Adjuvant-induced human monocyte secretome profiles reveal adjuvant- and age-specific protein signatures

Molecular and Cellular Proteomics

Volumn 15, Issue 6, 2016, Pages 1877-1894

  Oh, Djin Ye ^a,b,e   Dowling, David J ^a,b   Ahmed, Saima ^a   Choi, Hyungwon ^d   Brightman, Spencer ^a   Bergelson, Ilana ^a   Berger, Sebastian T ^a   Sauld, John F ^a   Pettengill, Matthew ^a,b   Kho, Alvin T ^a   Pollack, Henry J ^c   Steen, Hanno ^a   Levy, Ofer ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; ALUMINUM POTASSIUM SULFATE; LACTOFERRIN; PENTRAXIN 3; PHOSPHORYL LIPID A; PROTEIN; RESIQUIMOD; TRANSCRIPTOME; VACCINE; WART VIRUS VACCINE; ALUMINUM SULFATE; IMIDAZOLE DERIVATIVE; IMMUNOLOGICAL ADJUVANT; LIPID A; PROTEOME;

ADULT; ARTICLE; BLOOD; HUMAN; HUMAN CELL; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MONOCYTE; NEWBORN; PRIORITY JOURNAL; PROTEOMICS; AGE; ANALOGS AND DERIVATIVES; DRUG EFFECTS; INNATE IMMUNITY; PROCEDURES; SECRETION (PROCESS);

ADJUVANTS, IMMUNOLOGIC; ADULT; AGE FACTORS; ALUM COMPOUNDS; CHROMATOGRAPHY, LIQUID; HUMANS; IMIDAZOLES; IMMUNITY, INNATE; INFANT, NEWBORN; LIPID A; MASS SPECTROMETRY; MONOCYTES; PROTEOME; PROTEOMICS;

EID: 84971232127     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.055541     Document Type: Article

References (67)

1. Dowling, D. J., and Levy, O. (2014) Ontogeny of early life immunity. Trends Immunol. 35, 299-310
2. Kollmann, T. R., Levy, O., Montgomery, R. R., and Goriely, S. (2012) Innate immune function by Toll-like receptors: distinct responses newborns and the elderly. Immunity 37, 771-783
3. De Gregorio, E., D'Oro, U., and Wack, A. (2009) Immunology of TLR- independent vaccine adjuvants. Current Opinion Immunol. 21, 339-345
4. Dowling, D. J., and Levy, O. (2015) Pediatric vaccine adjuvants: Components of the modern vaccinologist's toolbox. Pediatr. Infect. Dis. J.
5. Belderbos, M. E., Levy, O., Stalpers, F., Kimpen, J. L., Meyaard, L., and Bont, L. (2012) Neonatal plasma polarizes TLR4-mediated cytokine responses towards low IL-12p70 and high IL-10 production via distinct factors. PLoS ONE 7, e33419
6. Coffman, R. L., Sher, A., and Seder, R. A. (2010) Vaccine adjuvants: putting innate immunity to work. Immunity 33, 492-503
7. Fox, C. B., and Barnes, V. L., Evers, T., Chesko, J. D., and Vedvick, T. S., Coler, R. N., Reed, S. G., and Baldwin, S. L. (2013) Adjuvanted pandemic influenza vaccine: variation of emulsion components affects stability, antigen structure, and vaccine efficacy. Influenza Respiratory Viruses 7, 815-826
8. Pomat, W. S., van den Biggelaar, A. H., Phuanukoonnon, S., Francis, J., Jacoby, P., Siba, P. M., Alpers, M. P., Reeder, J. C., Holt, P. G., Richmond, P. C., Lehmann, D., and Neonatal Pneumococcal Conjugate Vaccine Trial Study, T. (2013) Safety and immunogenicity of neonatal pneumococcal conjugate vaccination in Papua New Guinean children: a randomised controlled trial. PLoS ONE 8, e56698
9. Levy, O., Goriely, S., and Kollmann, T. R. (2013) Immune response to vaccine adjuvants during the first year of life. Vaccine 31, 2500-2505
10. Kool, M., Fierens, K., and Lambrecht, B. N. (2012) Alum adjuvant: some of the tricks of the oldest adjuvant. J. Med. Microbiol. 61, 927-934
11. Kuroda, E., Coban, C., and Ishii, K. J. (2013) Particulate adjuvant and innate immunity: past achievements, present findings, and future prospects. Int. Rev. Immunol. 32, 209-220
