An innovative approach to induce cross-protective immunity against porcine reproductive and respiratory syndrome virus in the lungs of pigs through adjuvanted nanotechnology-based vaccination

International Journal of Nanomedicine

Volumn 9, Issue 1, 2014, Pages 1519-1535

  Binjawadagi, Basavaraj ^a,b   Dwivedi, Varun ^a   Manickam, Cordelia ^a,b   Ouyang, Kang ^a   Torrelles, Jordi B ^b   Renukaradhya, Gourapura J ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Cross protection; M. tb WCL; Mucosal vaccine; PLGA nanoparticles; PRRSV

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; NANOPARTICLE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS VACCINE ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTERIVIRUS; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PROTECTION; CYTOKINE PRODUCTION; DRUG DELIVERY SYSTEM; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNOGENICITY; LUNG PARENCHYMA; MYCOBACTERIUM TUBERCULOSIS; NANOTECHNOLOGY; NONHUMAN; RESPIRATORY SYSTEM; RESPIRATORY TRACT MUCOSA; SWINE; VACCINATION; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS REPLICATION;

CROSS-PROTECTION; M. TB WCL; MUCOSAL VACCINE; PLGA NANOPARTICLES; PRRSV;

ANIMALS; CROSS PROTECTION; LACTIC ACID; LUNG; NANOCAPSULES; POLYGLYCOLIC ACID; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; SWINE; TREATMENT OUTCOME; VACCINES, INACTIVATED; VIRAL VACCINES;

EID: 84897034136     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S59924     Document Type: Article

References (74)

