TRPV1 Unlike TRPV2 Is Restricted to a Subset of Mechanically Insensitive Cutaneous Nociceptors Responding to Heat

Journal of Pain

Volumn 9, Issue 4, 2008, Pages 298-308

  Lawson, Jeffrey J ^a   McIlwrath, Sabrina L ^a   Woodbury, C Jeffery ^a   Davis, Brian M ^a   Koerber, H Richard ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

dorsal root ganglion; Mouse; sensory neuron; skin; TRP channel

Indexed keywords

VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 2;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEAT SENSITIVITY; HEAT TRANSFER; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MECHANICAL STIMULATION; MOUSE; NOCICEPTIVE RECEPTOR; NONHUMAN; NONMYELINATED NERVE; PAIN; SENSORY NERVE CELL;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM CHANNELS; DISEASE MODELS, ANIMAL; GANGLIA, SPINAL; HEAT; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MECHANORECEPTORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; NEURONS, AFFERENT; NOCICEPTORS; ORGAN CULTURE TECHNIQUES; PAIN; SKIN; TEMPERATURE SENSE; TRPV CATION CHANNELS;

EID: 40949151615     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2007.12.001     Document Type: Article

References (36)

1. Baumann T.K., Simone D.A., Shain C.N., and LaMotte R.H. Neurogenic hyperalgesia: The search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J Neurophysiol 66 (1991) 212-227
2. Breese N.M., George A.C., Pauers L.E., and Stucky C.L. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 115 (2005) 37-49
3. Cain D.M., Khasabov S.G., and Simone D.A. Response properties of mechanoreceptors and nociceptors in mouse glabrous skin: An in vivo study. J Neurophysiol 85 (2001) 1561-1574
4. Campbell J.N., Meyer R.A., and LaMotte R.H. Sensitization of myelinated nociceptive afferents that innervate monkey hand. J Neurophysiol 42 (1979) 1669-1679
5. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
6. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., and Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398 (1999) 436-441
7. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
8. Christianson J.A., McIlwrath S.L., Koerber H.R., and Davis B.M. Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 140 (2006) 247-257
9. Colbert H.A., Smith T.L., and Bargmann C.I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17 (1997) 8259-8269
10. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Clapham C., Atkinson K., Hughes S.A., Rance K., Grau E., Harper A.J., Pugh P.L., Rogers D.C., Bingham S., Randall A., and Sheardown S.A. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000) 183-187
11. Fitzgerald M., and Lynn B. The sensitization of high threshold mechanoreceptors with myelinated axons by repeated heating. J Physiol 265 (1977) 549-563
12. Galoyan S.M., Petruska J.C., and Mendell L.M. Mechanisms of sensitization of the response of single dorsal root ganglion cells from adult rat to noxious heat. Eur J Neurosci 18 (2003) 535-541
13. Garcia-Anoveros J., and Corey D.P. The molecules of mechanosensation. Annu Rev Neurosci 20 (1997) 567-594
14. Goodman M.B., and Schwarz E.M. Transducing touch in Caenorhabditis elegans. Annu Rev Physiol 65 (2003) 429-452
15. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Hogestatt E.D., Meng I.D., and Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 (2004) 260-265
16. Jordt S.E., McKemy D.D., and Julius D. Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13 (2003) 487-492
17. Koerber H.R., Druzinsky R.E., and Mendell L.M. Properties of somata of spinal dorsal root ganglion cells differ according to peripheral receptor innervated. J Neurophysiol 60 (1988) 1584-1596
18. Koltzenburg M., Stucky C.L., and Lewin G.R. Receptive properties of mouse sensory neurons innervating hairy skin. J Neurophysiol 78 (1997) 1841-1850
19. Kress M., Koltzenburg M., Reeh P.W., and Handwerker H.O. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68 (1992) 581-595
20. Lawson S.N. Peptides and cutaneous polymodal nociceptor neurones. Prog Brain Res 113 (1996) 369-385
21. Lawson S.N. Phenotype and function of somatic primary afferent nociceptive neurones with C-, Adelta- or Aalpha/beta-fibres. Exp Physiol 87 (2002) 239-244
22. Lynn B., and Carpenter S.E. Primary afferent units from the hairy skin of the rat hind limb. Brain Res 238 (1982) 29-43
23. Lynn B., and Shakhanbeh J. Properties of A delta high threshold mechanoreceptors in the rat hairy and glabrous skin and their response to heat. Neurosci Lett 85 (1988) 71-76
24. Orstavik K., Weidner C., Schmidt R., Schmelz M., Hilliges M., Jorum E., Handwerker H., and Torebjork E. Pathological C-fibres in patients with a chronic painful condition. Brain 126 (2003) 567-578
25. Petruska J.C., Napaporn J., Johnson R.D., Gu J.G., and Cooper B.Y. Subclassified acutely dissociated cells of rat DRG: histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol 84 (2000) 2365-2379
26. Price M.P., Snyder P.M., and Welsh M.J. Cloning and expression of a novel human brain Na+ channel. J Biol Chem 271 (1996) 7879-7882
27. Rau K.K., Jiang N., Johnson R.D., and Cooper B.Y. Heat sensitization in skin and muscle nociceptors expressing distinct combinations of TRPV1 and TRPV2 protein. J Neurophysiol 97 (2007) 2651-2662
28. Ritter A.M., and Mendell L.M. Somal membrane properties of physiologically identified sensory neurons in the rat: Effects of nerve growth factor. J Neurophysiol 68 (1992) 2033-2041
29. Schmidt R., Schmelz M., Forster C., Ringkamp M., Torebjork E., and Handwerker H. Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15 (1995) 333-341
30. Simone D.A., Baumann T.K., and LaMotte R.H. Dose-dependent pain and mechanical hyperalgesia in humans after intradermal injection of capsaicin. Pain 38 (1989) 99-107
31. Treede R.D., Meyer R.A., and Campbell J.N. Myelinated mechanically insensitive afferents from monkey hairy skin: Heat-response properties. J Neurophysiol 80 (1998) 1082-1093
32. Weidner C., Schmelz M., Schmidt R., Hansson B., Handwerker H.O., and Torebjork H.E. Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin. J Neurosci 19 (1999) 10184-10190
33. Willis W.D., and Coggeshall R.E. Sensory mechanisms of the spinal cord (2004), Kluwer Academic/Plenum Publishers, New York
34. Woodbury C.J., Ritter A.M., and Koerber H.R. Central anatomy of individual rapidly adapting low-threshold mechanoreceptors innervating the "hairy" skin of newborn mice: early maturation of hair follicle afferents. J Comp Neurol 436 (2001) 304-323
35. Woodbury C.J., Zwick M., Wang S., Lawson J.J., Caterina M.J., Koltzenburg M., Albers K.M., Koerber H.R., and Davis B.M. Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24 (2004) 6410-6415
36. Zwick M., Davis B.M., Woodbury C.J., Burkett J.N., Koerber H.R., Simpson J.F., and Albers K.M. Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci 22 (2002) 4057-4065