Cysteine mutagenesis improves the production without abrogating antigenicity of a recombinant protein vaccine candidate for human chagas disease

References

• Haberland A, Saravia SG, Wallukat G, Ziebig R, Schimke I. Chronic Chagas disease: from basics to laboratory medicine. Clin Chem Lab Med 2013; 51:271-94; PMID:23045386; http://dx.doi.org/10.1515/cclm-2012-0316
   PubMed Web of Science ®Google Scholar
• Bonney KM. Chagas disease in the 21st century: a public health success or an emerging threat? Parasite 2014; 21:11; PMID:24626257; http://dx.doi.org/10.1051/parasite/2014012
   PubMed Web of Science ®Google Scholar
• Garcia MN, Murray KO, Hotez PJ, Rossmann SN, Gorchakov R, Ontiveros A, Woc-Colburn L, Bottazzi ME, Rhodes CE, Ballantyne CM, et al. Development of chagas cardiac manifestations among Texas blood donors. Am J Cardiol 2015; 115:113-7; PMID:25456877; http://dx.doi.org/10.1016/j.amjcard.2014.09.050
   PubMed Web of Science ®Google Scholar
• Reithinger R, Tarleton RL, Urbina JA, Kitron U, Gurtler RE. Eliminating Chagas disease: challenges and a roadmap. Bmj 2009; 338:b1283; http://dx.doi.org/10.1136/bmj.b1283
   PubMedGoogle Scholar
• Sanchez-Burgos G, Mezquita-Vega RG, Escobedo-Ortegon J, Ramirez-Sierra MJ, Arjona-Torres A, Ouaissi A, et al. Comparative evaluation of therapeutic DNA vaccines against Trypanosoma cruzi in mice. FEMS Immunol Med Microbiol 2007; 50:333-41; PMID:17521394; http://dx.doi.org/10.1111/j.1574-695X.2007.00251.x
   PubMed Web of Science ®Google Scholar
• Rassi A, Jr, Rassi A, Little WC. Chagas' Heart Disease. Clin Cardiol 2000; 23:883-9; PMID:11129673; http://dx.doi.org/10.1002/clc.4960231205
   PubMed Web of Science ®Google Scholar
• Rassi A, Jr, Rassi A, Marin-Neto JA. Chagas Disease. Lancet 2010; 375:1388-402; PMID:20399979; http://dx.doi.org/10.1016/S0140-6736(10)60061-X
   PubMed Web of Science ®Google Scholar
• Andrade ZA. Pathogenesis of Chagas' Disease. Res Immunol 1991; 142:126-9; PMID:1907753; http://dx.doi.org/10.1016/0923-2494(91)90021-A
   PubMedGoogle Scholar
• Bestetti RB, Muccillo G. Clinical course of Chagas' heart disease: a comparison with dilated cardiomyopathy. Int J Cardiol 1997; 60:187-93; PMID:9226290; http://dx.doi.org/10.1016/S0167-5273(97)00083-1
   PubMed Web of Science ®Google Scholar
• Hotez PJ, Bottazzi ME, Franco-Paredes C, Ault SK, Periago MR. The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS neglected tropical diseases 2008; 2:e300; PMID:18820747; http://dx.doi.org/10.1371/journal.pntd.0000300
   PubMed Web of Science ®Google Scholar
• Castro JA, de Mecca MM, Bartel LC. Toxic side effects of drugs used to treat Chagas' disease (American trypanosomiasis). Hum Exp Toxicol 2006; 25:471-9; PMID:16937919; http://dx.doi.org/10.1191/0960327106het653oa
   PubMed Web of Science ®Google Scholar
• Pinazo MJ, Munoz J, Posada E, Lopez-Chejade P, Gallego M, Ayala E, del Cacho E, Soy D, Gascon J. Tolerance of benznidazole in treatment of Chagas' disease in adults. Antimicrob Agents Chemother 2010; 54:4896-9; PMID:20823286; http://dx.doi.org/10.1128/AAC.00537-10