12. Lisciandro, J. G., and Prescott, S. L., Nadal-Sims, M. G., Devitt, C. J., Pomat, W., Siba, P. M., Holt, P. G., Strickland, D., and van den Biggelaar, A. H. (2012) Comparison of neonatal T regulatory cell function in Papua New Guinean and Australian newborns. Pediatr. Allergy Immunol. 23, 173-180
13. van den Biggelaar, A. H., Richmond, P. C., Pomat, W. S., Phuanukoonnon, S., Nadal-Sims, M. A., Devitt, C. J., Siba, P. M., Lehmann, D., and Holt, P. G. (2009) Neonatal pneumococcal conjugate vaccine immunization primes T cells for preferential Th2 cytokine expression: a randomized controlled trial in Papua New Guinea. Vaccine 27, 1340-1347
14. Reed, S. G., and Orr, M. T., and Fox, C. B. (2013) Key roles of adjuvants in modern vaccines. Nat. Med. 19, 1597-1608
15. Verstraeten, T., Descamps, D., David, M. P., Zahaf, T., Hardt, K., Izurieta, P., Dubin, G., and Breuer, T. (2008) Analysis of adverse events of potential autoimmune aetiology in a large integrated safety database of AS04 adjuvanted vaccines. Vaccine 26, 6630-6638
16. Garcon, N., Chomez, P., and Van Mechelen, M. (2007) GlaxoSmithKline Adjuvant Systems in vaccines: concepts, achievements and perspectives. Expert Rev. Vaccines 6, 723-739
17. Kundi, M. (2007) New hepatitis B vaccine formulated with an improved adjuvant system. Expert Rev. Vaccines 6, 133-140
18. Philbin, V. J., and Dowling, D. J., Gallington, L. C., Cortes, G., Tan, Z., and Suter, E. E., Chi, K. W., Shuckett, A., Stoler-Barak, L., Tomai, M., and Miller, R. L., Mansfield, K., and Levy, O. (2012) Imidazoquinoline Toll-like receptor 8 agonists activate human newborn monocytes and dendritic cells through adenosine-refractory and caspase-1-dependent pathways. J. Allergy Clin. Immunol. 130, 195-204 e199
19. Kollmann, T. R., Crabtree, J., Rein-Weston, A., Blimkie, D., Thommai, F., Wang, X. Y., and Lavoie, P. M., Furlong, J., Fortuno, E. S., 3rd, Hajjar, A. M., Hawkins, N. R., Self, S. G., and Wilson, C. B. (2009) Neonatal innate TLR-mediated responses are distinct from those of adults. J. Immunol. 183, 7150-7160
20. Seubert, A., Monaci, E., Pizza, M., O'Hagan, D. T., and Wack, A. (2008) The adjuvants aluminum hydroxide and MF59 induce monocyte and granu-locyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J. Immunol. 180, 5402-5412
21. Zaitseva, M., Romantseva, T., Blinova, K., Beren, J., Sirota, L., Drane, D., and Golding, H. (2012) Use of human MonoMac6 cells for development of in vitro assay predictive of adjuvant safety in vivo. Vaccine 30, 4859-4865
22. Kwissa, M., and Nakaya, H. I., Oluoch, H., and Pulendran, B. (2012) Distinct TLR adjuvants differentially stimulate systemic and local innate immune responses in nonhuman primates. Blood 119, 2044-2055
23. Amenyogbe, N., Levy, O., and Kollmann, T. R. (2015) Systems vaccinology: a promise for the young and the poor. Phil. Trans. Roy. Soc. London. 370
24. Dowling, D. J., Tan, Z., Prokopowicz, Z. M., and Palmer, C. D., Matthews, M. A., Dietsch, G. N., and Hershberg, R. M., and Levy, O. (2013) The ultra-potent and selective TLR8 agonist VTX-294 activates human newborn and adult leukocytes. PLoS ONE 8, e58164
25. PrabhuDas, M., Adkins, B., Gans, H., King, C., Levy, O., Ramilo, O., and Siegrist, C. A. (2011) Challenges in infant immunity: implications for responses to infection and vaccines. Nat. Immunol. 12, 189-194
26. Sanchez-Schmitz, G., and Levy, O. (2011) Development of newborn and infant vaccines. Sci. Transl. Med. 3, 90ps27
27. Higbee, R. G., and Byers, A. M., Dhir, V., Drake, D., Fahlenkamp, H. G., Gangur, J., Kachurin, A., Kachurina, O., Leistritz, D., Ma, Y., Mehta, R., Mishkin, E., Moser, J., Mosquera, L., Nguyen, M., Parkhill, R., Pawar, S., Poisson, L., Sanchez-Schmitz, G., Schanen, B., Singh, I., Song, H., Tapia, T., Warren, W., and Wittman, V. (2009) An immunologic model for rapid vaccine assessment - a clinical trial in a test tube. Alt/Lab. Animals 37 19-27
