB/HDAC1 epigenetic regulation. Carcinogenesis. 2012;33(12):2477-87.
Filipovic R, Zecevic N. The effect of CXCL1 on human fetal oligodendrocyte progenitor cells. Glia. 2008;56(1):1-15.
Cao DL, Zhang ZJ, Xie RG, Jiang BC, Ji RR, Gao YJ. Chemokine CXCL1 enhances inflammatory pain and increases NMDA receptor activity and COX-2 expression in spinal cord neurons via activation of CXCR2. Exp Neurol. 2014;261:328-36.
Chen G, Park CK, Xie RG, Berta T, Nedergaard M, Ji RR. Connexin-43 induces chemokine release from spinal cord astrocytes to maintain late-phase neuropathic pain in mice. Brain. 2014;137(8):2193-209.
Xie WR, Deng H, Li H, Bowen TL, Strong JA, Zhang J-M. Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience. 2006;142(3):809-22.
Zhang Z-J, Cao D-L, Zhang X, Ji R-R, Gao Y-J. Chemokine contribution to neuropathic pain: respective induction of CXCL1 and CXCR2 in spinal cord astrocytes and neurons. Pain. 2013:154(10):2185-97.
Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SPH, Buneman OP, Davenport AP, McGrath JC, Peters JA, Southan C, Spedding M, Yu W, Harmar AJ. The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucleic Acids Res. 2014;42:1098-106.
Call DR, Nemzek JA, Ebong SJ, Bolgos GR, Newcomb DE, Wollenberg GK, Remick DG. Differential local and systemic regulation of the murine chemokines KC and MIP2. Shock. 2001;15(4):278-84.
Bhardwaj D, Náger M, Camats J, David M, Benguria A, Dopazo A, Cantí C, Herreros J. Chemokines induce axon outgrowth downstream of Hepatocyte Growth Factor and TCF/β-catenin signaling. Front Cell Neurosci. 2013;7:52.
Cao Y, Chen C, Weatherbee JA, Tsang M, Folkman J. gro-beta, a -C-X-C- chemokine, is an angiogenesis inhibitor that suppresses the growth of Lewis lung carcinoma in mice. J Exp Med. 1995;182(6):2069-77.
Kiguchi N, Kobayashi Y, Maeda T, Fukazawa Y, Tohya K, Kimura M, Kishioka S. Epigenetic augmentation of the macrophage inflammatory protein 2/C-X-C chemokine receptor type 2 axis through histone H3 acetylation in injured peripheral nerves elicits neuropathic pain. J Pharmacol Exp Ther. 2012;340(3):577-87.
Lax P, Limatola C, Fucile S, Trettel F, Di Bartolomeo S, Renzi M, Ragozzino DEF. Chemokine receptor CXCR2 regulates the functional properties of AMPA-type glutamate receptor GluR1 in HEK cells. J Neuroimmunol. 2002;129:66-73.
De Paola M, Buanne P, Biordi L, Bertini R, Ghezzi P, Mennini T. Chemokine MIP-2/CXCL2, acting on CXCR2, induces motor neuron death in primary cultures. Neuroimmunomodulat. 2007;14(6):310-6.
Kalehua A, Nagel J, Whelchel L, Gides J, Pyle R, Smith R, Kusiak J, Taub D. Monocyte chemoattractant protein-1 and macrophage inflammatory protein-2 are involved in both excitotoxin-induced neurodegeneration and regeneration. Exp Cell Res. 2004;297(1):197-211.
Vriens J, Appendino G, Nilius B. Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol. 2009;75(6):1262-79.
Kao DJ, Li AH, Chen JC, Luo RS, Chen YL, Lu JC, Wang HL. CC chemokine ligand 2 upregulates the current density and expression of TRPV1 channels and Nav1.8 sodium channels in dorsal root ganglion neurons. J Neuroinflamm. 2012;9:189.
Malek N, Pajak A, Kolosowska N, Kucharczyk M, Starowicz K. The importance of TRPV1-sensitisation factors for the development of neuropathic pain. Mol Cell Neurosci. 2015;65:1-10.
Schaible HG. Nociceptive neurons detect cytokines in arthritis. Arthritis Res Ther. 2014;16(5):470.
Zhang N, Inan S, Inan S, Cowan A, Sun R, Wang JM, Rogers TJ, Caterina M, Oppenheim JJ. A proinflammatory chemokine, CCL3, sensitizes the heat- and capsaicin-gated ion channel TRPV1. Proc Natl Acad Sci U S A. 2005;102(12):4536-41.
Wang JG, Strong JA, Xie W, Yang RH, Coyle DE, Wick DM, Dorsey ED, Zhang JM. The chemokine CXCL1/growth related oncogene increases sodium currents and neuronal excitability in small diameter sensory neurons. Mol Pain. 2008;4:38.
Yang RH, Strong JA, Zhang JM. NF-kappaB mediated enhancement of potassium currents by the chemokine CXCL1/growth related oncogene in small diameter rat sensory neurons. Mol Pain. 2009;5:26.
Dong F, Du YR, Xie W, Strong JA, He XJ, Zhang JM. Increased function of the TRPV1 channel in small sensory neurons after local inflammation or in vitro exposure to the pro-inflammatory cytokine GRO/KC. Neurosci Bull. 2012;28:155-64.
Bich-Hoai TT, Marin A, Dinu C, Banciu D, Maria-Luiza F, Ristoiu V. Hypoxia and high glucose activate tetrodotoxin-resistant Na(+) currents through PKA and PKC. Acta Neurobiol Exp (Wars). 2010;70(4):351-61.
Ristoiu V, Shibasaki K, Uchida K, Zhou Y, Ton BHT, Flonta ML, Tominaga M. Hypoxia-induced sensitization of transient receptor potential vanilloid 1 involves activation of hypoxia-inducible factor-1 alpha and PKC. Pain. 2011;152(4):936-45.
Breese NM, George AC, Pauers LE, Stucky CL. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain. 2005;115(1):37-49.
Qin X, Wan Y, Wang X. CCL2 and CXCL1 trigger calcitonin gene-related peptide release by exciting primary nociceptive neurons. J Neurosci Res. 2005;82(1):51-62.
Xu Y, Zhang J, Li L, Ye Z, Zhang Y, Gao X, Li F, Yan X, Liu Z, Liu L, Cao X. Complex regulation of capsaicin on intracellular second messengers by calcium dependent and independent mechanisms in primary sensory neurons. Neurosci Lett. 2012;517(1):30-5.
Price TJ, Jeske NA, Flores CM, Hargreaves KM. Pharmacological interactions between calcium/calmodulin-dependent kinase II α and TRPV1 receptors in rat trigeminal sensory neurons. Neurosci Lett. 2005;389(2):94-8.
Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE. Ca2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol. 2004;123(1):53-62.
Lishko P V., Procko E, Jin X, Phelps CB, Gaudet R. The Ankyrin Repeats of TRPV1 Bind Multiple Ligands and Modulate Channel Sensitivity. Neuron. 2007;54(6):905-18.
Nagy I, Sántha P, Jancsó G, Urbán L. The role of the vanilloid (capsaicin) receptor (TRPV1) in physiology and pathology. Eur J Pharmacol. 2004;500(1):351-69.
Sawynok J. Topical and peripherally acting analgesics. Pharmacol Rev. 2003;55(1):1-20.
Downloads
Published
How to Cite
Issue
Section
License
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.
