Diabetic Peripheral Neuropathy: Role of Reactive Oxygen and Nitrogen Species

Cell Biochemistry and Biophysics

Volumn 67, Issue 2, 2013, Pages 373-383

  Premkumar, Louis S ^a   Pabbidi, Reddy M ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetes; Inflammatory mediators; Nociceptive ion channels; Nociceptors; Pain; Peripheral neuropathy; Reactive oxygen nitrogen species

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ANIMAL; DIABETIC NEUROPATHY; HUMAN; HYPERGLYCEMIA; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SENSORY RECEPTOR;

ANIMALS; DIABETIC NEUROPATHIES; HUMANS; HYPERGLYCEMIA; MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SENSORY RECEPTOR CELLS;

EID: 84886579124     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12013-013-9609-5     Document Type: Review

References (136)

1. Amos, A., Mccarty, D., & Zimmet, P. (1997). The rising global burden of diabetes and its complications estimates and projections to the year 2010. Diabetic Medicine, 14, S1-S85.
2. King, H., Auber, R., & Herman, W. (1998). Global burden of diabetes, 1995-2025. Prevalence, numerical estimates and projections. Diabetes Care, 21, 1414-1431.
3. World Health Organisation. (1999). Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: Diagnosis and classification of diabetes mellitus. Geneva: Department of noncommunicable disease surveillance.
4. The Diabetes Control and Complications Trial Research Group. (1993). The effect of Intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The New England Journal of Medicine, 329, 977-986.
5. UK Prospective Diabetes Study (UKPDS) Group. (1998). Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes. (UKPDS 33). Lancet, 1998(352), 837-853.
6. Edwards, J. L., Vincent, A. M., & Cheng, H. T. (2008). Feldman EL Diabetic neuropathy: Mechanisms to management. Pharmacology & Therapeutics, 120, 1-34.
7. Sherrington, C. S. (1906). The integrative action of the nervous system. New Haven, CT: Yale University Press.
8. Burgess, P. R., & Perl, E. R. (1967). Myelinated afferent fibres responding specifically to noxious stimulation of the skin. Journal of Physiology, 190, 541-562.
9. Djouhri, L., Bleazard, L., & Lawson, S. N. (1998). Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones. Journal of Physiology, 513, 857-872.
10. Schmidt, R., Schmelz, M., Forster, C., Ringkamp, M., Torebjork, E., & Handwerker, H. (1995). Novel classes of responsive and unresponsive C nociceptors in human skin. Journal of Neuroscience, 15, 333-341.
11. Vinik, A. I., Holland, M. T., Le Beau, J. M., Liuzzi, F. J., Stansberry, K. B., & Colen, L. B. (1992). Diabetic neuropathies. Diabetes Care, 15, 1926-1975.
12. Sima, A. A., Thomas, P. K., Ishii, D., & Vinik, A. (1997). Diabetic neuropathies. Diabetologia, 40, B74-B77.
13. Ramji, N., Toth, C., Kennedy, J., & Zochodne, D. W. (2007). Does diabetes mellitus target motor neurons? Neurobiology of Diseases, 26, 301-311.
14. Zochodne, D. W., Ramji, N., & Toth, C. (2008). Neuronal targeting in diabetes mellitus: A story of sensory neurons and motor neurons. Neuroscientist, 14, 311-318.
15. Schmader, K. E. (2002). Epidemiology and impact on quality of life of postherpetic neuralgia and painful diabetic neuropathy. Clinical Journal of Pain, 18, 350-354.
16. Laudadio, C., & Sima, A. A. (2006). Progression rates of diabetic neuropathy in placebo patients in an 18-month clinical trial, Ponalrestat Study Group. Journal of Diabetes Complications, 12, 121-127.
17. Said, G., Slama, G., & Selva, J. (1983). Progressive centripetal degeneration of axons in small fibre diabetic polyneuropathy. Brain, 106, 791-807.
18. Said, G., Goulon-Goeau, C., Slama, G., & Tchobroutsky, G. (1992). Severe early-onset polyneuropathy in insulin-dependent diabetes mellitus. A clinical and pathological study. The New England Journal of Medicine, 326, 1257-1263.
