A therapeutic nanoparticle vaccine against Trypanosoma cruzi in a BALB/c mouse model of Chagas disease

References

• Global Burden of Disease Study C. Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2015; 386(9995):743-800; PMID:26063472; http://dx.doi.org/10.1016/S0140-6736(15)60692-4
   PubMed Web of Science ®Google Scholar
• Lee BY, Bacon KM, Bottazzi ME, Hotez PJ. Global economic burden of Chagas disease: a computational simulation model. Lancet Infect Dis 2013; 13(4):342-8
   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
• Rassi A, Jr, Rassi A, Marin-Neto JA. Chagas heart disease: pathophysiologic mechanisms, prognostic factors and risk stratification. Memorias do Instituto Oswaldo Cruz 2009; 104 Suppl 1:152-8; http://dx.doi.org/10.1590/S0074-02762009000900021
   PubMed Web of Science ®Google Scholar
• Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Wkly Epidemiol Rec 2015; 90:33-43; PMID:25671846
   PubMedGoogle 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
• Perez-Molina JA, Norman F, Lopez-Velez R. Chagas disease in non-endemic countries: epidemiology, clinical presentation and treatment. Curr Infect Dis Reports 2012; 14:263-74; http://dx.doi.org/10.1007/s11908-012-0259-3
   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. N Eng J Med 2015; 373:1295-306; http://dx.doi.org/10.1056/NEJMoa1507574
   PubMed Web of Science ®Google Scholar
• Bern C, Montgomery SP, Herwaldt BL, Rassi A, Jr, Marin-Neto JA, Dantas RO, Maguire JH, Acquatella H, Morillo C, Kirchhoff LV, et al. Evaluation and treatment of chagas disease in the United States: a systematic review. JAMA 2007; 298:2171-81; PMID:18000201; http://dx.doi.org/10.1001/jama.298.18.2171
   PubMed Web of Science ®Google Scholar
• Laucella SA, Postan M, Martin D, Hubby Fralish B, Albareda MC, Alvarez MG, Lococo B, Barbieri G, Viotti RJ, Tarleton RL. Frequency of interferon- gamma -producing T cells specific for Trypanosoma cruzi inversely correlates with disease severity in chronic human Chagas disease. J Infect Dis 2004; 189:909-18; PMID:14976609; http://dx.doi.org/10.1086/381682
   PubMed Web of Science ®Google Scholar
• Tarleton RL. Depletion of CD8+ T cells increases susceptibility and reverses vaccine-induced immunity in mice infected with Trypanosoma cruzi. J Immunol 1990; 144:717-24; PMID:2104903
   PubMed Web of Science ®Google Scholar
• Tarleton RL, Sun J, Zhang L, Postan M. Depletion of T-cell subpopulations results in exacerbation of myocarditis and parasitism in experimental Chagas' disease. Infect Immun 1994; 62:1820-9; PMID:8168945
   PubMed Web of Science ®Google Scholar
• Autran B, Carcelain G, Combadiere B, Debre P. Therapeutic vaccines for chronic infections. Science 2004; 305:205-8; PMID:15247470; http://dx.doi.org/10.1126/science.1100600
   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
• Lee BY, Bacon KM, Wateska AR, Bottazzi ME, Dumonteil E, Hotez PJ. Modeling the economic value of a Chagas' disease therapeutic vaccine. Hum Vacc Immunotherapeutics 2012; 8:1293-301
   PubMed Web of Science ®Google Scholar
• Engman DM, Krause KH, Blumin JH, Kim KS, Kirchhoff LV, Donelson JE. A novel flagellar Ca2+-binding protein in trypanosomes. J Biol Chem 1989; 264:18627-31; PMID:2681200
   PubMed Web of Science ®Google Scholar
• Krautz GM, Kissinger JC, Krettli AU. The targets of the lytic antibody response against Trypanosoma cruzi. Parasitol Today 2000; 16:31-4; PMID:10637586
