Fluorescent biosensors illuminate calcium levels within defined beta-cell endosome subpopulations

Cell Calcium

Volumn 57, Issue 4, 2015, Pages 263-274

  Albrecht, Tobias ^a   Zhao, Yongxin ^b   Nguyen, Trang Hai ^b   Campbell, Robert E ^b   Johnson, James D ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Ca2+ biosensor; Endosome; Fluorescence imaging; Glucose; Pancreatic beta cell; PH biosensor

Indexed keywords

CALCIUM ION; RAB PROTEIN; RAB5A PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; CALCIUM; FLUORESCENT DYE; GLUCOSE;

ACIDITY; ARTICLE; BIOSENSOR; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL PH; CELL SUBPOPULATION; CHILD; ENDOSOME; GEM GECO1; HUMAN; HUMAN CELL; ILLUMINATION; INTRACELLULAR SPACE; MALE; MKEIMA; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SCHOOL CHILD; ANIMAL; CALCIUM SIGNALING; CELL LINE; FLUORESCENCE IMAGING; GENETIC PROCEDURES; METABOLISM; MOUSE; PH; PROCEDURES; ULTRASTRUCTURE; UTILIZATION;

ANIMALS; BIOSENSING TECHNIQUES; CALCIUM; CALCIUM SIGNALING; CELL LINE; CHILD; ENDOSOMES; FLUORESCENT DYES; GLUCOSE; HUMANS; HYDROGEN-ION CONCENTRATION; INSULIN-SECRETING CELLS; MALE; MICE; OPTICAL IMAGING;

EID: 84930382639     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2015.01.008     Document Type: Article

References (52)

1. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
2. Johnson J.D., Bround M.J., White S.A., Luciani D.S. Nanospaces between endoplasmic reticulum and mitochondria as control centres of pancreatic beta-cell metabolism and survival. Protoplasma 2012, 249(Suppl. 1):S49-S58.
3. 2+ signals. Biochem. Cell Biol. 2000, 78:217-240.
4. Lindenburg L., Merkx M. Colorful calcium sensors. Chembiochem 2012, 13:349-351.
5. Demaurex N., Frieden M. Measurements of the free luminal ER Ca(2+) concentration with targeted cameleon fluorescent proteins. Cell Calcium 2003, 34:109-119.
6. 2+ channels in endoplasmic reticulum stress and beta-cell death. Diabetes 2009, 58:422-432.
7. Traub L.M., Kornfeld S. The trans-Golgi network: a late secretory sorting station. Curr. Opin. Cell Biol. 1997, 9:527-533.
8. Pizzo P., Lissandron V., Capitanio P., Pozzan T. Ca(2+) signalling in the Golgi apparatus. Cell Calcium 2011, 50:184-192.
9. Patel S., Muallem S. Acidic Ca(2+) stores come to the fore. Cell Calcium 2011, 50:109-112.
10. Brownlee C. Cellular calcium imaging: so, what's new?. Trends Cell Biol. 2000, 10:451-457.
11. Platta H.W., Stenmark H. Endocytosis and signaling. Curr. Opin. Cell Biol. 2011, 23:393-403.
12. 2+ homeostasis in beta-cells, American journal of physiology. Endocrinol. Metab. 2009, 296:E690-E701.
13. 2+ uniporter (MCU) contribute to metabolism-secretion coupling in clonal pancreatic beta-cells. J. Biol. Chem. 2012, 287:34445-34454.
14. Nakai J., Ohkura M., Imoto K. A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat. Biotechnol. 2001, 19:137-141.
15. Akerboom J., Chen T.W., Wardill T.J., Tian L., Marvin J.S., Mutlu S., Calderon N.C., Esposti F., Borghuis B.G., Sun X.R., Gordus A., Orger M.B., Portugues R., Engert F., Macklin J.J., Filosa A., Aggarwal A., Kerr R.A., Takagi R., Kracun S., Shigetomi E., Khakh B.S., Baier H., Lagnado L., Wang S.S., Bargmann C.I., Kimmel B.E., Jayaraman V., Svoboda K., Kim D.S., Schreiter E.R., Looger L.L. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 2012, 32:13819-13840.
16. 2+ indicators. Science 2011, 333:1888-1891.
17. Bolte S., Cordelieres F.P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 2006, 224:213-232.
18. Carpenter A.E., Jones T.R., Lamprecht M.R., Clarke C., Kang I.H., Friman O., Guertin D.A., Chang J.H., Lindquist R.A., Moffat J., Golland P., Sabatini D.M. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 2006, 7:R100.
19. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
20. Sternberg S.R. Biomedical image-processing. Computer 1983, 16:22-34.
21. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
22. 2+ buffers. Methods Cell Biol. 1994, 40:3-29.
23. Pryor P.R., Mullock B.M., Bright N.A., Lindsay M.R., Gray S.R., Richardson S.C., Stewart A., James D.E., Piper R.C., Luzio J.P. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 2004, 5:590-595.
24. Advani R.J., Yang B., Prekeris R., Lee K.C., Klumperman J., Scheller R.H. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 1999, 146:765-776.
25. Martinez-Arca S., Rudge R., Vacca M., Raposo G., Camonis J., Proux-Gillardeaux V., Daviet L., Formstecher E., Hamburger A., Filippini F., D'Esposito M., Galli T. A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9011-9016.
26. Martinez-Arca S., Alberts P., Zahraoui A., Louvard D., Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J. Cell Biol. 2000, 149:889-900.
27. Rink J., Ghigo E., Kalaidzidis Y., Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
28. Huotari J., Helenius A. Endosome maturation. EMBO J. 2011, 30:3481-3500.
29. Violot S., Carpentier P., Blanchoin L., Bourgeois D. Reverse pH-dependence of chromophore protonation explains the large Stokes shift of the red fluorescent protein mKeima. J. Am. Chem. Soc. 2009, 131:10356-10357.
30. Piatkevich K.D., Hulit J., Subach O.M., Wu B., Abdulla A., Segall J.E., Verkhusha V.V. Monomeric red fluorescent proteins with a large Stokes shift. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5369-5374.
31. 2+ homeostasis: different molecules for different purposes?. Cell. Mol. Life Sci. 2012, 69:1077-1104.
32. Johnson J.D., Misler S. Nicotinic acid-adenine dinucleotide phosphate-sensitive calcium stores initiate insulin signaling in human beta cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14566-14571.
33. Christensen K.A., Myers J.T., Swanson J.A. pH-dependent regulation of lysosomal calcium in macrophages. J. Cell Sci. 2002, 115:599-607.
34. Misler S., Barnett D.W., Gillis K.D., Pressel D.M. Electrophysiology of stimulus-secretion coupling in human beta-cells. Diabetes 1992, 41:1221-1228.
35. Sakurada M., Kanatsuka A., Saitoh T., Makino H., Yamamura K., Miyazaki J., Kikuchi M., Yoshida S. Relation between glucose-stimulated insulin secretion and intracellular calcium accumulation studied with a superfusion system of a glucose-responsive pancreatic beta-cell line MIN6. Endocrinology 1993, 132:2659-2665.
36. Orrenius S., Zhivotovsky B., Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 2003, 4:552-565.
37. Johnson J.D., Kuang S., Misler S., Polonsky K.S. Ryanodine receptors in human pancreatic beta cells: localization and effects on insulin secretion. FASEB J. 2004, 18:878-880.
38. Gerasimenko J.V., Tepikin A.V., Petersen O.H., Gerasimenko O.V. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 1998, 8:1335-1338.
39. Calcraft P.J., Ruas M., Pan Z., Cheng X., Arredouani A., Hao X., Tang J., Rietdorf K., Teboul L., Chuang K.-T., Lin P., Xiao R., Wang C., Zhu Y., Lin Y., Wyatt C.N., Parrington J., Ma J., Evans A.M., Galione A., Zhu M.X. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 2009, 459:596-600.
40. Wang X., Zhang X., Dong X.P., Samie M., Li X., Cheng X., Goschka A., Shen D., Zhou Y., Harlow J., Zhu M.X., Clapham D.E., Ren D., Xu H. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 2012, 151:372-383.
41. Lelouvier B., Puertollano R. Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway. J. Biol. Chem. 2011, 286:9826-9832.
42. Kamiya M., Johnsson K. Localizable and highly sensitive calcium indicator based on a BODIPY fluorophore. Anal. Chem. 2010, 82:6472-6479.
43. Raveh A., Valitsky M., Shani L., Coorssen J.R., Blank P.S., Zimmerberg J., Rahamimoff R. Observations of calcium dynamics in cortical secretory vesicles. Cell Calcium 2012, 52:217-225.
44. 2+ and pH probe. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E3539-E3548.
45. Dror V., Kalynyak T.B., Bychkivska Y., Frey M.H., Tee M., Jeffrey K.D., Nguyen V., Luciani D.S., Johnson J.D. Glucose and endoplasmic reticulum calcium channels regulate HIF-1beta via presenilin in pancreatic beta-cells. J. Biol. Chem. 2008, 283:9909-9916.
46. Rorsman P., Braun M., Zhang Q. Regulation of calcium in pancreatic alpha- and beta-cells in health and disease. Cell Calcium 2012, 51:300-308.
47. Johnson J.D., Luciani D.S. Mechanisms of pancreatic beta-cell apoptosis in diabetes and its therapies. Adv. Exp. Med. Biol. 2010, 654:447-462.
48. Dean P.M. Ultrastructural morphometry of the pancreatic beta-cell. Diabetologia 1973, 9:115-119.
49. Marbet P., Rahner C., Stieger B., Landmann L. Quantitative microscopy reveals 3D organization and kinetics of endocytosis in rat hepatocytes. Microsc. Res. Tech. 2006, 69:693-707.
50. Griffiths G., Back R., Marsh M. A quantitative analysis of the endocytic pathway in baby hamster kidney cells. J. Cell Biol. 1989, 109:2703-2720.
51. Hay J.C. Calcium: a fundamental regulator of intracellular membrane fusion?. EMBO Rep. 2007, 8:236-240.
52. Meier P.C., Zünd R.E. Statistical Methods in Analytical Chemistry 1993, 105. Wiley, New York.