Predicting and avoiding subcellular compartmentalization artifacts arising from acetoxymethyl ester calcium imaging probes. The case of fluo-3 AM and a general account of the phenomenon including a problem avoidance chart

References

• Adams SR (2010) How calcium indicators work. C. S. Harbor Protoc. 10: pdb.top70.
   Google Scholar
• Alano CC, Beutner G, Dirksen RT, Gross RA, Shue SS (2002) Mitochondrial permeability transition and calcium dynamics in striatal neurons upon intense NMDA receptor activation. J. Neurochem. 80: 531–538.
   PubMed Web of Science ®Google Scholar
• Almers W, Neher E (1985) The Ca2+ signal from fura-2 loaded mast cells depends strongly on the method of dye-loading. FEBS Lett. 192: 13–18.
   PubMedGoogle Scholar
• Alvarez-Pedraglio CG, Lavandera JL (2001) Chemoinformatic models to predict binding affinities to human serum albumin. J. Med. Chem. 44: 4370–4378.
   PubMedGoogle Scholar
• Babcock DF, Herrington J, Goodwin PC, Park YB, Hille B (1997) Mitochondrial participation in the intracellular Ca2+network. J. Cell Biol. 136: 833–844.
   PubMedGoogle Scholar
• Böcking A, von Deimling OV (1976) Esterases in histochemistry and ultrahistochemistry. Histochem. J. 8: 215–222.
   PubMedGoogle Scholar
• Broder J, Majumder A, Porter E, Srinivasamoorthy G, Keith C, Lauderdale J, Sornborger A (2007) Estimating weak ratiometric signals in imaging data. 1. Dual-channel data. J. Opt. Soc. Am., A 24: 2921–2931.
   Google Scholar
• Christensen H, Garton NJ, Horobin RW, Minnikin DE, Barer MR (1999) Lipid domains of mycobacteria studied with fluorescent molecular probes. Mol. Microbiol. 31: 1561–1572.
   PubMed Web of Science ®Google Scholar
• Collins TJ, Berridge MJ, Lipp P, Bootman MD (2002) Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21: 1616–1627.
   PubMed Web of Science ®Google Scholar
• Colston J, Horobin RW, Rashid-Doubell F, Pediani J, Johal KK (2003) Why fluorescent probes for endoplasmic reticulum are selective: an experimental and QSAR-modeling study. Biotech. & Histochem. 78: 323–332.
   PubMed Web of Science ®Google Scholar
• Crowe WE, Altamirano J, Huerto L, Alvarez-Leefmans FJ (1995) Volume changes in single N1E-115 neuroblastoma cells measured with a fluorescent probe. Neuroscience 69: 283–296.
   PubMedGoogle Scholar
• Davidson SM, Duchen MR (2012) Imaging mitochondrial calcium signalling with fluorescent probes and single or two photon confocal microscopy. Methods Mol. Biol. 810: 219–234.
   PubMedGoogle Scholar
• Davis BJ, Ornstein L (1959) High resolution enzyme localization with a new diazo reagent, ‘hexazonium pararosaniline.‘ J. Histochem. Cytochem.7: 297–298.
   Web of Science ®Google Scholar
• Dedkova EN, Blatter LA (2005) Modulation of mitochondrial Ca2+by nitric oxide in cultured bovine vascular endothelial cells. Am. J. Physiol. Cell Physiol. 289: C836-C845.
   Web of Science ®Google Scholar
• Di Virgilio F, Steinberg TH, Silverstein SC (1990) Inhibition of fura-2 sequestration and secretion with organic anion transport blockers. Cell Calcium 11: 57–62.
   PubMed Web of Science ®Google Scholar
• D’Souza GG, Cheng SM, Boddapati SV, Horobin RW, Weissig V (2008) Nanocarrier–assisted sub-cellular targeting to the site of mitochondria improves the pro-apoptotic activity of paclitaxel. J. Drug Target 16: 578–585.
   PubMed Web of Science ®Google Scholar
• Durrer A, Walther B, Racciatti A, Boss G, Testa G (1991) Structure-metabolism relationships in the hydrolysis of nicotinate esters by rat liver and brain subcellular fractions. Pharm. Res. 8: 832–839.
   PubMed Web of Science ®Google Scholar
• Dustin LB (2000) Ratiometric analysis of calcium mobilization. Clin. Appl. Immunol. Rev. 1: 5–15.
