Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice

Neuroscience Letters

Volumn 442, Issue 3, 2008, Pages 267-272

  Beiswenger, Kristina K ^a   Calcutt, Nigel A ^a   Mizisin, Andrew P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Diabetic neuropathy; Epidermal nerve fiber density; GAP 43; PGP9.5; Substance P; Thermal hypoalgesia

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DENERVATION; EPIDERMIS; HYPOALGESIA; MALE; MOUSE; NERVE FIBER; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; STREPTOZOCIN DIABETES; SWISS WEBSTER MOUSE;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; HEAT; MALE; MICE; NERVE FIBERS; PAIN THRESHOLD; SKIN; UBIQUITIN THIOLESTERASE;

EID: 48749104018     PISSN: 03043940     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neulet.2008.06.079     Document Type: Article

References (41)

1. K.K. Beiswenger, N.A. Calcutt, A.P. Mizisin, Epidermal nerve fiber quantification in the assessment of diabetic neuropathy, Acta Histochem., doi:10.1016/j.acthis.2007.12.004.
2. Calcutt N.A., Stiller C., Gustafsson H., and Malmberg A.B. Elevated substance-P-like immunoreactivity levels in spinal dialysates during the formalin test in normal and diabetic rats. Brain Res. 856 1-2 (2000) 20-27
3. Cao Y.Q., Mantyh P.W., Carlson E.J., Gillespie A.M., Epstein C.J., and Basbaum A.I. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 392 6674 (1998) 390-394
4. 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
5. Chateau Y., and Misery L. Connections between nerve endings and epidermal cells: are they synapses?. Exp. Dermatol. 13 1 (2004) 2-4
6. Chen Y.S., Chung S.S.M., and Chung S.K. Noninvasive monitoring of diabetes-induced cutaneous nerve fiber loss and hypoalgesia in thy1-YFP transgenic mice. Diabetes 54 (2005) 3112-3118
7. Chung M.K., Lee H., and Caterina M.J. Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J. Biol. Chem. 278 34 (2003) 32037-32046
8. De Graan P.N.E., Van Hoff C.O.M., Tilly B.D., Oestreicher A.B., Schotman P., and Gispen W.H. Phosphoprotein B-50 in nerve growth cones from fetal rat brain. Neurosci. Lett. 61 3 (1985) 235-241
9. Denda M., Fuziwara S., Inoue K., Denda S., Akamatsu H., Tomitaka A., and Matsunaga K. Immunoreactivity of VR1 on epidermal keratinocyte of human skin. Biophys. Res. Commun. 285 5 (2001) 1250-1252
10. Facer P., Casula M.A., Smith G.D., Benham C.D., Chessell I.P., Bountra C., Sinisi M., Birch R., and Anand P. Differential expression of the capsaicin receptor TRPV1 and related novel receptors TRPV3, TRPV4 and TRPM8 in normal human tissues and changes in traumatic and diabetic neuropathy. BMC Neurol. 7 (2007) 11
11. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1998) 77-88
12. Hong S., and Wiley J.W. Early painful diabetic neuropathy is associated with differential changes in the expression and function of vanilloid receptor 1. J. Biol. Chem. 280 1 (2005) 618-627
13. Kalichman M.W., Powell H.C., Calcutt N.A., and Mizisin A.P. Mast cell degranulation and blood-nerve barrier permeability in rat sciatic nerve after 7 days of hyperglycemia. Am. J. Physiol. 268 2 pt.2 (1995) H740-H748
14. Kanbayashi H., Itoh H., Kashiwaya T., Atoh K., and Makino I. Spatial distribution of nociceptive neuropeptide and nerve growth factor depletion in experimental diabetic peripheral nervous system. J. Int. Med. Res. 30 5 (2002) 512-519
15. Laneuville O., Dorais J., and Couture R. Characterization of the effects produced by neurokinins and three agonists selective for neurokinin receptor subtypes in a spinal nociceptive reflex of the rat. Life Sci. 42 13 (1988) 1295-1305
16. Lauria G., and Devigili G. Skin biopsy as a diagnostic tool in peripheral neuropathy. Nat. Clin. Prac. Neurol. 10 3 (2007) 546-557
17. Lauria G., Lombardi R., Borgna M., Penza P., Bianchi R., Savino C., Canta A., Nicolini G., Marmiroli P., and Cavaletti G. Intraepidermal nerve fiber density in rat foot pad: neuropathologic-neurophysiologic correlation. J. Peripher. Nerv. Syst. 10 (2005) 202-208
18. Malmberg A.B., Mizisin A.P., Calcutt N.A., von Stein T., Robbins W.R., and Bley K.R. Reduced heat sensitivity and epidermal nerve fiber immunostaining following single applications of a high-concentration capsaicin patch. Pain 111 3 (2004) 360-367
19. Nichols M.L., Allen B.J., Rogers S.D., Ghilardi J.R., Honore P., Luger N.M., Finke M.P., Li J., Lappi D.A., Simone D.A., and Mantyh P.W. Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286 5444 (1999) 1558-1561
20. Nolano M., Simone D.A., Wendelschafer-Crabb G., Johnson T., Hazen E., and Kennedy W.R. Topical capsaicin in humans: parallel loss of epidermal nerve fibers and pain sensation. Pain 81 1-2 (1999) 135-145
