Schmidt Signe Tandrup, Khadke Swapnil, Korsholm Karen Smith, Perrie Yvonne, Rades Thomas, Andersen Peter, Foged Camilla, Christensen Dennis
Department of Pharmacy, Faculty of Health and Medical Sciences, University of Copenhagen, Universitetsparken 2, 2100 Copenhagen Ø, Denmark; Statens Serum Institut, Department of Infectious Disease Immunology, Artillerivej 5, 2300 Copenhagen S, Denmark.
Aston Pharmacy School, Aston University, Birmingham B4 7ET, UK.
J Control Release. 2016 Oct 10;239:107-17. doi: 10.1016/j.jconrel.2016.08.034. Epub 2016 Aug 26.
A prerequisite for vaccine-mediated induction of CD8(+) T-cell responses is the targeting of dendritic cell (DC) subsets specifically capable of cross-presenting antigen epitopes to CD8(+) T cells. Administration of a number of cationic adjuvants via the intraperitoneal (i.p.) route has been shown to result in strong CD8(+) T-cell responses, whereas immunization via e.g. the intramuscular (i.m.) or subcutaneous (s.c.) routes often stimulate weak CD8(+) T-cell responses. The hypothesis for this is that self-drainage of the adjuvant/antigen to the lymphoid organs, which takes place upon i.p. immunization, is required for the subsequent activation of cross-presenting lymphoid organ-resident CD8α(+) DCs. In contrast, s.c. or i.m. immunization usually results in the formation of a depot at the site of injection (SOI), which hinders the self-drainage and targeting of the vaccine to cross-presenting CD8α(+) DCs. We investigated this hypothesis by correlating the biodistribution pattern and the adjuvanticity of the strong CD8(+) T-cell inducing liposomal cationic adjuvant formulation 09 (CAF09), which is composed of dimethyldioctadecylammonium bromide/monomycoloyl glycerol liposomes with polyinosinic:polycytidylic acid electrostatically adsorbed to the surface. Biodistribution studies with radiolabeled CAF09 and a surface-adsorbed model antigen [ovalbumin (OVA)] showed that a significantly larger fraction of the vaccine dose localized in the draining lymph nodes (dLNs) and the spleen 6h after i.p. immunization, as compared to after i.m. immunization. Studies with fluorescently labelled OVA+CAF09 demonstrated a preferential association of OVA+CAF09 to DCs/monocytes, as compared to macrophages and B cells, following i.p. immunization. Administration of OVA+CAF09 via the i.p. route did also result in DC activation, whereas no DC activation could be measured within the same period with unadjuvanted OVA and OVA+CAF09 administered via the s.c. or i.m. routes. In the dLNs, the highest level of activated, cross-presenting CD8α(+) DCs was detected at 24h post immunization, whereas an influx of activated, migrating and cross-presenting CD103(+) DCs to the dLNs could be measured after 48h. This suggests that the CD8α(+) DCs are activated by self-draining OVA+CAF09 in the lymphoid organs, whereas the CD103(+) DCs are stimulated by the OVA+CAF09 at the SOI. These results support the hypothesis that the self-drainage of OVA+CAF09 to the draining LNs is required for the activation of CD8α(+) DCs, while the migratory CD103(+) DCs may play a role in sustaining the subsequent induction of strong CD8(+) T-cell responses.
疫苗介导诱导CD8(+) T细胞应答的一个前提条件是靶向特定能够将抗原表位交叉呈递给CD8(+) T细胞的树突状细胞(DC)亚群。经腹腔(i.p.)途径给予多种阳离子佐剂已被证明可导致强烈的CD8(+) T细胞应答,而通过例如肌肉内(i.m.)或皮下(s.c.)途径免疫通常刺激较弱的CD8(+) T细胞应答。对此的假设是,腹腔免疫时佐剂/抗原向淋巴器官的自身引流是随后激活交叉呈递的淋巴器官驻留CD8α(+) DC所必需的。相比之下,皮下或肌肉内免疫通常会在注射部位(SOI)形成储存库,这会阻碍疫苗向交叉呈递的CD8α(+) DC的自身引流和靶向。我们通过关联强CD8(+) T细胞诱导脂质体阳离子佐剂制剂09(CAF09)的生物分布模式和佐剂活性来研究这一假设,CAF09由溴化二甲基二十八烷基铵/单霉菌酸甘油酯脂质体与静电吸附在表面的聚肌苷酸:聚胞苷酸组成。用放射性标记的CAF09和表面吸附的模型抗原[卵清蛋白(OVA)]进行的生物分布研究表明,与肌肉内免疫后相比,腹腔免疫后6小时疫苗剂量中显著更大比例的部分定位在引流淋巴结(dLNs)和脾脏中。用荧光标记的OVA+CAF09进行的研究表明,腹腔免疫后,与巨噬细胞和B细胞相比,OVA+CAF09优先与DC/单核细胞结合。通过腹腔途径给予OVA+CAF09也确实导致了DC激活,而在同一时期,通过皮下或肌肉内途径给予的无佐剂OVA和OVA+CAF09未检测到DC激活。在dLNs中,免疫后24小时检测到激活的、交叉呈递的CD8α(+) DC的最高水平,而48小时后可检测到激活的、迁移的和交叉呈递的CD103(+) DC流入dLNs。这表明CD8α(+) DC在淋巴器官中被自身引流的OVA+CAF09激活,而CD103(+) DC在SOI被OVA+CAF09刺激。这些结果支持了这样一种假设,即OVA+CAF09向引流淋巴结的自身引流是激活CD8α(+) DC所必需的,而迁移的CD103(+) DC可能在维持随后强烈的CD8(+) T细胞应答诱导中发挥作用。