Expression and purification of an engineered, yeast-expressed Leishmania donovani nucleoside hydrolase with immunogenic properties

References

• GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2015; 385:117-71; PMID:25530442; http://dx.doi.org/10.1016/S0140-6736(14)61682-2
   PubMed Web of Science ®Google Scholar
• Hotez PJ. Forgotten People, Forgotten Diseases: The Neglected Tropical Diseases and Their Impact on Global Health and Development ASM Press, 2013
   Google Scholar
• Lee BY, Bacon KM, Shah M, Kitchen SB, Connor DL, Slayton RB. The economic value of a visceral leishmaniasis vaccine in Bihar State, India. Am J Tropical Med Hyg 2012; 86:417-25; http://dx.doi.org/10.4269/ajtmh.2012.10-0415
   PubMed Web of Science ®Google Scholar
• Bacon KM, Hotez PJ, Kruchten SD, Kamhawi S, Elena M, Valenzuela JG, Lee BY. The potential economic value of a cutaneous leishmaniasis vaccine in seven endemic countries in the Americas. Vaccine 2013; 31:480-6; PMID:23176979; http://dx.doi.org/10.1016/j.vaccine.2012.11.032
   PubMed Web of Science ®Google Scholar
• Aguilar-be I, Zardo S, Souza EPD, Patrı G, Rosado-vallado M, Mut-martin M, Rosario M, Beatriz C, Sousa PD, Dumonteil E. Cross-Protective Efficacy of a Prophylactic Leishmania donovani DNA Vaccine against Visceral and Cutaneous Murine Leishmaniasis. Infection Immunity 2005; 73:812-9; PMID:15664920; http://dx.doi.org/10.1128/IAI.73.2.812-819.2005
   PubMed Web of Science ®Google Scholar
• Chale-balboa W, Mut-Martin M, Ramirez-Sierra M, Garcia-Miss M, Dumonteil E. A combination DNA vaccine encoding nucleoside hydrolase 36 and glycoproteine 63 protects female but not male hamsters against Leishmania mexicana. Parasite 2009; 16:227-30; PMID:19839269; http://dx.doi.org/10.1051/parasite/2009163227
   PubMed Web of Science ®Google Scholar
• Boitz JM, Ullman B, Jardim A, Carter N. Purine salvage in Leishmania : complex or simple by design? Trends Parasitol 2013; 28:345-52; http://dx.doi.org/10.1016/j.pt.2012.05.005
   Web of Science ®Google Scholar
• Datta AK, Datta R, Sen B. Antiparasitic chemotherapy: Tinkering with the purine salvage pathway. Adv Exp Med Biol 2008; 625:116-32; PMID:18365663; http://dx.doi.org/10.1007/978-0-387-77570-8_10
   PubMed Web of Science ®Google Scholar
• Cui L, Rajasekariah GR, Martin SK. A nonspecific nucleoside hydrolase from Leishmania donovani: implications for purine salvage by the parasite. Gene 2001; 280:153-62; PMID:11738828; http://dx.doi.org/10.1016/S0378-1119(01)00768-5
   PubMed Web of Science ®Google Scholar
• Palatnik-de-Sousa CB, Dutra HS, Borojevic R. Leishmania donovani surface glycoconjugate GP36 is the major immunogen component of the Fucose-Mannose Ligand (FML). Acta Tropica 1993; 53:59-72; PMID:8096110; http://dx.doi.org/10.1016/0001-706X(93)90006-W
   PubMed Web of Science ®Google Scholar
• Palatnik de Sousa C, Gomes E, de Souza E, dos Santos W, de Macedo S, de Medeiros L, Luz K. The FML (fucose mannose ligand) of Leishmania donovani: a new tool in diagnosis, prognosis, transfusional control and vaccination against human kala-azar. Rev Soc Bras Med Trop 1996; 29:153-63; PMID:8713607; http://dx.doi.org/10.1590/S0037-86821996000200008
   PubMedGoogle Scholar
• Gamboa-León R, Paraguai de Souza E, Borja-Cabrera GP, Santos FN, Myashiro LM, Pinheiro RO, Dumonteil E, Palatnik-de-Sousa CB. Immunotherapy against visceral leishmaniasis with the nucleoside hydrolase-DNA vaccine of Leishmania donovani. Vaccine 2006; 24:4863-73; http://dx.doi.org/10.1016/j.vaccine.2006.03.005