1. Holtkamp D, Kliebenstein J. PRRS Costs Industry $664 Million Annually [webpage on the Internet]. Pork Checkoff Study, 2011. Available from: http://www.pork.org/News/1265/PRRSCostsIndustry664Million.aspx. Accessed January 26, 2014.
2. Wang X, Eaton M, Mayer M, et al. Porcine reproductive and respiratory syndrome virus productively infects monocyte-derived dendritic cells and compromises their antigen-presenting ability. Arch Virol. 2007;152(2):289-303.
3. Nielsen HS, Oleksiewicz MB, Forsberg R, Stadejek T, Bøtner A, Storgaard T. Reversion of a live porcine reproductive and respiratory syndrome virus vaccine investigated by parallel mutations. J Gen Virol. 2001;82(Pt 6):1263-1272.
4. Kimman TG, Cornelissen LA, Moormann RJ, Rebel JM, Stockhofe-Zurwieden N. Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine. 2009;27(28):3704-3718.
5. Chadwick S, Kriegel C, Amiji M. Nanotechnology solutions for mucosal immunization. Adv Drug Deliv Rev. 2010;62(4-5):394-407.
6. Devalapally H, Chakilam A, Amiji MM. Role of nanotechnology in pharmaceutical product development. Pharm Sci. 2007;96(10): 2547-2565.
7. Ulmer JB, Valley U, Rappuoli R. Vaccine manufacturing: challenges and solutions. Nat Biotechnol. 2006;24(11):1377-1383.
8. Murtaugh MP, Xiao Z, Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol. 2002;15(4):533-547.
9. Bhavsar MD, Amiji MM. Polymeric nano-and microparticle technologies for oral gene delivery. Expert Opin Drug Deliv. 2007;4(3): 197-213.
10. Giri PK, Khuller GK. Is intranasal vaccination a feasible solution for tuberculosis? Expert Rev Vaccines. 2008;7(9):1341-1356.
11. McNeil SE. Nanotechnology for the biologist. J Leukoc Biol. 2005;78(3):585-594.
12. Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev. 2003;55(3):329-347.
13. Garg NK, Mangal S, Khambete H, Sharma PK, Tyagi RK. Mucosal delivery of vaccines: role of mucoadhesive/biodegradable polymers. Recent Pat Drug Deliv Formul. 2010;4(2):114-128.
14. Binjawadagi B, Dwivedi V, Manickam C, et al. Adjuvanted poly(lactic-co-glycolic) acid nanoparticle-entrapped inactivated porcine reproductive and respiratory syndrome virus vaccine elicits cross-protective immune response in pigs. Int J Nanomedicine. 2014;9: 679-694.
15. Dwivedi V, Manickam C, Patterson R, et al. Cross-protective immunity to porcine reproductive and respiratory syndrome virus by intranasal delivery of a live virus vaccine with a potent adjuvant. Vaccine. 2011;29(23):4058-4066.
16. Dwivedi V, Manickam C, Patterson R, Dodson K, Weeman M, Renukaradhya GJ. Intranasal delivery of whole cell lysate of Mycobacterium tuberculosis induces protective immune responses to a modified live porcine reproductive and respiratory syndrome virus vaccine in pigs. Vaccine 2011;29(23):4067-4076.
17. Renukaradhya GJ, Dwivedi V, Manickam C, Binjawadagi B, Benfield D. Mucosal vaccines to prevent porcine reproductive and respiratory syndrome: a new perspective. Anim Health Res Rev. 2012;13(1):21-37.
18. Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu Rev Immunol. 2002;20:395-425.
19. Werner GH, Maral R, Floch F, Migliore-Samour D, Jollès P. Adjuvant and immunostimulating activities of water-soluble substances extracted from Mycobacterium tuberculosis (var. hominis). Biomedicine. 1975;22(5):440-452.
20. Larson CL, Bell JF, List RH, Ribi E, Wicht WC. Symposium on relationship of structure of microorganisms to their immunological properties. ii. host-reactive properties of cell walls and protoplasm from mycobacteria. Bacteriol Rev. 1963;27:341-351.
21. White RG, Bernstock L, Johns RG, Lederer E. The influence of components of M. tuberculosis and other Mycobacteria upon antibody production to ovalbumin. Immunology. 1958;1(1):54-66.
22. Dwivedi V, Manickam C, Binjawadagi B, Joyappa D, Renukaradhya GJ. Biodegradable nanoparticle-entrapped vaccine induces cross-protective immune response against a virulent heterologous respiratory viral infection in pigs. PLoS One. 2012;7(12):e51794.
23. Dwivedi V, Manickam C, Binjawadagi B, Renukaradhya GJ. PLGA nanoparticle entrapped killed porcine reproductive and respiratory syndrome virus vaccine helps in viral clearance in pigs. Vet Microbiol. 2013;166(1-2):47-58.
24. Kim WI, Lee DS, Johnson W, Roof M, Cha SH, Yoon KJ. Effect of genotypic and biotypic differences among PRRS viruses on the serologic assessment of pigs for virus infection. Microbiol. 2007;123(1-3): 1-14.
25. Takayama K, Schnoes HK, Armstrong EL, Boyle RW. Site of inhibitory action of isoniazid in the synthesis of mycolic acids in Mycobacterium tuberculosis. J Lipid Res. 1975;16(4):308-317.
26. Jung K, Alekseev KP, Zhang X, Cheon DS, Vlasova AN, Saif LJ. Altered pathogenesis of porcine respiratory coronavirus in pigs due to immunosuppressive effects of dexamethasone: implications for corticosteroid use in treatment of severe acute respiratory syndrome coronavirus. J Virol. 2007;81(24):13681-13693.
