Correction: Aged insulin granules display reduced microtubule-dependent mobility and are disposed within actin-positive multigranular bodies (Proceedings of the National Academy of Sciences of the United States of America (2015) 112, 7 (E667-E676) DOI: 10.1073/pnas.1409542112);Aged insulin granules display reduced microtubule-dependent mobility and are disposed within actin-positive multigranular bodies

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 7, 2015, Pages E667-E676

  Hoboth, Peter ^a,b   Müller, Andreas ^a,b   Ivanova, Anna ^a,b   Mziaut, Hassan ^a,b   Dehghany, Jaber ^c   Sönmez, Anke ^a,b   Lachnit, Martina ^a,b   Meyer Hermann, Michael ^c,d   Kalaidzidis, Yannis ^e,f   Solimena, Michele ^a,b,e  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^e MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^f MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Bayesian probability theory; Diabetes; Islets; Processivity; Secretion

Indexed keywords

F ACTIN; GLUCOSE; INSULIN; JASPAMIDE; LATRUNCULIN A; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; ACTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL MOTILITY; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DEPOLYMERIZATION; ELECTRON MICROSCOPY; EXOCYTOSIS; GLUCOSE HOMEOSTASIS; IMMUNOCYTOCHEMISTRY; INS 1 CELL LINE; INSULIN RELEASE; LYSOSOME; MICROTUBULE; MIN6 CELL LINE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SECRETORY GRANULE; ANIMAL; CELL AGING; CONFOCAL MICROSCOPY; METABOLISM; PHYSIOLOGY; SECRETORY VESICLE; TUMOR CELL LINE;

ACTINS; ANIMALS; CELL AGING; CELL LINE, TUMOR; INSULIN; MICROSCOPY, CONFOCAL; MICROTUBULES; RATS; SECRETORY VESICLES;

EID: 84923163826     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505858112     Document Type: Erratum

References (68)

