Human sensory neurons: Membrane properties and sensitization by inflammatory mediators

Pain

Volumn 155, Issue 9, 2014, Pages 1861-1870

  Davidson, Steve ^a   Copits, Bryan A ^a   Zhang, Jingming ^b   Page, Guy ^b   Ghetti, Andrea ^b   Gereau, Robert W ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b ANABIOS CORPORATION   (United States)

Author keywords

Bradykinin; Dorsal root ganglia; Human; Itch; Nociception; Pain; Sensitization

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALLYL ISOTHIOCYANATE; BRADYKININ; CHLOROQUINE; HISTAMINE; PROSTAGLANDIN E2; CAPSAICIN;

ADOLESCENT; ADULT; AFTERHYPERPOLARIZATION; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; CLINICAL ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MEDIATOR; MEMBRANE STEADY POTENTIAL; NERVE POTENTIAL; NEUROPHYSIOLOGY; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; PRURITUS; RODENT; SENSITIZATION; SENSORY NERVE CELL; SPINAL GANGLION; WHOLE CELL PATCH CLAMP; YOUNG ADULT; ACTION POTENTIAL; DRUG EFFECTS; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ADOLESCENT; BRADYKININ; CAPSAICIN; CELL MEMBRANE; CHLOROQUINE; DINOPROSTONE; FEMALE; GANGLIA, SPINAL; HISTAMINE; HUMANS; MALE; PATCH-CLAMP TECHNIQUES; SENSORY RECEPTOR CELLS; YOUNG ADULT;

EID: 84926421971     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.06.017     Document Type: Article

References (56)

