CpG oligodeoxynucleotides facilitate delivery of whole inactivated H9N2 influenza virus via transepithelial dendrites of dendritic cells in nasal mucosa

Journal of Virology

Volumn 89, Issue 11, 2015, Pages 5904-5918

  Qin, Tao ^a   Yin, Yinyan ^a   Yu, Qinghua ^a   Huang, Lulu ^a   Wang, Xiaoqing ^a   Lin, Jian ^a   Yang, Qian ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; CPG-OLIGONUCLEOTIDE; IMMUNOLOGICAL ADJUVANT; INACTIVATED VACCINE; INFLUENZA VACCINE; OLIGODEOXYRIBONUCLEOTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELL MATURATION; CELL TRANSPORT; CERVICAL LYMPH NODE; COCULTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; EPITHELIUM CELL; IMMUNE RESPONSE; IMMUNOPOTENTIATION; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VIRUS A H9N2; MONOCULTURE; MOUSE; NONHUMAN; NOSE MUCOSA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSEPITHELIAL DENDRITE; VIRUS INACTIVATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL MOTION; IMMUNOLOGY; INFLUENZA A VIRUS (H9N2); LYMPH NODE; MUCOSAL DRUG ADMINISTRATION;

AVES; ORTHOMYXOVIRIDAE;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, MUCOSAL; ANIMALS; CELL MOVEMENT; DENDRITES; DENDRITIC CELLS; EPITHELIAL CELLS; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA VACCINES; LYMPH NODES; MICE, INBRED BALB C; MICE, INBRED C57BL; NASAL MUCOSA; OLIGODEOXYRIBONUCLEOTIDES; VACCINES, INACTIVATED;

EID: 84929630619     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00296-15     Document Type: Article

References (67)

1. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y. 2013. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368: 1888-1897. http://dx.doi.org/10.1056/NEJMoa1304459.
2. Xiong X, Martin SR, Haire LF, Wharton SA, Daniels RS, Bennett MS, McCauley JW, Collins PJ, Walker PA, Skehel JJ, Gamblin SJ. 2013. Receptor binding by an H7N9 influenza virus from humans. Nature 499: 496-499. http://dx.doi.org/10.1038/nature12372.
3. Kang H, Wang H, Yu Q, Yang Q. 2012. Effect of intranasal immunization with inactivated avian influenza virus on local and systemic immune responses in ducks. Poult Sci 91:1074-1080. http://dx.doi.org/10.3382/ps.2011-01817.
4. Rose MA, Zielen S, Baumann U. 2012. Mucosal immunity and nasal influenza vaccination. Expert Rev Vaccines 11:595-607. http://dx.doi.org/10.1586/erv.12.31.
5. Chen H. 2009. Avian influenza vaccination: the experience in China. Rev Sci Tech 28:267-274.
6. Geeraedts F, Goutagny N, Hornung V, Severa M, de Haan A, Pool J, Wilschut J, Fitzgerald KA, Huckriede A. 2008. Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog 4:e1000138. http://dx.doi.org/10.1371/journal.ppat.1000138.
7. Illum L. 2003. Nasal drug delivery-possibilities, problems and solutions. J Control Release 87:187-198. http://dx.doi.org/10.1016/S0168-3659(02)00363-2.
8. Wu Y, Wei W, Zhou M, Wang Y, Wu J, Ma G, Su Z. 2012. Thermalsensitive hydrogel as adjuvant-free vaccine delivery system for H5N1 intranasal immunization. Biomaterials 33:2351-2360. http://dx.doi.org/10.1016/j.biomaterials.2011.11.068.
9. Tamura S, Samegai Y, Kurata H, Nagamine T, Aizawa C, Kurata T. 1988. Protection against influenza virus infection by vaccine inoculated intranasally with cholera toxin B subunit. Vaccine 6:409-413. http://dx.doi.org/10.1016/0264-410X(88)90140-5.
10. Couch RB, Atmar RL, Cate TR, Quarles JM, Keitel WA, Arden NH, Wells J, Nino D, Wyde PR. 2009. Contrasting effects of type I interferon as a mucosal adjuvant for influenza vaccine in mice and humans. Vaccine 27:5344-5348. http://dx.doi.org/10.1016/j.vaccine.2009.06.084.