   PubMedGoogle Scholar
• Maldonado RA, Linss J, Thomaz N, Olson CL, Engman DM, Goldenberg S. Homologues of the 24-kDa flagellar Ca(2+)-binding protein gene of Trypanosoma cruzi are present in other members of the Trypanosomatidae family. Exp Parasitol 1997; 86:200-5
   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; PMID:7689612
   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 Letters 1995; 48:193-200; PMID:8867851
   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
   PubMed Web of Science ®Google Scholar
• Sanchez-Burgos G, Mezquita-Vega RG, Escobedo-Ortegon J, Ramirez-Sierra MJ, Arjona-Torres A, Ouaissi A, Rodrigues MM, Dumonteil E. Comparative evaluation of therapeutic DNA vaccines against Trypanosoma cruzi in mice. FEMS Immunol Medical Microbiol 2007; 50:333-41
   PubMedGoogle 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
   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
   PubMed Web of Science ®Google Scholar
• Godsel LM, Tibbetts RS, Olson CL, Chaudoir BM, Engman DM. Utility of recombinant flagellar calcium-binding protein for serodiagnosis of Trypanosoma cruzi infection. J Clin Microbiol 1995; 33:2082-5; PMID:7559952
   PubMed Web of Science ®Google Scholar
• Guevara AG, Taibi A, Alava J, Guderian RH, Ouaissi A. Use of a recombinant Trypanosoma cruzi protein antigen to monitor cure of Chagas disease. Transactions Royal Society Tropical Med Hygiene 1995; 89:447-8
   PubMed Web of Science ®Google Scholar
• Tzelepis F, de Alencar BC, Penido ML, Gazzinelli RT, Persechini PM, Rodrigues MM. Distinct kinetics of effector CD8+ cytotoxic T cells after infection with Trypanosoma cruzi in naive or vaccinated mice. Infect Immun 2006; 74:2477-81; PMID:16552083
   PubMed Web of Science ®Google Scholar
• Gupta S, Garg NJ. Prophylactic efficacy of TcVac2 against Trypanosoma cruzi in mice. PLoS Neglected tropical Dis 2010; 4:e797; PMID:20706586
   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
   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
• Reddy ST, Rehor A, Schmoekel HG, Hubbell JA, Swartz MA. In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J Controlled Release 2006; 112:26-34; http://dx.doi.org/10.1016/j.jconrel.2006.01.006
   PubMed Web of Science ®Google Scholar
• Conway MA, Madrigal-Estebas L, McClean S, Brayden DJ, Mills KH. Protection against Bordetella pertussis infection following parenteral or oral immunization with antigens entrapped in biodegradable particles: effect of formulation and route of immunization on induction of Th1 and Th2 cells. Vaccine 2001; 19:1940-50; PMID:11228364; http://dx.doi.org/10.1016/S0264-410X(00)00433-3
   PubMed Web of Science ®Google Scholar
• Audran R, Peter K, Dannull J, Men Y, Scandella E, Groettrup M, Gander B, Corradin G. Encapsulation of peptides in biodegradable microspheres prolongs their MHC class-I presentation by dendritic cells and macrophages in vitro. Vaccine 2003; 21:1250-5; PMID:12559806; http://dx.doi.org/10.1016/S0264-410X(02)00521-2
   PubMed Web of Science ®Google Scholar
• Evans JT, Ward JR, Kern J, Johnson ME. A single vaccination with protein-microspheres elicits a strong CD8 T-cell-mediated immune response against Mycobacterium tuberculosis antigen Mtb8.4. Vaccine 2004; 22:1964-72; PMID:15121309; http://dx.doi.org/10.1016/j.vaccine.2003.10.035
   PubMed Web of Science ®Google Scholar