28. Orr, M. T., and Kramer, R. M., Barnes, L. t., Dowling, Q. M., and Desbien, A. L., Beebe, E. A., Laurance, J. D., and Fox, C. B., Reed, S. G., Coler, R. N., and Vedvick, T. S. (2014) Elimination of the cold-chain dependence of a nanoemulsion adjuvanted vaccine against tuberculosis by lyophilization. J. Controlled Release 177, 20-26
29. Mosca, F., Tritto, E., Muzzi, A., Monaci, E., Bagnoli, F., Iavarone, C., O'Hagan, D., Rappuoli, R., and De Gregorio, E. (2008) Molecular and cellular signatures of human vaccine adjuvants. Proc. Natl. Acad. Sci. U.S.A. 105, 10501-10506
30. Caskey, M., Lefebvre, F., Filali-Mouhim, A., Cameron, M. J., and Goulet, J. P., Haddad, E. K., Breton, G., Trumpfheller, C., Pollak, S., Shimeliovich, I., Duque-Alarcon, A., Pan, L., Nelkenbaum, A., Salazar, A. M., and Schlesinger, S. J., Steinman, R. M., and Sekaly, R. P. (2011) Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J. Exp. Med. 208, 2357-2366
31. Li, S., Rouphael, N., Duraisingham, S., Romero-Steiner, S., Presnell, S., Davis, C., Schmidt, D. S., and Johnson, S. E., Milton, A., Rajam, G., Kasturi, S., and Carlone, G. M., Quinn, C., Chaussabel, D., Palucka, A. K., and Mulligan, M. J., Ahmed, R., Stephens, D. S., Nakaya, H. I., and Pulendran, B. (2014) Molecular signatures of antibody responses derived from a systems biology study of five human vaccines. Nat. Immunol. 15, 195-204
32. Nakaya, H. I., Wrammert, J., Lee, E. K., Racioppi, L., Marie-Kunze, S., Haining, W. N., and Means, A. R., Kasturi, S. P., Khan, N., Li, G. M., McCausland, M., Kanchan, V., Kokko, K. E., Li, S., Elbein, R., Mehta, A. K., Aderem, A., Subbarao, K., Ahmed, R., and Pulendran, B. (2011) Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12, 786-795
33. Querec, T. D., and Akondy, R. S., Lee, E. K., Cao, W., Nakaya, H. I., Teuwen, D., Pirani, A., Gernert, K., Deng, J., Marzolf, B., Kennedy, K., Wu, H., Bennouna, S., Oluoch, H., Miller, J., and Vencio, R. Z., Mulligan, M., Aderem, A., Ahmed, R., and Pulendran, B. (2009) Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10, 116-125
34. Tsang, J. S., and Schwartzberg, P. L., Kotliarov, Y., Biancotto, A., Xie, Z., and Germain, R. N., Wang, E., Olnes, M. J., Narayanan, M., Golding, H., Moir, S., Dickler, H. B., Perl, S., Cheung, F., Baylor, H. C., and Consortium, C. H. I. (2014) Global analyses of human immune variation reveal baseline predictors of postvaccination responses. Cell 157, 499-513
35. Wilhelm, M., Schlegl, J., Hahne, H., Moghaddas Gholami, A., Lieberenz, M., Savitski, M. M., Ziegler, E., Butzmann, L., Gessulat, S., Marx, H., Mathieson, T., Lemeer, S., Schnatbaum, K., Reimer, U., Wenschuh, H., Mollenhauer, M., Slotta-Huspenina, J., Boese, J. H., Bantscheff, M., Gerstmair, A., Faerber, F., and Kuster, B. (2014) Mass-spectrometry-based draft of the human proteome. Nature 509, 582-587
36. Gygi, S. P., Rochon, Y., Franza, B. R., and Aebersold, R. (1999) Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730
37. Meissner, F., and Scheltema, R. A., Mollenkopf, H. J., and Mann, M. (2013) Direct proteomic quantification of the secretome of activated immune cells. Science 340, 475-478
38. Bal, M. S., and Mandal, N. N., Das, M. K., Kar, S. K., and Sarangi, S. S., and Beuria, M. K. (2010) Transplacental transfer of filarial antigens from Wuchereria bancrofti-infected mothers to their offspring. Parasitology 137, 669-673
