The p75 neurotrophin receptor is required for the major loss of sympathetic nerves from islets under autoimmune attack

Diabetes

Volumn 63, Issue 7, 2014, Pages 2369-2379

  Taborsky Jr , Gerald J ^a,b   Mei, Qi ^b   Bornfeldt, Karin E ^b   Hackney, Daryl J ^c   Mundinger, Thomas 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

[No Author keywords available]

Indexed keywords

GLUCAGON; GLYCOPROTEIN; INSULIN; INSULIN PROMOTOR 2; NEUROPEPTIDE Y; NEUROTROPHIN RECEPTOR P75; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DIABETES MELLITUS; GLUCAGON RELEASE; HYPERGLYCEMIA; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SYMPATHETIC NERVE;

ANIMALS; AUTOIMMUNITY; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FEMALE; GLYCOPROTEINS; INSULIN; ISLETS OF LANGERHANS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, NERVE GROWTH FACTOR; SYMPATHETIC NERVOUS SYSTEM; VIRAL PROTEINS;

EID: 84903164475     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0778     Document Type: Article

References (38)

1. Kuehl M, Stevens MJ. Cardiovascular autonomic neuropathies as complications of diabetes mellitus. Nat Rev Endocrinol 2012;8:405-416
2. Duchen LW, Anjorin A, Watkins PJ, Mackay JD. Pathology of autonomic neuropathy in diabetes mellitus. Ann Intern Med 1980;92:301-303 (Pubitemid 10095640)
3. 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 (Pubitemid 16232399)
4. The DCCT Research Group. Factors in development of diabetic neuropathy. Baseline analysis of neuropathy in feasibility phase of Diabetes Control and Complications Trial (DCCT). Diabetes 1988;37:476-481
5. Tavakoli M, Quattrini C, Abbott C, et al. Corneal confocal microscopy: a novel noninvasive test to diagnose and stratify the severity of human diabetic neuropathy. Diabetes Care 2010;33:1792-1797
6. DCCT. The effect of intensive diabetes therapy on measures of autonomic nervous system function in the Diabetes Control and Complications Trial (DCCT). Diabetologia 1998;41:416-423
7. Navarro X, Sutherland DE, Kennedy WR. Long-term effects of pancreatic transplantation on diabetic neuropathy. Ann Neurol 1997;42:727-736 (Pubitemid 27481545)
8. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001;414:813-820 (Pubitemid 34000785)
9. + sensory neurons control β cell stress and islet inflammation in autoimmune diabetes. Cell 2006;127:1123-1135
10. Schmidt RE, Dorsey DA, Beaudet LN, et al. Non-obese diabetic mice rapidly develop dramatic sympathetic neuritic dystrophy: a new experimental model of diabetic autonomic neuropathy. Am J Pathol 2003;163:2077-2091 (Pubitemid 37310037)
11. Chiu YC, Hua TE, Fu YY, Pasricha PJ, Tang SC. 3-D imaging and illustration of the perfusive mouse islet sympathetic innervation and its remodelling in injury. Diabetologia 2012;55:3252-3261
12. Bolli G, de Feo P, Compagnucci P, et al. Abnormal glucose counterregulation in insulin-dependent diabetes mellitus. Interaction of anti-insulin antibodies and impaired glucagon and epinephrine secretion. Diabetes 1983;32:134-141 (Pubitemid 13180346)
13. Ahrén B. Autonomic regulation of islet hormone secretion - implications for health and disease. Diabetologia 2000;43:393-410 (Pubitemid 30237947)
14. Kurose T, Seino Y, Nishi S, et al. Mechanism of sympathetic neural regulation of insulin, somatostatin, and glucagon secretion. Am J Physiol 1990;258:E220-E227 (Pubitemid 20068600)
15. 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
