Unraveling the contribution of pancreatic beta-cell suicide in autoimmune type 1 diabetes

Journal of Theoretical Biology

Volumn 375, Issue , 2015, Pages 77-87

  Jaberi Douraki, Majid ^a   Schnell, Santiago ^b   Pietropaolo, Massimo ^b   Khadra, Anmar ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Beta cell homicide and suicide; ER stress in T1D; Mathematical model; Uncertainty and sensitivity analysis; Unfolded protein response

Indexed keywords

INSULIN;

ALGORITHM; ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; CELL DEATH; CYTOLOGY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; EXPERIMENTAL DIABETES MELLITUS; HOMEOSTASIS; HUMAN; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PANCREAS ISLET BETA CELL; PATHOLOGY; UNFOLDED PROTEIN RESPONSE;

ALGORITHMS; ANIMALS; APOPTOSIS; CELL DEATH; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED NOD; MODELS, BIOLOGICAL; UNFOLDED PROTEIN RESPONSE;

EID: 84901084963     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2014.05.003     Document Type: Article

References (67)

1. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. Molecular Biology of the Cell 2002, New York, Garland Science. 4th edition.
2. Aldridge B.B., Burke J.M., Lauffenburger D.A., Sorger P.K. Physicochemical modelling of cell signalling pathways. Nat. Cell Biol. 2006, 8:1195-1203.
3. Anelli T., Sitia R. Protein quality control in the early secretory pathway. EMBO J. 2008, 27:315-327.
4. Atkinson M.A., Bluestone J.A., Eisenbarth G.S., Hebrok M., Herold K.C., Accili D., Pietropaolo M., Arvan P.R., Von Herrath M., Markel D.S., Rhodes C.J. How does type 1 diabetes develop?. the notion of homicide or β-cell suicide revisited. Diabetes 2011, 60(5):1370-1379.
5. Atkinson M.A., Eisenbarth G.S. Type 1 diabetes. new perspectives on disease pathogenesis and treatment. Lancet 2001, 358(9277):221-229.
6. Bluestone J.A., Herold K., Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 2010, 464:1293-1300.
7. Böber E., Dündar B., Büyükgebiz A. Partial remission phase and metabolic control in type 1 diabetes mellitus in children and adolescents. J. Pediatr. Endocrinol. Metab. 2001, 14(4):435-442.
8. Bottazzo G.F. Lawrence lecture. Death of a beta cell. homicide or suicide?. Diabet. Med. 1986, 3:119-130.
9. Cardozo A.K., Ortis F., Storling J., Feng Y.M., Rasschaert J., et al. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic b-cells. Diabetes 2005, 54:452-461.
10. Chase H.P., MacKenzie T.A., Burdick J., Fiallo-Scharer R., Walravens P., Klingensmith G., Rewers M. Redefining the clinical remission period in children with type 1 diabetes. Pediatr. diabetes 2004, 5(1):16-19.
11. De Boer R.J., Perelson A.S. T cell repertoires and competitive exclusion. J. Theor. Biol. 1994, 169(4):375-390.
12. Dor Y., Brown J., Martinez O.I., Melton D.A. Adult pancreatic beta-cells are formed by self-duplication rather than stem cell differentiation. Nature 2004, 429:41-46.
13. Erguler K., Pieri M., Deltas C. A mathematical model of the unfolded protein stress response reveals the decision mechanism for recovery, adaptation and apoptosis. BMC Syst. Biol. 2013, 7(16):1-18.
14. Fontés G., Zarrouki B., Hagman D.K., et al. Glucolipotoxicity age-dependently impairs beta cell function in rats despite a marked increase in beta cell mass. Diabetologia 2010, 53:2369-2379.
15. Ghaemmaghami S., Huh W., Bower K., Howson R.W., Belle A., et al. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
16. Gyllenberg M., Yan P., Wang Y. A 3D competitive Lotka-Volterra system with three limit cycles. a falsification of a conjecture by Hofbauer and So. Appl. Math. Lett. 2006, 19(1):1-7.
17. Hofbauer J., Sigmund K. The Theory and Evolution of Dynamical Systems 1988, Cambridge University Press, Cambridge, UK.
18. Hofbauer J., So J.W.H. Multiple limit cycles for three dimensional competitive Lotka-Volterra equations. Appl. Math. Lett. 1994, 7:65-70.