   PubMed Web of Science ®Google Scholar
• Li L, Saade F, Petrovsky N. The future of human DNA vaccines. J Biotechnol 2013; 162:171-82; http://dx.doi.org/10.1016/j.jbiotec.2012.08.012
   Web of Science ®Google Scholar
• Grunwald T, Ulbert S. Improvement of DNA vaccination by adjuvants and sophisticated delivery devices : vaccine- platforms for the battle against infectious diseases. Clin Exp Vacc Res 2015; 4:1-10; http://dx.doi.org/10.7774/cevr.2015.4.1.1
   PubMed Web of Science ®Google Scholar
• Al-wabel MA, Tonui WK, Cui L, Martin SK, Titus RG. Protection of Susceptible BALB / c Mice from Challenge with Leishmania major by Nucleoside Hydrolase, a Soluble Exo-antigen of Leishmania. Am J Tropical Med Hyg 2007; 77:1060-5
   PubMed Web of Science ®Google Scholar
• Ferrer-Miralles N, Domingo-Espín J, Corchero JL, Vázquez E, Villaverde A. Microbial factories for recombinant pharmaceuticals. Microbial Cell Factories 2009; 8:17; PMID:19317892; http://dx.doi.org/10.1186/1475-2859-8-17
   PubMed Web of Science ®Google Scholar
• Buckholz R, Gleeson M. Yeast Systems for the Commercial Production of Heterologous Proteins. Nat Biotechnol 1991; 9:1067-72; http://dx.doi.org/10.1038/nbt1191-1067
   Web of Science ®Google Scholar
• Cregg JM, Vedvick T, Raschke W. Recent Advances in the Expression of Foreign Genes in Pichia pastoris. Nat Biotechnol 1993; 11:905-10; http://dx.doi.org/10.1038/nbt0893-905
   Web of Science ®Google Scholar
• Rabert C, Weinacker D, Pessoa A, Jr, Farias J. Recombinants proteins for industrial uses : utilization of Pichia pastoris expression system. Brazilian J Microbiol 2013; 44:351-6; http://dx.doi.org/10.1590/S1517-83822013005000041
   PubMed Web of Science ®Google Scholar
• Gemmill TR, Trimble RB. Overview of N - and O -linked oligosaccharide structures found in various yeast species. 1999; 1426:227-37; PMID:9878752
   PubMedGoogle Scholar
• Kocken CHM, Withers-Martinez C, Dubbeld Ma, van der Wel A, Hackett F, Blackman MJ, Thomas AW. High-Level Expression of the Malaria Blood-Stage Vaccine Candidate Plasmodium falciparum Apical Membrane Antigen 1 and Induction of Antibodies That Inhibit Erythrocyte Invasion. Infection Immunity 2002; 70:4471-6; PMID:12117958; http://dx.doi.org/10.1128/IAI.70.8.4471-4476.2002
   PubMed Web of Science ®Google Scholar
• Liu M, Chen H, Luo F, Li P, Pan Q, Xia B, Qi Z, Ho WZ, Zhang XL. Deletion of N-glycosylation sites of hepatitis C virus envelope protein E1 enhances specific cellular and humoral immune responses. Vaccine 2007; 25:6572-80; PMID:17675185; http://dx.doi.org/10.1016/j.vaccine.2007.07.003
   PubMed Web of Science ®Google Scholar
• Mori K, Sugimoto C, Ohgimoto S, Nakayama EE, Shioda T, Kusagawa S, Takebe Y, Kano M, Matano T, Yuasa T, et al. Influence of glycosylation on the efficacy of an Env-based vaccine against simian immunodeficiency virus SIVmac239 in a macaque AIDS model. J Virol 2005; 79:10386-96; PMID:16051831; http://dx.doi.org/10.1128/JVI.79.16.10386-10396.2005
   PubMed Web of Science ®Google Scholar
• Chen WH, Du L, Chag SM, Ma C, Tricoche N, Tao X, Seid CA, Hudspeth EM,Lustigman S, Tseng CTK, et al. Yeast-expressed recombinant protein of the receptor-binding domain in SARS-CoV spike protein with deglycosylated forms as a SARS vaccine candidate. Hum Vacc Immunotherapeutics 2014; 10:1-11; http://dx.doi.org/10.4161/hv.28050
