Enhanced immune response against pertussis toxoid by IgA-loaded chitosan-dextran sulfate nanoparticles

Journal of Pharmaceutical Sciences

Volumn 101, Issue 1, 2012, Pages 233-244

  Sharma, Sameer ^a,b   Mukkur, Trilochan Ks ^a   Benson, Heather Ae ^a   Chen, Yan ^a  

^a CURTIN UNIVERSITY   (Australia)

^b CSIRO   (Australia)

Author keywords

Chitosan; Dextran sulfate; Immunoglobulin A; Nanoparticles; Proteins; Vaccine adjuvants; Vaccine delivery

Indexed keywords

ANTIGEN; CHITOSAN DERIVATIVE; DEXTRAN SULFATE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOLOGICAL ADJUVANT; NANOPARTICLE; PERTUSSIS TOXIN; POLYELECTROLYTE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; FEMALE; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; MOUSE; NONHUMAN; PERTUSSIS; ZETA POTENTIAL;

EID: 82255192507     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.22763     Document Type: Article

References (64)

1. Bramwell VW, Perrie Y. 2005. Particulate delivery systems for vaccines. Crit Rev Ther Drug Carrier Syst 22(2):151-214.
2. Daemen T, de Mare A, Bungener L, de Jonge J, Huckriede A, Wilschut J. 2005. Virosomes for antigen and DNA delivery. Adv Drug Deliv Rev 57(3):451-463.
3. Kersten G, Hirschberg H. 2004. Antigen delivery systems. Expert Rev Vaccines 3(4):453-462.
4. Sharma S, Mukkur TK, Benson HA, Chen Y. 2009. Pharmaceutical aspects of intranasal delivery of vaccines using particulate systems. J Pharm Sci 98(3):812-843.
5. Gan Q, Wang T, Cochrane C, McCarron P. 2005. Modulation of surface charge, particle size and morphological properties of chitosan-TPP nanoparticles intended for gene delivery. Colloids Surf B 44(2-3):65-73.
6. Tiyaboonchai W, Limpeanchob N. 2007. Formulation and characterization of amphotericin B-chitosan-dextran sulfate nanoparticles. Int J Pharm 329(1-2):142-149.
7. Ma Z, Yeoh HH, Lim LY. 2002. Formulation pH modulates the interaction of insulin with chitosan nanoparticles. J Pharm Sci 91(6):1396-1404.
8. Janes KA, Calvo P, Alonso MJ. 2001. Polysaccharide colloidal particles as delivery systems for macromolecules. Adv Drug Deliv Rev 47(1):83-97.
9. Xu Y, Du Y. 2003. Effect of molecular structure of chitosan on protein delivery properties of chitosan nanoparticles. Int J Pharm 250(1):215-226.
10. Chen Y, Mohanraj V, Parkin J. 2003. Chitosan-dextran sulfate nanoparticles for delivery of an anti-angiogenesis peptide. Int J Pept Res Ther 10(5-6):621-629.
11. Chen Y, Mohanraj VJ, Wang F, Benson HA. 2007. Designing chitosan-dextran sulfate nanoparticles using charge ratios. AAPS PharmSciTech 8(4):E98.
12. Munoz FM. 2006. Pertussis in infants, children, and adolescents: Diagnosis, treatment, and prevention. Semin Pediatr Infect Dis 17(1):14-19.
13. Bamberger ES, Srugo I. 2008. What is new in pertussis? Eur J Pediatr 167(2):133-139.
14. Konig J, Bock A, Perraud AL, Fuchs TM, Beier D, Gross R. 2002. Regulatory factors of Bordetella pertussis affecting virulence gene expression. J Mol Microbiol Biotechnol 4(3):197-203.
15. 2005. Pertussis vaccines WHO position paper. Weekly epidemiological record. Geneva, Switzerland: World Health Organization, pp 29-40.
16. Mantis NJ, Cheung MC, Chintalacharuvu KR, Rey J, Corthesy B, Neutra MR. 2002. Selective adherence of IgA to murine Peyer's patch M cells: Evidence for a novel IgA receptor. J Immunol 169(4):1844-1851.
17. Weltzin R, Lucia-Jandris P, Michetti P. 1989. Binding and transepithelial transport of immunoglobulins by intestinal M cells: Demonstration using monoclonal IgA antibodies against enteric viral proteins. J Cell Biol 108(5):1673-1685.
18. Corthesy B. 2007. Roundtrip ticket for secretory IgA: Role in mucosal homeostasis? J Immunol 178(1):27-32.
19. Corthesy B. 2009. Secretory immunoglobulin A: Well beyond immune exclusion at mucosal surfaces. Immunopharmacol Immunotoxicol 31(2):174-179.
20. Favre L, Spertini F, Corthesy B. 2005. Secretory IgA possesses intrinsic modulatory properties stimulating mucosal and systemic immune responses. J Immunol 175(5):2793-2800.
21. Zhou F, Kraehenbuhl JP, Neutra MR. 1995. Mucosal IgA response to rectally administered antigen formulated in IgA-coated liposomes. Vaccine 13(7):637-644.