• Fifis T, Gamvrellis A, Crimeen-Irwin B, Pietersz GA, Li J, Mottram PL, McKenzie IF, Plebanski M. Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors. J Immunol 2004; 173:3148-54; PMID:15322175; http://dx.doi.org/10.4049/jimmunol.173.5.3148
   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
• Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev Vacc 2010; 9:1095-107; http://dx.doi.org/10.1586/erv.10.89
   PubMed Web of Science ®Google Scholar
• Vabulas RM, Pircher H, Lipford GB, Hacker H, Wagner H. CpG-DNA activates in vivo T cell epitope presenting dendritic cells to trigger protective antiviral cytotoxic T cell responses. J Immunol 2000; 164:2372-8; PMID:10679072; http://dx.doi.org/10.4049/jimmunol.164.5.2372
   PubMed Web of Science ®Google Scholar
• Speiser DE, Lienard D, Rufer N, Rubio-Godoy V, Rimoldi D, Lejeune F, Krieg AM, Cerottini JC, Romero P. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest 2005; 115:739-46; PMID:15696196; http://dx.doi.org/10.1172/JCI23373
   PubMed Web of Science ®Google Scholar
• Lindblad EB. Aluminium compounds for use in vaccines. Immunol Cell Biol 2004; 82:497-505; PMID:15479435; http://dx.doi.org/10.1111/j.0818-9641.2004.01286.x
   PubMed Web of Science ®Google Scholar
• Hedayat M, Netea MG, Rezaei N. Targeting of Toll-like receptors: a decade of progress in combating infectious diseases. Lancet Infect Dis 2011; 11:702-12; PMID:21719349; http://dx.doi.org/10.1016/S1473-3099(11)70099-8
   PubMed Web of Science ®Google Scholar
• Almeida IC, Milani SR, Gorin PA, Travassos LR. Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-α-galactosyl antibodies. J Immunol 1991; 146:2394-400; PMID:1706399
   PubMed Web of Science ®Google Scholar
• US. National Institutes of Health. ClinicalTrials.gov.Search term: “CpG7909.”
   Google Scholar
• Lu JM, Wang X, Marin-Muller C, Wang H, Lin PH, Yao Q, Chen C. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev Mol Diagn 2009; 9:325-41; PMID:19435455; http://dx.doi.org/10.1586/erm.09.15
   PubMed Web of Science ®Google Scholar
• Krieg AM. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 2006; 5:471-84; PMID:16763660; http://dx.doi.org/10.1038/nrd2059
   PubMed Web of Science ®Google Scholar
• Krishnamachari Y, Salem AK. Innovative strategies for co-delivering antigens and CpG oligonucleotides. Adv Drug Deliv Rev 2009; 61:205-17; PMID:19272328; http://dx.doi.org/10.1016/j.addr.2008.12.013
   PubMed Web of Science ®Google Scholar
• Diwan M, Elamanchili P, Cao M, Samuel J. Dose sparing of CpG oligodeoxynucleotide vaccine adjuvants by nanoparticle delivery. Curr Drug Deliv 2004; 1:405-12; PMID:16305402; http://dx.doi.org/10.2174/1567201043334597
   PubMedGoogle Scholar
• Diwan M, Tafaghodi M, Samuel J. Enhancement of immune responses by co-delivery of a CpG oligodeoxynucleotide and tetanus toxoid in biodegradable nanospheres. J Controlled Release 2002; 85:247-62; http://dx.doi.org/10.1016/S0168-3659(02)00275-4
   PubMed Web of Science ®Google Scholar
• Malyala P, Chesko J, Ugozzoli M, Goodsell A, Zhou F, Vajdy M, O'Hagan DT, Singh M. The potency of the adjuvant, CpG oligos, is enhanced by encapsulation in PLG microparticles. J Pharm Sci 2008; 97:1155-64; PMID:17683059; http://dx.doi.org/10.1002/jps.21065
   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
• Zhang L, Tarleton RL. Parasite persistence correlates with disease severity and localization in chronic Chagas' disease. J Infect Dis 1999; 180:480-6; PMID:10395865; http://dx.doi.org/10.1086/314889