19. Pinzur, M. S. (2002). The diabetic foot. Comprehensive Therapy, 28, 232-237.
20. Dworkin, R. H., O'Connor, A. B., Backonja, M., Farrar, J. T., Finnerup, N. B., Jensen, T. S., et al. (2007). Pharmacologic management of neuropathic pain: Evidence-based recommendations. Pain, 132, 237-251.
21. Aley, K. O., & Levine, J. D. (2001). Rapid onset pain induced by intravenous streptozotocin in the rat. Journal of Pain, 2, 146-150.
22. Chu, Q., Moreland, R., Yew, N. S., Foley, J., Ziegler, R., & Scheule, R. K. (2008). Systemic insulin-like growth factor-1 reverses hypoalgesia and improves mobility in a mouse model of diabetic peripheral neuropathy. Molecular Therapy, 16, 1400-1408.
23. Vareniuk, I., Pavlov, I. A., & Obrosova, I. G. (2008). Inducible nitric oxide synthase gene deficiency counteracts multiple manifestations of peripheral neuropathy in a streptozotocin-induced mouse model of diabetes. Diabetologia, 51, 2126-2133.
24. Oltman, C. L., Davidson, E. P., Coppey, L. J., Kleinschmidt, T. L., Lund, D. D., Adebara, E. T., et al. (2008). Vascular and neural dysfunction in Zucker diabetic fatty rats: A difficult condition to reverse. Diabetes, Obesity & Metabolism, 10, 64-74.
25. Pabbidi, R. M., Yu, S. Q., Peng, S., Khardori, R., Pauza, M. E., & Premkumar, L. S. (2008). Influence of TRPV1 on diabetes-induced alterations in thermal pain sensitivity. Molecular Pain, 1, 4-9.
26. Cameron, N. E., Eaton, S. E., & Tesfaye, S. (2001). Vascular factors and metabolic interactions in the pathogenesis of diabetic neuropathy. Diabetologia, 44, 1973-1988.
27. Glanni, C., & Dyck, P. J. (1995). Basement membrane thickening and pericyte degeneration precede development of diabetic polyneuropathy and are associated with its severity. Annals of Neurology, 37, 498-504.
28. Britland, S. T., Young, R. J., & Sharma, A. K. (1990). Relationship of endoneurial capillary abnormalities to type and severity of diabetic neuropathy. Diabetes, 39, 909-913.
29. Timpereley, W. R., Ward, J. D., & Preston, F. E. (1977). Clinical and histological studies in diabetic neuropathy. Diabetologia, 12, 237-243.
30. Sheetz, M. J., & King, Gl. (2002). Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA, 288, 2579-2588.
31. Brownlee, M. (2001). Biochemistry and molecular cell biology of diabetic complications. Nature, 414, 813-820.
32. Wimalawansa, S. J. (1996). Calcitonin gene-related peptide: Molecular genetics, physiology, pathology and therapeutic potentials. Endocrinology Reviews, 1996(17), 533-585.
33. Belai, I. A., & Burnstock, G. (1987). Selective damage of intrinsic calcitonin gene-related peptide-like immunoreactive enteric nerve fibers in streptozotocin-induced diabetic rats. Gastroenterology, 92, 730-734.
34. Rittenhouse, P. A., Marchand, I. E., Chen, J., Kream, R. M., & Leeman, S. E. (1995). Streptozotocin-induced diabetes is associated with altered expression of peptide-encoding mRNA in rat sensory neurons. Peptides, 17, 1017-1022.
35. Bennett, G. J., & Xie, Y. K. (1988). A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain, 33, 87-107.
36. Sheykhzade, M., Dalsgaard, G. T., Johansen, T., & Nyborg, N. C. B. (2000). The effect of long-term streptozotocin-induced diabetes on contractile and relaxation responses of coronary arteries: Selective attenuation of CGRP-induced relaxations. British Journal of Pharmacology, 129, 1212-1218.
37. Wilson, D. K., Bohren, K. M., Gabbay, K. K., & Quiocho, F. A. (1992). An unlikely sugar substrate site in the 1. 65 Å structure of the human aldose reductase holoenzyme implicated in diabetic complications. Science, 257, 81-84.
38. Lee, A. Y., & Chung, S. S. (1999). Contributions of polyol pathway to oxidative stress in diabetic cataract. FASEB Journal, 13, 23-30.
39. Thornalley, P. J. (1990). The glyoxalase system: New developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochemical Journal, 269, 1-11.