22. Munoz JJ, Arai H, Cole RL. 1981. Mouse-protecting and histamine-sensitizing activities of pertussigen and fimbrial hemagglutinin from Bordetella pertussis. Infect Immun 32(1):243-250.
23. Hewlett EL, Sauer KT, Myers GA, Cowell JL, Guerrant RL. 1983. Induction of a novel morphological response in Chinese hamster ovary cells by pertussis toxin. Infect Immun 40(3):1198-1203.
24. Amidi M, Romeijn SG, Borchard G, Junginger HE, Hennink WE, Jiskoot W. 2006. Preparation and characterization of protein-loaded N-trimethyl chitosan nanoparticles as nasal delivery system. J Control Release 111(1-2):107-116.
25. Le Saux N, Barrowman NJ, Moore DL, Whiting S, Scheifele D, Halperin S. 2003. Decrease in hospital admissions for febrile seizures and reports of hypotonic-hyporesponsive episodes presenting to hospital emergency departments since switching to acellular pertussis vaccine in Canada: A report from IMPACT. Pediatrics 112(5):e348.
26. Rosenthal S, Chen R, Hadler S. 1996. The safety of acellular pertussis vaccine vs. whole-cell pertussis vaccine. A postmarketing assessment. Arch Pediatr Adolesc Med 150(5):457-460.
27. Isbrucker RA, Bliu A, Prior F. 2010. Modified binding assay for improved sensitivity and specificity in the detection of residual pertussis toxin in vaccine preparations. Vaccine 28(15):2687-2692.
28. Corbel MJ, Xing DKL, Bolgiano B, Hockley DJ. 1999. Approaches to the control of acellular pertussis vaccines. Biologicals 27(2):133-141.
29. Gillenius P, Jaatmaa E, Askelof P, Granstrom M, Tiru M. 1985. The standardization of an assay for pertussis toxin and antitoxin in microplate culture of Chinese hamster ovary cells. J Biol Stand 13(1):61-66.
30. Corbel MJ, Xing DK. 2004. Toxicity and potency evaluation of pertussis vaccines. Expert Rev Vaccines 3(1):89-101.
31. Wong WS, Rosoff PM. 1996. Pharmacology of pertussis toxin B-oligomer. Can J Physiol Pharmacol 74(5):559-564.
32. Ibsen PH. 1996. The effect of formaldehyde, hydrogen peroxide and genetic detoxification of pertussis toxin on epitope recognition by murine monoclonal antibodies. Vaccine 14(5):359-368.
33. Nencioni L, Volpini G, Peppoloni S, Bugnoli M, De Magistris T, Marsili I, Rappuoli R. 1991. Properties of pertussis toxin mutant PT-9K/129G after formaldehyde treatment. Infect Immun 59(2):625-630.
34. Burns DL, Hausman SZ, Lindner W, Robey FA, Manclark CR. 1987. Structural characterization of pertussis toxin A subunit. J Biol Chem 262(36):17677-17682.
35. Fowler S, Xing DK, Bolgiano B, Yuen CT, Corbel MJ. 2003. Modifications of the catalytic and binding subunits of pertussis toxin by formaldehyde: Effects on toxicity and immunogenicity. Vaccine 21(19-20):2329-2337.
36. Kabanov VA, Zezin AB. 1984. A new class of complex water-soluble polyelectrolytes. Die Makromolekulare Chemie 6(S1):259-276.
37. Drogoz A, David L, Rochas C, Domard A, Delair T. 2007. Polyelectrolyte complexes from polysaccharides: Formation and stoichiometry monitoring. Langmuir 23(22):10950-10958.
38. Schatz C, Lucas JM, Viton C, Domard A, Pichot C, Delair T. 2004. Formation and properties of positively charged colloids based on polyelectrolyte complexes of biopolymers. Langmuir 20(18):7766-7778.
39. Mincheva R, Bougard F, Paneva D, Vachaudez M, Manolova N, Rashkov I, Dubois P. 2009. Natural polyampholyte-based core-shell nanoparticles with N-carboxyethylchitosan-containing core and poly(ethylene oxide) shell. Biomacromolecules 10(4):838-844.
40. Sarmento B, Ribeiro A, Veiga F, Ferreira D. 2006. Development and characterization of new insulin containing polysaccharide nanoparticles. Colloids Surf B 53(2):193-202.
41. Borges O, Cordeiro-da-Silva A, Romeijn SG, Amidi M, de Sousa A, Borchard G, Junginger HE. 2006. Uptake studies in rat Peyer's patches, cytotoxicty and release studies of alginate coated chitosan nanoparticles for mucosal vaccination. J Control Release 114(3):348-358.
42. Shahin R, Leef M, Eldridge J, Hudson M, Gilley R. 1995. Adjuvanticity and protective immunity elicited by Bordetella pertussis antigens encapsulated in poly(DL-lactide-co-glycolide) microspheres. Infect Immun 63(4):1195-1200.