   PubMed Web of Science ®Google Scholar
• Fabbro DL, Streiger ML, Arias ED, Bizai ML, del Barco M, Amicone NA. Trypanocide treatment among adults with chronic Chagas disease living in Santa Fe city (Argentina), over a mean follow-up of 21 years: parasitological, serological and clinical evolution. Revista Soc Bras Med Trop 2007; 40:1-10; PMID:17486245; http://dx.doi.org/10.1590/S0037-86822007000100001
   PubMed Web of Science ®Google Scholar
• Campos MC, Leon LL, Taylor MC, Kelly JM. Benznidazole-resistance in Trypanosoma cruzi: evidence that distinct mechanisms can act in concert. Mol Biochem Parasitol 2014; 193:17-9; PMID:24462750; http://dx.doi.org/10.1016/j.molbiopara.2014.01.002
   PubMed Web of Science ®Google Scholar
• Pinazo MJ, Guerrero L, Posada E, Rodriguez E, Soy D, Gascon J. Benznidazole-related adverse drug reactions and their relationship to serum drug concentrations in patients with chronic chagas disease. Antimicrob Agents Chemother 2013; 57:390-5; PMID:23114763; http://dx.doi.org/10.1128/AAC.01401-12
   PubMed Web of Science ®Google Scholar
• Le Loup G, Pialoux G, Lescure FX. Update in treatment of Chagas disease. Curr Opin Infect Dis 2011; 24:428-34; PMID:21857512; http://dx.doi.org/10.1097/QCO.0b013e32834a667f
   PubMed Web of Science ®Google Scholar
• Morillo CA, Marin-Neto JA, Avezum A, Sosa-Estani S, Rassi A, Jr, Rosas F, Villena E, Quiroz R, Bonilla R, Britto C, et al. Randomized Trial of Benznidazole for Chronic Chagas' Cardiomyopathy. New England journal of Medicine 2015; 373:1295-306; PMID:26323937; http://dx.doi.org/10.1056/NEJMoa1507574
   PubMed Web of Science ®Google Scholar
• Dumonteil E, Bottazzi ME, Zhan B, Heffernan MJ, Jones K, Valenzuela JG, Kamhawi S, Ortega J, Rosales SP, Lee BY, et al. Accelerating the development of a therapeutic vaccine for human Chagas disease: rationale and prospects. Expert Rev Vaccines 2012; 11:1043-55; PMID:23151163; http://dx.doi.org/10.1586/erv.12.85
   PubMed Web of Science ®Google Scholar
• Beaumier CM, Gillespie PM, Strych U, Hayward T, Hotez PJ, Bottazzi ME. Status of vaccine research and development of vaccines for Chagas disease. Vaccine 2016; 34(26):2996-3000
   PubMed Web of Science ®Google Scholar
• Serna C, Lara JA, Rodrigues SP, Marques AF, Almeida IC, Maldonado RA. A synthetic peptide from Trypanosoma cruzi mucin-like associated surface protein as candidate for a vaccine against Chagas disease. Vaccine 2014; 32:3525-32; PMID:24793944; http://dx.doi.org/10.1016/j.vaccine.2014.04.026
   PubMed Web of Science ®Google Scholar
• Pereira IR, Vilar-Pereira G, Marques V, da Silva AA, Caetano B, Moreira OC, Machado AV, Bruna-Romero O, Rodrigues MM, Gazzinelli RT, et al. A human type 5 adenovirus-based Trypanosoma cruzi therapeutic vaccine re-programs immune response and reverses chronic cardiomyopathy. PLoS Pathog 2015; 11:e1004594; PMID:25617628; http://dx.doi.org/10.1371/journal.ppat.1004594
   PubMed Web of Science ®Google Scholar