40. Hammes, H. P., Du, X., Edelstein, D., Taguchi, T., Matsumura, T., Ju, Q., et al. (2003). Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nature Medicine, 9, 294-299.
41. Sugimoto, K., Murakawa, Y., & Sima, A. A. (2000). Diabetic neuropathy a continuing enigma. Diabetes Metabolism Research and Reviews, 16, 408-433.
42. Way, K. J., Katai, N., & King, G. L. (2001). Protein kinase C and the development of diabetic vascular complications. Diabetic Medicine, 18, 945-959.
43. Eicheberg, J. (2002). Protein kinase C changes in diabetes: Is the concept relevant to neuropathy? International Review of Neurobiology, 50, 61-82.
44. Roberts, R. E., & McClean, W. G. (1997). Protein kinase C isozyme expression in sciatic nerves and spinal cords of experimentally diabetic rats. Brain Research, 754, 147-156.
45. Yamagishi, S., Uehara, K., Otsuki, S., & Yagihashi, S. (2003). Differential influence of increased polyol pathway on protein kinase C expressions between endoneurial and epineurial tissues in diabetic mice. Journal of Neurochemistry, 87, 497-507.
46. Shiba, T., Inoguchi, T., Sportman, J. R., Heath, W., Bursell, S., & King, G. L. (1993). Correlation of diacylglycerol and protein kinase C activity in rat retina to retinal circulation. American Journal of Physiology, 265, E783-E793.
47. Craven, P. A., & DeRubertis, F. R. (1989). Protein kinase C is activated in glomeruli from streptozotocin diabetic rats. Possible mediation by glucose. Journal of Clinical Investigation, 83, 1667-1675.
48. Nakamura, K. K., Hamada, Y., Nakayama, M., Chaya, S., Nakashima, E., Naruse, K., et al. (1999). A protein kinase C-[beta]-selective inhibitor ameliorates neural dysfunction in streptozocin-induced diabetic rats. Diabetes, 48, 2090-2095.
49. Sasase, T., Yamada, H., Sakoda, K., Imagawa, N., Abe, T., Ito, M., et al. (2005). Novel protein kinase C-beta isoform selective inhibitor JTT-010 ameliorates both hyper- and hypoalgesia in streptozotocin- induced diabetic rats. Diabetes, Obesity & Metabolism, 7, 586-594.
50. Kom-Litty, V., Sauer, U., Nerlich, A., Lehmann, R., & Schelicher, E. D. (1998). High glucose-induced transforming growth factor beta 1 production is mediated by the hexosamine pathway in porcine glomerular mesangial cells. Journal of Clinical Investigation, 101, 160-169.
51. Du, X. L., Edelstein, D., Dimmeler, S., Qida, J., Sui, C., & Brownlee, M. (2001). Hyperglycemia inhibits endothelial nitric oxide synthase activity by post translational modification at the AKT site. Journal of Clinical Investigation, 108, 1341-1348.
52. Nishikawa, T., Edelstein, D., Xl, Du., Yamagishi, S., Matsumura, T., Kaneda, Y., et al. (2000). Normalising mitochondrial superoxide production blocks three pathways of hyperglycemic damage. Nature, 2000(404), 787-790.
53. Korshunov, S. S., Skulachev, V. P., & Starkov, A. A. (1997). High protonic potential actuates a mechanism production of reactive oxygen species in mitochondria. FEBS Letters, 416, 15-18.
54. Harman, D. (1956). Aging: A theory based on free radical and radiation chemistry. Journals of Gerontology, 11, 298-300.
55. Deby, C., & Gouter, R. (1990). New perspectives on the biochemistry of superoxide anion and the efficacy of superoxide dismutases. Biochemical Pharmacology, 39, 399-405.
56. Fridovich, I. (1978). The biology of oxygen radicals. Science, 201, 875-880.
57. Jensen, M. P., & Riley, D. P. (2002). Peroxynitrite decomposition activity of iron porphyrin complexes. Inorganic Chemistry, 41, 4788-4797.
58. Ushio-Fukai, M., Alexander, R. W., Akers, M., & Griendling, K. K. (1998). p38 MAP kinase is a critical component of the redox-sensitive signaling pathways by angiotensin II: Role in vascular smooth muscle cell hypertrophy. Journal of Biological Chemistry, 273, 15022-15029.
