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Articles

Cloning, large-scale production and characterization of fusion protein (P-TUFT-ALT-2) of Brugian abundant larval transcript-2 with tuftsin in Pichia pastoris

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Pages 823-833 | Received 30 Apr 2018, Accepted 04 Aug 2018, Published online: 10 Oct 2018

References

  • World Health Organization. Lymphatic Filariasis Fact Sheet. Geneva: World Health Organization, 2016, c2016.
  • Jayakody, R. L.; De Silva, C. S. S.; Weerasinghe, W. M. T. Treatment of Bancroftian Filariasis with Albendazole: Evaluation of Efficacy and Adverse Reaction. Trop. Biomed. 1993, 10, 19–24.
  • Dreyer, G.; Addiss, D.; Noroes, J.; Amaral, F.; Rocha, A.; Coutinho, A. Direct Assessment of the Adulticidal Efficacy of Repeat High-Dose Invermectin in Bancrofitian Filariasis. Trop. Med. Int. Health. 1996, 1, 427–432.
  • Norões, J.; Dreyer, G.; Santos, A.; Mendes, V. G.; Medeiros, Z.; Addiss, D. Assessment of the Efficacy of Diethylcarbamazine on Adult Wuchereria bancrofti in vivo. Trans. R. Soc. Trop. Med. Hyg. 1997, 91, 78–81.
  • Molyneux, D. H.; Taylor, M. J. Current Status and Future Prospects of the Global Lymphatic Filariasis Programme. Curr. Opin. Infect. Dis. 2001, 14, 155–159.
  • Gyapong, J. O.; Kumaraswami, V.; Biswas, G.; Ottesen, E. A. Treatment Strategies Underpinning the Global Programme to Eliminate Lymphatic Filariasis. Expert Opin. Pharmacother. 2005, 6, 179–200.
  • Emilio, P. Filariasis: Diagnosis, Treatment and Prevention. Acta Biomed. 2008, 79, 106–109.
  • Price, V. L.; Kieny, M. P. Vaccines for Parasitic Diseases. Cdtid. 2001, 1, 315–324.
  • Vercruysse, J.; Schetters, T. P. M.; Knox, D. P. Control of Parasitic Disease Using Vaccines: An Answer to Drug Resistance? Rev. Sci. Tech. (International Office of Epizootics). 2007, 26, 105–115.
  • Selkirk, M. E.; Maizels, R. M.; Yazdanbakhsh, M. Immunity and the Prospects for Vaccination against Filariasis. Immunobiology. 1992, 184, 263–281.
  • Grieve, R. B.; Wisnewski, N.; Frank, G. R. Vaccine Research and Development for the Prevention of Filarial Nematode Infections. Pharm. Biotechnol. 1995, 6, 737–768.
  • Lightowlers, M. W.; Colebrook, A. L.; Gauci, C. G.; Gauci, S. M.; Kyngdon, C. T.; Monkhouse, J. L.; Vallejo Rodriquez, C.; Read, A. J.; Rolfe, R. A.; Sato, C. Vaccination Against Cestode Parasites: Anti-Helminth Vaccines That Work and Why. Vet. Parasitol. 2003, 115, 83–123.
  • Andure, D.; Reddy, M.; Pote, K.; Padalkar, R.; Khatri, V.; Amdare, N. Retracted: Role of Recombinant SXP/RAL-2 Family Protein Wuchereria bancrofti L2 (rWbL2) as Vaccine Candidate in Lymphatic Filariasis in Mastomys. Int. J. Res. Med. Sci. 2016, 4, 1140–1146.
  • Arumugam, S.; Wei, J.; Liu, Z.; Abraham, D.; Bell, A.; Bottazzi, M. E.; Hotez, P. J.; Zhan, B.; Lustigman, S.; Klei, T. R. Vaccination of Gerbils with Bm-103 and Bm-RAL-2 Concurrently or as a Fusion Protein Confers Consistent and Improved Protection against Brugia malayi Infection. PLoS Negl. Trop. Dis. 2016, 10, e0004586.
  • Murray, J.; Gregory, W. F.; Gomez-Escobar, N.; Atmadja, A. K.; Maizels, R. M. Expression and Immune Recognition of Brugia malayi VAL-1, a Homologue of Vespid Venom Allergens and Ancylostoma Secreted Proteins. Mol. Biochem. Parasitol. 2001, 118, 89–96.
