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Expression and in vitro anticancer activity of Lp16-PSP, a member of the YjgF/YER057c/UK114 protein family from the mushroom Lentinula edodes C91-3

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Abstract

Latcripin-16 (Lp16-PSP) is a gene that was extracted as a result of de novo characterization of the Lentinula edodes strain C91-3 transcriptome. The aim of the present study was to clone, express, and investigate the selective in vitro anticancer potential of Lp16-PSP in human cell lines. Lp16-PSP was analyzed using bioinformatics tools, cloned in a prokaryotic expression vector pET32a (+) and transformed into E. coli Rosetta gami. It was expressed and solubilized under optimized conditions. The differential scanning fluorometry (DSF)-guided refolding method was used with modifications to identify the proper refolding conditions for the Lp16-PSP protein. To determine the selective anticancer potential of Lp16-PSP, a panel of human cancerous and non-cancerous cell lines was used. Lp16-PSP protein was identified as endoribonuclease L-PSP protein and a member of the highly conserved YjgF/YER057c/UK114 protein superfamily. Lp16-PSP was expressed under optimized conditions (37 °C for 4 h following induction with 0.5 mM isopropyl β-d-1-thiogalactopyranoside). Solubilization was achieved with mild solubilization buffer containing 2 M urea using the freeze–thaw method. The DSF guided refolding method identified the proper refolding conditions (50 mM Tris–HCl, 100 mM NaCl, 1 mM EDTA, 400 mM Arginine, 0.2 mM GSH and 2 mM GSSG; pH 8.0) for Lp16-PSP, with a melting transition of ~ 58 °C. A final yield of ~ 16 mg of purified Lp16-PSP from 1 L of culture was obtained following dialysis and concentration by PEG 20,000. A Cell Counting Kit-8 assay revealed the selective cytotoxic effect of Lp16-PSP. The HL-60 cell line was demonstrated to be most sensitive to Lp16-PSP, with an IC50 value of 74.4 ± 1.07 µg/ml. The results of the present study suggest that Lp16-PSP may serve as a potential anticancer agent; however, further investigation is required to characterize this anticancer effect and to elucidate the molecular mechanism underlying the action of Lp16-PSP.

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References

  • Alavi M, Karimi N, Safaei M (2017) Application of various types of liposomes in drug delivery systems. Adv Pharm Bull 7:3–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230

    Article  CAS  PubMed  Google Scholar 

  • Arnold U, Ulbrich-Hofmann R (2006) Natural and engineered ribonucleases as potential cancer therapeutics. Biotechnol Lett 28:1615–1622

    Article  CAS  PubMed  Google Scholar 

  • Asagi K, Oka T, Arao K, Suzuki I, Thakur MK, Izumi K, Natori Y (1998) Purification, characterization and differentiation-dependent expression of a perchloric acid soluble protein from rat kidney. Nephron 79:80–90

    Article  CAS  PubMed  Google Scholar 

  • Baneyx F, Mujacic M (2004) Recombinant protein folding and misfolding in Escherichia coli. Nat Biotechnol 22:1399–1408

    Article  CAS  PubMed  Google Scholar 

  • Bartorelli A, Zanolo G, Fassio F, Botta M, Ferrara R, Bailo M, Cavalca CBV, Arzani C, Maraschin R (1994) Toxicological and antitumoral activity of UK101, a mammalian liver extract. J Tumor Marker Oncol 9(3):49

    Google Scholar 

  • Bassil NM, Abdel-Massih R, El-Chami N, Smith CA, Baydoun E (2012) Pleurotus ostreatus and Ruscus aculeatus extracts cause non-apoptotic jurkat cell death. J Plant Stud 1(1):14

    Article  Google Scholar 

  • Biter AB, de la Pena AH, Thapar R, Lin JZ, Phillips KJ (2016) DSF guided refolding as a novel method of protein production. Sci Rep 6:18906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, Frutiger S, Hochstrasser D (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14:1023–1031

    Article  CAS  PubMed  Google Scholar 

  • Bjellqvist B, Basse B, Olsen E, Celis JE (1994) Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15:529–539

    Article  CAS  PubMed  Google Scholar 

  • Burgess RR (2009) Refolding solubilized inclusion body proteins. Methods Enzymol 463:259–282

    Article  CAS  PubMed  Google Scholar 

  • Castro J, Ribó M, Navarro S, Nogués MV, Vilanova M, Benito A (2011) A human ribonuclease induces apoptosis associated with p21WAF1/CIP1induction and JNK inactivation. BMC Cancer 11:9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceciliani F, Faotto L, Negri A, Colombo I, Berra B, Bartorelli A, Ronchi S (1996) The primary structure of UK 114 tumor antigen. FEBS Lett 393:147–150

