doi:

DOI: 10.3724/SP.J.1259.2015.00394

Chinese Bulletin of Botany (植物学报) 2015/50:3 PP.394-404

pH-sensitive Fluorescent Proteins and Their Applications in Plant Cell Biology


Abstract:
pHluorin is a pH-sensitive variant of green fluorescent protein; its fluorescence signals display a strong pH dependence. Since the codon usage was optimized and the site of aberrant splicing was removed, pHluorin and its derivatives have been successfully expressed and used in animal, plant and fungi cells. These pH sensors have helped shed light on measure of the difference in pH of cellular microenvironment and many cell functions for which intracellular pH is an important modulator. Here, we review the characteristics of known pHluorins and their applications in cell biology, particularly plant cell biology. With the improvements in pHluorins by genetic engineering and the advancing in detection technology, the future for pHluorins in plant science is exciting.

Key words:endocytosis;exocytosis;in vivo pH measurement;molecular labelling;pHluorin

ReleaseDate:2015-07-13 09:55:54



邓超, 黄大昉, 宋福平 (2011). 绿色荧光蛋白及其应用. 中国生物工程杂志 31, 96-102.

黄国存, 朱生伟, 董越梅, 孙敬三 (1998). 绿色荧光蛋白及其在植物研究中的应用. 植物学通报 15, 24-30.

李晓娟, 王钦丽, 苏月, 林金星 (2009). 量子点标记及其在植物细胞生物学中的应用. 电子显微学报 28, 495-504.

王锋, 张春雨, 万里川, 王钦丽, 林金星 (2010). 光激活荧光蛋白及其在植物分子细胞生物学研究中的应用. 植物学报 45, 530-540.

周围, 朱丹, 梁滔, 李臣鸿, 吴政星 (2007). 利用TIRFM技术检测PC12细胞中类突触小囊泡的锚定和融合特性. 科学通报 52, 2276-2282.

Arosio D, Garau G, Ricci F, Marchetti L, Bizzarri R, Nifosì R, Beltram F (2007). Spectroscopic and structural study of proton and halide ion cooperative binding to GFP. Bi-ophys J 93, 232-244.

Ashby MC, Ibaraki K, Henley JM (2004). It's green outside:tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci 27, 257-261.

Bagar T, Altenbach K, Read ND, Benčina M (2009). Live-cell imaging and measurement of intracellular pH in filamen-tous fungi using a genetically encoded ratiometric probe. Eukaryot Cell 8, 703-712.

Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011). The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and neces-sary for plant growth and development. Plant Cell 23, 224-239.

Bizzarri R, Arcangeli C, Arosio D, Ricci F, Faraci P, Cardarelli F, Beltram F (2006). Development of a novel GFP-based ratiometric excitation and emission pH indicator for intracellular studies. Biophys J 90, 3300-3314.

Bizzarri R, Serresi M, Luin S, Beltram F (2009). Green fluorescent protein based pH indicators for in vivo use:a review. Anal Bioanal Chem 393, 1107-1122.

Demaurex N (2002). pH Homeostasis of cellular organelles. News Physiol Sci 17, 1-5.

Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schuma-cher K (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18, 715-730.

Esposito A, Gralle M, Dani MAC, Lange D, Wouters FS (2008). pHlameleons:a family of FRET-based protein sensors for quantitative pH imaging. Biochemistry 47, 13115-13126.

Felle HH (1998). The apoplastic pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes:aspects of regulation. J Exp Bot 49, 987-995.

Fricker M, Runions J, Moore I (2006). Quantitative fluo-rescence microscopy:from art to science. Annu Rev Plant Biol 57, 79-107.

Gao DJ, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004). Self-reporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134, 898-908.

Gehring CA, Irving HR, McConchie R, Parish RW (1997). Jasmonates induce intracellular alkalinization and closure of Paphiopedilum guard cells. Ann Bot 80, 485-489.

Gjetting KS, Ytting CK, Schulz A, Fuglsang AT (2012). Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J Exp Bot 63, 3207-3218.

Gonugunta VK, Srivastava N, Puli MR, Raghavendra AS (2008). Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid. Plant Cell Environ 31, 1717-1724.

Grignon C, Sentenac H (1991). pH and ionic conditions in the apoplast. Annu Rev Plant Physiol Plant Mol Biol 42, 103-128.

Hanna ST, Pigeau GM, Galvanovskis J, Clark A, Rorsman P, MacDonald PE (2009). Kiss-and-run exocytosis and fusion pores of secretory vesicles in human β-cells. Pflugers Arch 457, 1343-1350.