27. Renukaradhya GJ, Alekseev K, Jung K, Fang Y, Saif LJ. Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral Immunol. 2010;23(5):457-466.
28. Kaiser TJ, Christopher-Hennings J, Nelson EA. Measurement of immunoglobulin G, A and M concentrations in boar seminal plasma. Theriogenology. 2000;54(7):1171-1184.
29. Zhang L, Tian X, Zhou F. Intranasal administration of CpG oligonucleotides induces mucosal and systemic Type 1 immune responses and adjuvant activity to porcine reproductive and respiratory syndrome killed virus vaccine in piglets in vivo. Int Immunopharmacol. 2007;7(13):1732-1740.
30. Mulupuri P, Zimmerman JJ, Hermann J, et al. Antigen-specific B-cell responses to porcine reproductive and respiratory syndrome virus infection. J Virol. 2008;82(1):358-370.
31. Thompson AL, Johnson BT, Sempowski GD, et al. Maximal adjuvant activity of nasally delivered IL-1α requires adjuvant-responsive CD11c(+) cells and does not correlate with adjuvant-induced in vivo cytokine production. Immunol. 2012;188(6):2834-2846.
32. Ferreira MU, Katzin AM. The assessment of antibody affinity distribution by thiocyanate elution: a simple dose-response approach. J Immunol Methods. 1995;187(2):297-305.
33. Guo YJ, Sun SH, Zhang Y, et al. Protection of pigs against Taenia solium cysticercosis using recombinant antigen or in combination with DNA vaccine. Vaccine. 2004;22(29-30):3841-3847.
34. Adam A, Ciorbaru R, Petit JF, Lederer E. Isolation and properties of a macromolecular, water-soluble, immuno-adjuvant fraction from the cell wall of Mycobacterium smegmatis. Proc Natl Acad Sci U S A. 1972;69(4):851-854.
35. Azevedo MS, Yuan L, Pouly S, et al. Cytokine responses in gnotobiotic pigs after infection with virulent or attenuated human rotavirus. Virol. 2006;80(1):372-382.
36. Christopher-Hennings J, Holler LD, Benfield DA, Nelson EA. Detection and duration of porcine reproductive and respiratory syndrome virus in semen, serum, peripheral blood mononuclear cells, and tissues from Yorkshire, Hampshire, and Landrace boars. J Vet Diagn Invest. 2001;13(2):133-142.
37. Cai HY, Alexander H, Carman S, Lloyd D, Josephson G, Maxie MG. Restriction fragment length polymorphism of porcine reproductive and respiratory syndrome viruses recovered from Ontario farms, 1998-2000. Vet Diagn Invest. 2002;14(4):343-347.
38. Fang Y, Kim DY, Ropp S, et al. Heterogeneity in Nsp2 of European-like porcine reproductive and respiratory syndrome viruses isolated in the United States. Virus Res. 2004;100(2):229-235.
39. Manickam C, Dwivedi V, Patterson R, Papenfuss T, Renukaradhya GJ. Porcine reproductive and respiratory syndrome virus induces pronounced immune modulatory responses at mucosal tissues in the parental vaccine strain VR2332 infected pigs. Vet Microbiol. 2013;162(1):68-77.
40. Darwich L, Díaz I, Mateu E. Certainties, doubts and hypotheses in porcine reproductive and respiratory syndrome virus immunobiology. Virus Res. 2010;154(1-2):123-132.
41. Kamijuku H, Nagata Y, Jiang X, et al. Mechanism of NKT cell activation by intranasal coadministration of alpha-galactosylceramide, which can induce cross-protection against influenza viruses. Mucosal Immunol. 2008;1(3):208-218.
42. Guillonneau C, Mintern JD, Hubert FX, et al. Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proc Natl Acad Sci U S A. 2009;106(9):3330-3335.
43. Ogra PL. Mucosal immune response to poliovirus vaccines in childhood. Rev Infect Dis. 1984;6 Suppl 2:S361-S368.
44. Schmidt AC, Wenzke DR, McAuliffe JM, et al. Mucosal immunization of rhesus monkeys against respiratory syncytial virus subgroups A and B and human parainfluenza virus type 3 by using a live cDNA-derived vaccine based on a host range-attenuated bovine parainfluenza virus type 3 vector backbone. J Virol. 2002;76(3):1089-1099.
45. Imaoka K, Miller CJ, Kubota M, et al. Nasal immunization of nonhuman primates with simian immunodeficiency virus p55gag and cholera toxin adjuvant induces Th1/Th2 help for virus-specific immune responses in reproductive tissues. J Immunol. 1998;161(11):5952-5958.
46. Manocha M, Pal PC, Chitralekha KT, et al. Enhanced mucosal and systemic immune response with intranasal immunization of mice with HIV peptides entrapped in PLG microparticles in combination with Ulex Europaeus-I lectin as M cell target. Vaccine. 2005;23(48-49): 5599-5617.
47. Rossow KD, Benfield DA, Goyal SM, Nelson EA, Christopher-Hennings J, Collins JE. Chronological immunohistochemical detection and localization of porcine reproductive and respiratory syndrome virus in gnotobiotic pigs. Vet Pathol. 1996;33(5):551-556.
48. Ganter M, Hensel A. Cellular variables in bronchoalveolar lavage fluids (BALF) in selected healthy pigs. Res Vet Sci. 1997;63(3):215-217.
