Sensory Neurodegeneration in Diabetes

Ahn, 2005, Transcription factor NF-kappaB: A sensor for smoke and stress signals, The Annals of the New York Academy of Sciences, 1056, 218, 10.1196/annals.1352.026 Baggio, 2007, Biology of incretins: GLP-1 and GIP, Gastroenterology, 132, 2131, 10.1053/j.gastro.2007.03.054 Bennett, 2014, Mitotoxicity in distal symmetrical sensory peripheral neuropathies, Nature Reviews. Neurology, 10, 326, 10.1038/nrneurol.2014.77 Brownlee, 1988, Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications, The New England Journal of Medicine, 318, 1315, 10.1056/NEJM198805193182007 Brussee, 2004, Direct insulin signaling of neurons reverses diabetic neuropathy, Diabetes, 53, 1824, 10.2337/diabetes.53.7.1824 Cameron, 1991, Nerve blood flow in early experimental diabetes in rats: Relation to conduction deficits, The American Journal of Physiology, 261, E1 Cameron, 2005, Inhibitors of advanced glycation end product formation and neurovascular dysfunction in experimental diabetes, The Annals of the New York Academy of Sciences, 1043, 784, 10.1196/annals.1333.091 Chen, 2013, Repeated monitoring of corneal nerves by confocal microscopy as an index of peripheral neuropathy in type-1 diabetic rodents and the effects of topical insulin, Journal of the Peripheral Nervous System, 18, 306, 10.1111/jns5.12044 Cheng, 2010, Dynamic plasticity of axons within a cutaneous milieu, The Journal of Neuroscience, 30, 14735, 10.1523/JNEUROSCI.2919-10.2010 Cheng, 2015, Evidence for epigenetic regulation of gene expression and function in chronic experimental diabetic neuropathy, Journal of Neuropathology and Experimental Neurology, 74, 804, 10.1097/NEN.0000000000000219 Cheng, 2008, Activated RHOA and peripheral axon regeneration, Experimental Neurology, 212, 358, 10.1016/j.expneurol.2008.04.023 Cheng, 2003, Sensory neurons with activated caspase-3 survive long-term experimental diabetes, Diabetes, 52, 2363, 10.2337/diabetes.52.9.2363 Christie, 2014, Enhancing adult nerve regeneration through the knockdown of retinoblastoma protein, Nature Communications, 5, 3670, 10.1038/ncomms4670 Christie, 2010, PTEN inhibition to facilitate intrinsic regenerative outgrowth of adult peripheral axons, The Journal of Neuroscience, 30, 9306, 10.1523/JNEUROSCI.6271-09.2010 Court, 2008, Schwann cell to axon transfer of ribosomes: Toward a novel understanding of the role of glia in the nervous system, The Journal of Neuroscience, 28, 11024, 10.1523/JNEUROSCI.2429-08.2008 Diamond, 1987, Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats, Proceedings of the National Academy of Sciences of the United States of America, 84, 6596, 10.1073/pnas.84.18.6596 Diamond, 1992, Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat, The Journal of Neuroscience, 12, 1454, 10.1523/JNEUROSCI.12-04-01454.1992 Drel, 2007, A peroxynitrite decomposition catalyst counteracts sensory neuropathy in streptozotocin-diabetic mice, European Journal of Pharmacology, 569, 48, 10.1016/j.ejphar.2007.05.055 Ekberg, 2003, Amelioration of sensory nerve dysfunction by C-peptide in patients with type 1 diabetes, Diabetes, 52, 536, 10.2337/diabetes.52.2.536 Fernyhough, 2014, Mechanisms of disease: Mitochondrial dysfunction in sensory neuropathy and other complications in diabetes, Handbook of Clinical Neurology, 126, 353, 10.1016/B978-0-444-53480-4.00027-8 Fernyhough, 2005, Activation of nuclear factor-kappaB via endogenous tumor necrosis factor alpha regulates survival of axotomized adult sensory neurons, The Journal of Neuroscience, 25, 1682, 10.1523/JNEUROSCI.3127-04.2005 Fernyhough, 1993, Insulin and insulin-like growth factor I enhance regeneration in cultured adult rat sensory neurones, Brain Research, 607, 117, 10.1016/0006-8993(93)91496-F Folli, 1994, Insulin