43. Shahin RD, Cowell JL. 1994. Mouse respiratory infection models for pertussis. Methods Enzymol 235:47-58.
44. Ogunniyi AD, Folland RL, Briles DE, Hollingshead SK, Paton JC. 2000. Immunization of mice with combinations of pneumococcal virulence proteins elicits enhanced protection against challenge with Streptococcus pneumoniae. Infect Immun 68(5):3028-3033.
45. Pasare C, Medzhitov R. 2004. Toll-dependent control mechanisms of CD4 T cell activation. Immunity 21(5):733-741.
46. Gavin AL, Hoebe K, Duong B, Ota T, Martin C, Beutler B, Nemazee D. 2006. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science 314(5807):1936-1938.
47. Goebel EM, Zhang X, Harvill ET. 2009. Bordetella pertussis infection or vaccination substantially protects mice against B. bronchiseptica infection. PLoS One 4(8):e6778.
48. Denoël P, Poolman J, Carletti G, Veitch K. 2002. Effects of adsorption of acellular pertussis antigens onto different aluminium salts on the protective activity in an intranasal murine model of Bordetella pertussis infection. Vaccine 20(19-20):2551-2555.
49. Zeng M, Xu Q, Pichichero ME. 2007. Protection against anthrax by needle-free mucosal immunization with human anthrax vaccine. Vaccine 25(18):3588-3594.
50. Huang Y, Hajishengallis G, Michalek SM. 2001. Induction of protective immunity against Streptococcus mutans colonization after mucosal immunization with attenuated Salmonella enterica serovar typhimurium expressing an S. mutans adhesin under the control of in vivo-inducible nirB promoter. Infect Immun 69(4):2154-2161.
51. SayIn B, Somavarapu S, Li XW, Thanou M, Sesardic D, Alpar HO, Senel S. 2008. Mono-N-carboxymethyl chitosan (MCC) and N-trimethyl chitosan (TMC) nanoparticles for non-invasive vaccine delivery. Int J Pharm 363(1-2):139-148.
52. Mosmann TR, Sad S. 1996. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17(3):138-146.
53. Gracia A, Polewicz M, Halperin SA, Hancock REW, Potter AA, Babiuk LA, Gerdts V. 2011. Antibody responses in adult and neonatal BALB/c mice to immunization with novel Bordetella pertussis vaccine formulations. Vaccine 29(8):1595-1604.
54. Borges O, Silva M, de Sousa A, Borchard G, Junginger HE, Cordeiro-da-Silva A. 2008. Alginate coated chitosan nanoparticles are an effective subcutaneous adjuvant for hepatitis B surface antigen. Int Immunopharmacol 8(13-14):1773-1780.
55. Ogra PL. 1984. Mucosal immune response to poliovirus vaccines in childhood. Rev Infect Dis 6 Suppl 2:S361-S368.
56. Wang J, Thorson L, Stokes RW, Santosuosso M, Huygen K, Zganiacz A, Hitt M, Xing Z. 2004. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J Immunol 173(10):6357-6365.
57. Yoo MK, Kang SK, Choi JH, Park IK, Na HS, Lee HC, Kim EB, Lee NK, Nah JW, Choi YJ, Cho CS. 2010. Targeted delivery of chitosan nanoparticles to Peyer's patch using M cell-homing peptide selected by phage display technique. Biomaterials 31:7738-7747.
58. Slutter B, Plapied L, Fievez V, Sande MA, des Rieux A, Schneider YJ, Van Riet E, Jiskoot W, Preat V. 2009. Mechanistic study of the adjuvant effect of biodegradable nanoparticles in mucosal vaccination. J Control Release 138(2):113-121.
59. Yuan X, Yang X, Cai D, Mao D, Wu J, Zong L, Liu J. 2008. Intranasal immunization with chitosan/pCETP nanoparticles inhibits atherosclerosis in a rabbit model of atherosclerosis. Vaccine 26(29-30):3727-3734.
60. Ghendon Y, Markushin S, Krivtsov G, Akopova I. 2008. Chitosan as an adjuvant for parenterally administered inactivated influenza vaccines. Arch Virol 153(5):831-837.
61. Zhu B, Qie Y, Wang J, Zhang Y, Wang Q, Xu Y, Wang H. 2007. Chitosan microspheres enhance the immunogenicity of an Ag85B-based fusion protein containing multiple T-cell epitopes of Mycobacterium tuberculosis. Eur J Pharm Biopharm 66(3):318-326.
62. Zaharoff DA, Rogers CJ, Hance KW, Schlom J, Greiner JW. 2007. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine 25(11):2085-2094.
63. Agnihotri SA, Mallikarjuna NN, Aminabhavi TM. 2004. Recent advances on chitosan-based micro- and nanoparticles in drug delivery. J Control Release 100(1):5-28.
64. Bramwell VW, Perrie Y. 2005. The rational design of vaccines. Drug Discover Today 10(22):1527-1534.