Skip to main content
Log in

Neuronal Elements in the Pathogenesis of Type 1 Diabetes

  • Published:
Reviews in Endocrine and Metabolic Disorders Aims and scope Submit manuscript

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  1. Nepom GT. Class II antigens and disease susceptibility. Annu Rev Med 1995;46:17–25.

    Google Scholar 

  2. Thiessen S, Serra P, Amrani A, Verdaguer J, Santamaria P. T-Cell tolerance by dendritic cells and macrophages as a mechanism for the major histocompatibility complex-linked resistance to autoimmune diabetes. Diabetes 2002;51:325–338.

    Google Scholar 

  3. Wicker LS, Todd JA, Peterson LB. Genetic control of autoimmune diabetes in the NOD mouse. Annu Rev Immunol 1995;13:179–200.

    Google Scholar 

  4. Åkerblom HK, Knip M. Putative environmental factors in type 1 diabetes [see comments]. [Review] [273 refs]. Diabetes Metab Rev 1998;14:31–67.

    Google Scholar 

  5. Lipton RB, Atchison J, Dorman JS, Duquesnoy RJ, Eckenrode K, Orchard TJ, LaPorte RE, Riley WJ, Kuller LH, Drash AL, Becker DJ, Trucco M. Genetic, immunological, and metabolic determinants of risk for type 1 diabetes mellitus in families. Diabet Med 1992;9:224–232.

    Google Scholar 

  6. Lipton RB, Kocova M, LaPorte RE, Dorman JS, Orchad TJ, Riley WJ, Drash AL, Becker DJ, Trucco M. Autoimmunity and genetics contribute to the risk of insulin-dependent diabetes mellitus in families: Islet cell antibodies and HLA DQ heterodimers. Amer J Epidemiol 1992;136:503–512.

    Google Scholar 

  7. Hamalainen AM, Ilonen J, Simell O, Savola K, Kulmala P, Kupila A, Simell T, Erkkola R, Koskela P, Knip M. Prevalence and fate of type 1 diabetes-associated autoantibodies in cord blood samples from newborn infants of non-diabetic mothers. Diabetes Metab Res Rev 2002;18:57–63.

    Google Scholar 

  8. Kimpimaki T, Kupila A, Hamalainen AM, Kukko M, Kulmala P, Savola K, Simell T, Keskinen P, Ilonen J, Simell O, Knip M. The first signs of beta-cell autoimmunity appear in infancy in genetically susceptible children from the general population: The finnish type 1 diabetes prediction and prevention study. J Clin Endocrinol Metab 2001;86:4782–4788.

    Google Scholar 

  9. Atkinson MA, Leiter EH. The NOD mouse model of type 1 diabetes: As good as it gets? Nat Med 1999;5:601–604.

    Google Scholar 

  10. Durant S, Geutskens S, Van Blokland SC, Coulaud J, Alves V, Pleau JM, Versnel M, Drexhage HA, Homo-Delarche F. Proapoptosis and antiapoptosis-related molecules during postnatal pancreas development in control and nonobese diabetic mice: Relationship with innervation. Lab Invest 2003;83:227–239.

    Google Scholar 

  11. Trudeau JD, Dutz JP, Arany E, Hill DJ, Fieldus WE, Finegood DT. Neonatal beta-cell apoptosis: A trigger for autoimmune diabetes? Diabetes 2000;49:1–7.

    Google Scholar 

  12. Rosmalen JG, Martin T, Dobbs C, Voerman JS, Drexhage HA, Haskins K, Leenen PJ. Subsets of macrophages and dendritic cells in nonobese diabetic mouse pancreatic inflammatory infiltrates: Correlation with the development of diabetes. Lab Invest 2000;80:23–30.

    Google Scholar 

  13. Rosmalen JG, Pigmans MJ, Kersseboom R, Drexhage HA, Leenen PJ, Homo-Delarche F. Sex steroids influence pancreatic islet hypertrophy and subsequent autoimmune infiltration in nonobese diabetic (NOD) and NODscid mice. Lab Invest 2001;81:231–239.

