The stimulatory effect of the TLR4-mediated adjuvant glucopyranosyl lipid A is well preserved in old age

Biogerontology

Volumn 17, Issue 1, 2016, Pages 177-187

  Weinberger, Birgit ^a   Joos, Clemens ^a   Reed, Steven G ^b   Coler, Rhea ^b   Grubeck Loebenstein, Beatrix ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b INFECTIOUS DISEASE RESEARCH INSTITUTE   (United States)

Author keywords

Adjuvant; Ageing; Antigen presenting cells; Elderly; TLR 4

Indexed keywords

GLUCOPYRANOSYL LIPID A; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 6; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE; GLUCOPYRANOSYL LIPID-A; GLUCOSIDE; LIPID A; SUBUNIT VACCINE; TLR4 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOSTIMULATION; MONOCYTE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; AGING; AGONISTS; ANTIGEN PRESENTING CELL; CELL CULTURE; DRUG EFFECTS; FEMALE; IMMUNOLOGY; MALE; MIDDLE AGED; TREATMENT OUTCOME; VERY ELDERLY;

ADJUVANTS, IMMUNOLOGIC; ADULT; AGED; AGED, 80 AND OVER; AGING; ANTIGEN-PRESENTING CELLS; CELLS, CULTURED; CYTOKINES; FEMALE; GLUCOSIDES; HUMANS; LIPID A; MALE; MIDDLE AGED; TOLL-LIKE RECEPTOR 4; TREATMENT OUTCOME; VACCINES, SUBUNIT;

EID: 84955403645     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-015-9576-x     Document Type: Article

References (47)