11. Yang P, Tang C, Luo D, Zhan Z, Xing L, Duan Y, Jia W, Peng D, Liu X, Wang X. 2010. Cross-clade protection against HPAI H5N1 influenza virus challenge in BALB/c mice intranasally administered adjuvantcombined influenza vaccine. Vet Microbiol 146:17-23. http://dx.doi.org/10.1016/j.vetmic.2010.03.024.
12. Fu J, Liang J, Kang H, Lin J, Yu Q, Yang Q. 2013. Effects of different CpG oligodeoxynucleotides with inactivated avian H5N1 influenza virus on mucosal immunity of chickens. Poult Sci 92:2866-2875. http://dx.doi.org/10.3382/ps.2013-03205.
13. Zhang XW, Yu QH, Zhang XF, Yang Q. 2009. Co-administration of inactivated avian influenza virus with CpG or rIL-2 strongly enhances the local immune response after intranasal immunization in chicken. Vaccine 27:5628-5632. http://dx.doi.org/10.1016/j.vaccine.2009.07.023.
14. Xiang XX, Zhou XQ, Xie Q, Yu H, Zhou HJ. 2008. Effects of CpG-ODN combined with HBsAg on the phenotype, function and the activity of NF-kappa B and AP-1 of monocyte-derived dendritic cells in chronic hepatitis B patients. Zhonghua Gan Zang Bing Za Zhi 16:97-100. (In Chinese.).
15. Lambrecht BN, Hammad H. 2003. Taking our breath away: dendritic cells in the pathogenesis of asthma. Nat Rev Immunol 3:994-1003. http://dx.doi.org/10.1038/nri1249.
16. Kiyono H, Fukuyama S. 2004. NALT-versus Peyer's-patch-mediated mucosal immunity. Nat Rev Immunol 4:699-710. http://dx.doi.org/10.1038/nri1439.
17. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2:361-367. http://dx.doi.org/10.1038/86373.
18. Rimoldi M, Chieppa M, Vulcano M, Allavena P, Rescigno M. 2004. Intestinal epithelial cells control dendritic cell function. Ann NY Acad Sci 1029:66-74. http://dx.doi.org/10.1196/annals.1309.009.
19. Takano K, Kojima T, Go M, Murata M, Ichimiya S, Himi T, Sawada N. 2005. HLA-DR-and CD11c-positive dendritic cells penetrate beyond well-developed epithelial tight junctions in human nasal mucosa of allergic rhinitis. J Histochem Cytochem 53:611-619. http://dx.doi.org/10.1369/jhc.4A6539.2005.
20. Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, Vyas JM, Boes M, Ploegh HL, Fox JG, Littman DR, Reinecker HC. 2005. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307:254-258. http://dx.doi.org/10.1126/science.1102901.
21. Cardon LR, Burge C, Clayton DA, Karlin S. 1994. Pervasive CpG suppression in animal mitochondrial genomes. Proc Natl Acad Sci U S A 91:3799-3803. http://dx.doi.org/10.1073/pnas.91.9.3799.
22. Klinman DM. 2004. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat Rev Immunol 4:249-258. http://dx.doi.org/10.1038/nri1329.
23. Witschi C, Mrsny RJ. 1999. In vitro evaluation of microparticles and polymer gels for use as nasal platforms for protein delivery. Pharm Res 16:382-390. http://dx.doi.org/10.1023/A:1018869601502.
24. Amidi M, Romeijn SG, Borchard G, Junginger HE, Hennink WE, Jiskoot W. 2006. Preparation and characterization of protein-loaded Ntrimethyl chitosan nanoparticles as nasal delivery system. J Control Release 111:107-116. http://dx.doi.org/10.1016/j.jconrel.2005.11.014.
25. Hartshorn KL, Crouch EC, White MR, Eggleton P, Tauber AI, Chang D, Sastry K. 1994. Evidence for a protective role of pulmonary surfactant protein D (Sp-D) against influenza A viruses. J Clin Invest 94:311-319. http://dx.doi.org/10.1172/JCI117323.
26. Kang H, Yan M, Yu Q, Yang Q. 2013. Characteristics of nasal-associated lymphoid tissue (NALT) and nasal absorption capacity in chicken. PLoS One 8:e84097. http://dx.doi.org/10.1371/journal.pone.0084097.