    Article  CAS  PubMed  Google Scholar 

  • Daraee H, Etemadi A, Kouhi M, Alimirzalu S, Akbarzadeh A (2016) Application of liposomes in medicine and drug delivery. Artif Cells Nanomed Biotechnol 44:381–391

    Article  CAS  PubMed  Google Scholar 

  • Dias DA, Urban S, Roessner U (2012) A historical overview of natural products in drug discovery. Metabolites 2:303–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong M, He X, Liu RH (2007) Phytochemicals of black bean seed coats: isolation, structure elucidation, and their antiproliferative and antioxidative activities. J Agric Food Chem 55:6044–6051

    Article  CAS  PubMed  Google Scholar 

  • Drozdetskiy A, Cole C, Procter J, Barton GJ (2015) JPred4: a protein secondary structure prediction server. Nucleic Acids Res 43:W389–W394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erazo-Oliveras A, Najjar K, Dayani L, Wang T-Y, Johnson GA, Pellois J-P (2014) Protein delivery into live cells by incubation with an endosomolytic agent. Nat Methods 11:861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans GA (1990) Molecular cloning: a laboratory manual. Second edition. Volumes 1, 2, and 3. Current protocols in molecular biology. Volumes 1 and 2. Cell 61:17–18

  • Farewell A, Neidhardt FC (1998) Effect of temperature on in vivo protein synthetic capacity in Escherichia coli. J Bacteriol 180:4704–4710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farkas A, Nardai G, Csermely P, Tompa P, Friedrich P (2004) DUK114, the Drosophila orthologue of bovine brain calpain activator protein, is a molecular chaperone. Biochem J 383:165–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285

    Article  CAS  PubMed  Google Scholar 

  • Ghezzo F, Berta GN, Bussolati B, Bosio A, Corvetti G, di Carlo F, Bussolati G, Guglielmone R, Bartorelli A (1999) Perchloric acid-soluble proteins from goat liver inhibit chemical carcinogenesis of Syrian hamster cheek-pouch carcinoma. Br J Cancer 79:54–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goupil-Feuillerat N, Cocaign-Bousquet M, Godon JJ, Ehrlich SD, Renault P (1997) Dual role of alpha-acetolactate decarboxylase in Lactococcus lactis subsp. lactis. J Bacteriol 179:6285–6293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graslund S, Nordlund P, Weigelt J, Hallberg BM, Bray J, Gileadi O, Knapp S, Oppermann U, Arrowsmith C, Hui R, Ming J, Dhe-Paganon S, Park HW, Savchenko A, Yee A, Edwards A, Vincentelli R, Cambillau C, Kim R, Kim SH, Rao Z, Shi Y, Terwilliger TC, Kim CY, Hung LW, Waldo GS, Peleg Y, Albeck S, Unger T, Dym O, Prilusky J, Sussman JL, Stevens RC, Lesley SA, Wilson IA, Joachimiak A, Collart F, Dementieva I, Donnelly MI, Eschenfeldt WH, Kim Y, Stols L, Wu R, Zhou M, Burley SK, Emtage JS, Sauder JM, Thompson D, Bain K, Luz J, Gheyi T, Zhang F, Atwell S, Almo SC, Bonanno JB, Fiser A, Swaminathan S, Studier FW, Chance MR, Sali A, Acton TB, Xiao R, Zhao L, Ma LC, Hunt JF, Tong L, Cunningham K, Inouye M, Anderson S, Janjua H, Shastry R, Ho CK, Wang D, Wang H, Jiang M, Montelione GT, Stuart DI, Owens RJ, Daenke S, Schutz A, Heinemann U, Yokoyama S, Bussow K, Gunsalus KC (2008) Protein production and purification. Nat Methods 5:135–146

    Article  PubMed  Google Scholar 

  • Gurova K (2009) New hopes from old drugs: revisiting DNA-binding small molecules as anticancer agents. Future Oncol 5:1685

    Article  CAS  PubMed  Google Scholar 

  • Harvey AL (2008) Natural products in drug discovery. Drug Discov Today 13:894–901

    Article  CAS  PubMed  Google Scholar 

  • He H, Li D-W, Yang L-Y, Fu L, Zhu X-J, Wong W-K, Jiang F-L, Liu Y (2015) A novel bifunctional mitochondria-targeted anticancer agent with high selectivity for cancer cells. Sci Rep 5:13543

