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An Efficient Heterologous Escherichia Coli-Based Expression System For Bioscience, Biotechnology, and Biochemistry, 2021, Vol. 85, No. 3, 630-633 doi: 10.1093/bbb/zbaa058 Advance access publication date: 31 December 2020 NOTE NOTE An efficient heterologous Escherichia coli-based Downloaded from https://academic.oup.com/bbb/article/85/3/630/6056114 by guest on 24 September 2021 expression system for lectin production from Pleurocybella porrigens Tomohiro Suzuki ,1,∗,† Luna Nakamura,1,† Satomi Inayoshi,2 Yuki Tezuka,1 Akiko Ono ,1 Jae-Hoon Choi ,2,3 Hideo Dohra ,3 Tomohiro Sasanami ,2 Hirofumi Hirai,2,3 and Hirokazu Kawagishi 2,3,4 1Center for Bioscience Research and Education, Utsunomiya University, Mine-machi, Utsunomiya, Tochigi, Japan; 2Graduate School of Integrated Science and Technology, Shizuoka University, Ohya, Suruga-ku, Shizuoka, Japan; 3Research Institute of Green Science and Technology, Shizuoka University, Ohya, Suruga-ku, Shizuoka, Japan; and 4Graduate School of Science and Technology, Shizuoka University, Ohya, Suruga-ku, Shizuoka, Japan ∗Correspondence: Tomohiro Suzuki, [email protected] †Contributed equally to this work and share first-author status ABSTRACT In this study, we report a more efficient heterologous expression of lectin from Pleurocybella porrigens (PPL) using an Escherichia coli-based expression system. The yield (9.3 mg/L culture broth) of recombinant PPL (rPPL) using this expression system was increased approximately 9-fold compared to our previous study. The rPPL obtained in this study exhibited the same biochemical properties as the native PPL. Keywords: Heterologous expression, lectin, Pleurocybella porrigens, Escherichia coli The term “lectin” defines a protein (or glycoprotein) that is detection of characteristic glycans in tumor cells using lectins neither an enzyme nor an antibody. Lectins show specific can accelerate the detection of tumor development. For exam- carbohydrate-binding activity and are ubiquitous in plants, an- ple, α-1-6 fucosylation (core fucosylation) is a biomarker for imals, and microorganisms (Goldstein et al. 1980). Many lectins hepatocellular carcinoma. The mushroom lectin Aleuria aurantia contribute to diverse biological functions, such as host defense lectin (AAL) is used as a biomarker for liver cancer because it has mechanisms, inflammation, and cancer metastasis (Imberty an affinity for fucosyl residues (Wimmerova et al. 2003). Recently, et al. 2000; Carrizo et al. 2005). Lectins have a unique sugar- our research group discovered that a lectin from Pholiota squar- binding specificity and can be used as biomarkers for sugar rosa (PhoSL) specifically binds to core α-1-6 fucose and conse- chain detection. Abnormal glycosylation patterns, such as fu- quently has potential use as a novel diagnostic agent (Kobayashi cosylation, sialylation, or the aberrant expression of β-1,6- et al. 2012). Therefore, investigation of the detailed sugar-binding branched N-glycans or Tn antigen (truncated O-glycan) occur specificity of lectins is essential for enhancing their use andap- in many developmental stages in cancer (Syed et al. 2016). The plication in tumor diagnostic studies. Received: 28 September 2020; Accepted: 27 October 2020 © The Author(s) 2020. Published by Oxford University Press on behalf of Japan Society for Bioscience, Biotechnology, and Agrochemistry. All rights reserved. For permissions, please e-mail: [email protected] 630 An efficient heterologous Escherichia coli-based expression system for lectin production 631 Downloaded from https://academic.oup.com/bbb/article/85/3/630/6056114 by guest on 24 September 2021 Figure 1. Molecular properties of rPPL. (a) SDS-PAGE of rPPL expressed in E. coli. Lane M: marker proteins, Lane 1: soluble fraction of BL21-Codon Plus containing pCold I-ppl, Lane 2: inclusion body fraction of BL21-Codon Plus containing pCold I-ppl, Lane 3: purified rPPL. (b) MALDI-TOF mass spectrometry analysis of rPPL. The fungus Pleurocybella porrigens (Sugihiratake in Japan) be- then prepared using BugBuster Protein Extraction Reagent longs to the family Tricholomataceae (order Agaricales, class according to manufacturer’s protocols. The results of SDS-PAGE Agaricomycetes). It has been consumed as a foodstuff for a long analysis of these two fractions indicated that the target PPL time in Japan, particularly in the Hokuriku and Tohoku regions, band (around 15 kDa) was present in both fractions (Figure 1a). until 2004. In that year, acute encephalopathy was found to be The soluble fraction was then subjected to His GraviTrap affinity caused by eating this mushroom. To date, we have succeeded in chromatography (GE Healthcare, Uppsala, Sweden). the isolation, purification, characterization, and cloning of the After purification using the His-tag affinity column, thepu- full-length cDNA sequence of P.porrigens lectin (PPL) (Suzuki et al. rified protein was subjected to SDS-PAGE analysis. As a result, 2009). As reported previously, we constructed a heterologous ex- a single band around 15 kDa in size was observed (Figure 1a). pression system using the