1. De Camilli P, Jahn R (1990) Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52:625-645.
2. Arvan P, Castle D (1998) Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem J 332(Pt 3):593-610.
3. Rhodes CJ, White MF (2002) Molecular insights into insulin action and secretion. Eur J Clin Invest 32(Suppl 3):3-13.
4. Cerasi E, Luft R (1967) The plasma insulin response to glucose infusion in healthy subjects and in diabetes mellitus. Acta Endocrinol (Copenh) 55(2):278-304.
5. Curry DL, Bennett LL, Grodsky GM (1968) Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology 83(3):572-584.
6. Porte D, Jr, Pupo AA (1969) Insulin responses to glucose: Evidence for a two pool system in man. J Clin Invest 48(12):2309-2319.
7. Rorsman P, et al. (2000) The cell physiology of biphasic insulin secretion. News Physiol Sci 15(2):72-77.
8. Henquin JC, Ishiyama N, Nenquin M, Ravier MA, Jonas JC (2002) Signals and pools underlying biphasic insulin secretion. Diabetes 51(Suppl 1):S60-S67.
9. Kahn SE, et al. (2001) Importance of early phase insulin secretion to intravenous glucose tolerance in subjects with type 2 diabetes mellitus. J Clin Endocrinol Metab 86(12):5824-5829.
10. Fava E, et al. (2012) Novel standards in the measurement of rat insulin granules combining electron microscopy, high-content image analysis and in silico modelling. Diabetologia 55(4):1013-1023.
11. Barg S, Eliasson L, Renström E, Rorsman P (2002) A subset of 50 secretory granules in close contact with L-type Ca2+ channels accounts for first-phase insulin secretion in mouse beta-cells. Diabetes 51(Suppl 1):S74-S82.
12. Schulla V, et al. (2003) Impaired insulin secretion and glucose tolerance in beta cellselective Ca(v)1.2 Ca2+ channel null mice. EMBO J 22(15):3844-3854.
13. Ohara-Imaizumi M, et al. (2004) TIRF imaging of docking and fusion of single insulin granule motion in primary rat pancreatic beta-cells: Different behaviour of granule motion between normal and Goto-Kakizaki diabetic rat beta-cells. Biochem J 381(Pt 1):13-18.
14. Ohara-Imaizumi M, et al. (2007) Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis. J Cell Biol 177(4):695-705.
15. Shibasaki T, et al. (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci USA 104(49):19333-19338.
16. Yasuda T, et al. (2010) Rim2alpha determines docking and priming states in insulin granule exocytosis. Cell Metab 12(2):117-129.
17. Xie L, Zhu D, Gaisano HY (2012) Role of mammalian homologue of Caenorhabditis elegans unc-13-1 (Munc13-1) in the recruitment of newcomer insulin granules in both first and second phases of glucose-stimulated insulin secretion in mouse islets. Diabetologia 55(10):2693-2702.
18. Wang H, et al. (2013) The Rab27a effector exophilin7 promotes fusion of secretory granules that have not been docked to the plasma membrane. Mol Biol Cell 24(3): 319-330.
19. Zhu D, et al. (2013) Syntaxin-3 regulates newcomer insulin granule exocytosis and compound fusion in pancreatic beta cells. Diabetologia 56(2):359-369.
20. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T (2005) Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol 171(1):99-109.
21. Kasai K, Fujita T, Gomi H, Izumi T (2008) Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9(7):1191-1203.
22. Degtyar VE, Allersma MW, Axelrod D, Holz RW (2007) Increased motion and travel, rather than stable docking, characterize the last moments before secretory granule fusion. Proc Natl Acad Sci USA 104(40):15929-15934.
23. Seino S, Shibasaki T, Minami K (2011) Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J Clin Invest 121(6):2118-2125.
24. Schatz H, Nierle C, Pfeiffer EF (1975) (Pro-) insulin biosynthesis and release of newly synthesized (pro-) insulin from isolated islets of rat pancreas in the presence of amino acids and sulphonylureas. Eur J Clin Invest 5(6):477-485.
25. Gold G, Gishizky ML, Grodsky GM (1982) Evidence that glucose "marks" beta cells resulting in preferential release of newly synthesized insulin. Science 218(4567): 56-58.
26. Halban PA (1982) Differential rates of release of newly synthesized and of stored insulin from pancreatic islets. Endocrinology 110(4):1183-1188.
27. MacGregor RR, Hamilton JW, Cohn DV (1975) The by-pass of tissue hormone stores during the secretion of newly synthesized parathyroid hormone. Endocrinology 97(1): 178-188.
28. Piercy M, Shin SH (1981) Newly synthesized prolactin is preferentially secreted by the adenohypophysis in a primary cell culture system. Mol Cell Endocrinol 21(1):75-84.
29. Duncan RR, et al. (2003) Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422(6928):176-180.
30. Tsuboi T, Kitaguchi T, Karasawa S, Fukuda M, Miyawaki A (2010) Age-dependent preferential dense-core vesicle exocytosis in neuroendocrine cells revealed by newly developed monomeric fluorescent timer protein. Mol Biol Cell 21(1):87-94.
31. Ivanova A, et al. (2013) Age-dependent labeling and imaging of insulin secretory granules. Diabetes 62(11):3687-3696.
32. Juillerat A, et al. (2003) Directed evolution of O6-alkylguanine-DNA alkyltransferase for efficient labeling of fusion proteins with small molecules in vivo. Chem Biol 10(4): 313-317.
33. Keppler A, et al. (2004) Labeling of fusion proteins of O6-alkylguanine-DNA alkyltransferase with small molecules in vivo and in vitro. Methods 32(4):437-444.
34. Keppler A, Pick H, Arrivoli C, Vogel H, Johnsson K (2004) Labeling of fusion proteins with synthetic fluorophores in live cells. Proc Natl Acad Sci USA 101(27):9955-9959.