39. Levy, O., and Zarember, K. A., Roy, R. M., Cywes, C., Godowski, P. J., and Wessels, M. R. (2004) Selective impairment of TLR-mediated innate immunity in human newborns: neonatal blood plasma reduces monocyte TNF-alpha induction by bacterial lipopeptides, lipopolysaccharide, and imiquimod, but preserves the response to R-848. J. Immunol. 173, 4627-4634
40. Vizcaino, J. A., and Deutsch, E. W., Wang, R., Csordas, A., Reisinger, F., Rios, D., Dianes, J. A., Sun, Z., Farrah, T., Bandeira, N., Binz, P. A., Xenarios, I., Eisenacher, M., Mayer, G., and Gatto, L. (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. 32, 223-226
41. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
42. Caraux, G., and Pinloche, S. (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21, 1280-1281
43. Meunier, B., Dumas, E., Piec, I., Bechet, D., Hebraud, M., and Hocquette, J. F. (2007) Assessment of hierarchical clustering methodologies for proteomic data mining. J. Proteome Res. 6, 358-366
44. Makawita, S., Smith, C., Batruch, I., Zheng, Y., Ruckert, F., Grutzmann, R., Pilarsky, C., Gallinger, S., and Diamandis, E. P. (2011) Integrated proteomic profiling of cell line conditioned media and pancreatic juice for the identification of pancreatic cancer biomarkers. Mol. Cell. Proteomics 10, M111 008599
45. Choi, H., Fermin, D., and Nesvizhskii, A. I. (2008) Significance analysis of spectral count data in label-free shotgun proteomics. Mol. Cell. Proteomics 7, 2373-2385
46. Choi, H., Kim, S., Fermin, D., Tsou, C. C., and Nesvizhskii, A. I. (2015) QPROT: Statistical method for testing differential expression using protein-level intensity data in label-free quantitative proteomics. J. Proteomics
47. Ganapathi, L., Van Haren, S., Dowling, D. J., Bergelson, I., and Shukla, N. M., Malladi, S. S., Balakrishna, R., Tanji, H., Ohto, U., Shimizu, T., David, S. A., and Levy, O. (2015) The Imidazoquinoline Toll-Like Receptor-7/8 Agonist Hybrid-2 Potently Induces Cytokine Production by Human Newborn and Adult Leukocytes. PLoS ONE 10, e0134640
48. Zavialov, A. V., and Engstrom, A. (2005) Human ADA2 belongs to a new family of growth factors with adenosine deaminase activity. Biochem. J. 391, 51-57
49. Vahey, M. T., Wang, Z., Kester, K. E., Cummings, J., and Heppner, D. G., Jr., Nau, M. E., Ofori-Anyinam, O., Cohen, J., Coche, T., Ballou, W. R., and Ockenhouse, C. F. (2010) Expression of genes associated with immunoproteasome processing of major histocompatibility complex peptides is indicative of protection with adjuvanted RTS, S malaria vaccine. J. Infect Dis. 201, 580-589
50. Kester, K. E., and Cummings, J. F., Ofori-Anyinam, O., Ockenhouse, C. F., Krzych, U., Moris, P., Schwenk, R., Nielsen, R. A., Debebe, Z., Pinelis, E., Juompan, L., Williams, J., Dowler, M., Stewart, V. A., and Wirtz, R. A., Dubois, M. C., Lievens, M., Cohen, J., Ballou, W. R., Heppner, D. G., Jr., and Rts, S. V. E. G. (2009) Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS, S/AS01B and RTS, S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J. Infect. Dis. 200, 337-346
51. Bolstad, B. M., and Irizarry, R. A., Astrand, M., and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193
52. Bergsbaken, T., and Fink, S. L., and Cookson, B. T. (2009) Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiology 7, 99-109
53. Greenberg, D. P., and Vadheim, C. M., Wong, V. K., Marcy, S. M., Partridge, S., Greene, T., Chiu, C. Y., and Margolis, H. S., and Ward, J. I. (1996) Comparative safety and immunogenicity of two recombinant hepatitis B vaccines given to infants at two, four and six months of age. Pediatr. Infect. Dis. J. 15, 590-596
