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An Inulin-Specific Lectin with Anti-HIV-1 Reverse Transcriptase, Antiproliferative, and Mitogenic Activities from Theediblemushroomagaricus Bitorquis

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An Inulin-Specific Lectin with Anti-HIV-1 Reverse Transcriptase, Antiproliferative, and Mitogenic Activities from Theediblemushroomagaricus Bitorquis Hindawi BioMed Research International Volume 2019, Article ID 1341370, 9 pages https://doi.org/10.1155/2019/1341370 Research Article An Inulin-Specific Lectin with Anti-HIV-1 Reverse Transcriptase, Antiproliferative, and Mitogenic Activities from theEdibleMushroomAgaricus bitorquis Guo-Qing Zhang ,1 Qing-Jun Chen,2 Jing Hua,1 Zi-Lu Liu,1 Yue Sun,1 Xin Xu,1 Peng Han,1 and He-Xiang Wang 3 Key Laboratory of Urban Agriculture (North China) of Ministry of Agriculture, College of Biological Science and Engineering, Beijing University of Agriculture, Beijing , China Beijing Key Laboratory for Agricultural Application and New Technique, College of Plant Science and Technology, Beijing University of Agriculture, Beijing , China State Key Laboratory for Agrobiotechnology and Department of Microbiology, China Agricultural University, Beijing , China Correspondence should be addressed to He-Xiang Wang; [email protected] Received 20 December 2018; Accepted 27 February 2019; Published 19 March 2019 Academic Editor: Gail B. Mahady Copyright © 2019 Guo-Qing Zhang et al. Tis is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. A novel lectin (ABL) was purifed from the dried fruiting bodies of Agaricus bitorquis. An efcient 3-step purifcation protocol involved two consecutive steps of ion exchange chromatography on Q-Sepharose and SP-Sepharose and gel fltration by FPLC on Superdex 75. ABL is a monomeric protein with the molecular mass of 27.6 kDa, which is diferent from other lectins from genus Agaricus. Its N-terminal amino acid sequence is EYTISIRVYQTNPKGFNRPV which is unique and sharing considerably high similarity of other mushroom lectins. Te hemagglutinating activity of the lectin was inhibited by inulin. Based on hemagglutination tests, ABL prefers rabbit, human type A, and AB erythrocytes to human type B and O erythrocytes. Te lectin inhibits the activity of HIV-1 reverse transcriptase and the proliferation of leukemia cell (L1210) with an IC50 value of 4.69 and 4.97 �M, respectively. 3 Furthermore, ABL demonstrates the highest mitogenic activity with a response of 24177.7 ± 940.6 [ H-methyl] thymidine counts per minute (CPM) at a concentration of 0.91 �M. 1. Introduction Remarkably, numerous fungal lectins have been reported since their great therapeutic potentials as antitumor, antipro- Lectins are carbohydrate-binding proteins of nonimmune liferative, antivirus, immunomodulatory activities, etc. [5]. origin that specifcally recognize and bind to carbohydrate Mushrooms have been recognized for their nutritious and moieties of glycoproteins or glycolipids. Tey play crucial medicinal properties for thousands of years. More than 80% role in various biological and pathological processes, such of reported fungal lectins come from mushroom species as cellular signaling, cell-cell and host-pathogen interactions, and play crucial roles in dormancy, growth, morphogenesis, diferentiation, innate immune responses, serum glycopro- morphological changes, and molecular recognition during tein turnover, tissue metastasis, etc. [1, 2]. Lectins are widely their life cycles [1, 6]. Nowadays mushroom lectins have distributed in plants, fungi, animals, bacteria, and viruses. attracted considerable attention due to their treatment or Among all the sources, plant lectins have been most exten- prevention of cancer, viral diseases, atherosclerosis, hyper- sively investigated including classifcation, structure, and tension, hypercholesterolemia, etc. [4, 7]. functions. Tey act as the defensive system against animals Agaricus is a genus of mushrooms from phylum Basid- and phytopathogenic microorganisms and also mediate the iomycota, class Agaricomycetes, order Agaricales, and family interactions of plants and their mycorrhizal fungi [3, 4]. Agaricaceae with possibly over 300 members worldwide. 