The search for the mechanism of early sympathetic islet neuropathy in autoimmune diabetes

Diabetes, Obesity and Metabolism

Volumn 16, Issue , 2014, Pages 96-101

  Taborsky, G J ^a,b   Mei, Q ^b   Hackney, D J ^c   Mundinger, T O ^b  

^a VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Seattle Institute for Biomedical and Clinical Research   (United States)

Author keywords

Glucagon; Hypoglycaemia; Neuropathy; P75 neurotrophin receptor; Sympathetic; Type 1 diabetes

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUCAGON; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; TNFRSF16 PROTEIN, MOUSE;

AUTOIMMUNE DISEASE; AUTONOMIC DYSFUNCTION; CHRONIC DISEASE; EARLY SYMPATHETIC ISLET NEUROPATHY; GLUCAGON RELEASE; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; LYMPHOCYTIC INFILTRATION; NEUROPATHY; NONHUMAN; REVIEW; STIMULATION; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE; ADRENERGIC SYSTEM; ANIMAL; BIOLOGICAL MODEL; DIABETIC NEUROPATHY; EXPERIMENTAL AUTOIMMUNE NEURITIS; GENETICS; IMMUNOLOGY; INNERVATION; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET; PATHOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; HUMANS; ISLETS OF LANGERHANS; LYMPHOCYTE ACTIVATION; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURITIS, AUTOIMMUNE, EXPERIMENTAL; RECEPTORS, NERVE GROWTH FACTOR; SYMPATHETIC NERVOUS SYSTEM;

EID: 84908502629     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12341     Document Type: Review

References (49)

