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84 Khushbu Bhatt et al.
activation and expansion. A unique feature of this strategy is that cells can be easily
harvested and, unlike Dynabeads, they do not require magnetic separation. Moreover,
these highly ordered lattices enabled efficient delivery of lentiviral gene in addition to
T-cell expansion, which could ultimately allow straightforward CAR T-cell manipulation and manufacturing [118].
T-cell activation and the resulting differentiation into various phenotypes are widely
influenced by the biophysical properties of the platform used for stimulation, such as
organization and density of the signaling cues as well as the substrate stiffness, shape,
and surface area [119,120]. For instance, Cheung et al. designed an APC-mimetic scaffold
comprising high-aspect-ratio silica microrods to provide stimulatory and mitogenic signals to T cells. The microrods were coated with liposomes to constitute a lipid bilayer.
The stimulatory cues were provided through synthetic fluid lipid membranes to emulate
natural antigen presentation and facilitate physical TCR rearrangement. Additionally, the
mitogenic cytokines were slowly released from the silica microrods to mimic paracrine
delivery. The APC-mimetic scaffold promoted greater expansion of polyclonal T cells
and enriched antigen-specific rare T cells when compared to conventional methods such
as Dynabeads. A high-aspect-ratio facilitated the interaction of each silica microrod with
multiple T cells, allowing large cluster formation and enhanced cell–cell contact. Furthermore, the large size of the ellipsoidal silica microrods provided low-curvature surfaces to enable high-surface-area interactions with T cells, thus improving T-cell
expansion when compared to their spherical counterparts possessing higher-curvature
surfaces [113]. This technology has been fine-tuned to adjust the density of T cellactivating cues, leading to more robust T-cell expansion [113,121]. Dang et al. described
a polymeric scaffold made of poly(ε-caprolactone)-co-polydimethylsiloxane electrospun
fibers functionalized with CD3 and CD28 antibodies to improve T-cell proliferation.
The authors noted a 4-fold increase in T-cell expansion when compared to Dynabeads
and improved cytokine secretion with softer electrospun fibers [122].
Collectively, these studies have established that polymeric scaffolds could provide a
substantial benefit for T-cell expansion over standard methods. Furthermore, these scaffolds are a great tool for creating a 3-D niche that closely mimics the natural environment
for T-cell activation by providing stimulatory biochemical and biophysical cues (Fig. 3).
Additionally, polymeric scaffolds represent a versatile platform. To enhance the quality
and quantity of ex vivo activated and expanded T cells, a number of features could be
easily fine-tuned such as the density and organization of T-cell stimulatory signals,
ECM-mediated cues, as well as substrate stiffness and surface area.
The efficacy of adoptive T-cell therapies in treating solid tumors has been hindered by
low T-cell infiltration and proliferation, lack of survival and function, as well as immunosuppression within the tumor bed. Thus, increasing T-cell numbers and reinforcing
their functionality in the TME is essential for treating solid tumor cancers [123,124].
Polymeric scaffolds have been employed as delivery vehicles to deploy T cells directly
to tumors and to provide stimulatory cues for in situ T-cell proliferation and maintenance
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of their cytotoxic function (Fig. 4). Tsao et al. provided some early evidence that the
polymeric scaffolds could function as a T-cell depot by engineering PEG-g-chitosanbased thermosensitive hydrogels to treat glioblastoma. The authors showed that the
T cells migrated to tumors from the gel and could effectively kill U-87 MG glioblastoma
cells in vitro [125]. In another example, Monette et al. used chitosan-based thermoresponsive hydrogels that solidify at 37°C. The authors demonstrated that the encapsulated T cells proliferated in vitro and migrated towards a gradient of tumor cells. T-cell
expansion was dependent on pore size and scaffolds with higher porosity (50–500 μm)
resulted in optimal cell proliferation and migration [126]. Weiden et al. reported a similar
biomimetic and thermoresponsive polyisocyanopeptide-based hydrogel to facilitate
in vitro T-cell expansion and in vivo local delivery [127]. Since these studies utilized ther-
moresponsive hydrogels, these smart scaffolds could be easily injected as a liquid and
polymerize in the body, obviating the need for invasive surgical implantation. Furthermore, Stephan et al. established the potential of adoptively transferred T cells using an
implantable macroporous scaffold. The authors utilized CAR T-cell-laden alginate
hydrogels that were functionalized with GFOGER, a collagen mimetic peptide that
binds to lymphocytes, and embedded with silica microparticles that released IL-15
85Polymeric scaffolds for antitumor immune cell priming
Fig. 4 Schematic illustration of a polymeric scaffold-based adoptive T-cell transfer. After
harvesting naïve T cells from the leukapheresis procedure in cancer patients, they are transduced with
tumor antigen-specific T-cell receptor (TCR) or chimeric antigen receptor (CAR). These prestimulated
antigen-specific T cells are then loaded into a 3-D scaffold, which is integrated with biochemical cues
and cytokines to enhance proliferation and maintenance of their effector functions. Upon injection or
implantation around the tumor, T cells expand within the scaffold, and activated antitumor T cells are
slowly deployed to target and kill tumor cells.