receptor substrate-1 (IRS-1) distribution in the rat central nervous system, The Journal of Neuroscience, 14, 6412, 10.1523/JNEUROSCI.14-11-06412.1994 Francis, 2011, Motor end plate innervation loss in diabetes and the role of insulin, Journal of Neuropathology and Experimental Neurology, 70, 323, 10.1097/NEN.0b013e318215669a Frazier, 1972, Nerve growth factor and insulin, Science, 176, 482, 10.1126/science.176.4034.482 Giniger, 2002, How do Rho family GTPases direct axon growth and guidance? A proposal relating signaling pathways to growth cone mechanics, Differentiation, 70, 385, 10.1046/j.1432-0436.2002.700801.x Greenbaum, 1964, Pathological observations on six cases of diabetic neuropathy, Brain, 87, 201, 10.1093/brain/87.2.201 Grote, 2013, Peripheral nervous system insulin resistance in ob/ob mice, Acta Neuropathologica Communications, 1, 15, 10.1186/2051-5960-1-15 Grote, 2011, Insulin receptor substrate 2 expression and involvement in neuronal insulin resistance in diabetic neuropathy, Experimental Diabetes Research, 2011, 212571, 10.1155/2011/212571 Guo, 2011, Local insulin and the rapid regrowth of diabetic epidermal axons, Neurobiology of Disease, 43, 414, 10.1016/j.nbd.2011.04.012 Guo, 2014, Growth and turning properties of adult glial cell-derived neurotrophic factor coreceptor alpha 1 nonpeptidergic sensory neurons, Journal of Neuropathology and Experimental Neurology, 73, 820, 10.1097/NEN.0000000000000101 Hall, 1995, Voltage-dependent calcium currents are enhanced in dorsal root ganglion neurones from the Bio Bred/Worchester diabetic rat, Journal of Physiology, 486, 313, 10.1113/jphysiol.1995.sp020814 Himeno, 2011, Beneficial effects of exendin-4 on experimental polyneuropathy in diabetic mice, Diabetes, 60, 2397, 10.2337/db10-1462 Huang, 2003, Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia, Diabetes, 52, 2129, 10.2337/diabetes.52.8.2129 Jin, 2005, Ca2+-dependent regulation of rho GTPases triggers turning of nerve growth cones, The Journal of Neuroscience, 25, 2338, 10.1523/JNEUROSCI.4889-04.2005 Jolivalt, 2011, GLP-1 signals via ERK in peripheral nerve and prevents nerve dysfunction in diabetic mice, Diabetes, Obesity & Metabolism, 13, 990, 10.1111/j.1463-1326.2011.01431.x Kamiya, 2006, C-peptide reverses nociceptive neuropathy in type 1 diabetes, Diabetes, 55, 3581, 10.2337/db06-0396 Kamiya, 2006, Degeneration of the Golgi and neuronal loss in dorsal root ganglia in diabetic BioBreeding/Worcester rats, Diabetologia, 49, 2763, 10.1007/s00125-006-0379-0 Kamiya, 2005, Apoptotic stress is counterbalanced by survival elements preventing programmed cell death of dorsal root ganglions in subacute type 1 diabetic BB/Wor rats, Diabetes, 54, 3288, 10.2337/diabetes.54.11.3288 Kan, 2012, Glucagon-like peptide 1, insulin, sensory neurons, and diabetic neuropathy, Journal of Neuropathology and Experimental Neurology, 71, 494, 10.1097/NEN.0b013e3182580673 Kennedy, 2002, Influence of experimental diabetes on the microcirculation of injured peripheral nerve. Functional and morphological aspects, Diabetes, 51, 2233, 10.2337/diabetes.51.7.2233 Kennedy, 2005, Impaired peripheral nerve regeneration in diabetes mellitus, Journal of the Peripheral Nervous System, 10, 144, 10.1111/j.1085-9489.2005.0010205.x Kim, 2011, Hyperinsulinemia induces insulin resistance in dorsal root ganglion neurons, Endocrinology, 152, 3638, 10.1210/en.2011-0029 Kobayashi, 2015, Diabetic neuropathy and the sensory neuron: New molecular targets, American Academy of Neurology Korngut, 2012, Overexpression of human HSP27 protects sensory neurons from diabetes, Neurobiology of Disease, 47, 436, 10.1016/j.nbd.2012.04.017 Korngut, 2013, A pilot study of intranasal insulin for the treatment of diabetic peripheral neuropathy, Journal of the