A nonhuman primate toxicology and immunogenicity study evaluating aerosol delivery of AERAS-402/Ad35 vaccine: Evidence for transient t cell responses in peripheral blood and robust sustained responses in the lungs

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 8, 2014, Pages 2199-2210

  Hokey, David A ^a   Wachholder, Robert ^a   Darrah, Patricia A ^b   Bolton, Diane L ^c   Barouch, Dan H ^d,e   Hill, Krystal ^a   Dheenadhayalan, Veerabadran ^a   Schwander, Stephan ^f   Godin, C Steven ^g   Douoguih, Macaya ^h   Pau, Maria Grazia ^h   Seder, Robert A ^b   Roederer, Mario ^b   Sadoff, Jerald C ^h   Sizemore, Donata ⁱ  

^a AERAS   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c US Military HIV Research Program   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f RUTGERS SCHOOL OF PUBLIC HEALTH   (United States)

^g Smithers Viscient   (United States)

^h CRUCELL HOLLAND BV   (Netherlands)

ⁱ UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

Adenovirus; Aerosol; Cellular; Mucosal; Primate; T cell; Toxicology; Tuberculosis; Vaccine

Indexed keywords

ADENOVIRUS VACCINE; AERAS 402 VACCINE; GAMMA INTERFERON; INTERLEUKIN 2; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AERAS-402; AEROSOL; BCG VACCINE; DRUG CARRIER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG SAFETY; FEMALE; IMMUNITY; IMMUNOGENICITY; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; LUNG RESIDENT IMMUNITY; LUNG WEIGHT; LYMPHOCYTIC INFILTRATION; LYMPHOID HYPERPLASIA; LYMPHOID TISSUE; MALE; MEDIASTINUM LYMPH NODE; NASOPHARYNX; NONHUMAN; OROPHARYNX; PERIPHERAL BLOOD MONONUCLEAR CELL; RHESUS MONKEY; SINUS HISTIOCYTOSIS; VACCINATION; VIRUS NEUTRALIZATION; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; AEROSOL; ANIMAL; CYTOLOGY; GENETICS; HUMAN ADENOVIRUS C; IMMUNOLOGY; INHALATIONAL DRUG ADMINISTRATION; LUNG; T LYMPHOCYTE; TREATMENT OUTCOME; TUBERCULOSIS;

ADENOVIRUSES, HUMAN; ADMINISTRATION, INHALATION; AEROSOLS; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; DRUG CARRIERS; FEMALE; LUNG; MACACA MULATTA; MALE; T-LYMPHOCYTES; TREATMENT OUTCOME; TUBERCULOSIS; TUBERCULOSIS VACCINES;

EID: 84905968988     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.29108     Document Type: Article

References (52)