    Google Scholar 

  14. Rosmalen JG, Homo-Delarche F, Durant S, Kap M, Leenen PJ, Drexhage HA. Islet abnormalities associated with an early influx of dendritic cells and macrophages in NOD and NODscid mice. Lab Invest 2000;80:769–777.

    Google Scholar 

  15. Hoglund P, Mintern J, Waltzinger C, Heath W, Benoist C, Mathis D. Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J Exp Med 1999;189:331–339.

    Google Scholar 

  16. Zhang Y, O'Brien B, Trudeau J, Tan R, Santamaria P, Dutz JP. In situ beta cell death promotes priming of diabetogenic CD8 T lymphocytes. J Immunol 2002;168:1466–1472.

    Google Scholar 

  17. Winer S, Astsaturov I, Cheung RK, Gunaratnam L, Kubiak V, Moscarello MA, O'Connor P, McKerlie C, Becker DJ, Dosch H-M. Type I diabetes and MS patients target islet plus CNS-autoantigens, non-immunized NOD mice can develop autoimmune encephalitis. J Immunol 2001;166:2831–2841.

    Google Scholar 

  18. Salomon B, Rhee L, Bour-Jordan H, Hsin H, Montag A, Soliven B, Arcella J, Girvin AM, Padilla J, Miller SD, Bluestone JA. Development of spontaneous autoimmune peripheral polyneuropathy in b7-2-deficient nod mice. J Exp Med 2001;194:677–684.

    Google Scholar 

  19. Winer S, Tsui H, Lau A, Song A, Li X, Cheung RK, Sampson A, Afifiyan F, Elford A, Jackowski G, Becker DJ, Santamaria P, Ohashi P, Dosch H-M. Autoimmune islet destruction in spontaneous type 1 diabetes is not beta-cell exclusive. Nature Medicine 2003;9:198–205.

    Google Scholar 

  20. Ushiki T, Watanabe S. Distribution and ultrastructure of the autonomic nerves in the mouse pancreas. Microsc Res Tech 1997;37:399–406.

    Google Scholar 

  21. Sunami E, Kanazawa H, Hashizume H, Takeda M, Hatakeyama K, Ushiki T. Morphological characteristics of Schwann cells in the islets of Langerhans of the murine pancreas. Arch Histol Cytol 2001;64:191–201.

    Google Scholar 

  22. Persson-Sjogren S, Zashihin A, Forsgren S. Nerve cells associated with the endocrine pancreas in young mice: An ultrastructural analysis of the neuroinsular complex type I. Histochem J 2001;33:373– 378.

    Google Scholar 

  23. Brinn JE. Pancreatic islet cytology of Ictaluridac (Teleostei). Cell Tissue Res 1975;162:357–365.

    Google Scholar 

  24. Benthem L, Mundinger TO, Taborsky GJ Jr. Parasympathetic inhibition of sympathetic neural activity to the pancreas. Am J Physiol Endocrinol Metab 2001;280:E378–381.

    Google Scholar 

  25. 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.

    Google Scholar 

  26. Dunning BE, Taborsky GJ Jr. Neural control of islet function by norepinephrine and sympathetic neuropeptides. Adv Exp Med Biol 1991;291:107–127.

    Google Scholar 

  27. Dunning BE, Ahren B, Veith RC, Taborsky GJ Jr. Nonadrenergic sympathetic neural influences on basal pancreatic hormone secretion. Am J Physiol 1988;255:E785–792.

    Google Scholar 

  28. Ahren B, Taborsky GJ Jr. Effects of pancreatic noradrenaline infusion on basal and stimulated islet hormone secretion in the dog. Acta Physiol Scand 1988;132:143–150.

    Google Scholar 

  29. Strubbe JH, Steffens AB. Neural control of insulin secretion. Horm Metab Res 1993;25:507–512.

    Google Scholar 

  30. Gerich JE. Lilly lecture 1988. Glucose counterregulation and its impact on diabetes mellitus. Diabetes 1988;37:1608–1617.

    Google Scholar 

  31. Cryer PE, Binder C, Bolli GB, et al. Hypoglycemia in IDDM. Diabetes 1989;38:1193–1199.

    Google Scholar 

  32. Cajal SR. Terminacion de los nervios y tubos glandulares del pancreas de los vertebrados. Trav Lab Histol Faculd Med Barcelona 1891;XII:178–207.