Hanson GT, McAnaney TB, Park ES, Rendell MEP, Yar-brough DK, Chu SY, Xi LX, Boxer SG, Montrose MH, Remington SJ (2002). Green fluorescent protein variants as ratiometric dual emission pH sensors. 1. Structural characterization and preliminary application. Biochemistry 41, 15477-15488.

Hoffmann B, Kosegarten H (1995). FITC-dextran for measuring apoplast pH and apoplastic pH gradients between various cell types in sunflower leaves. Physiol Plant 95, 327-335.

Jankowski A, Kim JH, Collins RF, Daneman R, Walton P, Grinstein S (2001). In situ measurements of the pH of mammalian peroxisomes using the fluorescent protein pHluorin. J Biol Chem 276, 48748-48753.

Jin T, Sasaki A, Kinjo M, Miyazaki J (2010). A quantum dot-based ratiometric pH sensor. Chem Commun 46, 2408-2410.

Karagiannis J, Young PG (2001). Intracellular pH homeo-stasis during cell-cycle progression and growth state transition in Schizosaccharomyces pombe. J Cell Sci 114, 2929-2941.

Kirsch T, Paris N, Butler JM, Beevers L, Rogers JC (1994). Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl Acad Sci USA 91, 3403-3407.

Kneen M, Farinas J, Li YX, Verkman AS (1998). Green fluorescent protein as a noninvasive intracellular pH in-dicator. Biophys J 74, 1591-1599.

Kononenko NL, Diril MK, Puchkov D, Kintscher M, Koo SJ, Pfuhl G, Winter Y, Wienisch M, Klingauf J, Breustedt J, Schmitz D, Maritzen T, Haucke V (2013). Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2. Proc Natl Acad Sci USA 110, E526-E535.

Krebs M, Beyhl D, Görlich E, Al-Rasheid KAS, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010). Arabi-dopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107, 3251-3256.

Li ZY, Murthy VN (2001). Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31, 593-605.

Lippincott-Schwartz J, Roberts TH, Hirschberg K (2000). Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16, 557-589.

Lukyanov KA, Chudakov DM, Lukyanov S, Verkhusha VV (2005). Innovation:photoactivatable fluorescent proteins. Nat Rev Mol Cell Biol 6, 885-890.

Machen TE, Leigh MJ, Taylor C, Kimura T, Asano S, Moore HP (2003). pH of TGN and recycling endosomes of H+/K+-ATPase-transfected HEK-293 cells:implications for pH regulation in the secretory pathway. Am J Physiol Cell Physiol 285, C205-C214.

Mahon MJ (2011). pHluorin2:an enhanced, ratiometric, pH-sensitive green florescent protein. Adv Biosci Bio-technol 2, 132-137.

Malinow R, Malenka RC (2002). AMPA receptor traffic-king and synaptic plasticity. Annu Rev Neurosci 25, 103-126.

Martinière A, Desbrosses G, Sentenac H, Paris N (2013a). Development and properties of genetically encoded pH sensors in plants. Front Plant Sci 4, 523.

Martinière A, Bassil E, Jublanc E, Alcon C, Reguera M, Sentenac H, Blumwald E, Paris N (2013b). In vivo in-tracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. Plant Cell 25, 4028-4043.

Miesenböck G, De Angelis DA, Rothman JE (1998). Vi-sualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.

Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997). Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887.

Monshausen GB, Miller ND, Murphy AS, Gilroy S (2011). Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J 65, 309-318.

Moseyko N, Feldman LJ (2001). Expression of pH-sensitive green fluorescent protein in Arabidopsis thaliana. Plant Cell Environ 24, 557-563.

Mühling KH, Sattelmacher B (1995). Apoplastic ion con-centration of intact leaves of field bean (Vicia faba) as in-fluenced by ammonium and nitrate nutrition. J Plant Physiol 147, 81-86.

Nicholson-Tomishima K, Ryan TA (2004). Kinetic efficiency of endocytosis at mammalian CNS synapses re-quires synaptotagmin I. Proc Natl Acad Sci USA 101, 16648-16652.

Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Katsuta H, Ishida H, Nagamatsu S (2002). Monitoring of exocytosis and endocytosis of insulin secretory granules in the pancreatic beta-cell line MIN6 using pH-sensitive green fluorescent protein (pHluorin) and confocal laser microscopy. Biochem J 363, 73-80.

Orij R, Postmus J, Ter Beek A, Brul S, Smits GJ (2009). In vivo measurement of cytosolic and mitochondrial pH us-ing a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology 155, 268-278.

Prosser DC, Whitworth K, Wendland B (2010). Quantitative analysis of endocytosis with cytoplasmic pHluorin chimeras. Traffic 11, 1141-1150.

Quintero FJ, Martinez-Atienza J, Villalta I, Jiang XY, Kim WY, Ali Z, Fujii H, Mendoza I, Yun DJ, Zhu JK, Pardo JM (2011). Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci USA 108, 2611-2616.