1. Andersen P, Doherty TM. The success and failure of BCG - implications for a novel tuberculosis vaccine. Nat Rev Microbiol 2005; 3:656-62; PMID:16012514; http://dx.doi.org/10.1038/nrmicro1211
2. Barker LF, Brennan MJ, Rosenstein PK, Sadoff JC. Tuberculosis vaccine research: the impact of immunology. Curr Opin Immunol 2009; 21:331-8; PMID:19505813; http://dx.doi.org/10.1016/j.coi.2009.05.017
3. Rodrigues LC, Diwan VK, Wheeler JG. Protective effect of BCG against tuberculous meningitis and miliary tuberculosis: a meta-analysis. Int J Epidemiol 1993; 22:1154-8; PMID:8144299; http://dx.doi.org/10.1093/ije/22.6.1154
4. Trunz BB, Fine P, Dye C. Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet 2006; 367:1173-80; PMID:16616560; http://dx.doi.org/10.1016/S0140-6736(06)68507-3
5. Mangtani P, Abubakar I, Ariti C, Beynon R, Pimpin L, Fine PE, Rodrigues LC, Smith PG, Lipman M, Whiting PF, et al. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Clin Infect Dis 2014; 58:470-80; PMID:24336911; http://dx.doi.org/10.1093/cid/cit790
6. Global Tuberculosis Report 2012. Geneva, Switzerland: World Health Organization, 2012.
7. Cohn DL, Bustreo F, Raviglione MC; International Union Against Tuberculosis and Lung Disease. Drug-resistant tuberculosis: review of the worldwide situation and the WHO/IUATLD Global Surveillance Project. Clin Infect Dis 1997; 24(Suppl 1):S121-30; PMID:8994791; http://dx.doi.org/10.1093/clinids/24.Supplement-1.S121
8. Falzon D, Jaramillo E, Schünemann HJ, Arentz M, Bauer M, Bayona J, Blanc L, Caminero JA, Daley CL, Duncombe C, et al. WHO guidelines for the programmatic management of drug-resistant tuberculosis: 2011 update. Eur Respir J 2011; 38:516-28; PMID:21828024; http://dx.doi.org/10.1183/09031936.00073611
9. Udwadia ZF, Amale RA, Ajbani KK, Rodrigues C. Totally drug-resistant tuberculosis in India. Clin Infect Dis 2012; 54:579-81; PMID:22190562; http://dx.doi.org/10.1093/cid/cir889
10. Masjedi MR, Tabarsi P, Baghaei P, Jalali S, Farnia P, Chitsaz E, Amiri M, Mansouri D, Velayati AA. Extensively drug-resistant tuberculosis treatment outcome in Iran: a case series of seven patients. Int J Infect Dis 2010; 14:e399-402; PMID:19818664; http://dx.doi.org/10.1016/j.ijid.2009.07.002
11. Velayati AA, Farnia P, Masjedi MR, Ibrahim TA, Tabarsi P, Haroun RZ, Kuan HO, Ghanavi J, Farnia P, Varahram M. Totally drug-resistant tuberculosis strains: evidence of adaptation at the cellular level. Eur Respir J 2009; 34:1202-3; PMID:19880622; http://dx.doi.org/10.1183/09031936.00081909
12. Velayati AA, Masjedi MR, Farnia P, Tabarsi P, Ghanavi J, Ziazarifi AH, Hoffner SE. Emergence of new forms of totally drug-resistant tuberculosis bacilli: super extensively drug-resistant tuberculosis or totally drug-resistant strains in iran. Chest 2009; 136:420-5; PMID:19349380; http://dx.doi.org/10.1378/chest.08-2427
13. Tufariello JM, Chan J, Flynn JL. Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect Dis 2003; 3:578-90; PMID:12954564; http://dx.doi.org/10.1016/S1473-3099(03)00741-2
14. Chaisson RE, Martinson NA. Tuberculosis in Africa - combating an HIV-driven crisis. N Engl J Med 2008; 358:1089-92; PMID:18337598; http://dx.doi.org/10.1056/NEJMp0800809
15. Pacheco AG, Durovni B, Cavalcante SC, Lauria LM, Moore RD, Moulton LH, Chaisson RE, Golub JE. AIDS-related tuberculosis in Rio de Janeiro, Brazil. PLoS One 2008; 3:e3132; PMID:18781195; http://dx.doi.org/10.1371/journal.pone.0003132
16. Feller L, Wood NH, Chikte UM, Khammissa RA, Meyerov R, Lemmer J. Tuberculosis part 3: HIV-tuberculosis co-infection. SADJ 2009; 64:352-4; PMID:20034289
17. Chen CY, Huang D, Wang RC, Shen L, Zeng G, Yao S, Shen Y, Halliday L, Fortman J, McAllister M, et al. A critical role for CD8 T cells in a nonhuman primate model of tuberculosis. PLoS Pathog 2009; 5:e1000392; PMID:19381260; http://dx.doi.org/10.1371/journal.ppat.1000392
18. Lin PL, Rodgers M, Smith L, Bigbee M, Myers A, Bigbee C, Chiosea I, Capuano SV, Fuhrman C, Klein E, et al. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 2009; 77:4631-42; PMID:19620341; http://dx.doi.org/10.1128/IAI.00592-09
19. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004; 21:527-38; PMID:15485630; http://dx.doi.org/10.1016/j.immuni.2004.08.011
20. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, Rosemblatt M, Von Andrian UH. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 2003; 424:88-93; PMID:12840763; http://dx.doi.org/10.1038/nature01726
21. Picker LJ. Control of lymphocyte homing. Curr Opin Immunol 1994; 6:394-406; PMID:7917107; http://dx.doi.org/10.1016/0952-7915(94)90118-X
22. Stagg AJ, Kamm MA, Knight SC. Intestinal dendritic cells increase T cell expression of alpha4beta7 integrin. Eur J Immunol 2002; 32:1445-54; PMID:11981833; http://dx.doi.org/10.1002/1521-4141(200205)32:5〈1445::AIDIMMU1445〉 3.0.CO;2-E
23. Hokey DA, Misra A. Aerosol vaccines for tuberculosis: a fine line between protection and pathology. Tuberculosis (Edinb) 2011; 91:82-5; PMID:21067975; http://dx.doi.org/10.1016/j.tube.2010.09.007
24. Schwander S, Dheda K. Human lung immunity against Mycobacterium tuberculosis: insights into pathogenesis and protection. Am J Respir Crit Care Med 2011; 183:696-707; PMID:21075901; http://dx.doi.org/10.1164/rccm.201006-0963PP
25. Jin TH, Tsao E, Goudsmit J, Dheenadhayalan V, Sadoff J. Stabilizing formulations for inhalable powders of an adenovirus 35-vectored tuberculosis (TB) vaccine (AERAS-402). Vaccine 2010; 28:4369-75; PMID:20444437; http://dx.doi.org/10.1016/j.vaccine.2010.04.059
26. Lu D, Hickey AJ. Pulmonary vaccine delivery. Expert Rev Vaccines 2007; 6:213-26; PMID:17408371; http://dx.doi.org/10.1586/14760584.6.2.213
27. Sené C, Bout A, Imler JL, Schultz H, Willemot JM, Hennebel V, Zurcher C, Valerio D, Lamy D, Pavirani A. Aerosol-mediated delivery of recombinant adenovirus to the airways of nonhuman primates. Hum Gene Ther 1995; 6:1587-93; PMID:8664383; http://dx.doi.org/10.1089/hum.1995.6.12-1587
28. Hodge LM, Marinaro M, Jones HP, McGhee JR, Kiyono H, Simecka JW, Immunoglobulin A. Immunoglobulin A (IgA) responses and IgE-associated inflammation along the respiratory tract after mucosal but not systemic immunization. Infect Immun 2001; 69:2328-38; PMID:11254590; http://dx.doi.org/10.1128/IAI.69.4.2328-2338.2001
29. Simecka JW, Jackson RJ, Kiyono H, McGhee JR. Mucosally induced immunoglobulin E-associated inflammation in the respiratory tract. Infect Immun 2000; 68:672-9; PMID:10639432; http://dx.doi.org/10.1128/IAI.68.2.672-679.2000
30. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003; 3:23-35; PMID:12511873; http://dx.doi.org/10.1038/nri978
31. Radosevic K, Wieland CW, Rodriguez A, Weverling GJ, Mintardjo R, Gillissen G, Vogels R, Skeiky YA, Hone DM, Sadoff JC, et al. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of gamma interferon. Infect Immun 2007; 75:4105-15; PMID:17526747; http://dx.doi.org/10.1128/IAI.00004-07
32. Ronan EO, Lee LN, Tchilian EZ, Beverley PC. Nasal associated lymphoid tissue (NALT) contributes little to protection against aerosol challenge with Mycobacterium tuberculosis after immunisation with a recombinant adenoviral vaccine. Vaccine 2010; 28:5179-84; PMID:20558252; http://dx.doi.org/10.1016/j.vaccine.2010.05.075
33. Wang J, Thorson L, Stokes RW, Santosuosso M, Huygen K, Zganiacz A, Hitt M, Xing Z. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J Immunol 2004; 173:6357-65; PMID:15528375; http://dx.doi.org/10.4049/jimmunol.173.10.6357
34. Xing Z, McFarland CT, Sallenave JM, Izzo A, Wang J, McMurray DN. Intranasal mucosal boosting with an adenovirus-vectored vaccine markedly enhances the protection of BCG-primed guinea pigs against pulmonary tuberculosis. PLoS One 2009; 4:e5856; PMID:19516906; http://dx.doi.org/10.1371/journal.pone.0005856
35. Minne A, Louahed J, Mehauden S, Baras B, Renauld JC, Vanbever R. The delivery site of a monovalent influenza vaccine within the respiratory tract impacts on the immune response. Immunology 2007; 122:316-25; PMID:17521369; http://dx.doi.org/10.1111/j.1365-2567.2007.02641.x
36. Abel B, Tameris M, Mansoor N, Gelderbloem S, Hughes J, Abrahams D, Makhethe L, Erasmus M, de Kock M, van der Merwe L, et al. The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults. Am J Respir Crit Care Med 2010; 181:1407-17; PMID:20167847; http://dx.doi.org/10.1164/rccm.200910-1484OC