  • Gnanasekar, M.; Rao, K. V. N.; He, Y.-X.; Mishra, P. K.; Nutman, T. B.; Kaliraj, P.; Ramaswamy, K. Novel Phage Display Based Subtractive Screening to Identify Vaccine Candidates of Brugia malayi. Infect Immun. 2004, 72, 4707–4715.
  • Ramachandran, S.; Kumar, M. P.; Rami, R. M. V.; Chinnaiah, H. B.; Nutman, T.; Kaliraj, P.; McCarthy, J. The Larval Specific Lymphatic Filarial ALT-2: induction of protection using protein or DNA vaccination. Microbiol. Immunol. 2004, 48, 945–955.
  • Gregory, W. F.; Atmadja, A. K.; Allen, J. E.; Maizels, R. M. The Abundant Larval Transcript-1 and -2 Genes of Brugia malayi Encode Stage-Specific Candidate Vaccine Antigens for Filariasis. Infect. Immun. 2000, 68, 4174–4179.
  • Gomez-Escobar, N.; Bennett, C.; Prieto-Lafuente, L. Heterologous Expression of the Filarial Nematode Bmalt Gene Products Reveals Their Potential to Inhibit Immune Function. BMC Biol. 2005, 3, 8.
  • Thirugnanam, S.; Pandiaraja, P.; Ramaswamy, K.; Murugan, V.; Gnanasekar, M.; Nandakumar, K.; Reddy, M. V. R.; Kaliraj, P. Brugia malayi: Comparison of Protective Immune Responses Induced by Bmalt-2 DNA, Recombinant BmALT-2 Protein and Prime-Boost Vaccine Regimens in a Jird Model. Exp. Parasitol. 2007, 116, 483–491.
  • Paul, R.; Saha, G.; Selvaraja, V.; Kaliraj, P. Cloning, Expression and Characterization of Brugian Abundant Larval Protein Transcript-2 (BmALT-2) Expressed in Pichia pastoris. Biotechnol. Biotechnol/ Equip. 2017, 31, 403–407.
  • Anand, S. B.; Kodumudi, K. N.; Reddy, M. V.; Kaliraj, P. K. Combination of Two Brugia malayi Filarial Vaccine Candidate Antigens (BmALT-2 and BmVAH) Enhances Immune Responses and Protection in Jirds. J. Helminthol. 2011, 4, 1–11.
  • Li, B.-W.; Wang, Z.; Rush, A. C.; Mitreva, M.; Weil, G. J. Transcription Profiling Reveals Stage- and Function-Dependent Expression Patterns in the Filarial Nematode Brugia malayi. BMC Genomics. 2012, 13, 184.
  • Madhumathi, J.; Prince, P. R.; Rao, D. N.; et al. Epitope Mapping of Brugia malayi ALT-2 and the Development of a Multi-Epitope Vaccine for Lymphatic Filariasis. J. Helminthol. 2016, 19, 1–12.
  • Nishioka, K.; Babcock, G. F.; Phillips, J. H.; Noyes, R. D. Antitumor Effect of Tuftsin. Mol. Cell. Biochem. 1981, 41, 13–18. vol
  • Khare, S.; Bhutani, L. K.; Rao, D. N. Modulation of Peripheral Blood Derived Monocytes/Macrophages from Leprosy Patients for Immunogenic Functions in vitro by Tuftsin. Indian J. Med. Microbiol. 1993, 64, 164–175.
  • Pawan, K.; Dhawan, P.; Rao, D. N. Enhancement of the Immunogenicity of the RESA Peptides of P. falciparum by Polytuftsin and Its Possible Effects and Mechanism during Macrophage Activation. Proc. Int. Symposia Vectors Vector Borne Dis. 1995, 212, 27.
  • Gokulan, K.; Khare, S.; Rao, D. N. Increase in the Immunogenicity of HIV Peptide Antigens by Chemical Linkage to polytuftsin (TKPR40) DNA Cell Biol. 1999, 18, 623–626.
  • Owais, M.; Misra-Bhattacharya, S.; Haq, W.; Gupta, C. M. Immunomodulator Tuftsin Augments Antifilarial Activity of Diethylcarbamazine Against Experimental Brugian Filariasis. J. Drug Target. 2003, 11, 247–251.
  • Januchta, W.; Serocki, M.; Dzierzbicka, K.; Cholewiński, G.; Skladanowski, A. Synthesis of Functionalized New Conjugates of Batracylin with Tuftsin/Retro-Tuftsin Derivatives and Their Biological Evaluation. Eur. J. Med. Chem. 2015, 106, 85–94.
  • Buckholz, F. G.; Gleeson, M. A. G. Yeast Systems for the Commercial Production of Heterologous Proteins. Biotechnology (N.Y.). 1991, 9, 1067–1072.