1. Anand U, Facer P, Yiangou Y, Sinisi M, Fox M, McCarthy T, Bountra C, Korchev YE, Anand P. Angiotensin II type 2 receptor (AT2 R) localization and antagonistmediated inhibition of capsaicin responses and neurite outgrowth in human and rat sensory neurons. Eur J Pain 2013;17:1012-26.
2. Anand U, Otto WR, Casula MA, Day NC, Davis JB, Bountra C, Birch R, Anand P. The effect of neurotrophic factors on morphology, TRPV1 expression and capsaicin responses of cultured human DRG sensory neurons. Neurosci Lett 2006;399:51-6.
3. Anand U, Otto WR, Sanchez-Herrera D, Facer P, Yiangou Y, Korchev Y, Birch R, Benham C, Bountra C, Chessell IP, Anand P. Cannabinoid receptor CB2 localisation and agonist-mediated inhibition of capsaicin responses in human sensory neurons. PAIN 2008;138:667-80.
4. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 2004;41:849-57.
5. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009;139:267-84.
6. Baumann TK, Burchiel KJ, Ingram SL, Martenson ME. Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH. PAIN 1996;65:31-8.
7. Baumann TK, Chaudhary P, Martenson ME. Background potassium channel block and TRPV1 activation contribute to proton depolarization of sensory neurons from humans with neuropathic pain. Eur J Neurosci 2004;19:1343-51.
8. Bennett GJ. What is spontaneous pain and who has it? J Pain 2012;13:921-9.
9. Bhave G, Gereau IV RW. Posttranslational mechanisms of peripheral sensitization. J Neurobiol 2004;61:88-106.
10. Blair NT, Bean BP. Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTXresistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 2002;22:10277-90.
11. Boada MD, Woodbury CJ. Physiological properties of mouse skin sensory neurons recorded intracellularly in vivo: temperature effects on somal membrane properties. J Neurophysiol 2007;98:668-80.
12. Cesare P, Dekker LV, Sardini A, Parker PJ, McNaughton PA. Specific involvement of PKC-epsilon in sensitization of the neuronal response to painful heat. Neuron 1999;23:617-24.
13. Chen J, Zhang XF, Kort ME, Huth JR, Sun C, Miesbauer LJ, Cassar SC, Neelands T, Scott VE, Moreland RB, Reilly RM, Hajduk PJ, Kym PR, Hutchins CW, Faltynek CR. Molecular determinants of species-specific activation or blockade of TRPA1 channels. J Neurosci 2008;28:5063-71.
14. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 2001;411:957-62.
15. Cordoba-Rodriguez R, Moore KA, Kao JP, Weinreich D. Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons. Proc Natl Acad Sci USA 1999;96:7650-7.
16. Craig AD. A rat is not a monkey is not a human: comment on Mogil (Nat Rev Neurosci 2009;10:283-94). Nat Rev Neurosci 2009;10:466.
17. de la Roche J, Eberhardt MJ, Klinger AB, Stanslowsky N, Wegner F, Koppert W, Reeh PW, Lampert A, Fischer MJ, Leffler A. The molecular basis for speciesspecific activation of human TRPA1 protein by protons involves poorly conserved residues within transmembrane domains 5 and 6. J Biol Chem 2013;288:20280-92.
18. Dib-Hajj SD, Tyrrell L, Cummins TR, Black JA, Wood PM, Waxman SG. Two tetrodotoxin-resistant sodium channels in human dorsal root ganglion neurons. FEBS Lett 1999;462:117-20.
19. Djouhri L, Bleazard L, Lawson SN. Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones. J Physiol 1998;513:857-72.
20. Dong X, Han S, Zylka MJ, Simon MI, Anderson DJ. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 2001;106:619-32.
21. Dray A, Perkins M. Bradykinin and inflammatory pain. Trends Neurosci 1993;16:99-104.
22. Fang X, Djouhri L, McMullan S, Berry C, Waxman SG, Okuse K, Lawson SN. Intense isolectin-B4 binding in rat dorsal root ganglion neurons distinguishes C-fiber nociceptors with broad action potentials and high Nav1.9 expression. J Neurosci 2006;26:7281-92.
23. Gold MS, Dastmalchi S, Levine JD. Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 1996;71:265-75.
24. Han SK, Mancino V, Simon MI. Phospholipase Cbeta 3 mediates the scratching response activated by the histamine H1 receptor on C-fiber nociceptive neurons. Neuron 2006;52:691-703.
25. Harper AA, Lawson SN. Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 1985;359:31-46.
26. Holford LC, Case P, Lawson SN. Substance P, Neurofilament, peripherin and SSEA4 immunocytochemistry of human dorsal root ganglion neurons obtained from post-mortem tissue: a quantitative morphometric analysis. J Neurocytol 1994;23:577-89.
27. Ingram SL, Martenson ME, Baumann TK. Responses of cultured adult monkey trigeminal ganglion neurons to capsaicin. NeuroReport 1993;4:460-2.
28. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 2004;427:260-5.
29. Kajekar R, Myers AC. Effect of bradykinin on membrane properties of guinea pig bronchial parasympathetic ganglion neurons. Am J Physiol Lung Cell Mol Physiol 2000;278:L485-91.