    Article  PubMed  PubMed Central  Google Scholar 

  • Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545–W549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanova TS, Krupodorova TA, Barshteyn VY, Artamonova AB, Shlyakhovenko VA (2014) Anticancer substances of mushroom origin. Exp Oncol 36:58–66

    CAS  PubMed  Google Scholar 

  • Jiang J, Sliva D (2010) Novel medicinal mushroom blend suppresses growth and invasiveness of human breast cancer cells. Int J Oncol 37:1529–1536

    Article  PubMed  CAS  Google Scholar 

  • Joseph TP, Chanda W, Padhiar AA, Batool S, Liqun S, Zhong M, Huang M (2017) A preclinical evaluation of the antitumor activities of edible and medicinal mushrooms: a molecular insight. Integr Cancer Ther 1534735417736861

  • Kaczmarczyk SJ, Sitaraman K, Young HA, Hughes SH, Chatterjee DK (2011) Protein delivery using engineered virus-like particles. Proc Natl Acad Sci USA 108:16998–17003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanouchi H, Tachibana H, Oka T, Yamada K (2001) Recombinant expression of perchloric acid-soluble protein reduces cell proliferation. Cell Mol Life Sci CMLS 58:1340–1343

    Article  CAS  PubMed  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan RH, Rao KB, Eshwari AN, Totey SM, Panda AK (1998) Solubilization of recombinant ovine growth hormone with retention of native-like secondary structure and its refolding from the inclusion bodies of Escherichia coli. Biotechnol Prog 14:722–728

    Article  CAS  PubMed  Google Scholar 

  • Kim J-M, Yoshikawa H, Shirahige K (2001) A member of the YER057c/yjgf/Uk114 family links isoleucine biosynthesis and intact mitochondria maintenance in Saccharomyces cerevisiae. Genes Cells 6:507–517

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Song YS, Kim SK, Kim BC, Lim CJ, Park EH (2004) Anti-inflammatory and related pharmacological activities of the n-BuOH subfraction of mushroom Phellinus linteus. J Ethnopharmacol 93:141–146

    Article  PubMed  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. Methods Mol Biol 32:9–15

    CAS  PubMed  Google Scholar 

  • Lee JE, Raines RT (2008) Ribonucleases as novel chemotherapeutics: the ranpirnase example. BioDrugs 22:53–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leitner-Dagan Y, Ovadis M, Zuker A, Shklarman E, Ohad I, Tzfira T, Vainstein A (2006) CHRD, a plant member of the evolutionarily conserved YjgF family, influences photosynthesis and chromoplastogenesis. Planta 225:89–102

    Article  CAS  PubMed  Google Scholar 

  • Lilie H, Schwarz E, Rudolph R (1998) Advances in refolding of proteins produced in E. coli. Curr Opin Biotechnol 9:497–501

    Article  CAS  PubMed  Google Scholar 

  • Liu FY, Luo KW, Yu ZM, Co NN, Wu SH, Wu P, Fung KP, Kwok TT (2009) Suillin from the mushroom Suillus placidus as potent apoptosis inducer in human hepatoma HepG2 cells. Chem Biol Interact 181:168–174

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Zhong M, Lun Y, Wang X, Sun W, Li X, Ning A, Cao J, Zhang W, Liu L, Huang M (2012) A novel apoptosis correlated molecule: expression and characterization of protein latcripin-1 from Lentinula edodes C(91–3). Int J Mol Sci 13:6246–6265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Zeng J, Chen X, Xie W (2016) Crystal structures of RidA, an important enzyme for the prevention of toxic side products. Sci Rep 6:30494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Terrada D, Cheung SW, Finegold MJ, Knowles BB (2009) Hep G2 is a hepatoblastoma-derived cell line. Hum Pathol 40:1512–1515

    Article  CAS  PubMed  Google Scholar 

  • Lovell SC, Davis IW, Arendall WB, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 50:437–450

    Article  CAS  PubMed  Google Scholar 

  • Luqmani Y (2005) Mechanisms of drug resistance in cancer chemotherapy. Med Princ Pract 14:35–48

    Article  PubMed  Google Scholar 

  • Malik A, Alsenaidy AM, Elrobh M, Khan W, Alanazi MS, Bazzi MD (2016) Optimization of expression and purification of HSPA6 protein from Camelus dromedarius in E.coli. Saudi J Biol Sci 23:410–419

