Dilation of the endoplasmic reticulum in beta cells due to molecular overcrowding?. Kinetic simulations of extension limits and consequences on proinsulin synthesis

Biophysical Chemistry

Volumn 140, Issue 1-3, 2009, Pages 115-121

  Despa, F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Beta cell dysfunction mechanism; Diabetes; ER dilation; ER stress condition; Molecular crowding effect; Proinsulin denaturation

Indexed keywords

PROINSULIN;

ARTICLE; CHEMICAL REACTION KINETICS; CHEMICAL STRUCTURE; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; INSULIN RELEASE; INSULIN SYNTHESIS; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROCESS MODEL; PROTEIN DENATURATION; PROTEIN FOLDING;

COMPUTER SIMULATION; ENDOPLASMIC RETICULUM; HUMANS; INSULIN-SECRETING CELLS; MODELS, BIOLOGICAL; PROINSULIN; PROTEIN DENATURATION; PROTEIN FOLDING;

EID: 58549117847     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2008.12.003     Document Type: Article

References (59)

1. Howell S.L., and Bird G.St.J. Biosynthesis and secretion of insulin. Brit. Med. Bull. 45 (1989) 19-36
2. -/- mice reveals a role for translational control in secretory cell survival. Mol. Cell. 7 (2001) 1153-1163
3. Harding H.P., and Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51 (2002) S455-S461
4. Ron D. Proteotoxicity in the endoplasmic reticulum: lessons from the Akita diabetic mouse. J. Clin. Invest. 109 (2002) 443-445
5. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., Gannon M., Ma K., McNaughton K., and Cavener D.R. Mol. Cell. Biol. 22 (2002) 3864-3874
6. Oyadomari S., Araki E., and Mori M. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta cells. Apoptosis 7 (2002) 335-345
7. Araki E., Oyadomari S., and Mori M. Endoplasmic reticulum stress and diabetes mellitus. Intern. Med. 42 (2003) 7-14
8. Izumi T., Yokota-Hashimoto H., Shengli Z., Wang J., Halban P.A., and Takeuchi T. Dominant negative pathogenesis by mutant proinsulin in the Akita diabetic mouse. Diabetes 52 (2003) 409-416
9. Zuber C., Fan J.Y., Guhl B., and Roth J. Misfolded proinsulin accumulates in expanded pre-Golgi intermediates and endoplasmic reticulum subdomains in pancreatic beta cells of Akita mice. FASEB J. 18 (2004) 917-919
10. Nozaki J., Kubota H., Yoshida H., Naitoh M., Yoshinaga T., Mori K., Koizumi A., and Nagata K. The endoplasmicreticulum stress response is stimulated through the continuous activation of transcription factors ATF6 and XBP1 inIns2q/Akita pancreatic B cells. Genes Cells 9 (2004) 261-270
11. Hayden M.R., Tyagi S.C., Kerklo M.M., and Nicolls M.R. Type 2 diabetes mellitus as a conformational disease. JOP. J Pancreas (Online) 6 (2005) 287-302
12. Yoshinaga T., Nakatome K., Nozaki J., Naitoh M., Hoseki J., Kubota H., Nagata K., and Koizumi A. Proinsulin lacking the A7-B7 disulfide bond, Ins2Akita, tends to aggregate due to the exposed hydrophobic surface. Biol. Chem. 386 (2005) 1077-1085
13. Liu M., Li Y., Cavener D., and Arvan P. Proinsulin disulfide maturation and misfolding in the endoplasmic reticulum. J. Biol. Chem. 280 (2005) 13209-13212
14. Pirot P., Eizirik D.L., and Cardozo A.K. Interferon-r potentials endoplasmic reticulum stress-induced death by reducing pancreatic beta cell defence mechanisms. Diabetologia 49 (2006) 1229-1236
15. Laybutt D.R., Preston A.M., Akerfeldt M.C., Kench J.G., Busch A.K., Biankin A.V., and Biden T.J. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50 (2007) 752-763
16. Elouil M., Bensellam M., Guiot Y., et al. Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 50 (2007) 1442-1452
17. Liu M., Hodish I., Rhodes C.J., and Arvan P. Proinsulin maturation, misfolding, and proteotoxicity. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 15841-15846