  • Cregg, J. M.; Cereghino, J. L.; Shi, J.; Higgins, D. R. Recombinant Protein Expression in Pichia pastoris. Mol. Biotechnol. 2000, 16, 23–52.
  • Cereghino, L.; Sunga, G. P.; Line, A. J. Expression of Foreign Genes in the Yeast Pichia pastoris. Genet. Eng. Princ. Methods. 2000, 23, 157–169.
  • Romanos, M.; Scorer, C.; Sreekrishna, K.; Clare, J. The Generation of Multicopy Recombinant Strains. Methods Mol. Biol. 1998, 103, 55–72.
  • Vassileva, A.; Arora Chugh, D.; Swaminathan, S.; Khanna, N. Effect of Copy Number on the Expression Levels of Hepatitis B Surface Antigen in the Methylotrophic Yeast Pichia pastoris. Protein Expr. Purif. 2001, 21, 71–81.
  • Ingham, D. J.; Beer, S.; Money, S.; Hansen, G. Quantitative Real-Time PCR Assay for Determining Transgene Copy Number in Transformed Plants. BioTechniques. 2001, 31, 132–140.
  • Livak, K. J.; Schmittgen, T. D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001, 25, 402–408.
  • Zhang, W.; Inan, M.; Meagher, M. M. Fermentation Strategies for Recombinant Protein Expression in the Methylotrophic Yeast Pichia pastoris. Biotechnol. Bioprocess Eng. 2000, 5, 275–287.
  • iitd.vlab.co.in (2012.). Estimation of growth kinetic parameters in batch fermentation. Retrieved 22 November 2016, from iitd.vlab.co.in/?sub=63&brch=177&sim=1348&cnt=1.
  • Bradford, M. M. A Rapid and Sensitive Method for the Quantification of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 1976, 72, 248–254.
  • Pasamontes, L.; Egger, D.; Bienz, K. Production of Monoclonal and Mono-Specific Antibodies against Non-Capsid Proteins of Poliovirus. J. Gen. Virol. 1986, 67, 2415–2422.
  • Laemmli, U. K. Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature. 1970, 227, 680–685.
  • Towbin, H.; Staehelin, T.; Gordon, J. Electrophoretic Transfer of Proteins from Polyacrylamide Gels to Nitrocellulose Sheets: Procedure and Some Applications. 1979 Biotechnology. 1992, 24, 145–149.
  • Hamby, S. E.; Hirst, J. D. Prediction of Glycosylation Sites Using Random Forests. BMC Bioinformatics. 2008, 9, 500.
  • Chauhan, J. S.; Rao, A.; Raghava, G. P. S. In Silico Platform for Prediction of N-, O- and C-Glycosites in Eukaryotic Protein sequences. PLoS One. 2013, 8, e67008.
  • Fairbanks, G.; Steck, T. L.; Wallach, D. F. H. Electrophoretic Analysis of the Major Polypeptides of the Human Erythrocyte Membrane. Biochemistry. 1971, 10, 2606–2617.
  • Ausiello, C. M.; Spagnoli, G. C.; Boccanera, M.; Casalinuovo, I.; Malavasi, F.; Casciani, C. U.; Cassone, A. Proliferation of Human Peripheral Blood Mononuclear Cells Induced by Candida albicans and Its Cell Wall fractions. J. Med. Microbiol. 1986, 22, 195–202.
  • Meek, B.; Jan Diepersloot, R.; Van Gool, T.; Speijer, D.; Peek, R. IgM Recognition of Recombinant Toxoplasma gondii Antigens by Sera of Acutely or Latently Infected Humans. Diagn. Microbiol. Infect. Dis. 2003, 45, 45–52.
  • Cregg, J. M.; Vedvick, T. S.; Raschke, W. C. Recent Advances in the Expression of Foreign Genes in Pichia pastoris. Biotechnology (N.Y.) 1993, 11, 905–910.
  • Kalidas, C. Pichia pastoris in Encyclopedia of Food Microbiology. In Robinson, R.K., Batt, C.A. and Patel, P.D., Eds. Academic Press, San Diego, vol. 3, pp. 1686–1692.
  • Lau, Y. L.; Fong, M. Y. Toxoplasma gondii: Serological Characterization and Immunogenicity of Recombinant Surface Antigen 2 (SAG2) Expressed in the Yeast Pichia pastoris. Exp. Parasitol. 2008, 119, 373–378.