30. Liu Q, Tang Z, Surdenikova L, Kim S, Patel KN, Kim A, Ru F, Guan Y, Weng HJ, Geng Y, Undem BJ, Kollarik M, Chen ZF, Anderson DJ, Dong X. Sensory neuronspecific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 2009;139:1353-65.
31. Maddox FN, Valeyev AY, Poth K, Holohean AM, Wood PM, Davidoff RA, Hackman JC, Luetje CW. GABAA receptor subunit mRNA expression in cultured embryonic and adult human dorsal root ganglion neurons. Brain Res Dev 2004;149:143-51.
32. Martic-Kehl MI, Schibli R, Schubiger PA. Can animal data predict human outcome? Problems and pitfalls of translational animal research. Eur J Nucl Med Mol Imaging 2012;39:1492-6.
33. McCarthy PW, Lawson SN. Differing action potential shapes in rat dorsal root ganglion neurones related to their substance P and calcitonin gene-related peptide immunoreactivity. J Comp Neurol 1997;388:541-9.
34. Mogil JS. Animal models of pain: progress and challenges. Nat Rev Neurosci 2009;10:283-94.
35. Nicol GD, Vasko MR, Evans AR. Prostaglandins suppress an outward potassium current in embryonic rat sensory neurons. J Neurophysiol 1997;77:167-76.
36. Nicolson TA, Bevan S, Richards CD. Characterisation of the calcium responses to histamine in capsaicin-sensitive and capsaicin-insensitive sensory neurones. Neuroscience 2002;110:329-38.
37. Nieminen K, Suarez-Isla BA, Rapoport SI. Electrical properties of cultured dorsal root ganglion neurons from normal and trisomy 21 human fetal tissue. Brain Res 1988;474:246-54.
38. Perel P, Roberts I, Sena E, Wheble P, Briscoe C, Sandercock P, Macleod M, Mignini LE, Jayaram P, Khan KS. Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ 2007;334:197.
39. Ritter AM, Mendell LM. Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J Neurophysiol 1992;68:2033-41.
40. Schmelz M, Schmidt R, Weidner C, Hilliges M, Torebjork HE, Handwerker HO. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J Neurophysiol 2003;89:2441-8.
41. Scott BS, Petit TL, Becker LE, Edwards BA. Electric membrane properties of human DRG neurons in cell culture and the effect of high K medium. Brain Res 1979;178:529-44.
42. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, Richards DR, McDonald-Smith GP, Gao H, Hennessy L, Finnerty CC, Lopez CM, Honari S, Moore EE, Minei JP, Cuschieri J, Bankey PE, Johnson JL, Sperry J, Nathens AB, Billiar TR, West MA, Jeschke MG, Klein MB, Gamelli RL, Gibran NS, Brownstein BH, Miller-Graziano C, Calvano SE, Mason PH, Cobb JP, Rahme LG, Lowry SF, Maier RV, Moldawer LL, Herndon DN, Davis RW, Xiao W, Tompkins RG. Inflammation, host response to injury LSCRP. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 2013;110:3507-12.
43. Serrano A, Mo G, Grant R, Pare M, O'Donnell D, Yu XH, Tomaszewski MJ, Perkins MN, Seguela P, Cao CQ. Differential expression and pharmacology of native P2X receptors in rat and primate sensory neurons. J Neurosci 2012;32:11890-6.
44. Stucky CL, Dubin AE, Jeske NA, Malin SA, McKemy DD, Story GM. Roles of transient receptor potential channels in pain. Brain Res Rev 2009;60:2-23.
45. Stucky CL, Lewin GR. Isolectin B(4)-positive and-negative nociceptors are functionally distinct. J Neurosci 1999;19:6497-505.
46. Sugiura T, Tominaga M, Katsuya H, Mizumura K. Bradykinin lowers the threshold temperature for heat activation of vanilloid receptor 1. J Neurophysiol 2002;88:544-8.
47. Than JY, Li L, Hasan R, Zhang X. Excitation and modulation of TRPA1, TRPV1, and TRPM8 channel-expressing sensory neurons by the pruritogen chloroquine. J Biol Chem 2013;288:12818-27.
48. Usachev YM, DeMarco SJ, Campbell C, Strehler EE, Thayer SA. Bradykinin and ATP accelerate Ca(2+) efflux from rat sensory neurons via protein kinase C and the plasma membrane Ca(2+) pump isoform 4. Neuron 2002;33:113-22.
49. Valeyev AY, Hackman JC, Holohean AM, Wood PM, Katz JL, Davidoff RA. GABAInduced Cl-current in cultured embryonic human dorsal root ganglion neurons. J Neurophysiol 1999;82:1-9.
50. Valeyev AY, Hackman JC, Wood PM, Davidoff RA. Pharmacologically novel GABA receptor in human dorsal root ganglion neurons. J Neurophysiol 1996;76:3555-8.
51. van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, O'Collins V, Macleod MR. Can animal models of disease reliably inform human studies? PLoS Med 2010;7:e1000245.
52. Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 2001;534:813-25.
53. Vierck CJ, Hansson PT, Yezierski RP. Clinical and pre-clinical pain assessment: are we measuring the same thing? PAIN 2008;135:7-10.
54. Waddell PJ, Lawson SN. Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. Neuroscience 1990;36:811-22.
55. White FA, Bhangoo SK, Miller RJ. Chemokines: integrators of pain and inflammation. Nat Rev Drug Discov 2005;4:834-44.
56. Zylka MJ, Dong X, Southwell AL, Anderson DJ. Atypical expansion in mice of the sensory neuron-specific Mrg G protein-coupled receptor family. Proc Natl Acad Sci USA 2003;100:10043-8.