basidiomycete Phanerochaete sordida To confirm the detailed molecular weight of the purified lectin, YK-624, which resulted in the extracellular secretion of recom- MALDI-TOF-MS analysis was performed. For MALDI-TOF-MS binant PPL (rPPL) in its active form using a signal peptide of lignin analysis, super-DHB and Protein Calibration Standard I (Bruker, peroxidase (Suzuki et al. 2014). However, the expression of rPPL Billerica, MA, USA) were used as the matrix and mass cali- was quite low, with a yield of only 1 mg/L culture broth after bration standards, respectively. As a result, single (M + H]+) purification by acid-treated Sepharose 4B affinity chromatogra- and double ([M + 2H]2+) charged ions were observed as domi- phy, and its hemagglutination activity was 128 titer/mg protein. nant peaks at m/z 17,176 and 8,592, respectively (Figure 1b). The Thus, in the present study, we attempted to construct a more ef- molecular weight estimated from the amino acid sequence of ficient heterologous expression system of PPL in Escherichia coli rPPL was 17,217; therefore, the result of MALDI-TOF-MS analysis using the pCold I DNA vector and characterized the properties was consistent with that of the estimated molecular weight in of rPPL produced. SDS-PAGE. Furthermore, the purified protein was digested with Two oligonucleotide primers, pcold-ppl-F1 (5-CTCGAGGGAT trypsin in-gel and the total digest was subjected to LC-MS/MS. CCGCGTCCATCCCTGCCGGAACCTAC-3) and pcold-ppl-R1 (5- LC-MS/MS analyses using a Triple TOF 5600 mass spectrome- TATCTAGACTGCAGGTCAAACGGCTTCGAAGACCCAG-3), were ter (AB Sciex, Framingham, MA, USA) were performed using the designed to amplify the full-length sequence of the coding methods described in our previous study (Kruger et al. 2002). sequence of ppl for introduction into the pCold I DNA vector The results of protein identification using PEAKS Studio version (Takara, Shiga, Japan). To construct an expression vector (pCold 8.5 (Bioinformatics Solutions Inc., Waterloo, Canada) against I-ppl), we performed restriction enzyme treatment of pCold I the Swiss-Prot database identified PPL with a high sequence DNA (1000 μg/mL, 4407 bp) with EcoRI and SalI. The restric- coverage (76%), which indicated that the recombinant protein tion enzyme-treated pCold I DNA was ligated to the ppl gene was successfully expressed and purified. Purification using this sequence using the Gibson Assembly system (New England method was carried out in triplicate, and the average yield of BioLabs, Beverly, MA, USA), yielding the plasmid pCold I-ppl.The rPPL was determined to be 9.3 mg/L culture broth (Table S1). constructed pCold I-ppl was transformed into E. coli BL21-Codon After the purification procedure, the hemagglutination activity Plus (Takara), a competent cell system for protein expression. of rPPL was found to be 4.2 × 103 titer/mg protein. The rPPL The obtained transformed colony was then inoculated into LB obtained in this study showed higher hemagglutination activ- liquid medium supplemented with 50 μg/mL ampicillin and cul- ity than that reported previously (128 titer/mg protein) (Suzuki tured with shaking at 37 °C to an optical density (OD) at 600 nm et al. 2014). Since the purification method was different from our in the range of 0.4 to 0.8. The culture was chilled by cooling on previous study, there was possibility that the purity and hemag- ice for 30 min and then isopropyl β-D-1-thiogalactopyranoside glutination activity of rPPL obtained in this expression system (IPTG) (to a final concentration of 0.1 mM) was added to the was high. medium and cultured at 15 °C for 24 h. The cells were collected The rPPL obtained in this study was characterized using the by centrifugation (16,000 × g, 20 min, 4 °C) and lysed using method described previously (Suzuki et al. 2009). All tests were the BugBuster Protein Extraction Reagent (Merck Millipore, performed in duplicate. Furthermore, native PPL (nPPL) was pu- Billerica, MA, USA). Soluble and inclusion body fractions were rified in the same method as our previous reports in orderto 632 Bioscience, Biotechnology, and Biochemistry, 2021, Vol. 85, No. 3 Downloaded from https://academic.oup.com/bbb/article/85/3/630/6056114 by guest on 24 September 2021 Figure 2. Thermostability and pH stability testing of rPPL. (a) Thermostability of rPPL. (b) pH stability of rPPL. use nPPL as a control (Suzuki et al. 2009). The hemagglutination Table 1. Inhibition of native and recombinant PPL-mediated hemag- activity test was performed to investigate whether the lectin ob- glutination by monosaccharides, oligosaccharides, and glycoproteins tained in this study has lectin activity. Rabbit erythrocytes alone MICb and rabbit erythrocytes treated with actinase E (Pronase) were used in the assay. rPPL showed stronger hemagglutination ac- Inhibitora rPPL nPPL tivity in rabbit erythrocytes treated with actinase E compared to untreated rabbit erythrocytes, similar to nPPL (Table S2). The (mM) (mM) thermostability and pH stability of rPPL were tested to further N-acetylgalactosamine 0.39 0.1 determine its biochemical properties.
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