   Google Scholar
• Dvorak AM, Monahan-Early RA, Dvorak HF, Galli SJ (1987) Ultrastructural cytochemical and autoradiographic demonstration of nonspecific esterase(s) in guinea pig basophils. J. Histochem. Cytochem. 35: 351–360.
   PubMedGoogle Scholar
• Goligorsky MS, Hruska KA, Loftus DJ, Elson EL (1986) Alpha 1–adrenergic stimulation and cytoplasmic free calcium concentration in cultured renal proximal tubular cells: evidence for compartmentalization of quin-2 and fura-2. J. Cell. Physiol. 128: 466–474.
   PubMedGoogle Scholar
• Gomori G (1950) An improved histochemical technic for acid phosphatase. Stain Technol. 25: 81–85.
   Web of Science ®Google Scholar
• Hansch C, Leo A (1979) Substituent Constants for Correlation Analysis in Chemistry and Biology. Wiley, New York, pp. 18–43.
   Google Scholar
• Homma R, Baker BJ, Jin L, Garaschuk O, Konnerth A, Cohen LB, Zecevic D (2009) Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364: 2453–2467.
   PubMed Web of Science ®Google Scholar
• Horobin RW (2001) Uptake, distribution, and accumulation of dyes and fluorescent probes within living cells. A structure-activity modeling approach. Adv. Colour Sci. Technol. 4: 101–107.
   Google Scholar
• Horobin RW (2010) Can QSAR models describing small-molecule xenobiotics give useful tips for predicting uptake and localization of nanoparticles in living cells? And if not, why not? Chapter 11 in: Organelle-Specific Pharmaceutical Nanotechnology. Weissig V, D’Souza GGM, Eds., Wiley, Hoboken, NJ. pp. 193–206.
   Google Scholar
• Hoyland J (1993) Fluorescent probes in practice– potential artefacts. In: Fluorescent and Luminescent Probes for Biological Activity, Mason WT, Ed., Academic Press, London. pp. 223–228.
   Google Scholar
• Jobsis PD, Rothstein EC, Balaban RS (2007) Limited utility of acetoxymethyl (AM) based intracellular delivery systems, in vivo: interference by extracellular esterases. J. Microsc. 226: 74–81.
   PubMed Web of Science ®Google Scholar
• Kawanishi T, Blank LM, Harootunian AT, Smith MT, Tsien RY (1989) Ca2+oscillations induced by hormonal stimulation of individual fura-2-loaded hepatocytes. J. Biol. Chem. 264: 12859–12866.
   PubMed Web of Science ®Google Scholar
• Kuba K, Huan SY, NohmiM (1991) Spatial and dynamic changes in intracelluar Ca2+measured by confocal laser-scanning microscopy in bullfrog sympathetic ganglion cells. Neurosci. Res.10: 245–259.
   PubMedGoogle Scholar
• Lee HC, Mohabir R, Smith N, Franz MR, Clusin WT (1988) Effect of ischemia on calcium-dependent fluorescence transients in rabbit hearts containing indo-1. Correlation with monophasic action potentials and contraction. Circulation 78: 1047–1059.
   PubMedGoogle Scholar
• Leroy P, Tran NNP, Bellucci L, Capdeveille-Atkinson C, Nicolas A (1996) Measurement of the intracellular concentration of the calcium dye fura-2 and its esterified precursor using HPLC. LC-GC Internat. January: 28–32.
   Google Scholar
• Lund-Pero M, Jeppson B, Arneklo-Nobin B, Sjögren H-O, Holmgren K, Pero RW (1994) Non-specific steroidal esterase activity and distribution in human and other mammalian tissues. Clin. Chim. Acta 224: 9–20.
   PubMed Web of Science ®Google Scholar
• Monahan RA, Dvorak HF, Dvorak AM (1981) Ultrastructural localization of nonspecific esterase activity in guinea pig and human monocytes, macrophages and lymphocytes. Blood 58: 1089–1099.
   PubMed Web of Science ®Google Scholar
• Monahan-Early RA, Isomura T, Garcia RI, Galli SJ, Dvorak HF, Dvorak AM (1987) Nonspecific esterase activity expressed in Weibel-Palade bodies of cloned guinea pig aortic endothelial cells. J. Histochem. Cytochem. 35: 531–539.