1. Cryer PE. Glucagon in the pathogenesis of hypoglycemia and hyperglycemia in diabetes. Endocrinology 2012; 153: 1039-1048.
2. Taborsky GJ Jr, Mundinger TO. The role of the autonomic nervous system in mediating the glucagon response to hypoglycemia. Endocrinology 2012; 153: 1055-1062.
3. Havel PJ, Taborsky GJ Jr. The contribution of the autonomic nervous system to changes of glucagon and insulin secretion during hypoglycemic stress. Endocr Rev 1989; 10: 332-350.
4. Havel PJ, Veith RC, Dunning BE, Taborsky GJ Jr. Role for autonomic nervous system to increase pancreatic glucagon secretion during marked insulin-induced hypoglycemia in dogs. Diabetes 1991; 40: 1107-1114.
5. Havel PJ, Parry SJ, Stern JS et al. Redundant parasympathetic and sympathoadrenal mediation of increased glucagon secretion during insulin-induced hypoglycemia in conscious rats. Metabolism 1994; 43: 860-866.
6. Havel PJ, Akpan JO, Curry DL, Stern JS, Gingerich RL, Ahren B. Autonomic control of pancreatic polypeptide and glucagon secretion during neuroglucopenia and hypoglycemia in mice. Am J Physiol 1993; 265: 246-254.
7. Havel PJ, Valverde C. Autonomic mediation of glucagon secretion during insulin-induced hypoglycemia in rhesus monkeys. Diabetes 1996; 45: 960-966.
8. Havel PJ, Ahren B. Activation of autonomic nerves and the adrenal medulla contributes to increased glucagon secretion during moderate insulin-induced hypoglycemia in women. Diabetes 1997; 46: 801-807.
9. Marliss EB, Girardier L, Seydoux J et al. Glucagon release induced by pancreatic nerve stimulation in the dog. J Clin Invest 1973; 52: 1246-1259.
10. Ahren B, Veith RC, Taborsky GJ Jr. Sympathetic nerve stimulation versus pancreatic norepinephrine infusion in the dog: (1) effects on basal release of insulin and glucagon. Endocrinology 1987; 121: 323-331.
11. Havel PJ, Veith RC, Dunning BE, Taborsky GJ Jr. Pancreatic noradrenergic nerves are activated by neuroglucopenia but not hypotension or hypoxia in the dog: evidence for stress-specific and regionally-selective activation of the sympathetic nervous system. J Clin Invest 1988; 82: 1538-1545.
12. Havel PJ, Mundinger TO, Taborsky GJ Jr. Pancreatic sympathetic nerves contribute to increased glucagon secretion during severe hypoglycemia in dogs. Am J Physiol 1996; 270: 20-26.
13. Gerich J, Langlois M, Noacco C, Karam J, Forsham P. Lack of glucagon response to hypoglycemia in diabetes: evidence for an intrinsic pancreatic alpha cell defect. Science 1973; 182: 171-173.
14. Heller SR, Cryer PE. Reduced neuroendocrine and symptomatic responses to subsequent hypoglycemia after 1 episode of hypoglycemia in nondiabetic humans. Diabetes 1991; 40: 223-226.
15. DCCT. 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. N Engl J Med 1993; 329: 977-986.
16. Zhou H, Zhang T, Oseid E, Harmon J, Tonooka N, Robertson RP. Reversal of defective glucagon responses to hypoglycemia in insulin-dependent autoimmune diabetic BB rats. Endocrinology 2007; 148: 2863-2869.
17. Taborsky GJ Jr, Ahren B, Havel PJ. Autonomic mediation of glucagon secretion during hypoglycemia: implications for impaired alpha-cell responses in type 1 diabetes. Diabetes 1998; 47: 995-1005.
18. Gerich J, Davis J, Lorenzi M et al. Hormonal mechanisms of recovery from insulin-induced hypoglycemia in man. Am J Physiol 1979; 236: 380-385.
19. Raju B, Cryer PE. Loss of the decrement in intraislet insulin plausibly explains loss of the glucagon response to hypoglycemia in insulin-deficient diabetes: documentation of the intraislet insulin hypothesis in humans. Diabetes 2005; 54: 757-764.
20. Banarer S, McGregor VP, Cryer PE. Intraislet hyperinsulinemia prevents the glucagon response to hypoglycemia despite an intact autonomic response. Diabetes 2002; 51: 958-965.
21. White NH, Gingerich RL, Levandoski LA, Cryer PE, Santiago JV. Plasma pancreatic polypeptide response to insulin-induced hypoglycemia as a marker for defective glucose counterregulation in insulin-dependent diabetes mellitus. Diabetes 1985; 34: 870-875.
22. Mei Q, Foulis AK, Fligner C et al. Selective Loss of sympathetic nerves from the islet in human type 1 diabetes: a potential mechanism for impaired glucagon responses to hypoglycemia. Diabetes 2006; 55(Suppl. 1): A15.
23. Rodriguez-Diaz R, Abdulred MH, Formoso A et al. Autonomic axons in the human endocrine pancreas show unique innervation patterns. Cell Metab 2011; 14: 45-54.