Peripheral Nervous System, 18, S59 Korthals, 1988, Intima of epineurial arterioles is increased in diabetic polyneuropathy, Neurology, 38, 1582, 10.1212/WNL.38.10.1582 Levy, 1999, Local expression of inducible nitric oxide synthase in an animal model of neuropathic pain, Neuroscience Letters, 260, 207, 10.1016/S0304-3940(98)00982-3 Levy, 2001, Delayed peripheral nerve degeneration, regeneration, and pain in mice lacking inducible nitric oxide synthase, Journal of Neuropathology and Experimental Neurology, 60, 411, 10.1093/jnen/60.5.411 Levy, 2000, Transient action of the endothelial constitutive nitric oxide synthase (ecNOS) mediates the development of thermal hypersensitivity following peripheral nerve injury, The European Journal of Neuroscience, 12, 2323, 10.1046/j.1460-9568.2000.00129.x Luo, 1997, Rho family GTP-binding proteins in growth cone signalling, Current Opinion in Neurobiology, 7, 81, 10.1016/S0959-4388(97)80124-9 Ma, 2014, Heat shock protein 70 is necessary to improve mitochondrial bioenergetics and reverse diabetic sensory neuropathy following KU-32 therapy, The Journal of Pharmacology and Experimental Therapeutics, 348, 281, 10.1124/jpet.113.210435 Ma, 2015, Modulating molecular chaperones improves mitochondrial bioenergetics and decreases the inflammatory transcriptome in diabetic sensory neurons, ACS Chemical Neuroscience, 6, 1637, 10.1021/acschemneuro.5b00165 Malik, 2003, Corneal confocal microscopy: A non-invasive surrogate of nerve fibre damage and repair in diabetic patients, Diabetologia, 46, 683, 10.1007/s00125-003-1086-8 Malik, 1989, Microangiopathy in human diabetic neuropathy: Relationship between capillary abnormalities and the severity of neuropathy, Diabetologia, 32, 92, 10.1007/BF00505180 Malik, 1992, Endoneurial capillary abnormalities in mild human diabetic neuropathy, Journal of Neurology, Neurosurgery, and Psychiatry, 55, 557, 10.1136/jnnp.55.7.557 Massa, 2006, Small, nonpeptide p75NTR ligands induce survival signaling and inhibit proNGF-induced death, The Journal of Neuroscience, 26, 5288, 10.1523/JNEUROSCI.3547-05.2006 Newrick, 1986, Sural nerve oxygen tension in diabetes, British Medical Journal, 293, 1053, 10.1136/bmj.293.6554.1053 Ng, 2004, Rho GTPases regulate axon growth through convergent and divergent signaling pathways, Neuron, 44, 779, 10.1016/j.neuron.2004.11.014 Obrosova, 2005, Oxidative-nitrosative stress and poly(ADP-ribose) polymerase (PARP) activation in experimental diabetic neuropathy: The relation is revisited, Diabetes, 54, 3435, 10.2337/diabetes.54.12.3435 Obrosova, 2004, Role of poly(ADP-ribose) polymerase activation in diabetic neuropathy, Diabetes, 53, 711, 10.2337/diabetes.53.3.711 Perry, 2007, Evidence of GLP-1-mediated neuroprotection in an animal model of pyridoxine-induced peripheral sensory neuropathy, Experimental Neurology, 203, 293, 10.1016/j.expneurol.2006.09.028 Polydefkis, 2001, Skin biopsy as a tool to assess distal small fiber innervation in diabetic neuropathy, Diabetes Technology & Therapeutics, 3, 23, 10.1089/152091501750219994 Purves, 2002, Diminished transcription factor survival signals in dorsal root ganglia in rats with streptozotocin-induced diabetes, Annals of the New York Academy of Sciences, 973, 472, 10.1111/j.1749-6632.2002.tb04686.x Reddy, 2006, Inhibitors of the Maillard reaction and AGE breakers as therapeutics for multiple diseases, Drug Discovery Today, 11, 646, 10.1016/j.drudis.2006.05.016 Reger, 2008, Intranasal insulin improves cognition and modulates B-amyloid in early AD, Neurology, 70, 440, 10.1212/01.WNL.0000265401.62434.36 Rundles, 1945, Diabetic neuropathy—General review with report of 125 cases, Medicine, 24, 111, 10.1097/00005792-194505000-00001 Russell, 1999, Neurons undergo apoptosis in animal and cell culture models