Genetically encoded Ca2+ indicators: Using genetics and molecular design to understand complex physiology

Journal of Physiology

Volumn 578, Issue 1, 2007, Pages 55-67

  Kotlikoff, Michael I ^a  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; INDICATOR; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; RECOMBINANT PROTEIN; CALMODULIN; GENETICALLY ENCODED CALCIUM INDICATOR; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

BIOSENSOR; GENETIC ENGINEERING; GENETICALLY ENCODED CALCIUM INDICATOR; IN VIVO STUDY; MAMMAL; MOLECULE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ANIMAL; BACTERIAL ARTIFICIAL CHROMOSOME; CALCIUM SIGNALING; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HUMAN; MOUSE; PHYSIOLOGY; AMINO TERMINAL SEQUENCE; BLEACHING; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CELL LINEAGE; CIRCULAR PERMUTATION; MOLECULAR BIOLOGY; PROTEIN EXPRESSION; QUANTUM YIELD; TRANSGENICS;

ANIMALS; CALCIUM SIGNALING; CHROMOSOMES, ARTIFICIAL, BACTERIAL; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; INDICATORS AND REAGENTS; MICE; MICE, TRANSGENIC; RECOMBINANT PROTEINS;

EID: 33845782385     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.120212     Document Type: Review

References (68)