    Article  CAS  PubMed  Google Scholar 

  • Manjasetty BA, Delbruck H, Pham DT, Mueller U, Fieber-Erdmann M, Scheich C, Sievert V, Bussow K, Niesen FH, Weihofen W, Loll B, Saenger W, Heinemann U (2004) Crystal structure of Homo sapiens protein hp14.5. Proteins 54:797–800

    Article  CAS  PubMed  Google Scholar 

  • Morishita R, Kawagoshi A, Sawasaki T, Madin K, Ogasawara T, Oka T, Endo Y (1999) Ribonuclease activity of rat liver perchloric acid-soluble protein, a potent inhibitor of protein synthesis. J Biol Chem 274:20688–20692

    Article  CAS  PubMed  Google Scholar 

  • Mura S, Nicolas J, Couvreur P (2013) Stimuli-responsive nanocarriers for drug delivery. Nat Mater 12:991

    Article  CAS  PubMed  Google Scholar 

  • Mutti L, Gaudino G (2008) The therapeutic potential of the novel ribonuclease ranpirnase (Onconase®) in the treatment of malignant mesothelioma. Oncol Rev 2:61–65

    Article  Google Scholar 

  • Oka T, Tsuji H, Noda C, Sakai K, Hong YM, Suzuki I, Munoz S, Natori Y (1995) Isolation and characterization of a novel perchloric acid-soluble protein inhibiting cell-free protein synthesis. J Biol Chem 270:30060–30067

    Article  CAS  PubMed  Google Scholar 

  • Qi X, Sun Y, Xiong S (2015) A single freeze-thawing cycle for highly efficient solubilization of inclusion body proteins and its refolding into bioactive form. Microb Cell Fact 14:24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Racca S, Di Carlo F, Bartorelli A, Bussolati B, Bussolati G (1997) Growth inhibition of DMBA-induced rat mammary carcinomas by UK114 treatment. Virchows Arch 431:323–328

    Article  CAS  PubMed  Google Scholar 

  • Resurreccion NGU, Shen C-C, Ragasa CY (2016) Chemical constituents of Lentinus edodes. Der Pharm Lett 8:117–120

    Google Scholar 

  • Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320–W324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto Y, Watanabe H, Nagai M, Nakade K, Takahashi M, Sato T (2006) Lentinula edodes tlg1 encodes a thaumatin-like protein that is involved in lentinan degradation and fruiting body senescence. Plant Physiol 141:793–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasagawa T, Oka T, Tokumura A, Nishimoto Y, Munoz S, Kuwahata M, Okita M, Tsuji H, Natori Y (1999) Analysis of the fatty acid components in a perchloric acid-soluble protein. Biochim Biophys Acta 1437:317–324

    Article  CAS  PubMed  Google Scholar 

  • Saxena SK, Shogen K, Ardelt W (2003) ONCONASE® and its therapeutic potential. Lab Med 34:380–387

    Article  Google Scholar 

  • Sercombe L, Veerati T, Moheimani F, Wu SY, Sood AK, Hua S (2015) Advances and challenges of liposome assisted drug delivery. Front Pharmacol 6:286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Siegel RL, Miller KD, Jemal A (2020) Cancer statistics, 2020. CA Cancer J Clin 70:7–30

    Article  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh SM, Panda AK (2005) Solubilization and refolding of bacterial inclusion body proteins. J Biosci Bioeng 99:303–310

    Article  CAS  PubMed  Google Scholar 

  • Singh RS, Kaur HP, Kanwar JR (2016) Mushroom lectins as promising anticancer substances. Curr Protein Pept Sci 17:797–807

    Article  CAS  PubMed  Google Scholar 

  • Sinha S, Rappu P, Lange SC, Mantsala P, Zalkin H, Smith JL (1999a) Crystal structure of Bacillus subtilis YabJ, a purine regulatory protein and member of the highly conserved YjgF family. Proc Natl Acad Sci USA 96:13074–13079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha S, Rappu P, Lange SC, Mäntsälä P, Zalkin H, Smith JL (1999b) Crystal structure of Bacillus subtilis YabJ, a purine regulatory protein and member of the highly conserved YjgF family. Proc Natl Acad Sci 96:13074–13079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sippl MJ (1993) Recognition of errors in three-dimensional structures of proteins. Proteins 17:355–362