   PubMed Web of Science ®Google Scholar
• Cencig S, Coltel N, Truyens C, Carlier Y. Evaluation of benznidazole treatment combined with nifurtimox, posaconazole or AmBisome(R) in mice infected with Trypanosoma cruzi strains. Int J Antimicrob Agents 2012; 40:527-32; PMID:23063742; http://dx.doi.org/10.1016/j.ijantimicag.2012.08.002
   PubMed Web of Science ®Google Scholar
• Bustamante JM, Craft JM, Crowe BD, Ketchie SA, Tarleton RL. New, combined, and reduced dosing treatment protocols cure Trypanosoma cruzi infection in mice. J Infect Dis 2014; 209:150-62; PMID:23945371; http://dx.doi.org/10.1093/infdis/jit420
   PubMed Web of Science ®Google Scholar
• Olivieri BP, Molina JT, de Castro SL, Pereira MC, Calvet CM, Urbina JA, Araujo-Jorge TC. A comparative study of posaconazole and benznidazole in the prevention of heart damage and promotion of trypanocidal immune response in a murine model of Chagas disease. Int J Antimicrob Agents 2010; 36:79-83; PMID:20452188; http://dx.doi.org/10.1016/j.ijantimicag.2010.03.006
   PubMed Web of Science ®Google Scholar
• Santos DM, Carneiro MW, de Moura TR, Soto M, Luz NF, Prates DB, Irache JM, Brodskyn C, Barral A, Barral-Netto M, et al. PLGA nanoparticles loaded with KMP-11 stimulate innate immunity and induce the killing of Leishmania. Nanomedicine 2013; 9:985-95; PMID:23603355; http://dx.doi.org/10.1016/j.nano.2013.04.003
   PubMed Web of Science ®Google Scholar
• Tafaghodi M, Eskandari M, Kharazizadeh M, Khamesipour A, Jaafari MR. Immunization against leishmaniasis by PLGA nanospheres loaded with an experimental autoclaved Leishmania major (ALM) and Quillaja saponins. Trop Biomed 2010; 27:639-50; PMID:21399606
   PubMed Web of Science ®Google Scholar
• Gupta S, Garg NJ. A Two-Component DNA-Prime/Protein-Boost Vaccination Strategy for Eliciting Long-Term, Protective T Cell Immunity against Trypanosoma cruzi. PLoS Pathog 2015; 11:e1004828; PMID:25951312; http://dx.doi.org/10.1371/journal.ppat.1004828
   PubMed Web of Science ®Google Scholar
• Sah H. A new strategy to determine the actual protein content of poly(lactide-co-glycolide) microspheres. J Pharm Sci 1997; 86:1315-8; PMID:9383747; http://dx.doi.org/10.1021/js960363q
   PubMed Web of Science ®Google Scholar
• Quah BJ, Warren HS, Parish CR. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat Protoc 2007; 2:2049-56; PMID:17853860; http://dx.doi.org/10.1038/nprot.2007.296
   PubMed Web of Science ®Google Scholar
• Melo MF, Moreira OC, Tenorio P, Lorena V, Lorena-Rezende I, Junior WO, Gomes Y, Britto C. Usefulness of real time PCR to quantify parasite load in serum samples from chronic Chagas disease patients. Parasit Vectors 2015; 8:154; PMID:25890282; http://dx.doi.org/10.1186/s13071-015-0770-0
   PubMed Web of Science ®Google Scholar
• Piron M, Fisa R, Casamitjana N, Lopez-Chejade P, Puig L, Verges M, Gascon J, Gomez i Prat J, Portus M, Sauleda S. Development of a real-time PCR assay for Trypanosoma cruzi detection in blood samples. Acta Trop 2007; 103:195-200; PMID:17662227; http://dx.doi.org/10.1016/j.actatropica.2007.05.019
   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
• 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
• Cencig S, Coltel N, Truyens C, Carlier Y. Parasitic loads in tissues of mice infected with Trypanosoma cruzi and treated with AmBisome. PLoS Neglected Tropical Dis 2011; 5:e1216; PMID:21738811; http://dx.doi.org/10.1371/journal.pntd.0001216
   PubMedGoogle Scholar