• Bhatia V, Garg NJ. Previously unrecognized vaccine candidates control Trypanosoma cruzi infection and immunopathology in mice. Clin Vaccine Immunol 2008; 15:1158-64; PMID:18550728; http://dx.doi.org/10.1128/CVI.00144-08
   PubMed Web of Science ®Google Scholar
• Taibi A, Espinoza AG, Ouaissi A. Trypanosoma cruzi: analysis of cellular and humoral response against a protective recombinant antigen during experimental Chagas' disease. Immunol Lett 1995; 48:193-200; PMID:8867851; http://dx.doi.org/10.1016/0165-2478(95)02465-4
   PubMed Web of Science ®Google Scholar
• Taibi A, Plumas-Marty B, Guevara-Espinoza A, Schoneck R, Pessoa H, Loyens M, Piras R, Aguirre T, Gras-Masse H, Bossus M, et al. Trypanosoma cruzi: immunity-induced in mice and rats by trypomastigote excretory-secretory antigens and identification of a peptide sequence containing a T cell epitope with protective activity. J Immunol 1993; 151:2676-89
   PubMed Web of Science ®Google Scholar
• Dumonteil E, Escobedo-Ortegon J, Reyes-Rodriguez N, Arjona-Torres A, Ramirez-Sierra MJ. Immunotherapy of Trypanosoma cruzi infection with DNA vaccines in mice. Infect Immun 2004; 72:46-53; PMID:14688079; http://dx.doi.org/10.1128/IAI.72.1.46-53.2004
   PubMed Web of Science ®Google Scholar
• Limon-Flores AY, Cervera-Cetina R, Tzec-Arjona JL, Ek-Macias L, Sanchez-Burgos G, Ramirez-Sierra MJ, Cruz-Chan JV, VanWynsberghe NR, Dumonteil E. Effect of a combination DNA vaccine for the prevention and therapy of Trypanosoma cruzi infection in mice: role of CD4+ and CD8+ T cells. Vaccine 2010; 28:7414-9; PMID:20850536; http://dx.doi.org/10.1016/j.vaccine.2010.08.104
   PubMed Web of Science ®Google Scholar
• Quijano-Hernandez IA, Bolio-Gonzalez ME, Rodriguez-Buenfil JC, Ramirez-Sierra MJ, Dumonteil E. Therapeutic DNA vaccine against Trypanosoma cruzi infection in dogs. Ann N Y Acad Sci 2008; 1149:343-6; PMID:19120245; http://dx.doi.org/10.1196/annals.1428.098
   PubMed Web of Science ®Google Scholar
• Quijano-Hernandez IA, Castro-Barcena A, Vazquez-Chagoyan JC, Bolio-Gonzalez ME, Ortega-Lopez J, Dumonteil E. Preventive and therapeutic DNA vaccination partially protect dogs against an infectious challenge with Trypanosoma cruzi. Vaccine 2013; 31:2246-52; PMID:23499599; http://dx.doi.org/10.1016/j.vaccine.2013.03.005
   PubMed Web of Science ®Google Scholar
• Martinez-Campos V, Martinez-Vega P, Ramirez-Sierra MJ, Rosado-Vallado M, Seid CA, Hudspeth EM, Wei J, Liu Z, Kwityn C, Hammond M, et al. Expression, purification, immunogenicity, and protective efficacy of a recombinant Tc24 antigen as a vaccine against Trypanosoma cruzi infection in mice. Vaccine 2015; 33:4505-12; PMID:26192358; http://dx.doi.org/10.1016/j.vaccine.2015.07.017
   PubMed Web of Science ®Google Scholar
• Barry MA, Wang Q, Jones KM, Heffernan MJ, Buhaya MH, Beaumier CM, Keegan BP, Zhan B, Dumonteil E, Bottazzi ME, et al. A therapeutic nanoparticle vaccine against Trypanosoma cruzi in a BALB/c mouse model of Chagas disease. Hum Vaccin Immunother 2016; 12:976-87; PMID:26890466; http://dx.doi.org/10.1080/21645515.2015.1119346
   PubMed Web of Science ®Google Scholar