of diabetes, Neurobiology of Disease, 6, 347, 10.1006/nbdi.1999.0254 Saleh, 2013, Receptor for advanced glycation end-products (RAGE) activates divergent signaling pathways to augment neurite outgrowth of adult sensory neurons, Experimental Neurology, 249, 149, 10.1016/j.expneurol.2013.08.018 Schmelzer, 1989, Ischemic and reperfusion injury of rat peripheral nerve, Proceedings of the National Academy of Sciences of the United States of America, 86, 1639, 10.1073/pnas.86.5.1639 Schmidt, 1997, Axonal cytoskeletal pathology in aged and diabetic human sympathetic autonomic ganglia, Brain Research, 769, 375, 10.1016/S0006-8993(97)00806-8 Schmidt, 1998, Vacuolar neuritic dystrophy in aged mouse superior cervical sympathetic ganglia is strain-specific, Brain Research, 806, 141, 10.1016/S0006-8993(98)00678-7 Schmidt, 1997, Dystrophic axonal swellings develop as a function of age and diabetes in human dorsal root ganglia, Journal of Neuropathology and Experimental Neurology, 56, 1028, 10.1097/00005072-199709000-00008 Schmidt, 1982, Axonal dystrophy in experimental diabetic autonomic neuropathy, Diabetes, 31, 761, 10.2337/diab.31.9.761 Scott, 1999, Neurofilament and tubulin gene expression in progressive experimental diabetes: Failure of synthesis and export by sensory neurons, Brain, 122, 2109, 10.1093/brain/122.11.2109 Singh, 2014, Regeneration of diabetic axons is enhanced by selective knockdown of the PTEN gene, Brain, 137, 1051, 10.1093/brain/awu031 Singh, 2009, Insulin signaling and insulin resistance in sensory neurons, Journal of the Peripheral Nervous System, 13, 254 Singh, 2012, Resistance to trophic neurite outgrowth of sensory neurons exposed to insulin, Journal of Neurochemistry, 121, 263, 10.1111/j.1471-4159.2012.07681.x Singhal, 1997, Near nerve local insulin prevents conduction slowing in experimental diabetes, Brain Research, 763, 209, 10.1016/S0006-8993(97)00412-5 Sivitz, 2010, Mitochondrial dysfunction in diabetes: From molecular mechanisms to functional significance and therapeutic opportunities, Antioxidants & Redox Signaling, 12, 537, 10.1089/ars.2009.2531 Sugimoto, 2002, Expression and localization of insulin receptor in rat dorsal root ganglion and spinal cord, Journal of the Peripheral Nervous System, 7, 44, 10.1046/j.1529-8027.2002.02005.x Sugimoto, 2000, Insulin receptor in rat peripheral nerve: Its localization and alternatively spliced isoforms, Diabetes/Metabolism Research and Reviews, 16, 354, 10.1002/1520-7560(200009/10)16:5<354::AID-DMRR149>3.0.CO;2-H Tavakoli, 2010, Corneal confocal microscopy: A novel noninvasive test to diagnose and stratify the severity of human diabetic neuropathy, Diabetes Care, 33, 1792, 10.2337/dc10-0253 Tesfaye, 2005, Vascular risk factors and diabetic neuropathy, The New England Journal of Medicine, 352, 341, 10.1056/NEJMoa032782 Tesfaye, 1993, Impaired blood flow and arteriovenous shunting in human diabetic neuropathy: A novel technique of nerve photography and fluorescein angiography, Diabetologia, 36, 1266, 10.1007/BF00400804 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 Diabetes Control and Complications Trial Research Group, The New England Journal of Medicine, 329, 977, 10.1056/NEJM199309303291401 Theriault, 1997, Local human sural nerve blood flow in diabetic and other polyneuropathies, Brain, 120, 1131, 10.1093/brain/120.7.1131 Theriault, 1998, A prospective quantitative study of sensory deficits after whole sural nerve biopsies in diabetic and nondiabetic patients. Surgical approach and the role of collateral sprouting, Neurology, 50, 480, 10.1212/WNL.50.2.480 Thomsen, 2002, NO- and non-NO-, non-prostanoid-dependent vasodilatation in rat sciatic nerve during maturation and developing experimental diabetic neuropathy, The Journal of Physiology, 