Vapor nanobubble is the more reliable photothermal mechanism for inducing endosomal escape of siRNA without disturbing cell homeostasis

Fraire, Juan C.; Houthaeve, Gaëlle; Liu, Jing; Raes, Laurens; Vermeulen, Lotte; Stremersch, Stephan; Brans, Toon; Barriga, Gerardo García-Díaz; Keulenaer, Sarah De; Nieuwerburgh, Filip Van; Rycke, Riet De; Vandesompele, Jo; Mestdagh, Pieter; Raemdonck, Koen; Vos, Winnok H. De; Smedt, Stefaan De; Braeckmans, Kevin

doi:10.1016/j.jconrel.2019.12.050

Cited by 50 publications

(52 citation statements)

References 40 publications

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“…The photothermal effect can lead to endosomal escape mainly by two mechanisms ( Figure 10 B). The first one, known as the heating effect, is a light-activation where a PTA is excited to a high energy level that releases heat to destabilize endo-lysosomal membranes [ 336 ]. The second one occurs at very high heat releasing levels capable of generating a vapor layer surrounding the PTA.…”

Section: Enhancing Ion Endosomal Escapementioning

confidence: 99%

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Tailoring Iron Oxide Nanoparticles for Efficient Cellular Internalization and Endosomal Escape

et al. 2020

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Iron oxide nanoparticles (IONs) have been widely explored for biomedical applications due to their high biocompatibility, surface-coating versatility, and superparamagnetic properties. Upon exposure to an external magnetic field, IONs can be precisely directed to a region of interest and serve as exceptional delivery vehicles and cellular markers. However, the design of nanocarriers that achieve an efficient endocytic uptake, escape lysosomal degradation, and perform precise intracellular functions is still a challenge for their application in translational medicine. This review highlights several aspects that mediate the activation of the endosomal pathways, as well as the different properties that govern endosomal escape and nuclear transfection of magnetic IONs. In particular, we review a variety of ION surface modification alternatives that have emerged for facilitating their endocytic uptake and their timely escape from endosomes, with special emphasis on how these can be manipulated for the rational design of cell-penetrating vehicles. Moreover, additional modifications for enhancing nuclear transfection are also included in the design of therapeutic vehicles that must overcome this barrier. Understanding these mechanisms opens new perspectives in the strategic development of vehicles for cell tracking, cell imaging and the targeted intracellular delivery of drugs and gene therapy sequences and vectors.

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Section: Enhancing Ion Endosomal Escapementioning

confidence: 99%

“…In this mechanism, the endosomal escape is attributed to mechanical energy dissipation (expansion and collapse of the vapor nanobubbles) and not to the heat diffusion. This has been demonstrated by the negligible heating of the intracellular environment [ 308 , 336 ].…”

Section: Enhancing Ion Endosomal Escapementioning

confidence: 99%

Tailoring Iron Oxide Nanoparticles for Efficient Cellular Internalization and Endosomal Escape

et al. 2020

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“…mRNA is a large negatively charged, single-stranded nucleic acid that can be encapsulated in synthetic nanocarriers for protection against ubiquitous serum nucleases and enhancing endocytic uptake [17]. Gold nanoparticles, for example, have been extensively studied as drug and gene delivery carriers because of their favorable physicochemical properties [18][19][20][21][22][23][24]. However, carrier-induced cytotoxicity and low transfection efficiency are common disadvantages for T cells [3].…”

Section: Introductionmentioning

confidence: 99%

“…It should be noted, however, that electroporation was amply shown to come with significant loss of cell viability, induction of unwanted phenotypic changes or loss of cell functionality [17,[27][28][29][30]. Laser-assisted photoporation, sometimes also referred to as optoporation, recently came up as a promising gentler technique for intracellular delivery of biological macromolecules [23,24,31]. Wayteck et al, for instance, previously showed in a one-on-one comparison between photoporation and electroporation on murine T cells that a threefold higher percentage of siRNA-transfected viable cells was obtained by photoporation as it induced much less cytotoxicity compared to electroporation [32].…”

Section: Introductionmentioning

confidence: 99%

Intracellular Delivery of mRNA in Adherent and Suspension Cells by Vapor Nanobubble Photoporation

et al. 2020

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Efficient and safe cell engineering by transfection of nucleic acids remains one of the long-standing hurdles for fundamental biomedical research and many new therapeutic applications, such as CAR T cell-based therapies. mRNA has recently gained increasing attention as a more safe and versatile alternative tool over viral- or DNA transposon-based approaches for the generation of adoptive T cells. However, limitations associated with existing nonviral mRNA delivery approaches hamper progress on genetic engineering of these hard-to-transfect immune cells. In this study, we demonstrate that gold nanoparticle-mediated vapor nanobubble (VNB) photoporation is a promising upcoming physical transfection method capable of delivering mRNA in both adherent and suspension cells. Initial transfection experiments on HeLa cells showed the importance of transfection buffer and cargo concentration, while the technology was furthermore shown to be effective for mRNA delivery in Jurkat T cells with transfection efficiencies up to 45%. Importantly, compared to electroporation, which is the reference technology for nonviral transfection of T cells, a fivefold increase in the number of transfected viable Jurkat T cells was observed. Altogether, our results point toward the use of VNB photoporation as a more gentle and efficient technology for intracellular mRNA delivery in adherent and suspension cells, with promising potential for the future engineering of cells in therapeutic and fundamental research applications.

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“…Some lipid formulations used in transfection of siRNAs were shown to be particularly efficient in causing endosomal membrane damage [ 84 , 85 ]. Gold nanoparticles and nanodiamonds were also employed to physically disrupt the endosomal membrane [ 86 , 87 ].…”

Section: Introductionmentioning

confidence: 99%

“Repair Me if You Can”: Membrane Damage, Response, and Control from the Viral Perspective

Daussy

Wodrich

2020

Cells

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Cells are constantly challenged by pathogens (bacteria, virus, and fungi), and protein aggregates or chemicals, which can provoke membrane damage at the plasma membrane or within the endo-lysosomal compartments. Detection of endo-lysosomal rupture depends on a family of sugar-binding lectins, known as galectins, which sense the abnormal exposure of glycans to the cytoplasm upon membrane damage. Galectins in conjunction with other factors orchestrate specific membrane damage responses such as the recruitment of the endosomal sorting complex required for transport (ESCRT) machinery to either repair damaged membranes or the activation of autophagy to remove membrane remnants. If not controlled, membrane damage causes the release of harmful components including protons, reactive oxygen species, or cathepsins that will elicit inflammation. In this review, we provide an overview of current knowledge on membrane damage and cellular responses. In particular, we focus on the endo-lysosomal damage triggered by non-enveloped viruses (such as adenovirus) and discuss viral strategies to control the cellular membrane damage response. Finally, we debate the link between autophagy and inflammation in this context and discuss the possibility that virus induced autophagy upon entry limits inflammation.

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Vapor nanobubble is the more reliable photothermal mechanism for inducing endosomal escape of siRNA without disturbing cell homeostasis

Cited by 50 publications

References 40 publications

Tailoring Iron Oxide Nanoparticles for Efficient Cellular Internalization and Endosomal Escape

Tailoring Iron Oxide Nanoparticles for Efficient Cellular Internalization and Endosomal Escape

Intracellular Delivery of mRNA in Adherent and Suspension Cells by Vapor Nanobubble Photoporation

“Repair Me if You Can”: Membrane Damage, Response, and Control from the Viral Perspective

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