27. Wang Z, Gao J, Yu Q, Yang Q. 2012. Oral immunization with recombinant Lactococcus lactis expressing the hemagglutinin of the avian influenza virus induces mucosal and systemic immune responses. Future Microbiol 7:1003-1010. http://dx.doi.org/10.2217/fmb.12.69.
28. Wegmann F, Gartlan KH, Harandi AM, Brinckmann SA, Coccia M, Hillson WR, Kok WL, Cole S, Ho LP, Lambe T, Puthia M, Svanborg C, Scherer EM, Krashias G, Williams A, Blattman JN, Greenberg PD, Flavell RA, Moghaddam AE, Sheppard NC, Sattentau QJ. 2012. Polyethyleneimine is a potent mucosal adjuvant for viral glycoprotein antigens. Nat Biotechnol 30:883-888. http://dx.doi.org/10.1038/nbt.2344.
29. Barnier-Quer C, Elsharkawy A, Romeijn S, Kros A, Jiskoot W. 2013. Adjuvant effect of cationic liposomes for subunit influenza vaccine: influence of antigen loading method, cholesterol and immune modulators. Pharmaceutics 5:392-410. http://dx.doi.org/10.3390/pharmaceutics5030392.
30. Yin Y, Qin T, Yu Q, Yang Q. 2014. Bursopentin (BP5) from chicken bursa of fabricius attenuates the immune function of dendritic cells. Amino Acids 46:1763-1774. http://dx.doi.org/10.1007/s00726-014-1735-x.
31. Foster KA, Avery ML, Yazdanian M, Audus KL. 2000. Characterization of the Calu-3 cell line as a tool to screen pulmonary drug delivery. Int J Pharm 208:1-11. http://dx.doi.org/10.1016/S0378-5173(00)00452-X.
32. Sakuraba A, Sato T, Kamada N, Kitazume M, Sugita A, Hibi T. 2009. Th1/Th17 immune response is induced by mesenteric lymph node dendritic cells in Crohn's disease. Gastroenterology 137:1736-1745. http://dx.doi.org/10.1053/j.gastro.2009.07.049.
33. Guermonprez P, Valladeau J, Zitvogel L, Thery C, Amigorena S. 2002. Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol 20:621-667. http://dx.doi.org/10.1146/annurev.immunol.20.100301.064828.
34. Itagaki K, Adibnia Y, Sun SQ, Zhao C, Sursal T, Chen Y, Junger W, Hauser CJ. 2011. Bacterial DNA induces pulmonary damage via TLR-9 through cross-talk with neutrophils. Shock 36:548-552. http://dx.doi.org/10.1097/SHK.0b013e3182369fb2.
35. Geijtenbeek TBH, Groot PC, Nolte MA, van Vliet SJ, Gangaram-Panday ST, van Duijnhoven GCF, Kraal G, van Oosterhout AJM, van Kooyk Y. 2002. Marginal zone macrophages express a murine homologue of DC-SIGN that captures blood-borne antigens in vivo. Blood 100:2908-2916. http://dx.doi.org/10.1182/blood-2002-04-1044.
36. Kang YS, Yamazaki S, Iyoda T, Pack M, Bruening SA, Kim JY, Takahara K, Inaba K, Steinman RM, Park CG. 2003. SIGN-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int Immunol 15:177-186. http://dx.doi.org/10.1093/intimm/dxg019.
37. Taylor PR, Brown GD, Herre J, Williams DL, Willment JA, Gordon S. 2004. The role of SIGNR1 and the beta-glucan receptor (Dectin-1) in the nonopsonic recognition of yeast by specific macrophages. J Immunol 172: 1157-1162. http://dx.doi.org/10.4049/jimmunol.172.2.1157.
38. Kang YS, Kim JY, Bruening SA, Pack M, Charalambous A, Pritsker A, Moran TM, Loeffler JM, Steinman RM, Park CG. 2004. The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen. Proc Natl Acad Sci U S A 101:215-220. http://dx.doi.org/10.1073/pnas.0307124101.