1. Agrawal A, Agrawal S, Cao JN, Su H, Osann K, Gupta S (2007) Altered innate immune functioning of dendritic cells in elderly humans: a role of phosphoinositide 3-kinase-signaling pathway. J Immunol 178:6912–6922
2. Alderson MR, McGowan P, Baldridge JR, Probst P (2006) TLR4 agonists as immunomodulatory agents. J Endotoxin Res 12:313–319
3. Anderson RC, Fox CB, Dutill TS, Shaverdian N, Evers TL, Poshusta GR, Chesko J, Coler RN, Friede M, Reed SG, Vedvick TS (2010) Physicochemical characterization and biological activity of synthetic TLR4 agonist formulations. Colloids Surf B Biointerfaces 75:123–132
4. Arias MA, Van Roey GA, Tregoning JS, Moutaftsi M, Coler RN, Windish HP, Reed SG, Carter D, Shattock RJ (2012) Glucopyranosyl lipid adjuvant (GLA), a synthetic TLR4 agonist, promotes potent systemic and mucosal responses to intranasal immunization with HIVgp140. PLoS One 7:e41144
5. Behzad H, Huckriede AL, Haynes L, Gentleman B, Coyle K, Wilschut JC, Kollmann TR, Reed SG, McElhaney JE (2012) GLA-SE, a synthetic toll-like receptor 4 agonist, enhances T-cell responses to influenza vaccine in older adults. J Infect Dis 205:466–473
6. Castle SC (2000) Clinical relevance of age-related immune dysfunction. Clin Infect Dis 31:578–585
7. Castle SC, Uyemura K, Crawford W, Wong W, Makinodan T (1999) Antigen presenting cell function is enhanced in healthy elderly. Mech Ageing Dev 107:137–145
8. Cluff CW, Baldridge JR, Stover AG, Evans JT, Johnson DA, Lacy MJ, Clawson VG, Yorgensen VM, Johnson CL, Livesay MT, Hershberg RM, Persing DH (2005) Synthetic toll-like receptor 4 agonists stimulate innate resistance to infectious challenge. Infect Immun 73:3044–3052
9. Coler RN, Baldwin SL, Shaverdian N, Bertholet S, Reed SJ, Raman VS, Lu X, DeVos J, Hancock K, Katz JM, Vedvick TS, Duthie MS, Clegg CH, Van HN, Reed SG (2010) A synthetic adjuvant to enhance and expand immune responses to influenza vaccines. PLoS One 5:e13677
10. Coler RN, Bertholet S, Moutaftsi M, Guderian JA, Windish HP, Baldwin SL, Laughlin EM, Duthie MS, Fox CB, Carter D, Friede M, Vedvick TS, Reed SG (2011) Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS One 6:e16333
11. Grun JL, Maurer PH (1989) Different T helper cell subsets elicited in mice utilizing two different adjuvant vehicles: the role of endogenous interleukin 1 in proliferative responses. Cell Immunol 121:134–145
12. Herrero C, Sebastian C, Marques L, Comalada M, Xaus J, Valledor AF, Lloberas J, Celada A (2002) Immunosenescence of macrophages: reduced MHC class II gene expression. Exp Gerontol 37:389–394
13. Ho CS, Munster D, Pyke CM, Hart DN, Lopez JA (2002) Spontaneous generation and survival of blood dendritic cells in mononuclear cell culture without exogenous cytokines. Blood 99:2897–2904
14. Huckriede A, Bungener L, Stegmann T, Daemen T, Medema J, Palache AM, Wilschut J (2005) The virosome concept for influenza vaccines. Vaccine 23(1):S26–38–S26-S38
15. Jiang J, Bennett AJ, Fisher E, Williams-Bey Y, Shen H, Murasko DM (2009) Limited expansion of virus-specific CD8 T cells in the aged environment. Mech Ageing Dev 130:713–721
16. Jing Y, Shaheen E, Drake RR, Chen N, Gravenstein S, Deng Y (2009) Aging is associated with a numerical and functional decline in plasmacytoid dendritic cells, whereas myeloid dendritic cells are relatively unaltered in human peripheral blood. Hum Immunol 70:777–784
17. Ju X, Clark G, Hart DN (2010) Review of human DC subtypes. Methods Mol Biol 595:3–20. doi:10.1007/978-1-60761-421-0_1
18. Lee CC, Avalos AM, Ploegh HL (2012) Accessory molecules for Toll-like receptors and their function. Nat Rev Immunol 12:168–179
19. Lim KH, Staudt LM (2013) Toll-like receptor signaling. Cold Spring Harb Perspect Biol 5:a011247
20. Lim W, Ma W, Gee K, Aucoin S, Nandan D, Diaz-Mitoma F, Kozlowski M, Kumar A (2002) Distinct role of p38 and c-Jun N-terminal kinases in IL-10-dependent and IL-10-independent regulation of the costimulatory molecule B7.2 in lipopolysaccharide-stimulated human monocytic cells. J Immunol 168:1759–1769
21. Lung TL, Saurwein-Teissl M, Parson W, Schonitzer D, Grubeck-Loebenstein B (2000) Unimpaired dendritic cells can be derived from monocytes in old age and can mobilize residual function in senescent T cells. Vaccine 18:1606–1612
22. Marrack P, McKee AS, Munks MW (2009) Towards an understanding of the adjuvant action of aluminium. Nat Rev Immunol 9:287–293
23. Masihi KN, Lange W, Brehmer W, Ribi E (1986) Immunobiological activities of nontoxic lipid A: enhancement of nonspecific resistance in combination with trehalose dimycolate against viral infection and adjuvant effects. Int J Immunopharmacol 8:339–345