59. Barchowsky, A., Munro, S. R., Morana, S. J., Vincenti, M. P., & Treadwell, M. (1995). Oxidant-sensitive and phosphorylation-dependent activation of NF-kappa B and AP-1 in endothelial cells. American Journal of Physiology, 269, 829-836.
60. Tan, S., Sagara, Y., Liu, Y., Maher, P., & Schubert, D. (1998). The regulation of reactive oxygen species production during programmed cell death. Journal of Cell Biology, 141, 1423-1432.
61. Johnson, T. M., Yu, Z. X., Ferrans, V. J., Lowenstein, R. A., & Finkel, T. (1996). Reactive oxygen species are downstream mediators of p53-dependent apoptosis. Proceedings of the National Academy of Sciences of the United States of America, 21, 11848-11852.
62. Arvidson B. (1979). Distribution of protein tracers in peripheral ganglia. A light and electron microscopic study in rodents after various modes of tracer administration. Acta Universitatis Upsaliensis, 344, 1-72.
63. Zochodne, D. W., Verge, V. M. K., Cheng, C., Hong, S., & Johnston, J. (2001). Does diabetes target ganglion neurones? Brain, 124, 2319-2334.
64. Anand, P., Terenghi, G., Warnere, G., Kopelman, P., Williams-Chestnut, R. E., & Sinicropi, D. V. (1996). The role of endogenous growth factor in human diabetic neuropathy. Nature Medicine, 2, 703-707.
65. Lewin, G. R., & Mendell, L. M. (1993). Nerve growth factor and nociception. Trends in Neurosciences, 16, 353-359.
66. Kishi, M., Tanabe, J., Schmelzer, J. D., & Low, P. A. (2002). Morphometry of dorsal root ganglion in chronic experimental diabetic neuropathy. Diabetes, 51, 819-824.
67. Schmeichel, A. M., Schmelzer, J. D., & Low, P. A. (2003). Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes, 52, 165-171.
68. Srinivasan, S., Stevens, M., & Wiley, J. W. (2000). Diabetic peripheral neuropathy. Evidence for apoptosis and associated mitochondrial dysfunction. Diabetes, 11, 1932-1938.
69. Vincent, A. M., Olzmann, J. A., Brownlee, M., Sivitz, W. I., & Russell, J. W. (2004). Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes, 53, 726-734.
70. Geilen, C. C., Wieprecht, M., & Orfansos, C. E. (1996). The mitogen-activated protein kinases system (MAP kinase cascade): Its role in skin signal transduction: A review. Journal of Dermatological Science, 12, 255-262.
71. Tomlinson, D. R., & Gardiner, N. J. (2008). Glucose neurotoxicity. Nature Reviews Neuroscience, 9, 36-45.
72. Cantoni, O., Boscoboinik, D., Fiorani, M., Staule, B., & Azzi, A. (1996). The phoshorylation state of MAP-kinases modulates the cytotoxic response of smooth muscle cells to hydrogen peroxide. FEBS Letters, 389, 285-288.
73. Elbirt, K. K., Whitmarsh, A. J., Davis, R. J., & Bonkovsky, H. L. (1998). Mechanism of sodium arsenite-mediated induction of heme oxygenase-1 in hepatoma cells: Role mitogen-activated protein kinases. Journal of Biological Chemistry, 273, 8922-8931.
74. Purves, T., Middlemas, A., Agthong, S., Jude, E. B., Andrew, J. M., Boulton, A. J., et al. (2001). A role for mitogen-activated protein kinases in the etiology of diabetic neuropathy. FASEB Journal, 15, 2508-2514.
75. Ji, R., Samad, T. A., Jin, S. X., Schmoll, R., & Wooolf, C. J. (2002). P38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains hyperalgesia. Neuron, 36, 57-68.
76. Svensson, S. I., Fitzsimmons, B., Azizi, S., Powell, H. C., Hua, H. Y., & Yaksh, T. L. (2005). Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. Journal of Neurochemistry, 92, 1508-1520.
77. Turk, J., Corbett, J. A., Ramanadham, S., Bohrer, A., & McDaniel, L. (1993). Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets. Biochemical and Biophysical Research Communications, 197, 1458-1464.
