MagFRET: The first genetically encoded fluorescent Mg2+ sensor

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Lindenburg, Laurens H ^a   Vinkenborg, Jan L ^a,b   Oortwijn, Jorn ^a   Aper, Stijn J A ^a   Merkx, Maarten ^a  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b PHILIPS RESEARCH LABORATORIES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CENTRIN; CENTRIN 3; DIGITONIN; MAGNESIUM ION; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; BIOSENSOR; CELL LEVEL; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CELL STIMULATION; CELL STRAIN HEK293; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; EXTRACELLULAR MATRIX; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; MUTATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING;

BIOSENSING TECHNIQUES; CALCIUM-BINDING PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; MAGNESIUM; MODELS, MOLECULAR; MUTAGENESIS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE;

EID: 84891443584     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082009     Document Type: Article

References (60)

1. Shi J, Krishnamoorthy G, Yang Y, Hu L, Chaturvedi N, et al. (2002) Mechanism of magnesium activation of calcium-activated potassium channels. Nature 418: 876-880.
2. Nadler MJ, Hermosura MC, Inabe K, Perraud AL, Zhu Q, et al. (2001) LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411: 590-595.
3. Romani AM (2007) Magnesium homeostasis in mammalian cells. Front Biosci 12: 308-331.
4. Grubbs RD (2002) Intracellular magnesium and magnesium buffering. Biometals 15: 251-259.
5. 2+ concentration in rat heart mitochondria by using entrapped fluorescent probes. Biochem J 271: 627-634.
6. 2+. Magnes Res 19: 225-236.
7. Corkey BE, Duszynski J, Rich TL, Matschinsky B, Williamson JR (1986) Regulation of free and bound magnesium in rat hepatocytes and isolated mitochondria. J Biol Chem 261: 2567-2574.
8. 2+-selective channel. Curr Opin Struct Biol 16: 432-438.
9. Schlingmann KP, Waldegger S, Konrad M, Chubanov V, Gudermann T (2007) TRPM6 and TRPM7-Gatekeepers of human magnesium metabolism. Biochim Biophys Acta, Molecular Basis of Disease 1772: 813-821.
10. Hattori M, Tanaka Y, Fukai S, Ishitani R, Nureki O (2007) Crystal structure of the MgtE Mg2+ transporter. Nature 448: 1072-1075.
11. Konrad M, Weber S (2003) Recent advances in molecular genetics of hereditary magnesium-losing disorders. J Am Soc Nephrol 14: 249-260.
12. Killilea DW, Ames BN (2008) Magnesium deficiency accelerates cellular senescence in cultured human fibroblasts. Proc Natl Acad Sci U S A 105: 5768-5773.
13. Chaudhary DP, Sharma R, Bansal DD (2010) Implications of magnesium deficiency in type 2 diabetes: a review. Biol Trace Elem Res 134: 119-129.
14. Bo S, Pisu E (2008) Role of dietary magnesium in cardiovascular disease prevention, insulin sensitivity and diabetes. Curr Opin Lipidol 19: 50-56.
15. Rude RK, Gruber HE (2004) Magnesium deficiency and osteoporosis: animal and human observations. J Nutr Biochem 15: 710-716.
16. Li FY, Chaigne-Delalande B, Kanellopoulou C, Davis JC, Matthews HF, et al. (2011) Second messenger role for Mg2+ revealed by human T-cell immunodeficiency. Nature 475: 471-476.
17. Trapani V, Farruggia G, Marraccini C, Iotti S, Cittadini A, et al. (2010) Intracellular magnesium detection: imaging a brighter future. Analyst 135: 1855-1866.
18. Cohen SM, Burt CT (1977) 31P nuclear magnetic relaxation studies of phosphocreatine in intact muscle: determination of intracellular free magnesium. Proc Natl Acad Sci U S A 74: 4271-4275.
19. Resnick LM, Gupta RK, Laragh JH (1984) Intracellular free magnesium in erythrocytes of essential hypertension: relation to blood pressure and serum divalent cations. Proc Natl Acad Sci U S A 81: 6511-6515.
20. 2+ contents in erythrocytes: a simple but still undisclosed cell model. Magnes Res 20: 161-167.
21. Kim HM, Yang PR, Seo MS, Yi J-S, Hong JH, et al. (2007) Magnesium ion selective two-photon fluorescent probe based on a benzo[h]chromene derivative for in vivo imaging. J Org Chem 72: 2088-2096.
22. Hwan Myung K, Cheol J, Bo Ra K, Soon-Young J, Jin Hee H, et al. (2007) Environment-sensitive two-photon probe for intracellular free magnesium ions in live tissue. Angew Chem Int Ed Engl 46: 3460-3463.
23. Komatsu H, Miki T, Citterio D, Kubota T, Shindo Y, et al. (2005) Single molecular multianalyte (Ca2+, Mg2+) fluorescent probe and applications to bioimaging. J Am Chem Soc 127: 10798-10799.
24. 2+ imaging. J Am Chem Soc 126: 16353-16360.
25. Raju B, Murphy E, Levy LA, Hall RD, London RE (1989) A fluorescent indicator for measuring cytosolic free magnesium. Am J Physiol Cell Physiol 256: C540-548.
26. Paredes RM, Etzler JC, Watts LT, Zheng W, Lechleiter JD (2008) Chemical calcium indicators. Methods 46: 143-151.
27. Shindo Y, Fujii T, Komatsu H, Citterio D, Hotta K, et al. (2011) Newly developed Mg2+-selective fluorescent probe enables visualization of Mg2+ dynamics in mitochondria. PLoS One 6: e23684.
