Endocytosis-driven gold nanoparticle fractal rearrangement in cells and its influence on photothermal conversion

Mulens-Arias, Vladimir; Balfourier, Alice; Nicolas‐Boluda, Alba; Carn, Florent; Gazeau, Florence

doi:10.1039/d0nr05886f

Cited by 12 publications

(8 citation statements)

References 71 publications

(97 reference statements)

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“…AuNPs, despite having the lowest heating capacity in solution, induced a high level of cell apoptosis when irradiated. This can be explained by the lysosomal fractal aggregations of AuNPs inducing intracellular plasmon coupling and intralysosomal local heating as demonstrated earlier . Likewise the AuNP–5-FU complex maintains its heating capacity in CT26 cells, inducing 70% of cell death among the irradiated cell monolayer (Figure B).…”

Section: Resultssupporting

confidence: 61%

“…43 When internalized by cells, gold nanoparticles are conveyed into the harsh environment of lysosomes to be progressively degraded. 29 Lysosomal confinement and transformation 30,47 can directly affect their photothermal efficiency and intracellular thermal effect. After 24 h of incubation with AuNP and AuNP−5-FU complexes ([Au] = 10 μg/mL), the colon adenocarcinoma CT26 cells were washed and the cell monolayers were irradiated for 5 min with a NIR 808 nm laser at 2 W/cm 2 .…”

Section: Resultsmentioning

confidence: 99%

“…Moreover, we recently demonstrated that gold nanoparticles could be degraded intracellularly, which could limit their long-term persistence into vital structures . Also, we have demonstrated that AuNP (in particular, 16 nm AuNP) cell internalization can facilitate bringing the nanoparticles close enough to be susceptible to the plasmon coupling, thus showing an increase in the photothermal conversion efficiency . In addition to the heating generation, AuNPs could be harnessed as a drug carrier for a combined hyperthermia and chemotherapy effect, bringing a precision medicine approach to HIPEC.…”

mentioning

confidence: 99%

“…29 Also, we have demonstrated that AuNP (in particular, 16 nm AuNP) cell internalization can facilitate bringing the nanoparticles close enough to be susceptible to the plasmon coupling, thus showing an increase in the photothermal conversion efficiency. 30 In addition to the heating generation, AuNPs could be harnessed as a drug carrier for a combined hyperthermia and chemotherapy effect, bringing a precision medicine approach to HIPEC. The synergic effect of hyperthermia combined with chemotherapy relies on the increased tissue perfusion and cell uptake of drugs.…”

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confidence: 99%

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Tumor-Selective Immune-Active Mild Hyperthermia Associated with Chemotherapy in Colon Peritoneal Metastasis by Photoactivation of Fluorouracil–Gold Nanoparticle Complexes

et al. 2021

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Peritoneal metastasis (PM) is considered as the terminal stage of metastatic colon cancer, with still poor median survival rate even with the best recent chemotherapy treatment. The current PM treatment combines cytoreductive surgery, which consists of resecting all macroscopic tumors, with hyperthermic intraperitoneal chemotherapy (HIPEC), which uses mild hyperthermia to boost the diffusion and cytotoxic effect of chemotherapeutic drugs. As HIPEC is performed via a closed circulation of a hot liquid containing chemotherapy, it induces uncontrolled heating and drug distribution in the whole peritoneal cavity with important off-site toxicity and a high level of morbidity. Here, we propose a safer precision strategy using near-infrared (NIR) photoactivated gold nanoparticles (AuNPs) coupled to the chemotherapeutic drug 5-fluorouracil (5-FU) to enable a spatial and temporal control of mild chemo-hyperthermia targeted to the tumor nodules within the peritoneal cavity. Both the 16 nm AuNPs and the corresponding complex with 5-FU (AuNP–5-FU) were shown as efficient NIR photothermal agents in the microenvironment of subcutaneous colon tumors as well as PM in syngeneic mice. Noteworthy, NIR photothermia provided additional antitumor effects to 5-FU treatment. A single intraperitoneal administration of AuNP–5-FU resulted in their preferential accumulation in tumor nodules and peritoneal macrophages, allowing light-induced selective hyperthermia, extended tumor necrosis, and activation of a pro-inflammatory immune response while leaving healthy tissues without any damage. From a translational standpoint, the combined and tumor-targeted photothermal and chemotherapy mediated by the AuNP–drug complex has the potential to overcome the current off-target toxicity of HIPEC in clinical practice.