37. Hoft DF, Blazevic A, Stanley J, Landry B, Sizemore D, Kpamegan E, Gearhart J, Scott A, Kik S, Pau MG, et al. A recombinant adenovirus expressing immunodominant TB antigens can significantly enhance BCG-induced human immunity. Vaccine 2012; 30:2098-108; PMID:22296955; http://dx.doi.org/10.1016/j.vaccine.2012.01.048
38. Song K, Bolton DL, Wei CJ, Wilson RL, Camp JV, Bao S, Mattapallil JJ, Herzenberg LA, Herzenberg LA, Andrews CA, et al. Genetic immunization in the lung induces potent local and systemic immune responses. Proc Natl Acad Sci U S A 2010; 107:22213-8; PMID:21135247; http://dx.doi.org/10.1073/pnas.1015536108
39. Streilein JW. Ocular immune privilege: the eye takes a dim but practical view of immunity and inflammation. J Leukoc Biol 2003; 74:179-85; PMID:12885934; http://dx.doi.org/10.1189/jlb.1102574
40. Zuckerman JB, Robinson CB, McCoy KS, Shell R, Sferra TJ, Chirmule N, Magosin SA, Propert KJ, Brown-Parr EC, Hughes JV, et al. A phase I study of adenovirus-mediated transfer of the human cystic fibrosis transmembrane conductance regulator gene to a lung segment of individuals with cystic fibrosis. Hum Gene Ther 1999; 10:2973-85; PMID:10609658; http://dx.doi.org/10.1089/10430349950016384
41. McDonald RJ, Lukason MJ, Raabe OG, Canfield DR, Burr EA, Kaplan JM, Wadsworth SC, St George JA. Safety of airway gene transfer with Ad2/CFTR2: aerosol administration in the nonhuman primate. Hum Gene Ther 1997; 8:411-22; PMID:9054516; http://dx.doi.org/10.1089/hum.1997.8.4-411
42. Lerondel S, Vecellio None L, Faure L, Sizaret PY, Sene C, Pavirani A, Diot P, Le Pape A. Gene therapy for cystic fibrosis with aerosolized adenovirus-CFTR: characterization of the aerosol and scintigraphic determination of lung deposition in baboons. J Aerosol Med 2001; 14:95-105; PMID:11495490; http://dx.doi.org/10.1089/08942680152007945
43. Meyer KC, Sharma A. Regional variability of lung inflammation in cystic fibrosis. Am J Respir Crit Care Med 1997; 156:1536-40; PMID:9372672; http://dx.doi.org/10.1164/ajrccm.156.5.9701098
44. Garcia-Contreras L, Hickey AJ. Aerosol treatment of cystic fibrosis. Crit Rev Ther Drug Carrier Syst 2003; 20:317-56; PMID:14959788; http://dx.doi.org/10.1615/CritRevTherDrugCarrierSyst.v20.i5.10
45. Mikhak Z, Strassner JP, Luster AD. Lung dendritic cells imprint T cell lung homing and promote lung immunity through the chemokine receptor CCR4. J Exp Med 2013; 210:1855-69; PMID:23960189; http://dx.doi.org/10.1084/jem.20130091
46. Turner DL, Bickham KL, Farber DL, Lefranc¸ois L. Splenic priming of virus-specific CD8 T cells following influenza virus infection. J Virol 2013; 87:4496-506; PMID:23388712; http://dx.doi.org/10.1128/JVI.03413-12
47. Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006; 6:595-601; PMID:16868550; http://dx.doi.org/10.1038/nri1901
48. Dharmadhikari AS, Basaraba RJ, Van Der Walt ML, Weyer K, Mphahlele M, Venter K, Jensen PA, First MW, Parsons S, McMurray DN, et al. Natural infection of guinea pigs exposed to patients with highly drug-resistant tuberculosis. Tuberculosis (Edinb) 2011; 91:329-38; PMID:21478054; http://dx.doi.org/10.1016/j.tube.2011.03.002
49. Mills CC, O'Grady F, Riley RL. Tuberculin conversion in the "naturally infected" guinea pig. Bull Johns Hopkins Hosp 1960; 106:36-45; PMID:14422642
50. Swift D, Asgharian B, Kimbell J. Use of mathematical aerosol deposition models in predicting the distribution of inhaled therapeutic aerosols. In: Hickey A, ed. Inhaled Aerosols: Physical and Biological Basis for Therapy. New York, NY: Marcel Dekker, Inc., 2006.
51. Barouch DH, Kik SV, Weverling GJ, Dilan R, King SL, Maxfield LF, Clark S, Ng'ang'a D, Brandariz KL, Abbink P, et al. International seroepidemiology of adenovirus serotypes 5, 26, 35, and 48 in pediatric and adult populations. Vaccine 2011; 29:5203-9; PMID:21619905; http://dx.doi.org/10.1016/j.vaccine.2011.05.025
52. Sprangers MC, Lakhai W, Koudstaal W, Verhoeven M, Koel BF, Vogels R, Goudsmit J, Havenga MJ, Kostense S. Quantifying adenovirus-neutralizing antibodies by luciferase transgene detection: addressing preexisting immunity to vaccine and gene therapy vectors. J Clin Microbiol 2003; 41:5046-52; PMID:14605137; http://dx.doi.org/10.1128/JCM.41.11.5046-5052.2003