54. Poolman, J. T. (2014) Shortcomings of pertussis vaccines: why we need a third generation vaccine. Expert Rev. Vaccines 13, 1159-1162
55. Fierens, K., and Kool, M. (2012) The mechanism of adjuvanticity of aluminium-containing formulas. Current Pharmaceut. Design 18, 2305-2313
56. Jacobson, L. S., Lima, H., Jr., Goldberg, M. F., Gocheva, V., Tsiperson, V., Sutterwala, F. S., Joyce, J. A., Gapp, B. V., Blomen, V. A., Chandran, K., Brummelkamp, T. R., Diaz-Griffero, F., and Brojatsch, J. (2013) Cathepsin-mediated necrosis controls the adaptive immune response by Th2 (T helper type 2)-associated adjuvants. J. Biol. Chem. 288, 7481-7491
57. Pettengill, M. A., van Haren, S. D., and Levy, O. (2014) Soluble mediators regulating immunity in early life. Frontiers Immunol. 5, 457
58. Pettengill, M., Robson, S., Tresenriter, M., Millan, J. L., Usheva, A., Bingham, T., Belderbos, M., Bergelson, I., Burl, S., Kampmann, B., Gelinas, L., Kollmann, T., Bont, L., and Levy, O. (2013) Soluble ecto-5'-nucleotidase (5'-NT), alkaline phosphatase, and adenosine deaminase (ADA1) activities in neonatal blood favor elevated extracellular adenosine. J. Biol. Chem. 288, 27315-27326
59. Latz, E., Franko, J., Golenbock, D. T., and Schreiber, J. R. (2004) Haemophilus influenzae type b-outer membrane protein complex glycoconjugate vaccine induces cytokine production by engaging human toll-like receptor 2 (TLR2) and requires the presence of TLR2 for optimal immunogenicity. J. Immunol. 172, 2431-2438
60. Fransen, F., and Stenger, R. M., Poelen, M. C., van Dijken, H. H., Kuipers, B., Boog, C. J., van Putten, J. P., van Els, C. A., and van der Ley, P. (2010) Differential effect of TLR2 and TLR4 on the immune response after immunization with a vaccine against Neisseria meningitidis or Bordetella pertussis. PLoS ONE 5, e15692
61. David, S., Vermeer-de Bondt, P. E., and van der Maas, N. A. (2008) Reactogenicity of infant whole cell pertussis combination vaccine compared with acellular pertussis vaccines with or without simultaneous pneumococcal vaccine in the Netherlands. Vaccine 26, 5883-5887
62. Hayashi, F., and Means, T. K., and Luster, A. D. (2003) Toll-like receptors stimulate human neutrophil function. Blood 102, 2660-2669
63. Garlanda, C., Bottazzi, B., Salvatori, G., De Santis, R., Cotena, A., Deban, L., Maina, V., Moalli, F., Doni, A., Veliz-Rodriguez, T., and Mantovani, A. (2006) Pentraxins in innate immunity and inflammation. Novartis Foundation Symposium 279, 80-86; discussion 86-91, 216-219
64. Bradley, L. M., and Douglass, M. F., Chatterjee, D., Akira, S., and Baaten, B. J. (2012) Matrix metalloprotease 9 mediates neutrophil migration into the airways in response to influenza virus-induced toll-like receptor signaling. PLoS Pathogens 8, e1002641
65. Hu, F., and Ku, M. C., Markovic, D., a Dzaye, O. D., Lehnardt, S., Synowitz, M., Wolf, S. A., and Kettenmann, H. (2014) Glioma-associated microglial MMP9 expression is upregulated by TLR2 signaling and sensitive to minocycline. Int. J. Cancer 135, 2569-2578
66. Garcon, N., Segal, L., Tavares, F., and Van Mechelen, M. (2011) The safety evaluation of adjuvants during vaccine development: the AS04 experience. Vaccine 29, 4453-4459
67. Wilby, K. J., and Lau, T. T., Gilchrist, S. E., and Ensom, M. H. (2012) Mosquirix (RTS,S): a novel vaccine for the prevention of Plasmodium falciparum malaria. Ann. Pharmacotherapy 46, 384-393 bfl