    Google Scholar 

  33. Honjin R. The innervation of the pancreas of the mouse, with special reference to the structure of the peripheral extension of the vegetative nervous system. J Comp Neurol 1956;104:331–371.

    Google Scholar 

  34. Madureira ML. Ultrastructural characterization of a regular schwann-axon-islet complex after the autograft of pancreatic fragments into the spleen of the adult dog. Cell Transplant 1994;3:153– 162.

    Google Scholar 

  35. Bock P. Fine structure of the neuro-insular complex type II in the cat. Arch Histol Jpn 1986;49:189–197.

    Google Scholar 

  36. Reusens-Billen B, Pirlot X, Remacle C, Hoet JJ, de Gasparo M. Localization of GABA high-affinity binding sites in the pancreas of neonatal rat. Cell Tissue Res 1984;235:503–508.

    Google Scholar 

  37. Donev S, Petkov P, Marquie G, Duhault J. Ultrastructure of the neuro-insular complexes in the pancreas of sand rats (Psammomys obesus). Acta Diabetol Lat 1983;20:347–356.

    Google Scholar 

  38. Dahl E. The fine structure of the pancreatic nerves of the domestic fowl. Z Zellforsch Mikrosk Anat 1973;136:501–510.

    Google Scholar 

  39. Kobayashi S, Fujita T. Fine structure of mammalian and avian pancreatic islets with special reference to D cells and nervous elements. Z Zellforsch Mikrosk Anat 1969;100:340–363.

    Google Scholar 

  40. Araque A, Carmignoto G, Haydon PG. Dynamic signaling between astrocytes and neurons. Annu Rev Physiol 2001;63:795–813.

    Google Scholar 

  41. Gudino-Cabrera G, Nieto-Sampedro M. Schwann-like macroglia in adult rat brain. Glia 2000;30:49–63.

    Google Scholar 

  42. Mirsky R, Jessen KR. The neurobiology of Schwann cells. Brain Pathol 1999;9:293–311.

    Google Scholar 

  43. Pierucci D, Cicconi S, Bonini P, Ferrelli F, Pastore D, Matteucci C, Marselli L, Marchetti P, Ris F, Halban P, Oberholzer J, Federici M, Cozzolino F, Lauro R, Borboni P, Marlier LN. NGF-withdrawal induces apoptosis in pancreatic beta cells in vitro. Diabetologia 2001;44:1281–1295.

    Google Scholar 

  44. George M, Ayuso E, Casellas A, Costa C, Devedjian JC, Bosch F. Beta cell expression of IGF-I leads to recovery from type 1 diabetes. J Clin Invest 2002;109:1153–1163.

    Google Scholar 

  45. Teitelman G, Guz Y, Ivkovic S, Ehrlich M. Islet injury induces neurotrophin expression in pancreatic cells and reactive gliosis of periislet Schwann cells. J Neurobiol 1998;34:304–318.

    Google Scholar 

  46. Polak M, Scharfmann R, Seilheimer B, Eisenbarth G, Dressler D, Verma IM, Potter H. Nerve growth factor induces neuron-like differentiation of an insulin-secreting pancreatic beta cell line. Proc Natl Acad Sci USA 1993;90:5781–5785.

    Google Scholar 

  47. Scharfmann R, Tazi A, Polak M, Kanaka C, Czernichow P. Expression of functional nerve growth factor receptors in pancreatic beta-cell lines and fetal rat islets in primary culture. Diabetes 1993;42:1829–1836.

    Google Scholar 

  48. Fayad W, Czernichow P, Scharfmann R. Implication of nitric oxide in NGF-induced cell differentiation: Differences between neuronal and beta cells. J Neuroendocrinol 1997;9:807–812.

    Google Scholar 

  49. Armati PJ, Pollard JD, Gatenby P. Rat and human Schwann cells in vitro can synthesize and express MHC molecules. Muscle Nerve 1990;13:106–116.