39. Gonzalez SF, Lukacs-Kornek V, Kuligowski MP, Pitcher LA, Degn SE, Kim YA, Cloninger MJ, Martinez-Pomares L, Gordon S, Turley SJ, Carroll MC. 2010. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat Immunol 11:427-434. http://dx.doi.org/10.1038/ni.1856.
40. Zietara N, Lyszkiewicz M, Puchalka J, Pei G, Gutierrez MG, Lienenklaus S, Hobeika E, Reth M, Martins dos Santos VAP, Krueger A, Weiss S. 2013. Immunoglobulins drive terminal maturation of splenic dendritic cells. Proc Natl Acad Sci U S A 110:2282-2287. http://dx.doi.org/10.1073/pnas.1210654110.
41. McGettrick AF, O'Neill LAJ. 2010. Localisation and trafficking of Tolllike receptors: an important mode of regulation. Curr Opin Immunol 22:20-27. http://dx.doi.org/10.1016/j.coi.2009.12.002.
42. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. 2004. Innate antiviral responses by means of TLR7-mediated recognition of singlestranded RNA. Science 303:1529-1531. http://dx.doi.org/10.1126/science.1093616.
43. Mutwiri GK, Nichani AK, Babiuk S, Babiuk LA. 2004. Strategies for enhancing the immunostimulatory effects of CpG oligodeoxynucleotides. J Control Release 97:1-17. http://dx.doi.org/10.1016/j.jconrel.2004.02.022.
44. Izadpanah A, Dwinell MB, Eckmann L, Varki NM, Kagnoff MF. 2001. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am J Physiol Gastrointest Liver Physiol 280:G710-G719.
45. Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci U S A 98:13722-13727. http://dx.doi.org/10.1073/pnas.241308598.
46. Zeng H, Goldsmith C, Thawatsupha P, Chittaganpitch M, Waicharoen S, Zaki S, Tumpey TM, Katz JM. 2007. Highly pathogenic avian influenza H5N1 viruses elicit an attenuated type I interferon response in polarized human bronchial epithelial cells. J Virol 81:12439-12449. http://dx.doi.org/10.1128/JVI.01134-07.
47. Nielsen HM. 2014. Epithelial permeation and absorption mechanisms of biopharmaceuticals, p 99-122. In das Neves J, Sarmento G (ed), Mucosal delivery of biopharmaceuticals. Springer, New York, NY.
48. Guichard A, Cruz-Moreno B, Aguilar B, van Sorge NM, Kuang J, Kurkciyan AA, Wang Z, Hang S, Pineton de Chambrun GP, McCole DF, Watnick P, Nizet V, Bier E. 2013. Cholera toxin disrupts barrier function by inhibiting exocyst-mediated trafficking of host proteins to intestinal cell junctions. Cell Host Microbe 14:294-305. http://dx.doi.org/10.1016/j.chom.2013.08.001.
49. Akira S. 2006. TLR signaling. Curr Top Microbiol Immunol 311:1-16.
50. Chieppa M, Rescigno M, Huang AYC, Germain RN. 2006. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med 203:2841-2852. http://dx.doi.org/10.1084/jem.20061884.
51. Tengroth L, Millrud CR, Kvarnhammar AM, Kumlien Georen S, Latif L, Cardell LO. 2014. Functional effects of Toll-like receptor (TLR)3, 7, 9, RIG-I and MDA-5 stimulation in nasal epithelial cells. PLoS One 9:e98239. http://dx.doi.org/10.1371/journal.pone.0098239.
52. Kim DY, Sato A, Fukuyama S, Sagara H, Nagatake T, Kong IG, Goda K, Nochi T, Kunisawa J, Sato S, Yokota Y, Lee CH, Kiyono H. 2011. The airway antigen sampling system: respiratoryMcells as an alternative gateway for inhaled antigens. J Immunol 186:4253-4262. http://dx.doi.org/10.4049/jimmunol.0903794.
53. Thornton EE, Looney MR, Bose O, Sen D, Sheppard D, Locksley R, Huang X, Krummel MF. 2012. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J Exp Med 209:1183-1199. http://dx.doi.org/10.1084/jem.20112667.
54. Harkema JR, Carey SA, Wagner JG. 2006. The nose revisited: A brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicol Pathol 34:252-269. http://dx.doi.org/10.1080/01926230600713475.