    Article  CAS  PubMed  Google Scholar 

  • Su P, Feng T, Zhou X, Zhang S, Zhang Y, Cheng JE, Luo Y, Peng J, Zhang Z, Lu X, Zhang D, Liu Y (2015) Isolation of Rhp-PSP, a member of YER057c/YjgF/UK114 protein family with antiviral properties, from the photosynthetic bacterium Rhodopseudomonas palustris strain JSC-3b. Sci Rep 5:16121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur KG, Praveena T, Gopal B (2010) Mycobacterium tuberculosis Rv2704 is a member of the YjgF/YER057c/UK114 family. Proteins 78:773–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thohinung S, Kanokmedhakul S, Kanokmedhakul K, Kukongviriyapan V, Tusskorn O, Soytong K (2010) Cytotoxic 10-(indol-3-yl)-[13]cytochalasans from the fungus Chaetomium elatum ChE01. Arch Pharm Res 33:1135–1141

    Article  CAS  PubMed  Google Scholar 

  • Vallejo LF, Rinas U (2004) Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 3:11–11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Volz K (1999) A test case for structure-based functional assignment: the 1.2 Å crystal structure of the yjgF gene product from Escherichia coli. Protein Sci 8:2428–2437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walev I, Bhakdi SC, Hofmann F, Djonder N, Valeva A, Aktories K, Bhakdi S (2001) Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O. Proc Natl Acad Sci USA 98:3185–3190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wasser SP (2005) Shiitake (Lentinus edodes). Encyclopedia of dietary supplements, pp 653–664

  • Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35:W407–W410

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaleski-Larsen LA, Fabi SG (2016) Laser-assisted drug delivery. Dermatol Surg 42:919–931

    Article  CAS  PubMed  Google Scholar 

  • Zhang X-C, Wang Z, Zhang X, Le MH, Sun J, Xu D, Cheng J, Stacey G (2012) Evolutionary dynamics of protein domain architecture in plants. BMC Evol Biol 12:1–12

    Article  Google Scholar 

  • Zhao J, Kwan HS (1999) Characterization, molecular cloning, and differential expression analysis of laccase genes from the edible mushroom Lentinula edodes. Appl Environ Microbiol 65:4908–4913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Chen YH, Kwan HS (2000) Molecular cloning, characterization, and differential expression of a glucoamylase gene from the basidiomycetous fungus Lentinula edodes. Appl Environ Microbiol 66:2531–2535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong M, Liu B, Wang X, Liu L, Lun Y, Li X, Ning A, Cao J, Huang M (2013) De novo characterization of Lentinulaedodes C91–3 transcriptome by deep Solexa sequencing. Biochem Biophys Res Commun 431:111–115

    Article  CAS  PubMed  Google Scholar 

  • Zochowska M, Paca A, Schoehn G, Andrieu J-P, Chroboczek J, Dublet B, Szolajska E (2009) Adenovirus dodecahedron, as a drug delivery vector. PLoS ONE 4:e5569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Richardson Patrick Joseph for editorial assistance for his generous support, insightful comments, and suggestions.

Funding

The present study was supported by a Chinese Government Scholarship (CSC No. 2014GXY960), National Natural Science Foundation of China (Grant No. 81472836) and the Liaoning Provincial Program for Top Discipline of College of Basic Medical Sciences.

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  1. Department of Microbiology, College of Basic Medical Sciences, Dalian Medical University, 9 West Section, Lvshun South Road, Luvshoukon District, Dalian, 116044, Liaoning, People’s Republic of China

    Thomson Patrick Joseph, Warren Chanda, Yukun Fang, MinTao Zhong & Min Huang

  2. Center for Neuroscience, Shantou University Medical College, Shantou, People’s Republic of China

    Thomson Patrick Joseph

  3. Computational System Biology Laboratory, Department of Bioinformatics, Shantou University Medical College, Shantou, People’s Republic of China

    Qianqian Zhao

  4. Department of Biotechnology, College of Basic Medical Sciences, Dalian Medical University, Dalian, 116044, Liaoning, People’s Republic of China

    Sadia Kanwal

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TPJ designed the study and performed experiments. QZ, WC and SK designed the study and participated in the analysis of results, review and editing of the manuscript. FYK participated in the analysis of results, review and editing of the manuscript. MTZ has contributed in the project administration, interpretation of results and revision of the manuscript. The final manuscript was approved by MH.

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Correspondence to Min Huang.

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Joseph, T.P., Zhao, Q., Chanda, W. et al. Expression and in vitro anticancer activity of Lp16-PSP, a member of the YjgF/YER057c/UK114 protein family from the mushroom Lentinula edodes C91-3. Arch Microbiol 203, 1047–1060 (2021). https://doi.org/10.1007/s00203-020-02099-0

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