    Google Scholar 

  50. Kingston AE, Bergsteinsdottir K, Jessen KR, Van der Meide PH, Colston MJ, Mirsky R. Schwann cells co-cultured with stimulated T cells and antigen express major histocompatibility complex (MHC) class II determinants without interferon-gamma pretreatment: Synergistic effects of interferon-gamma and tumor necrosis factor on MHC class II induction. Eur J Immunol 1989;19:177–183.

    Google Scholar 

  51. Constantin G, Piccio L, Bussini S, Pizzuti A, Scarpini E, Baron P, Conti G, Pizzul S, Scarlato G. Induction of adhesion molecules on human schwann cells by proinflammatory cytokines, an immunofluorescence study. J Neurol Sci 1999;170:124–130.

    Google Scholar 

  52. Gold R, Toyka KV, Hartung HP. Synergistic effect of IFN-gamma and TNF-alpha on expression of immune molecules and antigen presentation by Schwann cells. Cell Immunol 1995;165:65–70.

    Google Scholar 

  53. Tsuyuki Y, Fujimaki H, Hikawa N, Fujita K, Nagata T, Minami M. IFN-gamma induces coordinate expression of MHC class Imediated antigen presentation machinery molecules in adult mouse Schwann cells. Neuroreport 1998;9:2071–2075.

    Google Scholar 

  54. Lilje O. The processing and presentation of endogenous and exogenous antigen by Schwann cells in vitro. Cell Mol Life Sci 2002;59:2191–2198.

    Google Scholar 

  55. Spierings E, de Boer T, Wieles B, Adams LB, Marani E, Ottenhoff TH. Mycobacterium leprae-specific, HLA class IIrestricted killing of human Schwann cells by CD4+ Th1 cells: A novel immunopathogenic mechanism of nerve damage in leprosy. J Immunol 2001;166:5883–5888.

    Google Scholar 

  56. Lilje O, Armati PJ. Restimulation of resting autoreactive T cells by Schwann cells in vitro. Exp Mol Pathol 1999;67:164–174.

    Google Scholar 

  57. Koski CL. Mechanisms of Schwann cell damage in inflammatory neuropathy. J Infect Dis 1997;176(Suppl 2):S169–S172.

    Google Scholar 

  58. Argall KG, Armati PJ, Pollard JD, Watson E, Bonner J. Interactions between CD4+ T-cells and rat Schwann cells in vitro. 1. Antigen presentation by Lewis rat Schwann cells to P2-specific CD4+T-cell lines. J Neuroimmunol 1992;40:1–18.

    Google Scholar 

  59. Lisak RP, Bealmear B. Differences in the capacity of gammainterferons from different species to induce class I and II major histocompatibility complex antigens on neonatal rat Schwann cells in vitro. Pathobiology 1992;60:322–329.

    Google Scholar 

  60. Bergsteinsdottir K, Kingston A, Mirsky R, Jessen KR. Rat Schwann cells produce interleukin-1. J Neuroimmunol 1991;34:15–23.

    Google Scholar 

  61. Steinhoff U, Schoel B, Kaufmann SH. Lysis of interferon-gamma activated Schwann cell by cross-reactive CD8+ alpha/beta T cells with specificity for the mycobacterial 65 kd heat shock protein. Int Immunol 1990;2:279–284.

    Google Scholar 

  62. Wekerle H, Schwab M, Linington C, Meyermann R. Antigen presentation in the peripheral nervous system: Schwann cells present endogenous myelin autoantigens to lymphocytes. Eur J Immunol 1986;16:1551–1557.

    Google Scholar 

  63. Wohlleben G, Ibrahim SM, Schmidt J, Toyka KV, Hartung HP, Gold R. Regulation of Fas and FasL expression on rat Schwann cells. Glia 2000;30:373–381.

    Google Scholar 

  64. Gold R, Zielasek J, Kiefer R, Toyka KV, Hartung HP. Secretion of nitrite by Schwann cells and its effect on T-cell activation in vitro. Cell Immunol 1996;168:69–77.

    Google Scholar 

  65. Murwani R, Hodgkinson S, Armati P. Tumor necrosis factor alpha and interleukin-6 mRNA expression in neonatal Lewis rat Schwann cells and a neonatal rat Schwann cell line following interferon gamma stimulation. J Neuroimmunol 1996;71:65–71.