   PubMed Web of Science ®Google Scholar
• Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 2011; 9:604-15; PMID:21747391; http://dx.doi.org/10.1038/nrmicro2608
   PubMed Web of Science ®Google Scholar
• Johansen P, Men Y, Merkle HP, Gander B. Revisiting PLA/PLGA microspheres: An analysis of their potential in parenteral vaccination. Eur J Pharmaceutics Biopharmaceutics 2000; 50:129-46; http://dx.doi.org/10.1016/S0939-6411(00)00079-5
   PubMed Web of Science ®Google Scholar
• O'Hagan DT, Singh M, Gupta RK. Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv Drug Delivery Rev 1998; 32:225-46; http://dx.doi.org/10.1016/S0169-409X(98)00012-X
   PubMed Web of Science ®Google Scholar
• Oyewumi M, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune response. Expert Rev Vacc 2010; 9:1095-107; http://dx.doi.org/10.1586/erv.10.89
   PubMed Web of Science ®Google Scholar
• Klinman DM, Klaschik S, Sato T, Tross D. CpG oligonucleotides as adjuvants for vaccines targeting infectious diseases. Adv Drug Delivery Rev 2009; 61:248-55; http://dx.doi.org/10.1016/j.addr.2008.12.012
   PubMed Web of Science ®Google Scholar
• Jaafari MR, Badiee A, Khamesipour A, Samiei A, Soroush D, Kheiri MT, Barkhordari F, McMaster WR, Mahboudi F. The role of CpG ODN in enhancement of immune response and protection in BALB/c mice immunized with recombinant major surface glycoprotein of Leishmania (rgp63) encapsulated in cationic liposome. Vaccine 2007; 25:6107-17; PMID:17629372; http://dx.doi.org/10.1016/j.vaccine.2007.05.009
   PubMed Web of Science ®Google Scholar
• Rhee EG, Mendez S, Shah JA, Wu CY, Kirman JR, Turon TN, Davey DF, Davis H, Klinman DM, Coler RN, et al. Vaccination with heat-killed leishmania antigen or recombinant leishmanial protein and CpG oligodeoxynucleotides induces long-term memory CD4+ and CD8+ T cell responses and protection against leishmania major infection. J Exp Med 2002; 195:1565-73; PMID:12070284; http://dx.doi.org/10.1084/jem.20020147
   PubMed Web of Science ®Google Scholar
• Ebrahimpoor S, Pakzad SR, Ajdary S. IgG1 and IgG2a Profile of Serum Antibodies to Leishmania major Amastigote in BALB / c and C57BL / 6 Mice. 2013; 12:361-7
   Google Scholar
• Shi W, Schramm V, Almo S. Nucleoside Hydrolase from Leishmania major. cloning, expression, catalytic properties, transition state inhibitors, and the 2.5-a crystal structure. J Biol Chem 1999; 274:21114-20; PMID:10409664; http://dx.doi.org/10.1074/jbc.274.30.21114
   PubMed Web of Science ®Google Scholar
• De Beer TaP, Berka K, Thornton JM, Laskowski Ra. PDBsum additions. Nucleic Acids Res 2014; 42:292-6; http://dx.doi.org/10.1093/nar/gkt940
   PubMed Web of Science ®Google Scholar
• Khurshid S, Saridakis E, Govada L, Chayen NE. Porous nucleating agents for protein crystallization. Nat Protocols 2014; 9:1621-33; PMID:24922271; http://dx.doi.org/10.1038/nprot.2014.109
   PubMed Web of Science ®Google Scholar
• Garrity R, Rimmelzwaan G, Minassian A, Tsai W, Lin G, de Jong J, Goudsmit J, Nara P. Refocusing Neutralizing Antibody Response. J Immunol 1997; 159:279-89; PMID:9200464
   PubMed Web of Science ®Google Scholar