Rayle DL, Cleland RE (1992). The Acid Growth Theory of auxin-induced cell elongation is alive and well. Plant Physiol 99, 1271-1274.

Robinson DG, Pimpl P (2014). Receptor-mediated transport of vacuolar proteins:a critical analysis and a new model. Protoplasma 251, 247-264.

Robinson DG, Pimpl P, Scheuring D, Stierhof YD, Sturm S, Viotti C (2012). Trying to make sense of retromer. Trends Plant Sci 17, 431-439.

Saint-Jean B, Seveno-Carpentier E, Alcon C, Neuhaus JM, Paris N (2010). The cytosolic tail dipeptide Ile-Met of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis. Plant Cell 22, 2825-2837.

Sankaranarayanan S, Ryan TA (2000). Real-time measu-rements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol 2, 197-204.

Sankaranarayanan S, Ryan TA (2001). Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 4, 129-136.

Schulte A, Lorenzen I, Böttcher M, Plieth C (2006). A novel fluorescent pH probe for expression in plants. Plant Methods 2, 7.

Sentenac H, Grignon C (1987). Effect of H+ excretion on the surface pH of corn root cells evaluated by using weak acid influx as a pH probe. Plant Physiol 84, 1367-1372.

Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Dis-cosoma sp. red fluorescent protein. Nat Biotechnol 22, 1567-1572.

Shen JB, Zeng YL, Zhuang XH, Sun L, Yao XQ, Pimpl P, Jiang LW (2013). Organelle pH in the Arabidopsis en-domembrane system. Mol Plant 6, 1419-1437.

Shimomura O, Johnson FH, Saiga Y (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59, 223-239.

Staal M, De Cnodder T, Simon D, Vandenbussche F, Van der Straeten D, Verbelen JP, Elzenga T, Vissenberg K (2011). Apoplastic alkalinization is instrumental for the inhibition of cell elongation in the Arabidopsis root by the ethy-lene precursor 1-aminocyclopropane-1-carboxylic acid. Plant Physiol 155, 2049-2055.

Taylor DP, Slattery J, Leopold AC (1996). Apoplastic pH in corn root gravitropism:a laser scanning confocal micro-scopy measurement. Physiol Plant 97, 35-38.

Terskikh A, Fradkov A, Ermakova G, Zaraisky A, Tan P, Kajava AV, Zhao XN, Lukyanov S, Matz M, Kim S, Weissman I, Siebert P (2000). "Fluorescent timer":protein that changes color with time. Science 290, 1585-1588.

Thibaud JB, Davidian JC, Sentenac H, Soler A, Grignon C (1988). H+ cotransports in corn roots as related to the surface pH shift induced by active H+ excretion. Plant Physiol 88, 1469-1473.

Toulon V, Sentenac H, Thibaud JB, Davidian JC, Moulineau C, Grignon C (1992). Role of apoplast acidification by the H+ pump:effect on the sensitivity to pH and CO2 of iron reduction by roots of Brassica napus L. Planta 186, 212-218.

Toulon V, Sentenac H, Thibaud JB, Soler A, Clarkson D, Grignon C (1989). Effect of HCO3-concentration in the absorption solution on the energetic coupling of H+-co-transports in roots of Zea mays L. Planta 179, 235-241.

Tsien RY (2005). Building and breeding molecules to spy on cells and tumors. FEBS Lett 579, 927-932.

Tsuboi T, Rutter GA (2003). Multiple forms of "kiss-and-run" exocytosis revealed by evanescent wave microscopy. Curr Biol 13, 563-567.

Wachter RM (2007). Chromogenic cross-link formation in green fluorescent protein. Acc Chem Res 40, 120-127.

Wan YL, Ash WM 3rd, Fan LS, Hao HQ, Kim MK, Lin JX (2011). Variable-angle total internal reflection fluores-cence microscopy of intact cells of Arabidopsis thaliana. Plant Methods 7, 27.

Wang QL, Zhao YY, Luo WX, Li RL, He QH, Fang XH, De Michele R, Ast C, von Wirén N, Lin JX (2013). Sin-gle-particle analysis reveals shutoff control of the Arabi-dopsis ammonium transporter AMT1;3 by clustering and internalization. Proc Natl Acad Sci USA 110, 13204-13209.

Yang TT, Cheng LZ, Kain SR (1996). Optimized codon usage and chromophore mutations provide enhanced sensitivity with the green fluorescent protein. Nucleic Acids Res 24, 4592-4593.

Zhang YF, Xie QG, Robertson JB, Johnson CH (2012). pHlash:a new genetically encoded and ratiometric luminescence sensor of intracellular pH. PLoS One 7, e43072.