24. McLachlan JA, Serkin CD, Morrey KM, Bakouche O (1995) Antitumoral properties of aged human monocytes. J Immunol 154:832–843
25. Mosca F, Tritto E, Muzzi A, Monaci E, Bagnoli F, Iavarone C, O’Hagan D, Rappuoli R, DeGregorio E (2008) Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA 105:10501–10506
26. Osugi Y, Vuckovic S, Hart DN (2002) Myeloid blood CD11c(+) dendritic cells and monocyte-derived dendritic cells differ in their ability to stimulate T lymphocytes. Blood 100:2858–2866
27. Ott G, Barchfeld GL, Chernoff D, Radhakrishnan R, van HP, van NG (1995) MF59 design and evaluation of a safe and potent adjuvant for human vaccines. Pharm Biotechnol 6:277–296
28. Panda A, Qian F, Mohanty S, van DD, Newman FK, Zhang L, Chen S, Towle V, Belshe RB, Fikrig E, Allore HG, Montgomery RR, Shaw AC (2010) Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J Immunol 184:2518–2527
29. Pantel A, Cheong C, Dandamudi D, Shrestha E, Mehandru S, Brane L, Ruane D, Teixeira A, Bozzacco L, Steinman RM, Longhi MP (2012) A new synthetic TLR4 agonist, GLA, allows dendritic cells targeted with antigen to elicit Th1 T-cell immunity in vivo. Eur J Immunol 42:101–109
30. Pawelec G (1999) Immunosenescence: impact in the young as well as the old? Mech Ageing Dev 108:1–7
31. Pereira LF, de Souza AP, Borges TJ, Bonorino C (2011) Impaired in vivo CD4+ T cell expansion and differentiation in aged mice is not solely due to T cell defects: decreased stimulation by aged dendritic cells. Mech Ageing Dev 132:187–194
32. Persing DH, Coler RN, Lacy MJ, Johnson DA, Baldridge JR, Hershberg RM, Reed SG (2002) Taking toll: lipid A mimetics as adjuvants and immunomodulators. Trends Microbiol 10:S32–S37
33. Plowden J, Renshaw-Hoelscher M, Engleman C, Katz J, Sambhara S (2004) Innate immunity in aging: impact on macrophage function. Aging Cell 3:161–167
34. Radford KJ, Turtle CJ, Kassianos AJ, Hart DN (2006) CD11c+ blood dendritic cells induce antigen-specific cytotoxic T lymphocytes with similar efficiency compared to monocyte-derived dendritic cells despite higher levels of MHC class I expression. J Immunother 29:596–605
35. Renshaw M, Rockwell J, Engleman C, Gewirtz A, Katz J, Sambhara S (2002) Cutting edge: impaired Toll-like receptor expression and function in aging. J Immunol 169:4697–4701
36. Robbins SH, Walzer T, Dembele D, Thibault C, Defays A, Bessou G, Xu H, Vivier E, Sellars M, Pierre P, Sharp FR, Chan S, Kastner P, Dalod M (2008) Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol 9:R17–R19
37. Saurwein-Teissl M, Zisterer K, Schmitt TL, Gluck R, Cryz S, Grubeck-Loebenstein B (1998) Whole virus influenza vaccine activates dendritic cells (DC) and stimulates cytokine production by peripheral blood mononuclear cells (PBMC) while subunit vaccines support T cell proliferation. Clin Exp Immunol 114:271–276
38. Saurwein-Teissl M, Romani N, Grubeck-Loebenstein B (2000) Dendritic cells in old age-neglected by gerontology? Mech Ageing Dev 20:123–130
39. Schneider LP, Schoonderwoerd AJ, Moutaftsi M, Howard RF, Reed SG, de Jong EC, Teunissen MB (2012) Intradermally administered TLR4 agonist GLA-SE enhances the capacity of human skin DCs to activate T cells and promotes emigration of Langerhans cells. Vaccine 30:4216–4224
40. Tan SY, Cavanagh LL, d’Advigor W, Shackel N, Fazekas de St GB, Weninger W (2012) Phenotype and functions of conventional dendritic cells are not compromised in aged mice. Immunol Cell Biol 90:722–732
41. Thoelen S, Van DP, Mathei C, Leroux-Roels G, Desombere I, Safary A, Vandepapeliere P, Slaoui M, Meheus A (1998) Safety and immunogenicity of a hepatitis B vaccine formulated with a novel adjuvant system. Vaccine 16:708–714
42. Uyemura K, Castle SC, Makinodan T (2002) The frail elderly: role of dendritic cells in the susceptibility of infection. Mech Ageing Dev 123:955–962
43. van Duin D, Allore HG, Mohanty S, Ginter S, Newman FK, Belshe RB, Medzhitov R, Shaw AC (2007) Prevaccine determination of the expression of costimulatory B7 molecules in activated monocytes predicts influenza vaccine responses in young and older adults. J Infect Dis 195:1590–1597
44. Walker WT, Faust SN (2010) Monovalent inactivated split-virion AS03-adjuvanted pandemic influenza A (H1N1) vaccine. Expert Rev Vaccines 9:1385–1398
45. Weinberger B, Herndler-Brandstetter D, Schwanninger A, Weiskopf D, Grubeck-Loebenstein B (2008) Biology of immune responses to vaccines in elderly persons. Clin Infect Dis 46:1078–1084
46. Wong C, Goldstein DR (2013) Impact of aging on antigen presentation cell function of dendritic cells. Curr Opin Immunol 25:535–541
47. Wong CP, Magnusson KR, Ho E (2010) Aging is associated with altered dendritic cells subset distribution and impaired proinflammatory cytokine production. Exp Gerontol 45:163–169