35. Keppler A, Arrivoli C, Sironi L, Ellenberg J (2006) Fluorophores for live cell imaging of AGT fusion proteins across the visible spectrum. Biotechniques 41(2):167-170, 172, 174-175.
36. Tirat A, Freuler F, Stettler T, Mayr LM, Leder L (2006) Evaluation of two novel tagbased labelling technologies for site-specific modification of proteins. Int J Biol Macromol 39(1-3):66-76.
37. Halban PA, Wollheim CB (1980) Intracellular degradation of insulin stores by rat pancreatic islets in vitro. An alternative pathway for homeostasis of pancreatic insulin content. J Biol Chem 255(13):6003-6006.
38. Sivia DS, Carlile CJ, Howells WS, König S (1992) Bayesian analysis of quasielastic neutron scattering data. Physica B 182:341-348.
39. Hao M, et al. (2005) Regulation of two insulin granule populations within the reserve pool by distinct calcium sources. J Cell Sci 118(Pt 24):5873-5884.
40. Lacy PE, Walker MM, Fink CJ (1972) Perifusion of isolated rat islets in vitro. Participation of the microtubular system in the biphasic release of insulin. Diabetes 21(10): 987-998.
41. Pipeleers DG, Pipeleers-Marichal MA, Kipnis DM (1976) Microtubule assembly and the intracellular transport of secretory granules in pancreatic islets. Science 191(4222): 88-90.
42. Suprenant KA, Dentler WL (1982) Association between endocrine pancreatic secretory granules and in-vitro-assembled microtubules is dependent upon microtubuleassociated proteins. J Cell Biol 93(1):164-174.
43. Dentler WL, Suprenant KA (1986) Isolation of microtubule-secretory granule complexes from the anglerfish endocrine pancreas. Ann N Y Acad Sci 466:813-831.
44. Varadi A, Ainscow EK, Allan VJ, Rutter GA (2002) Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic beta-cells. J Cell Sci 115(Pt 21):4177-4189.
45. Varadi A, Tsuboi T, Johnson-Cadwell LI, Allan VJ, Rutter GA (2003) Kinesin I and cytoplasmic dynein orchestrate glucose-stimulated insulin-containing vesicle movements in clonal MIN6 beta-cells. Biochem Biophys Res Commun 311(2):272-282.
46. Malaisse WJ, Hager DL, Orci L (1972) The stimulus-secretion coupling of glucoseinduced insulin release. IX. The participation of the beta cell web. Diabetes 21(2, Suppl):594-604.
47. Orci L, Gabbay KH, Malaisse WJ (1972) Pancreatic beta-cell web: Its possible role in insulin secretion. Science 175(4026):1128-1130.
48. van Obberghen E, et al. (1973) Dynamics of insulin release and microtubular-microfilamentous system. I. Effect of cytochalasin B. J Clin Invest 52(5):1041-1051.
49. Van Obberghen E, et al. (1975) Dynamics of insulin release and microtubular-microfilamentous system. VII. Do microfilaments provide the motive force for the translocation and extrusion of beta granules? Diabetes 24(10):892-901.
50. Li G, et al. (1994) Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HIT-T15 cells and pancreatic islets. Mol Biol Cell 5(11): 1199-1213.
51. Varadi A, Tsuboi T, Rutter GA (2005) Myosin Va transports dense core secretory vesicles in pancreatic MIN6 beta-cells. Mol Biol Cell 16(6):2670-2680.
52. Tomas A, Yermen B, Min L, Pessin JE, Halban PA (2006) Regulation of pancreatic betacell insulin secretion by actin cytoskeleton remodelling: Role of gelsolin and cooperation with the MAPK signalling pathway. J Cell Sci 119(Pt 10):2156-2167.
53. Uenishi E, et al. (2013) Actin dynamics regulated by the balance of neuronal Wiskott-Aldrich syndrome protein (N-WASP) and cofilin activities determines the biphasic response of glucose-induced insulin secretion. J Biol Chem 288(36):25851-25864.
54. Riedl J, et al. (2008) Lifeact: A versatile marker to visualize F-actin. Nat Methods 5(7): 605-607.
55. Halban PA (1991) Structural domains and molecular lifestyles of insulin and its precursors in the pancreatic beta cell. Diabetologia 34(11):767-778.
56. Orci L, et al. (1984) Insulin, not C-peptide (proinsulin), is present in crinophagic bodies of the pancreatic B-cell. J Cell Biol 98(1):222-228.
57. Harashima S, Clark A, Christie MR, Notkins AL (2005) The dense core transmembrane vesicle protein IA-2 is a regulator of vesicle number and insulin secretion. Proc Natl Acad Sci USA 102(24):8704-8709.
58. Ivarsson R, Obermüller S, Rutter GA, Galvanovskis J, Renström E (2004) Temperaturesensitive random insulin granule diffusion is a prerequisite for recruiting granules for release. Traffic 5(10):750-762.
59. Veliz LA, et al. (2010) Near-membrane dynamics and capture of TRPM8 channels within transient confinement domains. PLoS ONE 5(10):e13290.
60. Liu D, Meckel T, Long EO (2010) Distinct role of rab27a in granule movement at the plasma membrane and in the cytosol of NK cells. PLoS ONE 5(9):e12870.
61. Gross SP, Vershinin M, Shubeita GT (2007) Cargo transport: Two motors are sometimes better than one. Curr Biol 17(12):R478-R486.
62. Blocker A, Griffiths G, Olivo J-C, Hyman AA, Severin FF (1998) A role for microtubule dynamics in phagosome movement. J Cell Sci 111(Pt 3):303-312.
63. Halban PA, Mutkoski R, Dodson G, Orci L (1987) Resistance of the insulin crystal to lysosomal proteases: Implications for pancreatic B-cell crinophagy. Diabetologia 30(5): 348-353.
64. Chick WL, et al. (1977) A transplantable insulinoma in the rat. Proc Natl Acad Sci USA 74(2):628-632.
65. Asfari M, et al. (1992) Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130(1):167-178.
66. Tokuyasu KT (1980) Immunochemistry on ultrathin frozen sections. Histochem J 12(4): 381-403.
67. Schindelin J, et al. (2012) Fiji: An open source platform for biological image analysis. Nat Methods 9(7):676-682.
68. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122(5):735-749.