86 Khushbu Bhatt et al.
superagonist while simultaneously presenting CD3, CD28, and CD317 antibodies. The
delivered T cells expanded locally, persisted in vivo, and exhibited a non-exhaustive phenotype. Unlike locally or systemically infused T cells, their approach prevented tumor
relapse in a mouse breast cancer resection model and improved tumor clearance in a disseminated ovarian metastasis model [128]. In a consecutive study, the authors fabricated
the T cell-delivering polymeric scaffold to co-deliver STING agonist, a vaccine adjuvant.
CAR T cells alone failed to eliminate the tumors completely, likely due to immunosuppression, but the combination with STING agonist led to tumor regression: 40%
complete responses in the pancreatic tumor model and 60% complete responses in the
melanoma model [62]. Interestingly, this strategy did not require prior lymphodepletion
and cytokine infusion for T-cell reconstitution, survival, and proliferation. However, it
required surgical implantation. Overall, these studies established that polymeric scaffolds
integrated with migration-promoting and stimulatory cues can function as effective carriers for antitumor T cells. They can overcome tumor-induced immunosuppression and
gradually disperse antitumor T cells throughout the tumor milieu. This approach can significantly decrease the number of T cells required to mount an effective antitumor
response, thereby limiting undesired systemic side effects. However, further studies
are necessary to validate whether scaffold-based therapies can effectively eliminate distant
metastases as well.
5. Conclusion and future perspectives
Polymeric scaffolds have been extensively explored for the development of pro-
phylactic and therapeutic cancer vaccines, delivery of immunomodulators and ICIs,
as well as for the in vitro activation and expansion of T cells. The use of polymeric
scaffolds offers targeted and controlled delivery of immunomodulatory factors to induce
safe, effective, and long-lasting immune responses. Although polymeric scaffolds for
immune cell priming hold great promise for effective cancer immunotherapy, various
aspects of this approach need to be further explored. Currently, most of the scaffold-based
approaches utilize diffusion for controlling the release kinetics of immunomodulating
agents. This can be improved by developing polymeric systems with stimuli-responsive
properties which may allow more precise and on-demand release of multiple immunomodulators [129–132]. The correlation between the physicochemical properties of the
polymers and their influence on specific immune pathways needs to be further studied
[133]. Despite significant advances, our knowledge about the mechanisms by which
polymeric scaffolds mediate immune responses is still elementary [134]. Extensive characterization of the subtypes of antigen-presenting cells recruited within the immunomodulatory scaffold is required, thereby offering more insights into the desired
immune cell phenotype required for in situ vaccination purposes. Specifically, the design
of scaffolds to recruit DC subtypes with cross-presenting abilities, such as conventional
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type 1 DCs (cDC1s), has great potential to induce strong cytotoxic T-cell responses
[103]. This can be achieved by encapsulating chemokines that are more specific to cDC1s
such as X-C Motif Chemokine Ligand 1 (XCL1) and X-C Motif Chemokine Ligand 2
(XCL2) [103]. The next generation of scaffold-based vaccines should target DCs with
cancer neoantigens, i.e., mutations unique to an individual’s tumor. Cancer vaccines that
make use of these mutations represent a promising strategy for personalized
immunotherapies [103].
A few polymeric scaffolds have been developed for direct in vivo T-cell activation and
expansion [62,128]. However, they suffer from major limitations such as the decrease in
the number of antigen-specific T cells after 1–2 weeks. Thus, developing and characterizing scaffold-based systems that can improve in vivo T-cell persistence is warranted. This
strategy would circumvent the need for laborious and costly ex vivo T-cell expansion.
Apart from mounting effective antitumor immune responses against cancer, several
mechanisms in cancer-immunity cycle are inhibitory in nature and may dampen the
immune response [34]. For instance, “cold” tumors, tumors that contain few infiltrating
T cells, represent a therapeutic challenge for immunotherapy. Advanced and sophisticated polymer-based approaches to impede immunosuppression should be investigated
[135,136]. Future efforts should also harness the full potential of other immune cells such
as natural killer (NK) cells, B cells, TAMs, and MDSCs [137]. Additionally, combining
polymeric scaffold-based strategies with other immunotherapies, such as ICIs, may have a
synergistic impact and boost antitumor efficacy. Except for WDVAX (NCT01753089),
successful clinical translation of polymeric scaffold-based immunotherapies has been
quite limited. WDVAX is a PLGA-based implantable cancer vaccine for melanoma
and is currently in Phase I clinical trial [111]. When designing a scaffold, it is important
to take several properties into consideration such as the polymer composition, functionalization, microstructural features, degradation pattern, drug release profiles, mode of
administration, immunomodulatory action, and the short- and long-term safety for its
successful translation from bench to bedside [138]. Overcoming these shortcomings will
facilitate the development of more potent and innovative scaffold systems by leveraging
advanced and sophisticated polymers for efficient immune cell priming. Moreover, the
efficacy of polymeric scaffold-based approaches needs to be validated in relevant murine
tumor models that recapitulate tumor heterogeneity and aspects of immunotolerance
such as hypoxia-driven immunosuppression that are observed clinically in humans [138].
87Polymeric scaffolds for antitumor immune cell priming
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