  • Prince. Structural Elucidation and Immunoprophylactic Studies of Recombinant Parasitic Proteins for Therapeutic Intervention in Human Lymphatic Filariasis. PhD Thesis, Anna University Chennai, 2011.
  • Chen, R. Bacterial Expression Systems for Recombinant Protein Production: E. coli and beyond. Biotechnol. Adv. 2012, 30, 1102–1107.
  • Hu, H.; Gao, J.; He, J.; Yu, B.; Zheng, P.; Huang, Z.; Mao, X.; Yu, J.; Han, G.; Chen, D. Codon Optimization Significantly Improves the Expression Level of a Keratinase Gene in Pichia pastoris. PLoS One. 2013, 8, e58393.
  • Liu, S. H.; Chou, W. I.; Sheu, C. C.; Chang, M. D. Improved Secretory Production of Glucoamylase in Pichia pastoris by Combination of Genetic Manipulations. Biochem. Biophys. Res. Commun. 2005, 326, 817–824.
  • Athmaram, T. N.; Saraswat, S.; Santhosh, S. R.; Singh, A. K.; Suryanarayana, V. V. S.; Priya, R.; Gopalan, N.; Parida, M.; Rao, P. V. L.; Vijayaraghavan, R. Yeast Expressed Recombinant Hemagglutinin Protein of Novel H1N1 Elicits Neutralising Antibodies in Rabbits and Mice. Virol. J. 2011, 8, 524.
  • Hartwig, D.; Oliveira, T. L.; Seixas, F. K.; Forster, K. M.; Rizzi, C.; Hartleben, C. P.; McBride, A. J.; Dellagostin, O. A. High Yield Expression of Leptospirosis Vaccine Candidates LigA and LipL32 in the Methylotrophic Yeast Pichia pastoris. Microb. Cell Fact. 2010, 9, 98.
  • Bo, H.; Minjian, L.; Guoqiang, H.; Zhaoxia, L.; Zhu, Z.; Li, L. Expression of Hepatitis B Virus S Gene in Pichia pastoris and Application of the Product for Detection of anti-HBs Antibody. J. Biochem. Mol. Biol. 2005, 38, 683–689.
  • Jacob, D.; Ruffie, C.; Dubois, M.; Combredet, C.; Amino, R.; Formaglio, P.; Gorgette, O.; Pehau-Arnaudet, G.; Guery, C.; Puijalon, O.; et al. Whole Pichia pastoris Yeast Expressing Measles Virus Nucleoprotein as a Production and Delivery System to Multimerize Plasmodium Antigens. PLoS One. 2014, 9, e86658.
  • Zhang, W.; Bevins, M. A.; Plantz, B. A.; Smith, L. A.; Meagher, M. M. Modeling Pichia pastoris Growth on Methanol and Optimizing the Production of a Recombinant Protein, the Heavy-Chain Fragment C of Botulinum Neurotoxin, Serotype A. Biotechnol. Bioeng. 2000, 70, 1–8.
  • Damasceno, L. M.; Anderson, K. A.; Ritter, G.; Cregg, J. M.; Old, L. J.; Batt, C. A. Cooverexpression of Chaperones for Enhanced Secretion of a Single-Chain Antibody Fragment in Pichia pastoris. Appl. Microbiol. Biotechnol. 2007, 74, 381–389.
  • Du, C.; Long, H.; Anfeng, X.; Cao, M. Secretory Expression and Purification of the Recombinant Duck Interleukin-2 in Pichia pastoris. J. Microbiol. Biotechnol. 2011, 21, 1264–1269.
  • Ghosalkar, A.; Sahai, V.; Srivastava, A. Secretory Expression of Interferon-Alpha 2b in Recombinant Pichia pastoris Using Three Different Secretion Signals. Protein Expr. Purif. 2008, 60, 103–109.
  • Lee, C. Y.; Nakano, A.; Shiomi, N.; Lee, E. K.; Katoh, S. Effects of Substrate Feed Rates on Heterologous Protein Expression by Pichia pastoris in DO-Stat Fed-Batch Fermentation. Enzyme Microb. Technol. 2003, 33, 358–365.
  • Nakano, A.; Lee, C. Y.; Yoshida, A.; Matsumoto, T.; Shiomi, N.; Katoh, S. Effects of Methanol Feeding Methods on Chimeric α-Amylase Expression in Continuous Culture of Pichia pastoris. J. Biosci. Bioeng. 2006, 101, 227–231.
  • Yamane, T.; Kume, T.; Sada, E.; Takamatsu, T. A Simple Optimization Technique for Fed-Batch Culture. J. Ferment. Technol. 1977, 55, 587–598.
