TRPV1 channels are critical brain inflammation detectors and neuropathic pain biomarkers in mice

Nature Communications

Volumn 8, Issue , 2017, Pages

  Marrone, Maria Cristina ^a,b   Morabito, Annunziato ^a,c   Giustizieri, Michela ^a,b   Chiurchiù, Valerio ^b,d   Leuti, Alessandro ^b   Mattioli, Marzia ^a,b   Marinelli, Sara ^a,e   Riganti, Loredana ^e   Lombardi, Marta ^f   Murana, Emanuele ^c   Totaro, Antonio ^b   Piomelli, Daniele ^g   Ragozzino, Davide ^c,h   Oddi, Sergio ^b,i   Maccarrone, Mauro ^b,d   Verderio, Claudia ^e   Marinelli, Silvia ^a,b  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^e CNR   (Italy)

^f HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^g ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^h IRCCS NEUROMED   (Italy)

ⁱ UNIVERSITY OF TERAMO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; INTERLEUKIN 10; VANILLOID RECEPTOR 1; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

BIOMARKER; BRAIN; CELLS AND CELL COMPONENTS; CHEMORECEPTION; DISABILITY; GENE; GENE EXPRESSION; NERVOUS SYSTEM; RODENT; SENSORY SYSTEM;

ACTION POTENTIAL; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; ASTROCYTE; CELL BODY; CELL COMMUNICATION; CHRONIC PAIN; CINGULATE GYRUS; CONTROLLED STUDY; CORTICAL EXCITABILITY; CYTOPLASM; DENDRITE; ENCEPHALITIS; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOSOME; EXTRACELLULAR SPACE; GLUTAMATERGIC SYNAPSE; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MEMBRANE MICROPARTICLE; MEMBRANE STEADY POTENTIAL; MICROGLIA; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NEUROPATHIC PAIN; NEUROTRANSMISSION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; SPINAL CORD; SPINAL GANGLION; THALAMUS; ANIMAL; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; NEURALGIA; PHYSIOLOGY; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

MUS;

ANIMALS; BIOMARKERS; CELL-DERIVED MICROPARTICLES; ENCEPHALITIS; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROGLIA; NEURALGIA; NEURONS; SYNAPTIC TRANSMISSION; TRPV CATION CHANNELS;

EID: 85026197255     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15292     Document Type: Article

References (74)