19. Homann D., Eisenbarth G.S. An immunologic homunculus for type 1 diabetes. J. Clin. Investig. 2006, 116:1212-1215.
20. Jacob J., Baltimore D. Modelling T-cell memory by genetic marking of memory T cells in vivo. Nature 1999, 399:593-597.
21. Jo J., Choi M.Y., Koh D.S. Size distribution of mouse Langerhans islets. Biophys. J. 2007, 93:2655-2666.
22. Jost J.L., Drake J.F., Fredrickson A.G., Tsuchiya H.M. Inter-actions of Tetrahymena pyrisformis, Escherichia cole, Azotobacter vinelandii, and glucose in a minimal medium. J. Bacteriol. 1973, 113:834-840.
23. Jaberi-Douraki, M., Pietropaolo, M., Khadra, A., 2014. Predictive models of type 1 diabetes progression: understanding T-cell cycles and their implications on autoantibody release. PLoS ONE 9(4): e93326. http://dx.doi.org/10.1371/journal.pone.0093326.
24. Kholodenko B.N. Cell-signalling dynamics in time and space. Nat. Rev. Mol. Cell Biol. 2006, 7:165-176.
25. Kitano H. Systems biology. a brief overview. Science 2002, 295:1662-1664.
26. Khadra A., Pietropaolo M., Nepom G.T., Sherman A. Investigating the role of T-cell avidity and killing efficacy in relation to type 1 Diabetes prediction. PLOS One 2011, 6(5):e14796.
27. Khadra A., Santamaria P., Edelstein-Keshet L. The role of low avidity T cells in the protection against type 1 diabetes. a modeling investigation. J. Theor. Biol. 2009, 256:126-141.
28. Khadra A., Santamaria P., Edelstein-Keshet L. The pathogenicity of selfantigen decreases at high levels of autoantigenicity. a computational approach. Int. Immunol. 2010, 22:571-582.
29. Khadra A., Tsai S., Santamaria P., Edelstein-Keshet L. On how monospecific memory-like autoregulatory CD8+ T cells can blunt diabetogenic autoimmunity. a computational approach. J. Immunol. 2010, 185:5962-5972.
30. Kim P., Lee P., Levy D. Modeling regulation mechanisms in the immune system. J. Theor. Biol. 2007, 246:33-69.
31. Kopito R.R., Ron D. Conformational disease. Nat. Cell Biol. 2000, 2:E207-E209.
32. Kurrer, M.O., Pakala, S.V., Hanson, H.L., Katz, J.D., 1997. β cell apoptosis in T cell-mediated autoimmune diabetes. Proc. Natl. Acad. Sci. 94 (1), 213-218.
33. Liu, M., Hodish, I., Rhodes, C.J., Arvan, P., 2007. Proinsulin maturation, misfolding, and proteotoxicity. Proc. Natl. Acad. Sci. 104, 15841-15846.
34. Lu Z., Luo Y. Two limit cycles in three-dimensional Lotka-Volterra systems. Comput. Math. Appl. 2002, 44(1):51-66.
35. Lu Z., Luo Y. Three limit cycles for a three-dimensional Lotka-Volterra competitive system with a heteroclinic cycle. Comput. Math. Appl. 2003, 46(2):231-238.
36. Mahaffy J.M., Edelstein-Keshet L. Modeling cyclic waves of circulating Tcells in autoimmune diabetes. SIAM J. Appl. Math. 2007, 67:915-1937.
37. Marchetti P., Bugliani M., Lupi R., et al. The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients. Diabetologia 2007, 50:2486-2494.
38. + T-cells in autoimmune diabetes. implications for antigen-specific therapy. Int. Immunol. 2006, 18:1067-1077.
39. Marino S., Hogue I.B., Ray C.J., Kirschner D.E. A methodology for performing global uncertainty and sensitivity analysis in systems biology. J. Theor. Biol. 2008, 254(1):178-196.
40. May R.M., Leonard W.J. Nonlinear aspects of competition between three species. SIAM J. Appl. Math. 1975, 29(2):243-253.
41. Mickens R.E. Nonstandard Finite Difference Models of Differential Equations 1994, World Scientific, Singapore, pp. 311-313.
42. Mickens R.E. Advances in the Applications of Nonstandard Finite Difference Schemes 2005, World Scientific, Clark Atlanta University, USA.
43. Moriwaki M., Itoh N., Miyagawa J., Yamamoto K., Imagawa A., Yamagata K., et al. Fas and Fas ligand expression in inflamed islets in pancreas sections of patients with recent-onset Type I diabetes mellitus. Diabetologia 1999, 42(11):1332-1340.