55. Lelouard H, Fallet M, de Bovis B, Meresse S, Gorvel JP. 2012. Peyer's patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology 142:592-601.e3. http://dx.doi.org/10.1053/j.gastro.2011.11.039.
56. Swiatczak B, Rescigno M. 2012. How the interplay between antigen presenting cells and microbiota tunes host immune responses in the gut. Semin Immunol 24:43-49. http://dx.doi.org/10.1016/j.smim.2011.11.004.
57. Lantier L, Lacroix-Lamande S, Potiron L, Metton C, Drouet F, Guesdon W, Gnahoui-David A, Le Vern Y, Deriaud E, Fenis A, Rabot S, Descamps A, Werts C, Laurent F. 2013. Intestinal CD103+ dendritic cells are key players in the innate immune control of Cryptosporidium parvum infection in neonatal mice. PLoS Pathog 9:e1003801. http://dx.doi.org/10.1371/journal.ppat.1003801.
58. Mazzini E, Massimiliano L, Penna G, Rescigno M. 2014. Oral tolerance can be established via gap junction transfer of fed antigens from CX3CR1(+) macrophages to CD103(+) dendritic cells. Immunity 40: 248-261. http://dx.doi.org/10.1016/j.immuni.2013.12.012.
59. Schulz O, Jaensson E, Persson EK, Liu XS, Worbs T, Agace WW, Pabst O. 2009. Intestinal CD103(+), but not CX3CR1(+), antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206:3101-3114. http://dx.doi.org/10.1084/jem.20091925.
60. Hagenaars N, Mania M, de Jong P, Que I, Nieuwland R, Slutter B, Glansbeek H, Heldens J, van den Bosch H, Lowik C, Kaijzel E, Mastrobattista E, Jiskoot W. 2010. Role of trimethylated chitosan (TMC) in nasal residence time, local distribution and toxicity of an intranasal influenza vaccine. J Control Release 144:17-24. http://dx.doi.org/10.1016/j.jconrel.2010.01.027.
61. Desch AN, Randolph GJ, Murphy K, Gautier EL, Kedl RM, Lahoud MH, Caminschi I, Shortman K, Henson PM, Jakubzick CV. 2011. CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J Exp Med 208:1789-1797. http://dx.doi.org/10.1084/jem.20110538.
62. Lukens MV, Kruijsen D, Coenjaerts FE, Kimpen JL, van Bleek GM. 2009. Respiratory syncytial virus-induced activation and migration of respiratory dendritic cells and subsequent antigen presentation in the lungdraining lymph node. J Virol 83:7235-7243. http://dx.doi.org/10.1128/JVI.00452-09.
63. Sung SSJ, Fu SM, Rose CE, Gaskin F, Ju ST, Beaty SR. 2006. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176: 2161-2172. http://dx.doi.org/10.4049/jimmunol.176.4.2161.
64. Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN. 2009. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 15:410-416. http://dx.doi.org/10.1038/nm.1946.
65. Cremel M, Berlier W, Hamzeh H, Cognasse F, Lawrence P, Genin C, Bernengo JC, Lambert C, Dieu-Nosjean MC, Delezay O. 2005. Characterization of CCL20 secretion by human epithelial vaginal cells: involvement in Langerhans cell precursor attraction. J Leukoc Biol 78:158-166. http://dx.doi.org/10.1189/jlb.0305147.
66. Vanbervliet A, Homey B, Durand I, Massacrier C, Ait-Yahia S, de Bouteiller O, Vicari A, Caux C. 2002. Sequential involvement of CCR2 and CCR6 ligands for immature dendritic cell recruitment: possible role at inflamed epithelial surfaces. Eur J Immunol 32:231-242. http://dx.doi.org/10.1002/1521-4141(200201)32:1<231::AID-IMMU231>3.0.CO;2-8.
67. Anosova NG, Chabot S, Shreedhar V, Borawski JA, Dickinson BL, Neutra MR. 2008. Cholera toxin, E coli heat-labile toxin, and non-toxic derivatives induce dendritic cell migration into the follicle-associated epithelium of Peyer's patches. Mucosal Immunol 1:59-67. http://dx.doi.org/10.1038/mi.2007.7.