1. Caterina, M. J. et al. The capsaicin receptor: A heat-Activated ion channel in the pain pathway. Nature 389, 816-824 (1997).
2. Acs, G., Biro, T., Acs, P., Modarres, S. & Blumberg, P. M. Differential activation and desensitization of sensory neurons by resiniferatoxin. J. Neurosci. 17, 5622-5628 (1997).
3. Bohlen, C. J. et al. A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell 141, 834-845 (2010).
4. Szallasi, A. & Blumberg, P. M. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol. Rev. 51, 159-212 (1999).
5. Van Der Stelt, M. & Di Marzo, V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur. J. Biochem. 271, 1827-1834 (2004).
6. Zygmunt, P. M. et al. Monoacylglycerols activate TRPV1-A link between phospholipase C and TRPV1. PLoS ONE 8, e81618 (2013).
7. Tominaga, M. et al. The cloned capsaicin receptor integrates multiple painproducing stimuli. Neuron 21, 531-543 (1998).
8. Kim, Y. H. et al. TRPV1 in GABAergic interneurons mediates neuropathic mechanical allodynia and disinhibition of the nociceptive circuitry in the spinal cord. Neuron 74, 640-647 (2012).
9. Kim, Y. S. et al. Central terminal sensitization of TRPV1 by descending serotonergic facilitation modulates chronic pain. Neuron 81, 873-887 (2014).
10. Sharif Naeini, R., Witty, M. F., Seguela, P. & Bourque, C. W. An N-Terminal variant of Trpv1 channel is required for osmosensory transduction. Nat. Neurosci. 9, 93-98 (2006).
11. Doyle, M. W., Bailey, T. W., Jin, Y. H. & Andresen, M. C. Vanilloid receptors presynaptically modulate cranial visceral afferent synaptic transmission in nucleus tractus solitarius. J. Neurosci. 22, 8222-8229 (2002).
12. Marinelli, S., Vaughan, C.W., Christie, M. J. & Connor, M. Capsaicin activation of glutamatergic synaptic transmission in the rat locus coeruleus in vitro. J. Physiol. 543, 531-540 (2002).
13. Marinelli, S. et al. Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J. Neurosci. 23, 3136-3144 (2003).
14. Gibson, H. E., Edwards, J. G., Page, R. S., Van Hook, M. J. & Kauer, J. A. TRPV1 channels mediate long-Term depression at synapses on hippocampal interneurons. Neuron 57, 746-759 (2008).
15. Edwards, J. G. TRPV1 in the central nervous system: synaptic plasticity, function, and pharmacological implications. Prog. Drug Res. 68, 77-104 (2014).
16. Cavanaugh, D. J. et al. Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J. Neurosci. 31, 5067-5077 (2011).
17. Mezey, E. et al. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl Acad. Sci. USA 97, 3655-3660 (2000).
18. Toth, A. et al. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 135, 162-168 (2005).
19. Cristino, L. et al. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139, 1405-1415 (2006).
20. Puente, N. et al. The transient receptor potential vanilloid-1 is localized at excitatory synapses in the mouse dentate gyrus. Brain Struct. Funct. 220, 1187-1194 (2014).
21. Chavez, A. E., Chiu, C. Q. & Castillo, P. E. TRPV1 activation by endogenous anandamide triggers postsynaptic long-Term depression in dentate gyrus. Nat. Neurosci. 13, 1511-1518 (2010).
22. Grueter, B. A., Brasnjo, G. & Malenka, R. C. Postsynaptic TRPV1 triggers cell type-specific long-Term depression in the nucleus accumbens. Nat. Neurosci. 13, 1519-1525 (2010).
23. Zschenderlein, C., Gebhardt, C., von Bohlen Und Halbach, O., Kulisch, C. & Albrecht, D. Capsaicin-induced changes in LTP in the lateral amygdala are mediated by TRPV1. PLoS ONE 6, e16116 (2011).
24. Puente, N. et al. Polymodal activation of the endocannabinoid system in the extended amygdala. Nat. Neurosci. 14, 1542-1547 (2011).
25. Kim, S. R., Kim, S. U., Oh, U. & Jin, B. K. Transient receptor potential vanilloid subtype 1 mediates microglial cell death in vivo and in vitro via Ca2+mediated mitochondrial damage and cytochrome c release. J. Immunol. 177, 4322-4329 (2006).