2 BioMed Research International Members of the genus Agaricus are characterized by having with 10 mM NH4OAc bufer (pH 4.6). Afer removal of an a feshy cap and stipe and chocolate-brown spores. Some unadsorbed fraction (SP1), two adsorbed fractions (SP2 and species are commercially manufactured including A. bis- SP3) were eluted by using a linear concentration gradient of porus, A. blazei, A. bitorquis, etc. In recent years, lectins 0-1000mMNaClinthesamebufer(pH4.6).Lectinactive from Agaricus were widely reported including purifcation, fraction SP3 was fnally applied to to gel fltration by fast properties, and therapeutic applications. A. bisporus lectins protein liquid chromatography (FPLC, GE Healthcare, USA) can inhibit the growth of colon cancer cell, breast cancer cell, on a Superdex 75 gel fltration column (0.2 M NH4HCO3 and human retinal pigment epithelial cells [8]. A. blazei lectin bufer, pH 9.4) using an AKTA Purifer (GE Healthcare, claimed to exert an in vitro antitumor activity in leukemic USA). Te second fraction (SU2) was the purifed lectin. cells with no signifcant efects on normal lymphatic cells [9]. A. bitorquis is an edible mushroom species and can be .. Determination of Molecular Mass. Molecular mass (Mr) commercially produced similar to the common button mush- of the purifed lectin was determined based on FPLC-gel room A. bisporus. It is an important supplement cultivation fltration and sodium dodecyl sulphate-polyacrylamide gel species of the button mushroom production in China. Up electrophoresis (SDS-PAGE). During the FPLC chromatog- till now, only hemagglutination activity of A. bitorquis from raphy, Mr of natural proteins were calculated using the Australia was reported [10]. In the present study, we aimed standard curve of Log Mr versus elution volume made by to purify a novel lectin from the artifcially cultivated A. molecular mass standards (GE Healthcare, USA). SDS-PAGE bisporus and fnd out its properties and potential therapeutic was performed using the standard procedure with a 12% applications. resolving gel and a 5% stacking gel. Mr of denatured proteins was obtained using another standard curve of Log Mr versus 2. Materials and Methods relative mobilities of molecular mass standards (Genview, USA). Mr of the present purifed laccase was evaluated based .. Assay for Hemagglutinating Activity. Hemagglutinating on the two curves [13]. activity was determined in the 96-well microtiter plates with a fnal volume of 50 �l. A serial twofold dilution of the lectin . N-Terminal Amino Acid Sequencing. Afer SDS-PAGE, solution (25 �l) was mixed with a 2 % rabbit erythrocyte the purifed enzyme on the gel was transferred to a polyvinyli- suspension (25 �l) in phosphate-bufered saline (pH 7.2) and dene difuoride (PVDF,Bio-Rad, USA) membrane by electro- incubated at room temperature for 1 h. Te hemagglutination blotting and stained with CBB R-250. Te stained band was titer, one hemagglutination unit, was defned as the reciprocal then excised and analyzed by the automated Edman degrada- of the highest dilution exhibiting hemagglutination. Specifc tion method using an HP G1000A Edman degradation unit activity is the number of hemagglutination units/mg protein (Hewlett Packard Company, USA) and an HP1000 HPLC [11]. Te hemagglutination profles of the lectin towards system (Hewlett Packard Company, USA) [11]. erythrocytes from other origins were similarly determined. Humanblood(A,B,O,andABtypes)wasdonatedbyhealthy . Assay of Hemagglutinating Inhibition by Carbohydrates. volunteers, and the blood type was confrmed by clinical tests. Te hemagglutinating inhibition tests to investigate inhibi- tion of lectin induced hemagglutination by various carbo- .. Purification of Lectin. Te mushroom A. bitorquis was hydrates [11]. Serial twofold dilutions of sugar samples (200 artifcially cultivated in woodland of Beijing mountain areas mM to 1.56 mM) were prepared in phosphate-bufered saline. using a commercial strain from Hebei Province in China All of the dilutions were mixed with an equal volume (25 � and followed the cultivation method of Chen et al. described L) of the purifed lectin solution with 16 hemagglutination [14]. Dried fruiting bodies (100 g) were homogenized and units. Te mixture was allowed to stand for 60 minutes at ∘ ∘ � extracted in 0.15 M NaCl (1 L) at 4 Covernight.Subsequently, 4 C, and then mixed with 50 L of a 2% rabbit erythrocyte the homogenate was centrifuged at 9500 rpm for 20 min at suspension. Te assay for lectin activity was conducted as ∘ 4 C. Te supernatant was collected and ammonium sulphate described above. Te minimum concentration of the sugar was added to the supernatant to 80% saturation. Te mixture in the fnal reaction mixture which completely inhibited ∘ was lef at 4 C for 8 hours before another centrifugation 16 hemagglutination units of the lectin preparation was ∘ at 9500 rpm for 20 min at 4 C. Ten the precipitate was calculated. Te carbohydrates tested included D-fructose, D- dissolved and dialyzed to remove ammonium sulphate before galactose, D-maltose, D-mannose, D-melibiose, D-xylose, L- applying to a Q- Sepharose (GE Healthcare, USA) column rhamnose, L-sorbose, cellobiose, inulin, and rafnose. (2.5×20 cm) which had previously been equilibrated with and was then eluted with 10 mM Tris-HCl bufer (pH 7.6). .. Assay of HIV- Reverse Transcriptase (HIV- RT) Afer removal of the unadsorbed fraction (Q1) containing Inhibitory Activity. Inhibitory activity towards human slight hemagglutinating activity, two adsorbed fractions (Q2 immunodefciency virus type 1 (HIV-1) reverse
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