21. Obrosova I.G., Ilnytska O., Lyzogubov V.V., Pavlov I.A., Mashtalir N., Nadler J.L., and Drel V.R. High-fat diet induced neuropathy of pre-diabetes and obesity: effects of "healthy" diet and aldose reductase inhibition. Diabetes 56 10 (2007) 2598-2608
22. Pabbidi R.M., Yu S.Q., Peng S., Khardori R., Pauza M.E., and Premkumar L.S. Influence of TRPV1 on diabetes-induced alterations in thermal pain sensitivity. Mol. Pain 4 (2008) 9
23. Peier A.M., Reeve A.J., Andersson D.A., Moqrich A., Earley T.J., Hergarden A.C., Story G.M., Colley S., Hogenesch J.B., McIntyre P., Bevan S., and Patapoutian A. A heat-sensitive TRP channel expressed in keratinocytes. Science 296 5575 (2002) 2046-2049
24. Pirart J., Lauvaux J.P., and Rey W. Blood sugar and diabetic complications. N. Engl. J. Med. 298 (1978) 1149
25. Pittenger G.L., Ray M., Burcus N.I., McNulty P., Basta B., and Vinik A.I. Intraepidermal nerve fibers are indicators of small-fiber neuropathy in both diabetic and nondiabetic patients. Diabetes Care 27 (2004) 1974-1979
26. Quattrini C., Tavakoli M., Jeziorska M., Kallinikos P., Tesfaye S., Finnigan J., Marshall A., Boulton A.J., Efron N., and Malik R.A. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 56 8 (2007) 2148-2154
27. Robinson J.P., Willars G.B., Tomlinson D.R., and Keen P. Axonal transport and tissue contents of substance P in rats with long-term streptozotocin-diabetes. Effects of the aldose reductase inhibitor 'statil'. Brain Res. 426 2 (1987) 339-348
28. Shun C.T., Chang Y.C., Wu H.P., Hsieh S.C., Lin W.M., Lin Y.H., Tai T.Y., and Hsieh S.T. Skin denervation in type 2 diabetes: correlations with diabetic duration and functional impairments. Brain 127 (2004) 1593-1605
29. Simone D.A., Nolano M., Johnson T., Wendelschafer-Crabb G., and Kennedy W.R. Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: correlation with sensory function. J. Neurosci. 18 21 (1998) 8947-8959
30. Smith A.G., Russell J., Feldman E.L., Goldstein J., Peltier A., Smith S., Hamwi J., Pollari D., Bixby B., Howard J., and Singleton J.R. Lifestyle intervention for pre-diabetic neuropathy. Diabetes Care 29 6 (2006) 1294-1299
31. Sorensen L., Molyneaux L., and Yue D.K. The relationship among pain, sensory loss, and small nerve fibers in diabetes. Diabetes Care 29 (2006) 883-887
32. Spravchikov N., Sizyakov G., Gartsbein M., Accili D., Tennenbaum T., and Wertheimer E. Glucose effects on skin keratinocytes: implications for diabetes skin complications. Diabetes 50 (2001) 1627-1635
33. Thomas P.K. Classification, differential diagnosis, and staging of diabetic peripheral neuropathy-current state and perspectives of diabetes research: chronic complications. Diabetes 46 (1997) S54-S57
34. Tomlinson D.R., Robinson J.P., Willars G.B., and Keen P. Deficient axonal transport of substance P in streptozotocin-induced diabetic rats. Effects of sorbinil and insulin. Diabetes 37 4 (1998) 488-493
35. Verze L., Paraninfo A., Ramieri G., Viglietti C., and Panzica G.C. Immunocytochemical evidence of plasticity in the nervous structures of the rat lower lip. Cell Tissue Res. 297 (1999) 203-211
36. Vierck C.J., Kline R.H., and Wiley R.G. Intrathecal substance p-saporin attenuates operant escape from nociceptive thermal stimuli. Neuroscience 119 1 (2003) 223-232
37. Wertheimer E., Spravchikov M., Trebicz M., Gartsbein M., Accili D., Avinoah I., Nofeh-Moses S., Sizyakov G., and Tennenbaum T. The regulation of skin proliferation and differentiation in the IR null mouse: implications for skin complications of diabetes. Endocrinology 142 (2001) 1234-1241
38. Wertheimer E., Trebicz M., Eldar T., Gartsbein M., Nofeh-Moses S., and Tennenbaum T. Differential roles of insulin receptor and insulin-like growth factor receptor in differentiation of murine skin keratinocytes. J. Invest. Dermatol. 115 1 (2000) 24-29
39. Wilkinson K.D., Lee K.M., Deshpande S., Duerksen-Hughes P., Boss J.M., and Pohl J. The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246 4930 (1989) 670-673
40. Willars G.B., Calcutt N.A., Compton A.M., Tomlinson D.R., and Keen P. Substance P levels in peripheral nerve, skin, atrial myocardium and gastrointestinal tract of rats with long-term diabetes mellitus. Effects of aldose reductase inhibition. J. Neurol. Sci. 91 1-2 (1989) 153-164
41. Yeomans D.C., Pirec V., and Proudfit H.K. Nociceptive responses to high and low rates of noxious cutaneous heating are mediated by different nociceptors in the rat: behavioral evidence. Pain 68 1 (1996) 133-140