26. Sappington, R. M. & Calkins, D. J. Contribution of TRPV1 to microglia-derived IL-6 and NFkappaB translocation with elevated hydrostatic pressure. Invest. Ophthalmol. Vis. Sci. 49, 3004-3017 (2008).
27. Schilling, T. & Eder, C. Importance of the non-selective cation channel TRPV1 for microglial reactive oxygen species generation. J. Neuroimmunol. 216, 118-121 (2009).
28. Hassan, S. et al. Cannabidiol enhances microglial phagocytosis via transient receptor potential (TRP) channel activation. Br. J. Pharmacol. 171, 2426-2439 (2014).
29. Miyake, T., Shirakawa, H., Nakagawa, T. & Kaneko, S. Activation of mitochondrial transient receptor potential vanilloid 1 channel contributes to microglial migration. Glia 63, 1870-1882 (2015).
30. Park, E. S., Kim, S. R. & Jin, B. K. Transient receptor potential vanilloid subtype 1 contributes to mesencephalic dopaminergic neuronal survival by inhibiting microglia-originated oxidative stress. Brain Res. Bull. 89, 92-96 (2012).
31. Vogt, B. A. Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 6, 533-544 (2005).
32. Prada, I., Furlan, R., Matteoli, M. & Verderio, C. Classical and unconventional pathways of vesicular release in microglia. Glia 61, 1003-1017 (2013).
33. Antonucci, F. et al. Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. EMBO J. 31, 1231-1240 (2012).
34. Evans, J. M. Straightforward Statistics for the Behavioral Sciences (Pacific Grove, CA, Brooks/Cole Publishing, 1996).
35. Patapoutian, A., Tate, S. & Woolf, C. J. Transient receptor potential channels: Targeting pain at the source. Nat. Rev. Drug Discov. 8, 55-68 (2009).
36. Steenland, H. W., Ko, S. W., Wu, L. J. & Zhuo, M. Hot receptors in the brain. Mol. Pain 2, 34 (2006).
37. Mallet, C. et al. TRPV1 in brain is involved in acetaminophen-induced antinociception. PLoS ONE 5, e12748 (2010).
38. Palazzo, E. et al. Moving towards supraspinal TRPV1 receptors for chronic pain relief. Mol. Pain 6, 66 (2010).
39. Giordano, C. et al. TRPV1-dependent and-independent alterations in the limbic cortex of neuropathic mice: impact on glial caspases and pain perception. Cereb. Cortex 22, 2495-2518 (2012).
40. Jurik, A., Ressle, A., Schmid, R. M., Wotjak, C. T. & Thoeringer, C. K. Supraspinal TRPV1 modulates the emotional expression of abdominal pain. Pain 155, 2153-2160 (2014).
41. Kerckhove, N. et al. Ca(v)3.2 calcium channels: The key protagonist in the supraspinal effect of paracetamol. Pain 155, 764-772 (2014).
42. Silva, M. et al. Endovanilloid control of pain modulation by the rostroventromedial medulla in an animal model of diabetic neuropathy. Neuropharmacology 107, 49-57 (2016).
43. Pascual, O., Ben Achour, S., Rostaing, P., Triller, A. & Bessis, A. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc. Natl Acad. Sci. USA 109, E197-E205 (2012).
44. Zhang, J. et al. Microglial CR3 activation triggers long-Term synaptic depression in the hippocampus via NADPH oxidase. Neuron 82, 195-207 (2014).
45. Riazi, K. et al. Microglia-dependent alteration of glutamatergic synaptic transmission and plasticity in the hippocampus during peripheral inflammation. J. Neurosci. 35, 4942-4952 (2015).
46. Ma, L., Nagai, J. & Ueda, H. Microglial activation mediates de novo lysophosphatidic acid production in a model of neuropathic pain. J. Neurochem. 115, 643-653 (2010).
47. Velasco, M., O'Sullivan, C. & Sheridan, G. K. Lysophosphatidic acid receptors (LPARs): potential targets for the treatment of neuropathic pain. Neuropharmacology 113, 608-617 (2016).
48. Nieto-Posadas, A. et al. Lysophosphatidic acid directly activates TRPV1 through a C-Terminal binding site. Nat. Chem. Biol. 8, 78-85 (2012).
49. Tikka, T. M. & Koistinaho, J. E. Minocycline provides neuroprotection against N-methyl-D-Aspartate neurotoxicity by inhibiting microglia. J. Immunol. 166, 7527-7533 (2001).