24. Mundinger TO, Mei Q, Figlewicz DP, Lernmark A, Taborsky GJ Jr. Impaired glucagon response to sympathetic nerve stimulation in the BB diabetic rat: effect of early sympathetic islet neuropathy. Am J Physiol Endocrinol Metab 2003; 285: E1047-1054.
25. Taborsky GJ Jr, Mei Q, Hackney DJ, Figlewicz DP, LeBoeuf R, Mundinger TO. Loss of islet sympathetic nerves and impairment of glucagon secretion: relationship to invasive insulitis. Diabetologia 2009; 52: 2602-2611.
26. Taborsky GJ Jr, Mei Q, Bornfeldt KE, Hackney DJ, Mundinger TO. The p75 neurotrophin receptor is required for the major loss of sympathetic nerves from islets under autoimmune attack. Diabetes 2014; 63: 2369-2379.
27. DCCT. Factors in development of diabetic neuropathy. Baseline analysis of neuropathy in feasibility phase of Diabetes Control and Complications Trial (DCCT). The DCCT Research Group. Diabetes 1988; 37: 476-481.
28. Marliss EB, Nakhooda AF, Poussier P, Sima AAF. The diabetic syndrome of the BB Wistar rat: possible relevance to type I (insulin-dependent) diabetes in man. Diabetologia 1982; 22: 225-232.
29. Signore A, Pozzilli P, Gale EA, Andreani D, Beverley PC. The natural history of lymphocyte subsets infiltrating the pancreas of NOD mice. Diabetologia 1989; 32: 282-289.
30. Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 1991; 65: 319-331.
31. Jacob RJ, Dziura J, Morgen JP, Shulman GI, Sherwin RS. Time course of the defective alpha-cell response to hypoglycemia in diabetic BB rats. Metabolism 1996; 45: 1422-1426.
32. Benson JW Jr, Johnson DG, Palmer JP, Werner PL, Ensinck JW. Glucagon and catecholamine secretion during hypoglycemia in normal and diabetic man. J Clin Endocrinol Metab 1977; 44: 459-464.
33. Mundinger TO, Mei Q, Figlewicz DP, Lernmark A, Taborsky GJ Jr. Impaired glucagon response to sympathetic nerve stimulation in the BB diabetic rat: effect of early sympathetic islet neuropathy. Am J Physiol Endocrinol Metab 2003; 285: E1047-E1054.
34. Yagihashi S, Sima AA. Diabetic autonomic neuropathy. The distribution of structural changes in sympathetic nerves of the BB rat. Am J Pathol 1985; 121: 138-147.
35. Mei Q, Mundinger TO, Lernmark A, Taborsky GJ Jr. Early, selective, and marked loss of sympathetic nerves from the islets of biobreeder diabetic rats. Diabetes 2002; 51: 2997-3002.
36. Rosenbaum T, Vidaltamayo R, Sanchez-Soto MC, Zentella A, Hiriart M. Pancreatic B cells synthesize and secrete nerve growth factor. Proc Natl Acad Sci U S A 1998; 95: 7784-7788.
37. Singh KK, Park KJ, Hong EJ et al. Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat Neurosci 2008; 11: 649-658.
38. Zoubina E, Smith PG. Axonal degeneration and regeneration in rat uterus during the estrous cycle. Auton Neurosci 2000; 84: 176-185.
39. Krizsan-Agbas D, Pedchenko T, Hasan W, Smith PG. Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur J Neurosci 2003; 18: 2760-2768.
40. Lorentz CU, Parrish DC, Alston EN et al. Sympathetic denervation of peri-infarct myocardium requires the p75 neurotrophin receptor. Exp Neurol 2013; 249: 111-119.
41. Ernfors P, Lee KF, Jaenisch R. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 1994; 368: 147-150.
42. Kerschensteiner M, Gallmeier E, Behrens L et al. Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation? J Exp Med 1999; 189: 865-870.
43. Kruse N, Cetin S, Chan A, Gold R, Luhder F. Differential expression of BDNF mRNA splice variants in mouse brain and immune cells. J Neuroimmunol 2007; 182: 13-21.
44. Edling AE, Nanavati T, Johnson JM, Tuohy VK. Human and murine lymphocyte neurotrophin expression is confined to B cells. J Neurosci Res 2004; 77: 709-717.
45. Yang J, Siao CJ, Nagappan G et al. Neuronal release of proBDNF. Nat Neurosci 2009; 12: 113-115.
46. Martinic MM, von Herrath MG. Real-time imaging of the pancreas during development of diabetes. Immunol Rev 2008; 221: 200-213.
47. Korsgren O, Jansson L, Andersson A, Sundler F. Reinnervation of transplanted pancreatic islets. Transplantation 1993; 56: 138-143.
48. Mehra S, Tavakoli M, Kallinikos PA et al. Corneal confocal microscopy detects early nerve regeneration after pancreas transplantation in patients with type 1 diabetes. Diabetes Care 2007; 30: 2608-2612.
49. Raivich G, Kreutzberg GW. Nerve growth factor and regeneration of peripheral nervous system. Clin Neurol Neurosurg 1993; 95: S84-88.