  • Kotze, L.; Smith, J. J.; Haan, R. D.; van Zyl, W. H.; Gorgens, J. F. Expression of Human Papillomavirus Type 16 (HPV16) L1 Protein in Pichia pastoris. African J. Biotechnol. 2011, 10, 214–219.
  • Min, C. K.; Lee, J. W.; Chung, K. H.; Park, H. W. Control of Specific Growth Rate to Enhance the Production of a Novel Disintegrin, Saxatilin, in Recombinant Pichia pastoris. J. Biosci. Bioeng. 2010, 110, 314–319.
  • Li, W.; Gao, X.; Ren, J.; An, T.; Liu, Y. High Expression and Purification of Amino-Terminal Fragment of Human Amyloid Precursor Protein in Pichia pastoris and Partial Analysis of Its Properties. BioMed. Res. Int. 2013, 2013, 1–9.
  • Baumgartner, P.; Raemaekers, J. M.; Durieux, A.; Gatehouse, A.; Davies, H.; Taylor, M. Large-Scale Production, Purification, and Characterization of Recombinant Phaseolus vulgaris Phytohemagglutinin E-Form Expressed in the Methylotrophic Yeast Pichia pastoris. Protein Expr. Purif. 2002, 26, 394–405.
  • Zou, L.; Miles, A. P.; Wang, J.; Stowers, A. W. Expression of Malaria Transmission-Blocking Vaccine Antigen Pfs25 in Pichia pastoris for Use in Human Clinical Trials. Vaccine. 2003, 21, 1650–1657.
  • Thiruvengadam, G.; Init, I.; Fong, M. Y.; Lau, Y. L. Optimization of the Expression of Surface Antigen SAG1/2 of Toxoplasma gondii in the Yeast Pichia pastoris. Trop. Biomed. 2011, 28, 506–513.
  • Wang, S. H.; Zheng, H. J.; Dissanayake, S.; Cheng, W. F.; Tao, Z. H.; Lin, S. Z.; Piessens, W. F. Evaluation of Recombinant Chitinase and SXP1 Antigens as Antimicrofilarial Vaccines. American Journal of Tropical Medicine & Hygiene 1997, 56, 474–481.
  • Tomé-Amat, J.; Fleischer, L.; Parker, S. A.; Bardliving, C. L.; Batt, C. A. Secreted Production of Assembled Norovirus Virus-like Particles from Pichia pastoris. Microb. Cell Fact. 2014, 13, 134.
  • Kwon, W. T.; Lee, W. L.; Park, P. J.; Park, T. K.; Kang, H. Protective Immunity of Pichia pastoris-Expressed Recombinant Envelope Protein of Japanese Encephalitis Virus. J. Microbiol. Biotechnol. 2012, 22, 1580–1587.
  • Macauley-Patrick, S.; Fazenda, M. L.; McNeil, B.; Harvey, L. M. Heterologous Protein Production Using the Pichia pastoris Expression System. Yeast. 2005, 22, 249–270.
  • Liu, X.; Guo, J.; Han, S.; Yao, L.; Chen, A.; Yang, Q.; Bo, H.; Xu, P.; Yin, J.; Zhang, Z. Enhanced Immune Response Induced by a Potential Influenza a Vaccine Based on Branched M2e Polypeptides Linked to Tuftsin. Vaccine. 2012, 30, 6527–6533.
  • An, Y.; Li, L.; Yang, D.; Jia, N.; Xu, C.; Wang, Q.; Wang, S.; Yuan, S. Anticancer Activity of Tuftsin-Derived T Peptide in Postoperative Residual Tumors. Anticancer. Drugs. 2014, 25, 857–867.
  • Xu, Y.; Zhu, J.; Xiang, K. e. Synthesis and Immunomodulatory Activity of [60] Fullerene-Tuftsin Conjugates. Biomaterials. 2011, 32, 9940–9949.
  • Chandrashekar, R.; Rao, U. R.; Subrahmanyam, D. Antibody Mediated Cytotoxicity Effects in Vitro and in Vivo of Rat Cells on Infective Larvae of Brugia malayi. Int. J. Parasitol. 1990, 20, 725–730.
  • Paul, R.; Jaiswal, S.; Natarajan, M.; Kaliraj, P. Elucidation of Immunological Response and Its Regulatory Network by P-TUFT-ALT-2: A Promising Fusion Protein Vaccine for Human Lymphatic Filariasis. R. Soc. Open Sci. 2018, 5, 172039.

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