    Google Scholar 

  66. Constable AL, Armati PJ, Hartung HP. DMSO induction of the leukotriene LTC4 by Lewis rat Schwann cells. J Neurol Sci 1999;162:120–126.

    Google Scholar 

  67. Constable AL, Armati PJ, Toyka KV, Hartung HP. Production of prostanoids by Lewis rat Schwann cells in vitro. Brain Res 1994;635:75–80.

    Google Scholar 

  68. Tofaris GK, Patterson PH, Jessen KR, Mirsky R. Denervated Schwann cells attract macrophages by secretion of leukemia inhibitory factor (LIF) and monocyte chemoattractant protein-1 in a process regulated by interleukin-6 and LIF. J Neurosci 2002;22:6696–6703.

    Google Scholar 

  69. Wohlleben G, Hartung HP, Gold R. Humoral and cellular immune functions of cytokine-treated Schwann cells. Adv Exp Med Biol 1999;468:151–156.

    Google Scholar 

  70. Gonzalez A, Andre-Schmutz I, Carnaud C, Mathis D, Benoist C. Damage control, rather than unresponsiveness, effected by protective DX5+ T cells in autoimmune diabetes. Nat Immunol 2001;2:1117–1125.

    Google Scholar 

  71. Ji H, Korganow AS, Mangialaio S, Hoglund P, Andre I, Luhder F, Gonzalez A, Poirot L, Benoist C, Mathis D. Different modes of pathogenesis in T-cell-dependent autoimmunity: Clues from two TCR transgenic systems. Immunol Rev 1999;169:139–146.

    Google Scholar 

  72. Judkowski V, Pinilla C, Schroder K, Tucker L, Sarvetnick N, Wilson DB. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J Immunol 2001;166:908–917.

    Google Scholar 

  73. Miller KE, Richards BA, Kriebel RM. Glutamine-, glutamine synthetase-, glutamate dehydrogenase-and pyruvate carboxylaseimmunoreactivities in the rat dorsal root ganglion and peripheral nerve. Brain Res 2002;945:202–211.

    Google Scholar 

  74. Kim J, Richter W, Aanstoot HJ, Shi Y, Fu Q, Rajotte R, Warnock G, Baekkeskov S. Differential expression of GAD65 and GAD67 in human, rat, and mouse pancreatic islets. Diabetes 1993;42:1799–1808.

    Google Scholar 

  75. DiLorenzo TP, Graser RT, Ono T, Christianson GJ, Chapman HD, Roopenian DC, Nathenson SG, Serreze DV. Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobese diabetic mice and use a prevalent T cell receptor α chain gene rearrangement. Proc Natl Acad Sci USA 1998;95:12538–12543.

    Google Scholar 

  76. Amrani A, Verdaguer J, Serra P, Tafuro S, Tan R, Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 2000;406:739–742.

    Google Scholar 

  77. Atouf F, Czernichow P, Scharfmann R. Expression of neuronal traits in pancreatic beta cells. Implication of neuron-restrictive silencing factor/repressor element silencing transcription factor, a neuronrestrictive silencer. J Biol Chem 1997;272:1929–1934.

    Google Scholar 

  78. Amrani A, Verdaguer J, Serra P, Tafuro S, Tan R, Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 2000;406:739–742.

    Google Scholar 

  79. Ohashi PS, Oehen S, Buerki K, Pircher H, Ohashi CT, Odermatt B, Malissen B, Zinkernagel RM, Hengartner H. Ablation of “tolerance” and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 1991;65:305–317.

    Google Scholar 

  80. Hamilton-Williams EE, Palmer SE, Charlton B, Slattery RM. Beta cell MHC class I is a late requirement for diabetes. Proc Natl Acad Sci USA 2003;100:6688–6693.

    Google Scholar 

  81. 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.

    Google Scholar 

  82. Saravia-Fernandez F, Faveeuw C, Blasquez-Bulant C, Tappaz M, Throsby M, Pelletier G, Vaudry H, Dardenne M, Homo-Delarche F. Localization of gamma-aminobutyric acid and glutamic acid decarboxylase in the pancreas of the nonobese diabetic mouse. Endocrinology 1996;137:3497–3506.