78. Nukatsuka, M., Yoshimura, Y., Nishida, M., & Kawada, J. (1990). Allopurinol protects pancreatic beta cells from the cytotoxic effect of streptozotocin in vitro study. Journal of Pharmacobio-Dynamics, 13, 259-262.
79. Sofue, M., Yoshimura, Y., Nishida, M., & Kawada, J. (1991). Uptake of nicotinamide by rat pancreatic beta cells with regard to streptozotocin action. Journal of Endocrinology, 13, 135-138.
80. Suzukawa, K., Miura, K., Mitsushita, J., Resau, J., Hirose, K., Crystal, R., & Kamata, T. (2000). Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J Biol Chem, 275(18), 13175-13178.
81. Pabbidi, R. M., Cao, D. S., Parihar, A., Pauza, M. E., & Premkumar, L. S. (2008). Direct role of streptozotocin in inducing thermal hyperalgesia by enhanced expression of TRPV1 in sensory neurons. Molecular Pharmacology, 73, 995-1004.
82. Puntambekar, P., Mukherjea, D., Jajoo, S., & Ramkumar, V. (2005). Essential role of Rac1/NADPH oxidase in nerve growth factor induction of TRPV1 expression. Journal of Neurochemistry, 95, 1689-1703.
83. Angel, P., & Karin, M. (1991). The role of jun, fos and the AP-1 complex in cell proliferation and transformation. Biochimica et Biophysica Acta, 1072, 129-157.
84. Devary, Y., Gottlieb, R. A., Laus, L. F., & Karin, M. (1991). Rapid and preferential activation of the c-jun gene during the mammalian UV response. Molecular and Cellular Biology, 11, 2804-2811.
85. 2 and antioxidants have opposite effects on activation of NF-kB and AP-1 in intact cells: AP-1 as secondary antioxidant response factor. EMBO Journal, 12, 2005-2015.
86. Schmidt, R. E., Dorsey, D. A., Beaudet, L. N., & Peterson, R. G. (2003). Analysis of the zucker diabetic fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomic neuropathy. American Journal of Pathology, 163, 21-28.
87. Chattopadhyay, M., Mata, M., Goss, J., Wolfe, D., Huang, S., Glorioso, J. C., et al. (2007). Prolonged preservation of nerve function in diabetic neuropathy in mice by herpes simplex virus-mediated gene transfer. Diabetologia, 50, 1550-1558.
88. Ieda, M., Kanazawa, H., Ieda, Y., Kimura, K., Matsumura, K., Tomita, Y., et al. (2006). Nerve growth factor is critical for cardiac sensory innervation and rescues neuropathy in diabetic hearts. Circulation, 114, 2351-2363.
89. Roux, P. P., & Blenis, J. (2004). ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiology and Molecular Biology Reviews, 68, 320-344.
90. Tomlinson, D. R., & Gardiner, N. J. (2008). Diabetic neuropathies: Components of etiology. Journal of the Peripheral Nervous System, 13, 112-121.
91. Premkumar, L. S., & Ahern, G. P. (2000). Induction of vanilloid receptor channel activity by protein kinase C. Nature, 408, 985-990.
92. van Buren, J. J., Bhat, S., Rotello, R., Pauza, M. E., & Premkumar, L. S. (2005). Sensitization and translocation of TRPV1 by insulin and IGF-I. Molecular Pain, 1, 17.
93. Hong, S., & Wiley, J. W. (2005). Early painful diabetic neuropathy is associated with differential changes in the expression and function of vanilloid receptor 1. Journal of Biological Chemistry, 280, 618-627.
94. Kamei, J., Zushida, K., Mortia, K., Sasaki, M., & Tanaka, S. (2001). Role of vanilloid VR1 receptor in thermal allodynia and hyperalgesia in diabetic mice. European Journal of Pharmacology, 422, 83-86.
95. Rashid, M. H., Inoue, M., Kondo, S., Kawashima, T., Bakoshi, S., & Ueda, H. (2003). Novel expression of vanilloid receptor 1 on capsaicin-insensitive fibers accounts for the analgesic effect of capsaicin cream in neuropathic pain. Journal of Pharmacology and Experimental Therapeutics, 304, 940-948.