28. Hurley TW, Ryan MP, Brinck RW (1992) Changes of cytosolic Ca2+ interfere with measurements of cytosolic Mg2+ using mag-fura-2. Am J Physiol Cell Physiol 263: C300-307.
29. Zhou H, Clapham DE (2009) Mammalian MagT1 and TUSC3 are required for cellular magnesium uptake and vertebrate embryonic development. Proc Natl Acad Sci U S A 106: 15750-15755.
30. Xie J, Sun B, Du J, Yang W, Chen HC, et al. (2011) Phosphatidylinositol 4,5-bisphosphate (PIP(2)) controls magnesium gatekeeper TRPM6 activity. Sci Rep 1: 146.
31. Palmer AE, Qin Y, Park JG, McCombs JE (2011) Design and application of genetically encoded biosensors. Trends Biotechnol 29: 144-152.
32. Miyawaki A, Llopis J, Heim R, Michael McCaffery J, Adams JA, et al. (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.
33. Palmer AE, Giacomello M, Kortemme T, Hires SA, Lev-Ram V, et al. (2006) Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13: 521-530.
34. Zhao YX, Araki S, Jiahui WH, Teramoto T, Chang YF, et al. (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 333: 1888-1891.
35. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-U113.
36. Vinkenborg JL, Nicolson TJ, Bellomo EA, Koay MS, Rutter GA, et al. (2009) Genetically encoded FRET sensors to monitor intracellular Zn2+ homeostasis. Nat Methods 6: 737-740.
37. Dittmer PJ, Miranda JG, Gorski JA, Palmer AE (2009) Genetically encoded sensors to elucidate spatial distribution of cellular zinc. J Biol Chem 284: 16289-16297.
38. Miranda JG, Weaver AL, Qin Y, Park JG, Stoddard CI, et al. (2012) New alternately colored FRET sensors for simultaneous monitoring of Zn2+ in multiple cellular locations. PLoS One 7: e49371.
39. Qiao W, Mooney M, Bird AJ, Winge DR, Eide DJ (2006) Zinc binding to a regulatory zinc-sensing domain monitored in vivo by using FRET. Proc Natl Acad Sci U S A 103: 8674-8679.
40. Wegner SV, Arslan H, Sunbul M, Yin J, He C (2010) Dynamic copper(I) imaging in mammalian cells with a genetically encoded fluorescent copper(I) sensor. J Am Chem Soc 132: 2567-2569.
41. Koay MS, Janssen BM, Merkx M (2013) Tuning the metal binding site specificity of a fluorescent sensor protein: from copper to zinc and back. Dalton Trans 42: 3230-3232.
42. Cox JA, Tirone F, Durussel I, Firanescu C, Blouquit Y, et al. (2005) Calcium and magnesium binding to human centrin 3 and interaction with target peptides. Biochemistry 44: 840-850.
43. Golynskiy MV, Rurup WF, Merkx M (2010) Antibody detection by using a FRET-based protein conformational switch. ChemBioChem 11: 2264-2267.
44. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein. J Biol Chem 276: 29188-29194.
45. Bootman MD (2012) Calcium signaling. Cold Spring Harb Perspect Biol 4: a011171.
46. Kalderon D, Roberts BL, Richardson WD, Smith AE (1984) A short amino acid sequence able to specify nuclear location. Cell 39: 499-509.
47. Fischer-Fantuzzi L, Vesco C (1988) Cell-dependent efficiency of reiterated nuclear signals in a mutant simian virus 40 oncoprotein targeted to the nucleus. Mol Cell Biol 8: 5495-5503.
48. Jiang T, Danilo P Jr, Steinberg SF (1998) The thrombin receptor elevates intracellular calcium in adult rat ventricular myocytes. J Mol Cell Cardiol 30: 2193-2199.
49. Hui KY, Jakubowski JA, Wyss VL, Angleton EL (1992) Minimal sequence requirement of thrombin receptor agonist peptide. Biochem Biophys Res Commun 184: 790-796.
50. Isshiki M, Ando J, Korenaga R, Kogo H, Fujimoto T, et al. (1998) Endothelial Ca2+ waves preferentially originate at specific loci in caveolin-rich cell edges. Proc Natl Acad Sci U S A 95: 5009-5014.
51. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101: 10554-10559.
52. Qi Z, Murase K, Obata S, Sokabe M (2000) Extracellular ATP-dependent activation of plasma membrane Ca2+ pump in HEK-293 cells. Br J Pharmacol 131: 370-374.
53. 7Li NMR and fluorescence spectroscopy. Met Based Drugs 7: 357-364.
54. Schweigel M, Park HS, Etschmann B, Martens H (2006) Characterization of the Na+-dependent Mg2+ transport in sheep ruminal epithelial cells. Am J Physiol Gastrointest Liver Physiol 290: G56-65.
55. Okumoto S, Looger LL, Micheva KD, Reimer RJ, Smith SJ, et al. (2005) Detection of glutamate release from neurons by genetically encoded surface-displayed FRET nanosensors. Proc Natl Acad Sci U S A 102: 8740-8745.
56. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41: 6573-6582.
57. Kohn JE, Plaxco KW (2005) Engineering a signal transduction mechanism for protein-based biosensors. Proc Natl Acad Sci U S A 102: 10841-10845.
58. Wang W, Barnabei MS, Asp ML, Heinis FI, Arden E, et al. (2013) Noncanonical EF-hand motif strategically delays Ca2+ buffering to enhance cardiac performance. Nat Med 19: 305-312.
59. Lindenburg L, Merkx M (2012) Colorful calcium sensors. ChemBioChem 13: 349-351.
60. Trapani V, Schweigel-Rontgen M, Cittadini A, Wolf FI (2012) Intracellular magnesium detection by fluorescent indicators. Methods Enzymol 505: 421-444.