1. Adams SR, Harootunian AT, Buechler YJ, Taylor SS & Tsien RY (1991). Fluorescence ratio imaging of cyclic AMP in single cells. Nature 349, 694-697.
2. Bacskai BJ, Hochner B, Mahaut-Smith M, Adams SR, Kaang BK, Kandel ER & Tsien RY (1993). Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260, 222-226.
3. Baird GS, Zacharias DA & Tsien RY (1999). Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A 96, 11241-11246.
4. Baker LC, London B, Choi BR, Koren G & Salama G (2000). Enhanced dispersion of repolarization and refractoriness in transgenic mouse hearts promotes reentrant ventricular tachycardia. Circ Res 86, 396-407.
5. Benaim G & Villalobo A (2002). Phosphorylation of calmodulin. Functional implications. Eur J Biochem 269, 3619-3631.
6. Copeland NG, Jenkins NA & Court DL (2001). Recombineering: A powerful new tool for mouse functional genomics. Nat Rev Genet 2, 769-779.
7. Dickson RM, Cubitt AB, Tsien RY & Moerner WE (1997). On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388, 355-358.
8. Eberhard M & Erne P (1989). Kinetics of calcium binding to fluo-3 determined by stopped-flow fluorescence. Biochem Biophys Res Commun 163, 309-314.
9. Eberhard M & Erne P (1991). Calcium binding to fluorescent calcium indicators: Calcium green, calcium orange and calcium crimson. Biochem Biophys Res Commun 180, 209-215.
10. 2+ channels revealed by FRET in single living cells. Neuron 31, 973-985.
11. Fiala A & Spall T (2003). In vivo calcium imaging of brain activity in Drosophila by transgenic cameleon expression. Sci STKE 2003, PL6.
12. Giepmans BN, Adams SR, Ellisman MH & Tsien RY (2006). The fluorescent toolbox for assessing protein location and function. Science 312, 217-224.
13. Gong SC, Yang XW, Li CJ & Heintz N (2002). Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6K gamma origin of replication. Genome Res 12, 1992-1998.
14. Griesbeck O (2004). Fluorescent proteins as sensors for cellular functions. Curr Opin Neurobiol 14, 636-641.
15. Griesbeck O, Baird GS, Campbell RE, Zacharias DA & Tsien RY (2001). Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem 276, 29188-29194.
16. Gross S & Piwnica-Worms D (2005). Spying on cancer: Molecular imaging in vivo with genetically encoded reporters. Cancer Cell 7, 5-15.
17. Guerrero G, Siegel MS, Roska B, Loots E & Isacoff EY (2002). Tuning FlaSh: Redesign of the dynamics, voltage range, and color of the genetically encoded optical sensor of membrane potential. Biophys J 83, 3607-3618.
18. Hancock JF, Magee AI, Childs JE & Marshall CJ (1989). All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57, 1167-1177.
19. 2+ indicator proteins in transgenic mice under TET control. PLoS Biol 2, 763-775.
20. Heim N & Griesbeck O (2004). Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J Biol Chem 279, 14280-14286.
21. Heim R & Tsien RY (1996). Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6, 178-182.
22. Heintz N (2001). BAC to the future: The use of bac transgenic mice for neuroscience research. Nat Rev Neurosci 2, 861-870.
23. Higashijima S, Masino MA, Mandel G & Fetcho JR (2003). Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J Neurophysiol 90, 3986-3997.
24. Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY & Dostmann WR (2001). Spatiotemporal dynamics of guanosine 3′,5′-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci U S A 98, 2437-2442.
25. Huang WY, Aramburu J, Douglas PS & Izumo S (2000). Transgenic expression of green fluorescence protein can cause dilated cardiomyopathy. Nat Med 6, 482-483.
26. 2+ in single suprachiasmatic nucleus neurons. Neuron 38, 253-263.
27. Ikura M, Clore GM, Gronenborn AM, Zhu G, Klee CB & Bax A (1992). Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638.
28. 2+-sensing transgenic mice: postsynaptic signaling in smooth muscle. J Biol Chem 279, 21461-21468.
29. Jurado LA, Chockalingam PS & Jarrett HW (1999). Apocalmodulin. Physiol Rev 79, 661-682.
30. Karasawa S, Araki T, Nagai T, Mizuno H & Miyawaki A (2004). Cyan-emitting and orange-emitting fluorescent proteins as a donor/ acceptor pair for fluorescence resonance energy transfer. Biochem J 381, 307-312.
31. Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY & Schafer WR (2000). Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26, 583-594.
32. Lee EC, Yu DG, de Velasco JM, Tessarollo L, Swing DA, Court DL, Jenkins NA & Copeland NG (2001). A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65.
33. 2+ sensor. Proc Natl Acad Sci U S A 103, 13232-13237.
34. Mank M, Reiff DF, Heim N, Friedrich MW, Borst A & Griesbeck O (2006). A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys J 90, 1790-1796.
35. Miyawaki A (2003). Fluorescence imaging of physiological activity in complex systems using GFP-based probes. Curr Opin Neurobiol 13, 591-596.
36. 2+ measurements using improved cameleons. Proc Natl Acad Sci U S A 96, 2135-2140.
37. 2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887.
38. Mizuno H, Sawano A, Eli P, Hama H & Miyawaki A (2001). Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer. Biochemistry 40, 2502-2510.
39. 2+. Proc Natl Acad Sci U S A 98, 3197-3202.
40. 2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101, 10554-10559.
41. 2+ probe composed of a single green fluorescent protein. Nat Biotechnol 19, 137-141.
42. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P & Miesenbock G (2002). Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474.
43. Nguyen AW & Daugherty PS (2005). Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat Biotechnol 23, 355-360.
44. Nyqvist D, Mattsson G, Kohler M, Lev-Ram V, Andersson A, Carlsson PO, Nordin A, Berggren PO & Jansson L (2005). Pancreatic islet function in a transgenic mouse expressing fluorescent protein. J Endocrinol 186, 333-341.
45. 2+ imaging of dendritic spines. Anal Chem 77, 5861-5869.
46. 2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13, 521-530.
47. 2+ indicators. J Neurosci 24, 9572-9579.
48. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J & Borst A (2005). In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25, 4766-4778.
49. 2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. A new class of fluorescent indicators. J Biol Chem 272, 13270-13274.
50. 2+ and cytosolic cAMP dynamics in mouse skeletal muscle. J Cell Biol 173, 187-193.
51. 2+ uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol 166, 527-536.
52. Rudolf R, Mongillo M, Rizzuto R & Pozzan T (2003). Looking forward to seeing calcium. Nat Rev Mol Cell Biol 4, 579-586.
53. Sanbe A, Gulick J, Hanks MC, Liang Q, Osinska H & Robbins J (2003). Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Circ Res 92, 609-616.
54. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE & Tsien RY (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22, 1567-1572.
55. Siegel MS & Isacoff EY (1997). A genetically encoded optical probe of membrane voltage. Neuron 19, 735-741.
56. Siemering KR, Golbik R, Sever R & Haseloff J (1996). Mutations that suppress the thermosensitivity of green fluorescent protein. Curr Biol 6, 1653-1663.
57. Takahashi N, Nemoto T, Kimura R, Tachikawa A, Miwa A, Okado H, Miyashita Y, Iino M, Kadowaki T & Kasai H (2002). Two-photon excitation imaging of pancreatic islets with various fluorescent probes. Diabetes 51 (Suppl. 1), S25-S28.
58. 2+ indicator GCaMP2. Proc Natl Acad Sci U S A 103, 4753-4758.
59. Tallini YN, Shu B, Greene KS, Deng KY, Doran R, Fisher PJ, Zipfel W & Kotlikoff MI (2006 b). BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol Genomics (in press).
60. 2+ imaging by a new calmodulin-GFP fusion molecule. Nat Struct Biol 8, 1069-1073.
61. Tsai PS, Friedman B, Ifarraguerri AI, Thompson BD, Lev-Ram V, Schaffer CB, Xiong Q, Tsien RY, Squier JA & Kleinfeld D (2003). All-optical histology using ultrashort laser pulses. Neuron 39, 27-41.
62. Tsien RY (2003). Breeding molecules to spy on cells. Harvey Lect 99, 77-93.
63. Verkhusha VV & Lukyanov KA (2004). The molecular properties and applications of Anthozoa fluorescent proteins and chromoproteins. Nat Biotechnol 22, 289-296.
64. Wang JW, Wong AM, Flores J, Vosshall LB & Axel R (2003). Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271-282.
65. Warming S, Costantino N, Court DL, Jenkins NA & Copeland NG (2005). Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33, e36.
66. Zaccolo M & Pozzan T (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295, 1711-1715.
67. Zacharias DA, Violin JD, Newton AC & Tsien RY (2002). Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916.
68. Zhang J, Campbell RE, Ting AY & Tsien RY (2002). Creating new fluorescent probes for cell biology. Nat Rev Mol Cell Biol 3, 906-918.