96. Julius, D., & Basbaum, A. I. (2001). Molecular mechanisms of nociception. Nature, 413, 203-210.
97. Woolf, C. J., & Salter, M. W. (2000). Neuronal plasticity: Increasing the gain in pain. Science, 288, 1765-1769.
98. Nordin, M., Nystrom, B., Wallin, U., & Hagbarth, K. E. (1984). Ectopic sensory discharges and paresthesiae in patients with disorders of peripheral nerves, dorsal roots and dorsal columns. Pain, 20, 231-245.
99. Wall, P. D., & Gutnick, M. (1994). Ongoing activity in peripheral nerves: The physiology and pharmacology of impulses originating from a neuroma. Experimental Neurology, 43, 580-589.
100. Wall, P. D., & Devor, M. (1983). Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve ligated rats. Pain, 17, 321-339.
101. + channels. Journal of Neurophysiology, 72, 349-359.
102. Janig, W., Levine, J. D., & Michaelis, M. (1996). Interactions of sympathetic and primary afferent neurons following nerve injury and tissue trauma. Progress in Brain Research, 113, 161-184.
103. Ramer, M. S., & Bisby, M. A. (1997). Rapid sprouting of sympathetic axons in dorsal root ganglia of rats with a chronic constriction injury. Pain, 70, 237-244.
104. Goswami, C., & Hucho, T. (2007). TRPV1 expression-dependent initiation and regulation of filopodia. Journal of Neurochemistry, 103, 1319-1333.
105. Maggi, C. A., & Meli, A. (1988). The sensory-efferent function of capsaicin-sensitive neurons. General Pharmacology, 19, 1-43.
106. McDonald, D. M., Bowden, J. J., Baluk, P. P., & Bunnett, N. W. (1996). Neurogenic inflammation. A model for studying efferent actions of sensory nerves. Advances in Experimental Medicine and Biology, 410, 453-462.
107. Moreau, M. E., Garbacki, N., Molinaro, G., Brown, N. J., Marceau, F., & Adam, A. (2005). The kallikrein-kinin system: Current and future pharmacological targets. Journal of Pharmacological Sciences, 99, 6-38.
108. Wang, H., Kohno, T., Amaya, F., Brenner, G. J., Ito, N., Allchorne, A., et al. (2005). Bradykinin produces pain hypersensitivity by potentiating spinal cord glutamatergic synaptic transmission. Journal of Neuroscience, 25, 7986-7992.
109. Zahner, M. R., Li, D. P., Chen, S. R., & Pan, H. L. (2003). Cardiac vanilloid receptor 1-expressing afferent nerves and their role in the cardiogenic sympathetic reflex in rats. Journal of Physiology, 551, 515-523.
110. Seyedi, N., Maruyama, R., & Levi, R. (1999). Bradykinin activates a cross-signaling pathway between sensory and adrenergic nerve endings in the heart: A novel mechanism of ischemic norepinephrine release? Journal of Pharmacology and Experimental Therapeutics, 290, 656-663.
111. Suzuki, R., & Dickenson, A. (2005). Spinal and supraspinal contributions to central sensitization in peripheral neuropathy. Neurosignals, 14, 175-181.
112. Lauria, G., Morbin, M., Lombardi, R., Capobianco, R., Camozzi, F., Pareyson, D., et al. (2006). Expression of capsaicin receptor immunoreactivity in human peripheral nervous system and in painful neuropathies. Journal of the Peripheral Nervous System, 11, 262-271.
113. Facer, P., Casula, M. A., Smith, G. D., Benham, C. D., Chessell, I. P., Bountra, C., et al. (2007). 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 Neurology, 7, 11.
114. 2+ concentration in the spinal dorsal horn in an animal model of neuropathic pain. Pain, 68, 85-96.
115. Rabben, T., Skjelbred, P., & Oye, I. (1999). Prolonged analgesic effect of ketamine, an N-methyl-d-aspartate receptor inhibitor, in patients with chronic pain. Journal of Pharmacology and Experimental Therapeutics, 289, 1060-1066.
116. Stiller, C. O., Cui, J. G., O'Connor, W. T., Brodin, E., Meyerson, B. A., & Linderoth, B. (1996). Release of gamma-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery, 39, 367-374.
117. Zeilhofer, H. U. (2005). The glycinergic control of spinal pain processing. Cellular and Molecular Life Sciences, 62, 2027-2035.