   PubMedGoogle Scholar
• Moore EDW, Becker PL, Fogarty KE, Williams DA, Fay FS (1990) Ca2+imaging in single living cells: theoretical and practical issues. Cell Calcium 11: 157–179.
   PubMed Web of Science ®Google Scholar
• Nathanson MH, Burgstahler AD (1992) Subcellular distribution of cytosolic Ca2 +in isolated rat hepatocyte couplets: evaluation using confocal microscopy. Cell Calcium 13: 89–98.
   PubMed Web of Science ®Google Scholar
• Nutt LK, Pataer A, Pahlert J, Fang B, Roth J, McConkey DJ, Swishert SG (2002) Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2+stores. J. Biol. Chem. 277: 9219–9225.
   PubMed Web of Science ®Google Scholar
• Oakes SG, Martin WJ, Lisek CA, Powis G (1988) Incomplete hydrolysis of the calcium indicator precursor fura-2 pentaacetoxymethyl ester (fura-2 AM) by cells. Anal. Biochem. 169: 159–166.
   PubMedGoogle Scholar
• Paredes RM, Etzler JC, Watts LT, Zheng W, Lechleiter JD (2008) Chemical calcium indicators. Methods 46: 143–151.
   PubMed Web of Science ®Google Scholar
• Peng X-B, Sun M-X, Yang HY (2009) Comparative detection of calcium fluctuations in single female sex cells of tobacco to distinguish calcium signals triggered by in vitro fertilization. J. Integr. Plant Biol. 51: 782–791.
   PubMedGoogle Scholar
• Persidsky MD, Baille GS (1977) Fluorometric test of cell membrane integrity. Cryobiology 14: 322–331.
   PubMed Web of Science ®Google Scholar
• Rashid F, Horobin RW (1990) Interaction of molecular probes with living cells and tissues. 2. A structure-activity analysis of mitochondrial staining by cationic probes, and a discussion of the synergistic nature of image-based and biochemical approaches. Histochemistry 94: 303–308.
   PubMedGoogle Scholar
• Rashid F, Horobin RW (1991) Accumulation of fluorescent non-cationic probes in mitochondria of cultured cells: observations, a proposed mechanism and some implications. J. Microsc. 163: 233–241.
   PubMed Web of Science ®Google Scholar
• Rashid F, Horobin RW, Williams MA (1991) Predicting the behaviour and selectivity of fluorescent probes for lysosomes and related structures by means of structure-activity models. Histochem. J. 23: 450–459.
   PubMedGoogle Scholar
• Roe MW, Lemasters JJ, Herman B (1990) Assessment of fura-2 for measurements of cytosolic free calcium. Cell Calcium 11: 63–73.
   PubMed Web of Science ®Google Scholar
• Spurgeon HA, Stern MD, Baartz G, Raffaeli SR, Hansford RG, Talo A, Lakatta EG, Capogrossi MC (1990) Simultaneous measurement of Ca2+, contraction, and potential in cardiac myocytes. Am. J. Physiol. 258: H574-H586.
   Google Scholar
• Swanson SJ, Choi WG, Chanoca A, Gilroy S (2011) In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. Ann. Rev. Plant Biol. 62: 273–297.
   PubMedGoogle Scholar
• Tenopoulou M, Kurz T, Doulias P-T, Galaris D, Brunk UT (2007) Does the calcein-AM method assay the total cellular ‘labile iron pool’ or only a fraction of it?Biochem. J. 403: 261–266.
   PubMed Web of Science ®Google Scholar
• Thomas D, Tovey SC, Collins TJ, Bootman MD, Berridge MJ, Lipp P (2000) A comparison of fluorescent Ca2+indicator properties and their use in measuring elementary and global Ca2+ signals. Cell Calcium 28: 213–223.
   PubMed Web of Science ®Google Scholar
• Wahl M, Lucherini MJ, Gruenstein E (1990) Intracellular Ca2+measurement with Indo-1 in substrate-attached cells: advantages and special considerations. Cell Calcium 11: 487–500.
   PubMedGoogle Scholar
• Williams DA, Fogarty KE, Tsien RY, Fay FS (1985) Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2. Nature 318: 558–561.
   PubMed Web of Science ®Google Scholar
• Wright KM, Horobin RW and Oparka K (1996) Phloem mobility of fluorescent xenobiotics in Arabidopsis: applicability of a general structure-activity relations model. J. Exp. Bot. 47: 1779–1787.
   Google Scholar