    Google Scholar 

  83. Tominaga M, Maruyama H, Vasko MR, Baetens D, Orci L, Unger RH. Morphologic and functional changes in sympathetic nerve relationships with pancreatic alpha-cells after destruction of beta-cells in rats. Diabetes 1987;36:365–373.

    Google Scholar 

  84. Ejskjaer NT, Zanone MM, Peakman M. Autoimmunity in diabetic autonomic neuropathy: Does the immune system get on your nerves? Diabet Med 1998;15:723–729.

    Google Scholar 

  85. Cachia MJ, Peakman M, Zanone M, Watkins PJ, Vergani D. Reproducibility and persistence of neural and adrenal autoantibodies in diabetic autonomic neuropathy. Diabet Med 1997;14:461– 465.

    Google Scholar 

  86. Diaz B, Serna J, De Pablo F, de la Rosa EJ. In vivo regulation of cell death by embryonic (pro)insulin and the insulin receptor during early retinal neurogenesis. Development 2000;127:1641–1649.

    Google Scholar 

  87. Alarcon C, Serna J, Perez-Villamil B, de Pablo F. Synthesis and differentially regulated processing of proinsulin in developing chick pancreas, liver and neuroretina. FEBS Lett 1998;436:361–366.

    Google Scholar 

  88. Hernandez-Sanchez C, Lopez-Carranza A, Alarcon C, de La Rosa EJ, de Pablo F. Autocrine/paracrine role of insulin-related growth factors in neurogenesis: Local expression and effects on cell proliferation and differentiation in retina. Proc Natl Acad Sci USA 1995;92:9834–9838.

    Google Scholar 

  89. Dorn A, Rinne A, Hahn HJ, Bernstein HG, Ziegler M. Cpeptide immunoreactive neurons in human brain. Acta Histochem 1982;70:326–330.

    Google Scholar 

  90. Dorn A, Rinne A, Bernstein HG, Hahn HJ, Ziegler M. Insulin and C-peptide in human brain neurons (insulin/C-peptide/brain peptides/immunohistochemistry/radioimmunoassay). J Hirnforsch 1983;24:495–499.

    Google Scholar 

  91. Frolich L, Blum-Degen D, Bernstein HG, Engelsberger S, Humrich J, Laufer S, Muschner D, Thalheimer A, Turk A, Hoyer S, Zochling R, Boissl KW, Jellinger K, Riederer P. Brain insulin and insulin receptors in aging and sporadic Alzheimer's disease. J Neural Transm 1998;105:423–438.

    Google Scholar 

  92. Hart AW, Baeza N, Apelqvist A, Edlund H. Attenuation of FGF signalling in mouse beta-cells leads to diabetes. Nature 2000;408:864– 868.

    Google Scholar 

  93. Bush TG. Enteric glial cells. An upstream target for induction of necrotizing enterocolitis and Crohn's disease? Bioessays 2002;24:130–140.

    Google Scholar 

  94. Oehmichen M, Reifferscheid P. Intramural ganglion cell degeneration in inflammatory bowel disease. Digestion 1977;15:482–496.

    Google Scholar 

  95. Cornet A, Savidge TC, Cabarrocas J, et al. Enterocolitis induced by autoimmune targeting of enteric glial cells: A possible mechanism in Crohn's disease? Proc Natl Acad Sci USA 2001;98:13306–13311.

    Google Scholar 

  96. Neumark T, Dombay M, Gaspardy G. Ultrastructural studies in rheumatoid polyneuropathy. Acta Morphol Acad Sci Hung 1979;27:205–220.

    Google Scholar 

  97. Fox RI, Stern M, Michelson P. Update in Sjogren syndrome. Curr Opin Rheumatol 2000;12:391–398.

    Google Scholar 

  98. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Yang H, UIloa L, Al-Abed Y, Czura CJ, Tracey KJ. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003;421:384–388.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsui, H., Winer, S., Jakowsky, G. et al. Neuronal Elements in the Pathogenesis of Type 1 Diabetes. Rev Endocr Metab Disord 4, 301–310 (2003). https://doi.org/10.1023/A:1025374531151

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025374531151

Navigation