• Nico D, Claser C, Borja-Cabrera GP, Travassos LR, Palatnik M, Soares IDS, Rodrigues MM, Palatnik-de-Sousa CB. Adaptive immunity against Leishmania nucleoside hydrolase maps its c-terminal domain as the target of the CD4+ T cell-driven protective response. PLoS Neglected Tropical Dis 2010; 4:e866; http://dx.doi.org/10.1371/journal.pntd.0000866
   Google Scholar
• Paraguai de Souza E, Bernardo R, Palatnik M, Sousa C. Vaccination of Balb / c mice against experimental visceral leishmaniasis with the GP36 glycoprotein antigen of Leishmania donovani. Vaccine 2001; 19:3104-15; PMID:11312005; http://dx.doi.org/10.1016/S0264-410X(01)00031-7
   PubMed Web of Science ®Google Scholar
• Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein Identification and analysis tools on the ExPASy Server. Methods Mol Biol 2005; 112:571-608
   Google Scholar
• Liu C, Hashizume T, Kurita-Ochiai T, Fujihashi K, Yamamoto M. Oral immunization with Porphyromonas gingivalis outer membrane protein and CpGoligodeoxynucleotides elicits T helper 1 and 2 cytokines for enhanced protective immunity. Mol Oral Microbiol 2010; 25:178-89; PMID:20502628; http://dx.doi.org/10.1111/j.2041-1014.2009.00560.x
   PubMed Web of Science ®Google Scholar
• Chu RS, Targoni OS, Krieg aM, Lehmann PV, Harding CV. CpG oligodeoxynucleotides Act as Adjuvants that Switch on T Helper 1 (Th1) Immunity. J Exp Med 1997; 186:1623-31; PMID:9362523; http://dx.doi.org/10.1084/jem.186.10.1623
   PubMed Web of Science ®Google Scholar
• Gupta R, Jung E, Brunak S. Predication of N-glycosylation sites in human proteins. Center for Biological Sequence Analysis at Technical University of Denmark DTU, 2004
   Google Scholar
• Stratton J, Chiruvolu V, Meagher M. High cell-density fermentation. Meth Mol Biol (Clifton, NJ) 1998; 103:107-20
   PubMedGoogle Scholar
• Guex N, Peitsch MC, Schwede T. Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 2009; 30 Suppl 1:S162-73; PMID:19517507; http://dx.doi.org/10.1002/elps.200900140
   PubMedGoogle Scholar
• Silva JC, Gorenstein MV, Li GZ, Vissers JPC, Geromanos SJ. Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol Cell Proteomics 2006; 5:144-56; PMID:16219938; http://dx.doi.org/10.1074/mcp.M500230-MCP200
   PubMed Web of Science ®Google Scholar
• Wang Q, Tan MT, Keegan BP, Barry MA, Heffernan MJ. Time course study of the antigen-specific immune response to a PLGA microparticle vaccine formulation. Biomaterials 2014; 35:8385-93; PMID:24986256; http://dx.doi.org/10.1016/j.biomaterials.2014.05.067
   PubMed Web of Science ®Google Scholar
• Patel MM, Zeles MG, Manning MC, Randolph TW, Anchordoquy TJ. Degradation kinetics of high molecular weight poly(L-lactide) microspheres and release mechanism of lipid:DNA complexes. J Pharmaceutical Sci 2004; 93:2573-84; http://dx.doi.org/10.1002/jps.20176
   PubMed Web of Science ®Google Scholar
• Sah H. A new strategy to determine the actual protein content of poly(lactide-co-glycolide) microspheres. J Pharmaceutical Sci 1997; 86:1315-8; http://dx.doi.org/10.1021/js960363q
   PubMed Web of Science ®Google Scholar
• Frey A, Di Canzio J, Zurakowski D. A statistically defined endpoint titer determination method for immunoassays. J Immunological Meth 1998; 221:35-41; http://dx.doi.org/10.1016/S0022-1759(98)00170-7
   PubMed Web of Science ®Google Scholar
• Parkin DW, Horensteingn Ba, Abdulahg DR, Estupiiang B, Schrammgii VL. Nucleoside Hydrolase from Crithidia fasciculuta. J Biol Chem 1991; 266:20658-65; PMID:1939115
   PubMed Web of Science ®Google Scholar