50. Plane, J. M., Shen, Y., Pleasure, D. E. & Deng, W. Prospects for minocycline neuroprotection. Arch. Neurol. 67, 1442-1448 (2010).
51. Henneberger, C., Papouin, T., Oliet, S. H. & Rusakov, D. A. Long-Term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236 (2010).
52. Gabrielli, M. et al. Active endocannabinoids are secreted on extracellular membrane vesicles. EMBO Rep. 16, 213-220 (2015).
53. Verderio, C. et al. Myeloid microvesicles are a marker and therapeutic target for neuroinflammation. Ann. Neurol. 72, 610-624 (2012).
54. Bianco, F. et al. Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J. Immunol. 174, 7268-7277 (2005).
55. Bach, A. et al. Benzoxazolone carboxamides as potent acid ceramidase inhibitors: synthesis and structure-Activity relationship (SAR) studies. J. Med. Chem. 58, 9258-9272 (2015).
56. Bianco, F. et al. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J. 28, 1043-1054 (2009).
57. Amantini, C. et al. Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J. Neurochem. 102, 977-990 (2007).
58. Streit, W. J., Mrak, R. E. & Griffin, W. S. Microglia and neuroinflammation: A pathological perspective. J. Neuroinflammation 1, 14 (2004).
59. Kettenmann, H., Hanisch, U. K., Noda, M. & Verkhratsky, A. Physiology of microglia. Physiol. Rev. 91, 461-553 (2011).
60. Turrigiano, G. G. The self-Tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422-435 (2008).
61. Kauer, J. A. & Gibson, H. E. Hot flash: TRPV channels in the brain. Trends Neurosci. 32, 215-224 (2009).
62. Ferrini, F. & De Koninck, Y. Microglia control neuronal network excitability via BDNF signalling. Neural Plast. 2013, 429815 (2013).
63. Chávez, A. E., Hernández, V. M., Rodenas-Ruano, A., Chan, C. S. & Castillo, P. E. Compartment-specific modulation of GABAergic synaptic transmission by TRPV1 channels in the dentate gyrus. J. Neurosci. 34, 16621-16629 (2014).
64. Houdebine, L. M. & Attal, J. Internal ribosome entry sites (IRESs): reality and use. Transgenic Res. 8, 157-177 (1999).
65. Mizuguchi, H., Xu, Z., Ishii-Watabe, A., Uchida, E. & Hayakawa, T. IRESdependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol. Ther. 1, 376-382 (2000).
66. Witting, A., Walter, L., Wacker, J., Möller, T. & Stella, N. P2X7 receptors control 2-Arachidonoylglycerol production by microglial cells. Proc. Natl Acad. Sci. USA 101, 3214-3219 (2004).
67. Raboune, S. et al. Novel endogenous N-Acyl amides activate TRPV1-4 receptors, BV-2 microglia, and are regulated in brain in an acute model of inflammation. Front. Cell Neurosci. 8, 195 (2014).
68. Schilling, T., Stock, C., Schwab, A. & Eder, C. Functional importance of Ca2+activated K+ channels for lysophosphatidic acid-induced microglial migration. Eur. J. Neurosci. 19, 1469-1474 (2004).
69. Nguyen, D. B. et al. Characterization of microvesicles released from human red blood cells. Cell Physiol. Biochem. 38, 1085-1099 (2016).
70. Marinelli, S. et al. N-Arachidonoyl-dopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32, 298-308 (2007).
71. Maione, S. et al. TRPV1 channels control synaptic plasticity in the developing superior colliculus. J Physiol. 587(Pt 11): 2521-2535 (2009).
72. Fogaça, M. V., Aguiar, D. C., Moreira, F. A. & Guimaraes, F. S. The endocannabinoid and endovanilloid systems interact in the rat prelimbic medial prefrontal cortex to control anxiety-like behaviour. Neuropharmacology 63, 202-210 (2012).
73. Casarotto, P. C. et al. Opposing roles for cannabinoid receptor type-1 (CB(1)) and transient receptor potential vanilloid type-1 channel (TRPV1) on the modulation of panic-like responses in rats. Neuropsychopharmacology 37, 478-486 (2012).
74. Maione, S. et al. Functional Interaction Between TRPV1 and-Opioid Receptors in the Descending Antinociceptive Pathway Activates Glutamate Transmission and Induces Analgesia. J Neurophysiol 101, 2411-2422 (2009).