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A Novel Yellowish-Green Fluorescent Protein from the Marine Copepod

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A Novel Yellowish-Green Fluorescent Protein from the Marine Copepod Gene 372 (2006) 18–25 www.elsevier.com/locate/gene A novel yellowish-green fluorescent protein from the marine copepod, Chiridius poppei, and its use as a reporter protein in HeLa cells ⁎ Hiromi Masuda a,b,c, ,1, Yasuhiro Takenaka b,c,1, Atsushi Yamaguchi d, Satoshi Nishikawa e, Hiroshi Mizuno a,b,c a VALWAY Technology Center, NEC Soft, Ltd., 1-18-7, Koto-ku, Tokyo 136-8627, Japan b Department of Biochemistry, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan c Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba, Ibaraki 305-8566, Japan d Faculty of Fisheries Science, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-0821, Japan e Age Dimension Research Center, National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Higashi, Tsukuba, Ibaraki 305-8562, Japan Received 5 July 2005; received in revised form 17 November 2005; accepted 24 November 2005 Available online 14 February 2006 Received by T. Sekiya Abstract A crustacean gene, encoding for a new class of GFP-like protein, has been isolated from a cDNA library of the deep-sea (benthic) copepod crustacean, Chiridius poppei, by expression cloning. The cDNA library was constructed in a pBluescript II vector and screened using a non-UV transilluminator, obtaining a positive clone. The clone consisted of a 781-bp fragment of cDNAwith a 660-bp open reading frame, which encoded for a 219-amino acid polypeptide with a calculated molecular mass of 24.7 kDa. The protein was overexpressed in Escherichia coli, purified to homogeneity by anion-exchange and size-exclusion chromatographies. The protein, CpYGFP, had excitation and emission maxima at 507 and 517 nm, respectively. CpYGFP existed as a dimer in solution and could be expressed either alone or as a fusion protein in HeLa cells. Dual labeling experiments carried out with CpYGFP-actin and DsRed2-Nuc demonstrated the usefulness of CpYGFP as a reporter in the subcellular localization of actin. © 2006 Elsevier B.V. All rights reserved. Keywords: Green fluorescent protein; Crustacea; Copepoda; Expression cloning; Actin; DsRed 1. Introduction for studying protein localization, protein trafficking and gene expression in living cells (Ogawa et al., 1995). The special The green fluorescent protein from the hydrozoan jellyfish advantage of GFP is that it possesses a chromophore in its Aequorea victoria has been a very versatile and useful marker primary structure which emits a greenish fluorescence upon irradiation with long UV light. The chromophore is formed post-translationally by an autocatalytic modification of a tri- Abbreviations: CpYGFP, yellowish-green fluorescent protein of Chiridius peptide in the primary structure without participation of any poppei; GFP, green fluorescent protein; EGFP, enhanced GFP; EYFP, enhanced external cofactor (Nishiuchi et al., 1998). Besides Aequorea yellow fluorescent protein; GST-tagged, glutathione S-transferase-tagged; GFP, numerous GFP-like proteins have been isolated from DsRed2-Nuc, DiscomaRed2-Nuclear localization signal; CMV, cytomegalovi- rus; CBB, Coomassie Brilliant Blue; PFA, paraformaldehyde; TCA, trichlor- hydrozoans and anthozoans of the phylum Cnidaria (Chalfie, oacetic acid; MALDI-TOF MS, matrix-assisted laser desorption/ionization time- 1995; Matz et al., 1999), but not from members of other phyla. of-flight mass spectrometry. Extensive characterization of GFP from Renilla reniformis, the ⁎ Corresponding author. Institute for Biological Resources and Functions, bioluminescent sea pansy, has also been carried out (Ward and National Institute of Advanced Industrial Science and Technology (AIST), 1-1-1 Cormier, 1979; Ward, 1981). In addition, a colorless, non-fluo- Higashi, Tsukuba, Ibaraki 305-8566, Japan. Tel.: +81 29 861 6085; fax: +81 29 861 6159. rescent GFP homologue has also been cloned from Aequorea E-mail address: [email protected] (H. Masuda). coerulescens, a medusae, of the same genus as A. victoria 1 These authors contributed equally. (Gurskaya et al., 2003). Green, yellow, and red fluorescent 0378-1119/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.gene.2005.11.031 H. Masuda et al. / Gene 372 (2006) 18–25 19 proteins have also been cloned from anthozoan species, notably carbenicillin plates were visually screened using a non-UV corals (Verkhusha and Lukyanov, 2004). At the present time, transilluminator. A single positive clone was isolated, resus- the sequences of more than a hundred GFP-like proteins have pended in LB medium and subjected to a second screening. The been deposited in the GenBank. Phylogenetic analysis of these plasmidwaspurifiedusingQIAprepSpinMiniprepKit proteins has provided important insight into the evolutionary (Qiagen) and sequenced using an ABI PRISM 3100 Gene history of these proteins. Analyzer (Applied Biosystems). Recently, the genes of a new class of