543, 977, 10.1113/jphysiol.2002.023564 Thornalley, 2003, Use of aminoguanidine (Pimagedine) to prevent the formation of advanced glycation endproducts, Archives of Biochemistry and Biophysics, 419, 31, 10.1016/j.abb.2003.08.013 Toth, 2006, Rescue and regeneration of injured peripheral nerve axons by intrathecal insulin, Neuroscience, 139, 429, 10.1016/j.neuroscience.2005.11.065 Toth, 2007, Intranasal insulin delivery reduces morphological, electrophysiological, behavioral, and molecular changes of diabetic neuropathy without change in glycemia, Journal of the Peripheral Nervous System, 12, 86 Toth, 2004, RAGE in the nervous system: Insights into a new pathophysiological relationship to diabetic complications within the central and peripheral nervous system, Canadian Journal of Neurological Sciences, 31, S13 Tucker, 2006, Laminin and growth factor receptor activation stimulates differential growth responses in subpopulations of adult DRG neurons, The European Journal of Neuroscience, 24, 676, 10.1111/j.1460-9568.2006.04963.x Vareniuk, 2009, Peripheral neuropathy in mice with neuronal nitric oxide synthase gene deficiency, International Journal of Molecular Medicine, 23, 571 Vareniuk, 2008, Inducible nitric oxide synthase gene deficiency counteracts multiple manifestations of peripheral neuropathy in a streptozotocin-induced mouse model of diabetes, Diabetologia, 51, 2126, 10.1007/s00125-008-1136-3 Voitenko, 2000, Effect of streptozotocin-induced diabetes on the activity of calcium channels in rat dorsal horn neurons, Neuroscience, 95, 519, 10.1016/S0306-4522(99)00453-4 Willis, 2006, The evolving roles of axonally synthesized proteins in regeneration, Current Opinion in Neurobiology, 16, 111, 10.1016/j.conb.2006.01.002 Xu, 2004, Insulin as an in vivo growth factor, Experimental Neurology, 188, 43, 10.1016/j.expneurol.2004.03.008 Yasuda, 1987, Abnormalities of endoneurial microvessels and sural nerve pathology in diabetic neuropathy, Neurology, 37, 20, 10.1212/WNL.37.1.20 Zhang, 2001, Human C-peptide dose dependently prevents early neuropathy in the BB/Wor-rat, International Journal of Experimental Diabetes Research, 2, 187, 10.1155/EDR.2001.187 Zherebitskaya, 2009, Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: Role of glucose-induced oxidative stress, Diabetes, 58, 1356, 10.2337/db09-0034 Zochodne, 2002, Nerve and ganglion blood flow in diabetes: An appraisal, 161 Zochodne, 2007, Diabetes mellitus and the peripheral nervous system: Manifestations and mechanisms, Muscle & Nerve, 36, 144, 10.1002/mus.20785 Zochodne, 2014, Mechanisms of diabetic neuron damage: Molecular pathways, Handbook of Clinical Neurology, 126, 379, 10.1016/B978-0-444-53480-4.00028-X Zochodne, 1992, Normal blood flow but lower oxygen tension in diabetes of young rats: Microenvironment and the influence of sympathectomy, Canadian Journal of Physiology and Pharmacology, 70, 651, 10.1139/y92-083 Zochodne, 1999, Evidence for nitric oxide and nitric oxide synthase activity in proximal stumps of transected peripheral nerves, Neuroscience, 91, 1515, 10.1016/S0306-4522(98)00729-5 Zochodne, 1999, Increased peripheral nerve microvessels in early experimental diabetic neuropathy: Quantitative studies of nerve and dorsal root ganglia, Journal of the Neurological Sciences, 166, 40, 10.1016/S0022-510X(99)00111-2 Zochodne, 2008, Neuronal targeting in diabetes mellitus: A story of sensory neurons and motor neurons, The Neuroscientist, 14, 311, 10.1177/1073858408316175 Zochodne, 2004, Accelerated diabetic neuropathy in axons without neurofilaments, Brain, 127, 2193, 10.1093/brain/awh251 Zochodne, 2001, Does diabetes target ganglion neurons? Progressive sensory neuron involvement in long term experimental diabetes, Brain, 124, 2319, 10.1093/brain/124.11.2319