18. Støy J., Edghill E.L., Flanagan S.E., Ye H., Paz V.P., Pluzhnikov A., Below J.E., Hayes M.G., Cox N.J., Lipkind G.M., Lipton R.B., Greeley S.A., Patch A.M., Ellard S., Steiner D.F., Hattersley A.T., Philipson L.H., and Bell G.I. Neonatal Diabetes International Collaborative Group. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 15040-15044
19. Marchetti P., Bugliani M., Lupi R., Marselli M., Masini M., Boggi U., Filipponi F., Weir G.C., Eizirik D.L., and Cnop M. The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients. Diabetologia 50 (2007) 2486-2494
20. Despa F., and Ionescu-Tirgoviste C. Accumulation of toxic residues in beta cells can impair conversion of proinsulin to insulin via molecular crowding effects. Proc. Rom. Acad. B 4 (2007) 225-233
21. Schuit F.C., In't Veld P.A., and Pipeleers D.G. Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 3865-3869
22. Alarcón C., Lincoln B., and Rhodes C.J. The biosynthesis of the subtilisin-related proprotein convertase PC3, but no that of the PC2 convertase, is regulated by glucose in parallel to proinsulin biosynthesis in rat pancreatic islets. J. Biol. Chem. 268 (1993) 4276-4280
23. Alarćon C., Leahy J.L., Schuppin G.T., and Rhodes C.J. Increased secretory demand rather than a defect in the proinsulin conversion mechanism causes hyperproinsulinemia in a glucose-infusion rat model of non-insulin-dependent diabetes mellitus. J. Clin. Invest. 95 (1995) 1032-1039
24. Schuppin G.T., and Rhodes C.J. Specific co-ordinated regulation of PC3 and PC2 gene expression with that of preproinsulin in insulin-producing beta TC3 cells. Biochem. J. 313 (1996) 259-268
25. Kaufman R.J. Orchestrating the unfolded protein response in health and disease. J. Clin. Invest. 110 (2002) 1389-1398
26. Rhodes C.J. Type 2 diabetes - a matter of beta-cell life and death. Science 307 (2005) 380-384
27. Schroder M., and Kaufman R.J. ER stress and unfolded protein response. Mutat. Res. 569 (2005) 29-63
28. Marciniak S.J., and Ron D. Endoplasmic reticulum stress signaling in disease. Physiol. Rev. 86 (2006) 1133-1149
29. Poland D. Free energy distributions in proteins. Proteins 45 (2001) 325-336
30. Despa F., and Berry R.S. Inter-basin dynamics on multidimensional potential surfaces. I. Escape rates on complex basin surfaces. J. Chem. Phys. 115 (2001) 8274-9278
31. Ellis J.R. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struck. Biol. 11 (2001) 114-119
32. Ellis J.R., and Minton A.P. Cell biology: join the crowd. Nature 425 (2003) 27-28
33. Hall D., and Minton A.P. Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim. Biophys. Acta 1649 (2003) 127-139
34. Cheung S., Klimov D.K., and Thirumalai D. Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4753-4758
35. Rivas G., Fernandez J.A., and Minton A.P. Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: theory, experiment, and biological significance. Biochemistry 38 (1999) 9379-9388
36. van Den Berg B., Dobson C.M., and Ellis J.R. Effects of macromolecular crowding on protein folding and aggregation. EMBO Journal 18 (1999) 6927-6933
37. Rivas G., Fernandez J.A., and Minton A.P. Direct observation of the enhancement of non-cooperative protein self-assembly by macromolecular crowding. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 3150-3155
38. Despa F., Orgill D.P., and Lee R.C. Effects of crowding on the thermal stability of heterogeneous protein solutions. Ann. Biomed. Eng. 33 (2005) 1125-1131
39. Despa F., Orgill D.P., and Lee R.C. Molecular crowding effects on protein stability. Ann. N.Y. Acad. Sci. 1066 (2005) 54-66
40. Leach A. Molecular Modelling: Principles and Applications. 2nd edn (1997), Pearson Education Ltd., United Kingdom
41. Boublìk T. Statistical thermodynamics of convex molecule fluids. Mol. Phys. 27 (1974) 1415-1427