44. Morran M.P., Casu A., Arena V.C., Pietropaolo S., Zhang Y.J., et al. Humoral autoimmunity against the extracellular domain of the neuroendocrine autoantigen IA-2 heightens the risk of type 1 diabetes. Endocrinology 2010, 151:2528-2537.
45. Morran M.P., Omenn G.S., Pietropaolo M. Immunology and genetics of type 1 diabetes. Mt. Sinai J. Med. 2008, 75:314-327.
46. Muhammad B.J., Swift P.G., Raymond N.T., Botha J.L. Partial remission phase of diabetes in children younger than age 10 years. Arch. Dis. Child. 1999, 80(4):367-369.
47. Nepom G.T. Approaching the Heisenberg principle of immunology. Clin. Immunol. 2008, 129:1-2.
48. O'Sullivan-Murphy B., Urano F. ER Stress as a trigger for β-cell dysfunction and autoimmunity in type 1 diabetes. Diabetes 2012, 61(4):780-781.
49. Petrovsky N., Silva D., Socha L., Slattery R., Charlton B. The role of Fas ligand in beta cell destruction in autoimmune diabetes of NOD mice. Ann. N. Y. Acad. Sci. 2002, 958(1):204-208.
50. Pietropaolo M., Towns R., Eisenbarth G.S. Humoral autoimmunity in type 1 diabetes. prediction, significance, and detection of distinct disease subtypes. Cold Spring Harb. Perspect. Med. 2012, a012831.
51. Robles D.T., Eisenbarth G.S., Wang T., Erlich H.A., Bugawan T.L., et al. Identification of children with early onset and high incidence of anti-islet autoantibodies. Clin. Immunol. 2002, 102(3):217-224.
52. Rutkowski D.T., Kaufman R.J. A trip to the ER. coping with stress. Trends Cell Biol. 2004, 14:20-28.
53. Schuit, F.C., Tveld, P.A.I., Pipeleers, D.G., 1988. Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pacreatic beta-cells. Proc. Natl. Acad. Sci USA 85, 3865-3869.
54. Schnell S. A model of the unfolded protein response. pancreatic β-cell as a case study. Cell. Physiol. Biochem. 2009, 23(4-6):233-244.
55. Schnell S., Grima R., Maini P.K. Multiscale modeling in biology. Am. Sci. 2007, 95:134-142.
56. Skowera A., Ellis R.J., Varela-Calviño R., Arif S., Huang G.C., et al. CTLs are targeted to kill β cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope. J. Clin. Investig. 2008, 118:3390-3402.
57. Standifer N.E., Burwell E.A., Gersuk V.H., Greenbaum C.J., Nepom G.T. Changes in autoreactive T cell avidity during type 1 diabetes development. Clin. Immunol. 2009, 132:312-320.
58. Sugarman J., Tsai S., Santamaria P., Khadra A. Quantifying the importance of pMHC valency, total pMHC dose and frequency on nanoparticle therapeutic efficacy. Immunol. Cell Biol. 2013, 91:350-359.
59. Effect of intensive therapy on residual beta-cell function in patients with type 1 diabetes in the diabetes control and complications trial. A randomized, controlled trial. Ann. Intern. Med. 1998, 128:517-523. The Diabetes Control and Complications Trial Research Group.
60. Valitutti S., Müller S., Cella M., Padovan E., Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 1995, 375:148-151.
61. + T cells to antigen stimulation in vivo. Nat. Immunol. 2000, 1:47-53.
62. Viola A., Lanzavecchia A. T cell activation determined by T cell receptor number and tunable thresholds. Science 1996, 273:104-106.
63. von Herrath M., Sanda S., Herold K. Type 1 diabetes as a relapsing-remitting disease?. Nat. Rev. Immunol. 2007, 7:988-994.
64. Wang Q., Huang W., Li B.L. Limit cycles and singular point quantities for a 3D Lotka-Volterra system. Appl. Math. Comput. 2011, 217(21):8856-8859.
65. Wells A.D., Gudmundsdottir H., Turka L.A. Following the fate of individual T cells throughout activation and clonal expansion. signals from T cell receptor and CD28 differentially regulate the induction and duration of a proliferative response. J. Clin. Investig. 1997, 100:3173-3183.
66. Zeeman M.L. Hopf bifurcations in competitive three dimensional Lotka-Volterra systems. Dyn. Stab. Syst. 1993, 8:189-217.
67. Zeeman M.L., van den Driessche P. Three-Dimensional Competitive Lotka-Volterra Systems with no Periodic Orbits. SIAM J. Appl. Math. 1998, 58(1):227-234.