• Cozzolino M, Amori I, Pesaresi MG, Ferri A, Nencini M, Carri MT. Cysteine 111 affects aggregation and cytotoxicity of mutant Cu,Zn-superoxide dismutase associated with familial amyotrophic lateral sclerosis. J Biol Chem 2008; 283:866-74; PMID:18006498; http://dx.doi.org/10.1074/jbc.M705657200
   PubMed Web of Science ®Google Scholar
• O'Dwyer R, Razzaque R, Hu X, Hollingshead SK, Wall JG. Engineering of cysteine residues leads to improved production of a human dipeptidase enzyme in E. coli. Appl Biochem Biotechnol 2009; 159:178-90; PMID:18931951; http://dx.doi.org/10.1007/s12010-008-8379-9
   PubMed Web of Science ®Google Scholar
• Peng D, Wang F, Li N, Zhang Z, Song R, Zhu Z, Ruan L, Sun M. Single cysteine substitution in Bacillus thuringiensis Cry7Ba1 improves the crystal solubility and produces toxicity to Plutella xylostella larvae. Environ Microbiol 2011; 13:2820-31; PMID:21895913; http://dx.doi.org/10.1111/j.1462-2920.2011.02557.x
   PubMed Web of Science ®Google Scholar
• Wang H, He L, Lensch M, Gabius HJ, Fee CJ, Middelberg AP. Single-site Cys-substituting mutation of human lectin galectin-2: modulating solubility in recombinant production, reducing long-term aggregation, and enabling site-specific monoPEGylation. Biomacromolecules 2008; 9:3223-30; PMID:18942878; http://dx.doi.org/10.1021/bm800801b
   PubMed Web of Science ®Google Scholar
• Xie X, Pashkov I, Gao X, Guerrero JL, Yeates TO, Tang Y. Rational improvement of simvastatin synthase solubility in Escherichia coli leads to higher whole-cell biocatalytic activity. Biotechnol Bioeng 2009; 102:20-8; PMID:18988191; http://dx.doi.org/10.1002/bit.22028
   PubMed Web of Science ®Google Scholar
• Yamamoto I, Ishihara K, Muramatsu K, Wada Y, Kiwaki M, Kushiro A, Okuda K. Expression of Porphyromonas gingivalis gingipain antigen Hgp44 domain on surface of Lactococcus lactis. Bull Tokyo Dent Coll 2013; 54:233-41; PMID:24521549; http://dx.doi.org/10.2209/tdcpublication.54.233
   PubMedGoogle Scholar
• Wingard JN, Ladner J, Vanarotti M, Fisher AJ, Robinson H, Buchanan KT, Engman DM, Ames JB. Structural Insights into Membrane Targeting by the Flagellar Calcium-binding Protein (FCaBP), a Myristoylated and Palmitoylated Calcium Sensor in Trypanosoma cruzi. J Biol Chem 2008; 283:23388-96; PMID:18559337
   PubMedGoogle Scholar
• Sreerama N, Woody RW. Computation and analysis of protein circular dichroism spectra. Methods Enzymol 2004; 383:318-51; PMID:15063656; http://dx.doi.org/10.1016/S0076-6879(04)83013-1
   PubMed Web of Science ®Google Scholar
• Gupta S, Garg NJ. Prophylactic efficacy of TcVac2 against Trypanosoma cruzi in mice. PLoS Negl Trop Dis 2010; 4:e797; PMID:20706586; http://dx.doi.org/10.1371/journal.pntd.0000797
   PubMed Web of Science ®Google Scholar
• Gupta S, Garg NJ. Delivery of antigenic candidates by a DNA/MVA heterologous approach elicits effector CD8(+)T cell mediated immunity against Trypanosoma cruzi. Vaccine 2012; 30:7179-86; PMID:23079191; http://dx.doi.org/10.1016/j.vaccine.2012.10.018