42. Lebowitz J.L., Helfand E., and Praestgaard E. Scaled particle theory of fluid mixtures. J. Chem. Phys. 43 (1965) 774-779
43. Minton A.P. Confinement as a determinant of macromolecular structure and reactivity. II. Effects of weakly attractive interactions between confined macrosolutes and confining structures. Biophys. J. 68 (1995) 1311-1322
44. Minton A.P. Effect of a concentrated "inert" macromolecular cosolute on the stability of a globular protein with respect to denaturation by heat and by chaotropes: a statistical-thermodynamic model. Biophys. J. 78 (2000) 101-109
45. Minton A.P. Influence of macromolecular crowding upon the stability and state of association of proteins: predictions and observations. J. Pharmaceutical Sci. 94 (2005) 1668-1675
46. Despa F., and Berry R.S. How much can an intermediate state influence competing reactive pathways?. J. Chem. Phys. 120 (2004) 5164-5168
47. Verkman A.S. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 27 (2002) 27-33
48. Sidrauski C., Chapman R., and Walter P. The unfolded protein response: an intracellular signalling pathway with many surprising features. Trends Cell Biol. 8 (1998) 245-249
49. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankne B.A., and Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403 (2000) 98-103
50. Butler A.E., Janson J., Soeller W.C., and Butler P.C. Increased beta-cell apoptosis prevents adaptive increase in beta-cell mass in mouse model of type 2 diabetes: evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes 52 (2003) 2304-2314
51. Butler A.E., Jang J., Gurlo T., Carty M.D., Soeller W.C., and Butler P.C. Diabetes due to a progressive defect in beta-cell mass in rats transgenic for human islet amyloid polypeptide (HIP Rat): a new model for type 2 diabetes. Diabetes 53 (2004) 1509-1516
52. Hayden M.R., and Tyagi S.C. A" is for amylin and amyloid in type 2 diabetes mellitus. JOP. J Pancreas (Online) 2 (2001) 124-139
53. Roberts A.N., Leighton B., Todd J.A., Cockburn D., Schofield P.N., Sutton R., Holt S., Boyd Y., Day A.J., Foot E.A., Willis A.C., Reid K.B.M., and Cooper G.J.S. Molecular and functional characterization of amylin, a peptide associated with type 2 diabetes mellitus. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 9662-9666
54. Westermark P., Li Z.C., Westermark G.T., Leckstrom A., and Steiner D.F. Effects of beta cell granule components on human islet amyloid polypeptide fibril formation. FEBS Lett. 379 (1996) 203-206
55. Paulsson J.F., Andersson A., Westermark P., and Westermark G.T. Intracellular amyloid-like deposits contain unprocessed pro-islet amyloid polyppetide (proIAPP) in beta cells of transgenic overexpressing the gene for human IAPP and transplanted human islets. Diabetologia 49 (2006) 1237-1246
56. Lin C.Y., Gurlo T., Kayed R., et al. Toxic human islet amyloid polypeptide (h-IAPP) oligomers are intracellular and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPP-induced beta-cell apoptosis in h-IAPP transgenic mice. Diabetes 56 (2007) 1324-1332
57. Zraika S., Hull R.L., Udayasankar J., Clark A., Utzschneider K.M., Tong J., Gerchman F., and Kahn S.E. Identification of the amyloid-degrading enzyme neprilysin in mouse islets and potential role in islet amyloidogenesis. Diabetes 56 (2007) 304-310
58. Huang X.F., and Arvan P. Intracellular transport of proinsulin in pancreatic beta-cells. Structural maturation probed by disulfide accessibility. J. Biol. Chem. 270 (1995) 20417-20423
59. Steiner D.F., Chan S.J., Welsh J.M., Nielsen D., Michael J., Tager H.S., and Rubenstein A.H. Models of peptide biosynthesis: the molecular and cellular basis of insulin production. Clin. Invest. Med. 9 (1986) 328-336