118. Leenders, A. G., & Sheng, Z. H. (2005). Modulation of neurotransmitter release by the second messenger-activated protein kinases: Implications for presynaptic plasticity. Pharmacology & Therapeutics, 105, 69-84.
119. Premkumar, L. S., Qi, Z. H., van Buren, J., & Raisinghani, M. (2004). Enhancement of potency and efficacy of NADA by PKC-mediated phosphorylation of vanilloid receptor. Journal of Neurophysiology, 91, 1442-1449.
120. Premkumar, L. S., Raisinghani, M., Pingle, S. C., Long, C., & Pimentel, F. (2005). Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. Journal of Neuroscience, 25, 11322-11329.
121. Premkumar, L. S., & Sikand, P. (2008). TRPV1: A target for next generation analgesics. Current Opinion in Pharmacology, 6, 151-163.
122. Jeffry, J. A., Yu, S. Q., Sikand, P., Parihar, A., Evans, M. S., & Premkumar, L. S. (2009). Selective targeting of TRPV1 expressing sensory nerve terminals in the spinal cord for long lasting analgesia. PLoS One, 4, e7021.
123. Lindsay, T. J., Rodgers, B. C., Savath, V., & Hettinger, K. (2010). Treating diabetic peripheral neuropathic pain. American Family Physician, 82, 151-158.
124. Wong, M. C., Chung, J. W., & Wong, T. K. (2007). Effects of treatments for symptoms of painful diabetic neuropathy: systematic review. BMJ, 335(7610), 87.
125. Argoff, C. E., Backonja, M. M., & Belgrade, M. J., et al. (2006). Diabetic peripheral neuropathic pain: Consensus guidelines for treatment. Mayo ClinicProceedings, 81(4 Suppl), S12-S25.
126. Saarto, T., & Wiffen, P. J. (2007). Antidepressants for neuropathic pain. Cochrane Databaseof Systematic Reviews, 4, CD005454.
127. Vinik, A. (2005). Clinical review: Use of antiepileptic drugs in the treatment of chronic painful diabetic neuropathy. Journal of Clinical Endocrinology and Metabolism, 90, 4936-4945.
128. Freeman, R., Durso-Decruz, E., & Emir, B. (2008). Efficacy, safety, and tolerability of pregabalin treatment for painful diabetic peripheral neuropathy: Findings from seven randomized, controlled trials across a range of doses. Diabetes Care, 31, 1448-1454.
129. Wernicke, J. F., Pritchett, Y. L., D'Souza, D. N., et al. (2006). A randomized controlled trial of duloxetine in diabetic peripheral neuropathic pain. Neurology, 67, 1411-1420.
130. Eisenberg, E., McNicol, E., & Carr, D. B. (2003). Opioids for neuropathic pain. Cochrane Databaseof Systematic Reviews, 3, CD006146.
131. Hollingshead, J., Dühmke, R. M., & Cornblath, D. R. (2006). Tramadol for neuropathic pain. Cochrane Databaseof Systematic Reviews, 3, CD003726.
132. Harati, Y., Gooch, C., Swenson, M., et al. (1998). Double-blind randomized trial of tramadol for the treatment of the pain of diabetic neuropathy. Neurology, 50, 1842-1846.
133. Mason, L., Moore, R. A., Derry, S., Edwards, J. E., & McQuay, H. J. (2004). Systematic review of topical capsaicin for the treatment of chronic pain. BMJ, 328, 991.
134. Meier, T., Wasner, G., Faust, M., et al. (2003). Efficacy of lidocaine patch 5% in the treatment of focal peripheral neuropathic pain syndromes: A randomized, double-blind, placebo-controlled study. Pain, 106, 151-158.
135. Sima, A. A., Calvani, M., Mehra, M., Amato, A., & Acetyl-l-Carnitine Study Group. (2005). Acetyl-l-carnitine improves pain, nerve regeneration, and vibratory perception in patients with chronic diabetic neuropathy: An analysis of two randomized placebo-controlled trials. Diabetes Care, 28, 89-94.
136. Ametov, A. S., Barinov, A., Dyck, P. J., et al. (2003). SYDNEY Trial Study Group. The sensory symptoms of diabetic polyneuropathy are improved with alpha-lipoic acid: The SYDNEY trial. Diabetes Care, 26, 770-776. (published correction appears in Diabetes Care 2003;26: 2227).