   PubMed Web of Science ®Google Scholar
• Colombo N, Cabrele C. Synthesis and conformational analysis of Id2 protein fragments: impact of chain length and point mutations on the structural HLH motif. J Pept Sci 2006; 12:550-8; PMID:16733829; http://dx.doi.org/10.1002/psc.764
   PubMed Web of Science ®Google Scholar
• Valencia A, Serrano L, Caballero R, Anderson PS, Lacal JC. Conformational alterations detected by circular dichroism induced in the normal ras p21 protein by activating point mutations at position 12, 59, or 61. Euro J Biochemistry / FEBS 1988; 174:621-7; http://dx.doi.org/10.1111/j.1432-1033.1988.tb14143.x
   PubMedGoogle Scholar
• Indu S, Kochat V, Thakurela S, Ramakrishnan C, Varadarajan R. Conformational analysis and design of cross-strand disulfides in antiparallel β-sheets. Proteins 2011; 79:244-60; PMID:21058397; http://dx.doi.org/10.1002/prot.22878
   PubMed Web of Science ®Google Scholar
• Gupta S, Garg NJ. TcVac3 induced control of Trypanosoma cruzi infection and chronic myocarditis in mice. PloS One 2013; 8:e59434; PMID:23555672; http://dx.doi.org/10.1371/journal.pone.0059434
   PubMed Web of Science ®Google Scholar
• Wang W, Singh SK, Li N, Toler MR, King KR, Nema S. Immunogenicity of protein aggregates–concerns and realities. Int J Pharm 2012; 431:1-11; PMID:22546296; http://dx.doi.org/10.1016/j.ijpharm.2012.04.040
   PubMed Web of Science ®Google Scholar
• Ratanji KD, Derrick JP, Dearman RJ, Kimber I. Immunogenicity of therapeutic proteins: influence of aggregation. J Immunotoxicol 2014; 11:99-109; PMID:23919460; http://dx.doi.org/10.3109/1547691X.2013.821564
   PubMed Web of Science ®Google Scholar
• Singh M, Kazzaz J, Ugozzoli M, Baudner B, Pizza M, Giuliani M, Hawkins LD, Otten G, O'Hagan DT. MF59 oil-in-water emulsion in combination with a synthetic TLR4 agonist (E6020) is a potent adjuvant for a combination Meningococcus vaccine. Hum Vaccines Immunother 2012; 8:486-90; PMID:22832252; http://dx.doi.org/10.4161/hv.19229
   PubMed Web of Science ®Google Scholar
• Cencig S, Coltel N, Truyens C, Carlier Y. Parasitic loads in tissues of mice infected with Trypanosoma cruzi and treated with AmBisome. PLoS Negl Trop Dis 2011; 5:e1216; PMID:21738811; http://dx.doi.org/10.1371/journal.pntd.0001216
   PubMedGoogle Scholar
• Caldas S, Caldas IS, Diniz Lde F, Lima WG, Oliveira Rde P, Cecilio AB, Ribeiro I, Talvani A, Bahia MT. Real-time PCR strategy for parasite quantification in blood and tissue samples of experimental Trypanosoma cruzi infection. Acta Trop 2012; 123:170-7; PMID:22609548; http://dx.doi.org/10.1016/j.actatropica.2012.05.002
   PubMed Web of Science ®Google Scholar
• Gangisetty O, Reddy DS. The optimization of TaqMan real-time RT-PCR assay for transcriptional profiling of GABA-A receptor subunit plasticity. J Neurosci Methods 2009; 181:58-66; PMID:19406150; http://dx.doi.org/10.1016/j.jneumeth.2009.04.016
   PubMed Web of Science ®Google Scholar
• Crowther JR. The ELISA guidebook. Methods Molecular Biol 2000; 149:Iii–iv, 1-413; PMID:11028258
   PubMedGoogle Scholar