49. Kugathasan K, Roediger EK, Small CL, McCormick S, Yang P, Xing Z. CD11c+ antigen presenting cells from the alveolar space, lung parenchyma and spleen differ in their phenotype and capabilities to activate naïve and antigen-primed T cells. BMC Immunol. 2008;9:48.
50. Plagemann PG, Rowland RR, Cafruny WA. Polyclonal hypergammaglobulinemia and formation of hydrophobic immune complexes in porcine reproductive and respiratory syndrome virus-infected and uninfected pigs. Viral Immunol. 2005;18(1):138-147.
51. Butler JE, Wertz N, Weber P, Lager KM. Porcine reproductive and respiratory syndrome virus subverts repertoire development by proliferation of germline-encoded B cells of all isotypes bearing hydrophobic heavy chain CDR3. J Immunol. 2008;180(4):2347-2356.
52. Kim H, Kim HK, Jung JH, et al. The assessment of efficacy of porcine reproductive respiratory syndrome virus inactivated vaccine based on the viral quantity and inactivation methods. Virol J. 2011;8:323.
53. Vanhee M, Delputte PL, Delrue I, Geldhof MF, Nauwynck HJ. Development of an experimental inactivated PRRSV vaccine that induces virus-neutralizing antibodies. Vet Res. 2009;40(6):63.
54. Rajapaksa TE, Bennett KM, Hamer M, Lytle C, Rodgers VG, Lo DD. Intranasal M cell uptake of nanoparticles is independently influenced by targeting ligands and buffer ionic strength. Biol Chem. 2010;285(31):23739-23746.
55. Araujo L, Löbenberg R, Kreuter J. Influence of the surfactant concentration on the body distribution of nanoparticles. Drug Target. 1999;6(5):373-385.
56. Heegaard PM, Dedieu L, Johnson N, et al. Adjuvants and delivery systems in veterinary vaccinology: current state and future developments. Arch Virol. 2011;156(2):183-202.
57. Harmala LA, Ingulli EG, Curtsinger JM, et al. The adjuvant effects of Mycobacterium tuberculosis heat shock protein 70 result from the rapid and prolonged activation of antigen-specific CD8+ T cells in vivo. J Immunol. 2002;169(10):5622-5629.
58. Bansal K, Elluru SR, Narayana Y, et al. PE_PGRS antigens of Mycobacterium tuberculosis induce maturation and activation of human dendritic cells. J Immunol. 2010;184(7):3495-3504.
59. Lycke N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol. 2012;12(8):592-605.
60. Binjawadagi B, Dwivedi V, Manickam C, Torrelles JB, Renukaradhya GJ. Intranasal delivery of an adjuvanted modified live porcine reproductive and respiratory syndrome virus vaccine reduces ROS production. Viral Immunol. 2011;24(6):475-482.
61. Dwivedi V, Manickam C, Binjawadagi B, Linhares D, Murtaugh MP, Renukaradhya GJ. Evaluation of immune responses to porcine reproductive and respiratory syndrome virus in pigs during early stage of infection under farm conditions. Virol J. 2012;9:45.
62. Manickam C, Dwivedi V, Miller J, Papenfuss T, Renukaradhya GJ. Mycobacterium tuberculosis whole cell lysate enhances proliferation of CD8 positive lymphocytes and nitric oxide secretion in the lungs of live porcine respiratory and reproductive syndrome virus vaccinated pigs. Viral Immunol. 2013;26(1):102-108.
63. Amorij JP, Kersten GF, Saluja V, et al. Towards tailored vaccine delivery: needs, challenges and perspectives. Control Release. 2012;161(2):363-376.
64. Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10(11): 787-796.
65. Lopez OJ, Osorio FA. Role of neutralizing antibodies in PRRSV protective immunity. Vet Immunol Immunopathol. 2004;102(3):155-163.
66. Spellberg B, Edwards JE. Type 1/Type 2 immunity in infectious diseases. Clin Infect Dis. 2001;32(1):76-102.
67. Schliehe C, Redaelli C, Engelhardt S, et al. CD8-dendritic cells and macrophages cross-present poly(D, L-lactate-co-glycolate) acid microsphere-encapsulated antigen in vivo. J Immunol. 2011;187(5): 2112-2121.
68. Demento SL, Cui W, Criscione JM, et al. Role of sustained antigen release from nanoparticle vaccines in shaping the T cell memory phenotype. Biomaterials. 2012;33(19):4957-4964.
69. Ma W, Chen M, Kaushal S, et al. PLGA nanoparticle-mediated delivery of tumor antigenic peptides elicits effective immune responses. Int J Nanomedicine. 2012;7:1475-1487.
70. Sansonetti PJ, Di Santo JP. Debugging how bacteria manipulate the immune response. Immunity. 2007;26(2):149-161.
71. Olin MR, Batista L, Xiao Z, et al. Gammadelta lymphocyte response to porcine reproductive and respiratory syndrome virus. Viral Immunol. 2005;18(3):490-499.
72. Chong CS, Cao M, Wong WW, et al. Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J Control Release. 2005;102(1): 85-99.
73. Zimmerman JJ, Benfield D, Dee S, et al. Porcine reproductive and respiratory syndrome virus (Porcine Arterivirus). In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, editors. Diseases of Swine, Tenth Edition: Wiley-Blackwell, Hoboken, NJ, USA; 2012:461-486.
74. Wills RW, Zimmerman JJ, Yoon KJ, et al. Porcine reproductive and respiratory syndrome virus: a persistent infection. Vet Microbiol. 1997;55(1-4):231-240.