16. Havel PJ, Veith RC, Dunning BE, Taborsky GJ Jr. Pancreatic noradrenergic nerves are activated by neuroglucopenia but not by 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 (Pubitemid 19007756)
17. Dunning BE, Scott MF, Neal DW, Cherrington AD. Direct quantification of norepinephrine spillover and hormone output from the pancreas of the conscious dog. Am J Physiol 1997;272:E746-E755
18. Cryer PE. Minireview: Glucagon in the pathogenesis of hypoglycemia and hyperglycemia in diabetes. Endocrinology 2012;153:1039-1048
19. Taborsky GJ Jr, Mundinger TO. Minireview: The role of the autonomic nervous system in mediating the glucagon response to hypoglycemia. Endocrinology 2012;153:1055-1062
20. 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
21. Taborsky GJ Jr, Mei Q, Hackney DJ, Figlewicz DP, LeBoeuf R, Mundinger TO. Loss of islet sympathetic nerves and impairment of glucagon secretion in the NOD mouse: relationship to invasive insulitis. Diabetologia 2009;52:2602-2611
22. Persson-Sjögren S, Holmberg D, Forsgren S. Remodeling of the innervation of pancreatic islets accompanies insulitis preceding onset of diabetes in the NOD mouse. J Neuroimmunol 2005;158:128-137 (Pubitemid 39626079)
23. Mei Q, Foulis AK, Fligner C, Hull R. H. N, Gilliam L, Taborsky GJ, Jr.: 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
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-E1054 (Pubitemid 37296326)
25. Zoubina EV, Fan Q, Smith PG. Variations in uterine innervation during the estrous cycle in rat. J Comp Neurol 1998;397:561-571 (Pubitemid 28354328)
26. Singh KK, Park KJ, Hong EJ, et al. Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat Neurosci 2008;11:649-658 (Pubitemid 351748111)
27. Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of antiself (virus) immune response. Cell 1991;65:319-331 (Pubitemid 121006061)
28. Quinson N, Robbins HL, Clark MJ, Furness JB. Locations and innervation of cell bodies of sympathetic neurons projecting to the gastrointestinal tract in the rat. Arch Histol Cytol 2001;64:281-294 (Pubitemid 32847598)
29. von Herrath MG, Dockter J, Oldstone MB. How virus induces a rapid or slow onset insulin-dependent diabetes mellitus in a transgenic model. Immunity 1994;1:231-242
30. Rodriguez-Diaz R, Abdulred MH, Formoso A, et al. Innervation patterns of autonomic axons in the human endocrine pancreas. Cell Metab 2011;14:45-54
31. Gilliam LK, Palmer JP, Taborsky GJ Jr. Tyramine-mediated activation of sympathetic nerves inhibits insulin secretion in humans. J Clin Endocrinol Metab 2007;92:4035-4038 (Pubitemid 47607657)
32. Jahed A, Kawaja MD. The influences of p75 neurotrophin receptor and brain-derived neurotrophic factor in the sympathetic innervation of target tissues during murine postnatal development. Auton Neurosci 2005;118:32-42 (Pubitemid 40431622)
33. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 2001;24:677-736 (Pubitemid 32695243)
34. Sofroniew MV, Howe CL, Mobley WC. Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 2001;24:1217-1281 (Pubitemid 32695259)
35. Lu B, Pang PT, Woo NH. The yin and yang of neurotrophin action. Nat Rev Neurosci 2005;6:603-614 (Pubitemid 41059335)
36. Rosenbaum T, Vidaltamayo R, Sánchez-Soto MC, Zentella A, Hiriart M. Pancreatic beta cells synthesize and secrete nerve growth factor. Proc Natl Acad Sci U S A 1998;95:7784-7788 (Pubitemid 28293331)
37. Teng HK, Teng KK, Lee R, et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 2005;25:5455-5463 (Pubitemid 40770927)
38. Matsumoto T, Rauskolb S, Polack M, et al. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 2008;11:131-133 (Pubitemid 351170498)