fluorescent proteins have been cloned from 6 marine copepods of the family Pon- 2.3. Sequence analysis tellidae (phylum Arthropoda, Class Crustacea) (Shagin et al., 2004). Although some spectrometric characterization of Multiple amino acid sequence alignment of CpYGFP with copepod GFP-like proteins was described in the report, protein those of other copepod GFP-like proteins was carried out using properties such as stability or pH dependency and applicational program CLUSTAL W (ver. 1.60) (Jeanmougin et al., 1998) probability to monitor the target protein tagged with those GFP- with default parameters, except for an open gap penalty of 20 like proteins in living cells were not clearly mentioned. Among and an extended gap penalty of 1.0 (for multiple sequence other copepods studied, the luciferase genes of Gaussia prin- alignment). For the phylogenetic tree, entire amino acid ceps (Verhaegen and Christopoulos, 2002) and Metridia longa sequences were aligned by Clustal X (ver. 1.83) (Thompson (Markova et al., 2004) have been cloned, but no fluorescent et al., 1997). The tree was constructed using neighbor-joining proteins have been reported. In this paper, we describe the method and drawn using program NJPLOT. cloning, expression, purification and some characteristic prop- erties of a yellowish-green fluorescent protein, CpYGFP, from 2.4. Expression and purification of C. poppei YGFP in the marine copepod, Chiridius poppei, family Aetideidae. In Escherichia coli addition, data are presented showing the use of CpYGFP as a reporter protein in HeLa cells. The coding region of CpYGFP was amplified by Pyrobest DNA Polymerase (Takara Bio) from template plasmid isolated 2. Materials and methods by expression screening and cloned into pET101/D-TOPO vector (Invitrogen). CpYGFP protein was expressed in BL21- 2.1. Collection of copepod, C. poppei CodonPlus®(DE3)-RIL E. coli host cells (Stratagene) at 37 °C. Cells were harvested at 6 h after 1 mM IPTG induction, Zooplankton samples were collected from sea water being resuspended in 20 mM Tris–HCl buffer, pH 8.5, and sonicated pumped from a depth of 321 m in Toyama Bay (maximum at 4 °C. The CpYGFP in the soluble protein fraction was sub- depth 1 200 m) and distributed to holding tanks in the Hotaruika jected to chromatographic purification using a linear NaCl (“firefly squid”) Museum located on shore in Namerikawa, gradient (0–120 mM) and DEAE sepharose F.F., HiTrap Phenyl Japan. A fine mesh net placed at the mouth of one of the outflow HP, and HiLoad 16/60 Superdex 200 pg columns installed on an pipes was used to filter the zooplanktons. Live copepods exhi- ÄKTA 10S Explorer System (Amersham Bioscience) (data not biting significant fluorescence on exposure to light from Dark shown). Fractions collected were analyzed by SDS-PAGE Reader (Clare Chemical Research, Inc., Dolores, CO) (http:// (12.5%) under reducing conditions. www.clarechemical.com/), a non-UV transilluminator, were isolated with a transfer pipet, pooled and maintained in test 2.5. Characterization of CpYGFP tubes at 4 °C. The copepods were examined under a stereo fluorescence microscope (VB-G25/S20/L11, Keyence, Osaka, To determine thermostability of CpYGFP, 10 μl of purified Japan), equipped with a “GFP” filter (Excitation BP 470/40, FT recombinant CpYGFP (0.58 mg/ml), diluted with 192 μlof 510) and cooled CCD camera (VB-7010, Keyence, Osaka, 20 mM Tris–HCl, pH 8.5, was incubated in a block-heater over Japan). After removing the sea water from the test tubes, the a range of 4–80 °C for 10 min, then cooled on ice for 10 min. copepods were suspended in TRIzol reagent (Invitrogen) and The effect of pH on fluorescence intensity was analyzed by stored at −80 °C. mixing 10 μl of the CpYGFP solution with 192 μl of dilution buffer and the mixture was adjusted to give a pH between 3.0 2.2. Preparation and screening of cDNA expression library and 13.6 (for details, see legend in Fig. 5). The effect of chemicals on fluorescence intensity was measured by adding About 300 specimens in 6 ml of TRIzol reagent were used to various amounts of reagent grade chemicals to 10 μlof prepare total RNA. About 7.1 μg of mRNA was purified from CpYGFP solution, mixing and incubating for 10 min at 4 °C. 228 μg of total RNA using an Oligotex-dT30 mRNA Purifi- Fluorescence intensity was measured at its peak wavelength of cation Kit (Takara Bio, Shiga, Japan). cDNA was synthesized 517 nm using a F-4500 fluorescence spectrophotometer (Hita- from 5 μg of mRNA using a cDNA Synthesis Kit (Stratagene), chi High Technologies, Tokyo). Protein concentration was de- digested with XhoI, and cloned into EcoRV–XhoIsiteof termined using a Bradford assay kit (Bio-Rad) with bovine pBluescript II SK(+) vector (Stratagene). The cDNA library serum albumin as a standard. Recombinant Aequorea GFP was was introduced into TOP10 host strain (Invitrogen) by purchased from Clontech (Cat. No. 632373), and its fluorescent electroporation. About 3×105 colonies growing on LB- intensity was measured at 507 nm.
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