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Section: Resultssupporting

confidence: 61%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Tumor-Selective Immune-Active Mild Hyperthermia Associated with Chemotherapy in Colon Peritoneal Metastasis by Photoactivation of Fluorouracil–Gold Nanoparticle Complexes

et al. 2021

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“…Targeted drug delivery using nanoparticle has become a prime focus in cancer treatment to improve its therapeutic outcome [1][2][3]. Extensive research has been documented to evaluate the efficacy of targeted drug delivery using gold nanoparticles, and identified their uptake mechanisms such as phagocytosis, macropinocytosis, micropinocytosis and receptor mediated endocytosis [4][5][6][7]. These studies have enabled the researchers to achieve significant strides in comprehending alteration in signaling mechanisms, cellular morphology and linear nanomechanical properties (NMPs) that include membrane stiffness, deformation and adhesion using atomic force microscope (AFM) [8][9][10][11][12].…”

Section: Introductionmentioning

confidence: 99%

Poroelastic Attributes: A Real-time Determinant Membrane Nanorheology for Receptor Dependent Endocytosis of Targeted Gold Nanoparticles

Kulkarni

Mukhopadhyay

Bhattacharya

2021

Preprint

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BackgroundEfficacy of targeted drug delivery using nanoparticles relies on several factors including the uptake mechanisms such as phagocytosis, macropinocytosis, micropinocytosis and receptor mediated endocytosis. These mechanisms have been studied with respect to the alteration in signaling mechanisms, cellular morphology, and linear nanomechanical properties (NMPs). Commonly employed classical contact mechanics models to address cellular NMPs fail to address mesh like structure consisting of bilayer lipids and proteins of cell membrane. To overcome this technical challenge, we employed poroelastic model which accounts for the biphasic nature of cells including their porous behavior exhibiting both solid like (fluid storage) and liquid like (fluid dissipate) behavior ResultsIn this study, we employed atomic force microscopy to monitor the influence of surface engineering of gold nanoparticles (GNPs) to the alteration of nonlinear NMPs such as drained Poisson’s ratio, effective shear stress, diffusion constant and pore dimensions of cell membranes during their uptake. Herein, we used pancreatic cancer (PDAC) cell lines including Panc1, AsPC-1 and endothelial cell HUVECs to understand the receptor-dependent and -independent endocytosis of two different GNPs derived using plectin-1 targeting peptide (PTP-GNP) and corresponding scrambled peptide (sPEP-GNP). Compared to untreated cells, in case of receptor dependent endocytosis of PTP-GNPs diffusion coefficient altered ~1264-fold and ~1530-fold and pore size altered ~320-fold and ~260-fold in Panc1 and AsPC-1 cells respectively. Whereas for receptor independent mechanisms, we observed modest alteration in diffusion coefficient and pore size, in these cells compared to untreated cells. Effective shear stress corresponding to 7.38±0.15 kPa and 20.49±0.39 kPa in PTP-GNP treatment in Panc1 and AsPC-1, respectively was significantly more than that for sPEP-GNP. These results demonstrate that with temporal recruitment of plectin-1 during receptor mediated endocytosis affects the poroelastic attributes of the membrane. ConclusionThis study confirms that nonlinear NMPs of cell membrane are directly associated with the uptake mechanism of nanoparticles and can provide promising insights of the nature of endocytosis mechanism involved for organ specific drug delivery using nanoparticles. Hence, nanomechanical analysis of cell membrane es using this noninvasive, label-free and live-cell analytical tool can therefore be instrumental to evaluate therapeutic benefit of nanoformulations.

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Prospecting Cellular Gold Nanoparticle Biomineralization as a Viable Alternative to Prefabricated Gold Nanoparticles

Schwartz-Duval

Sokolov

2022

Advanced Science

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Gold nanoparticles (GNPs) have shown considerable potential in a vast number of biomedical applications. However, currently there are no clinically approved injectable GNP formulations. Conversely, gold salts have been used in the clinic for nearly a century. Further, there is evidence of GNP formation in patients treated with gold salts (i.e., chrysiasis). Recent reports evaluating this phenomenon in human cells and in murine models indicate that the use of gold ions for in situ formation of theranostic GNPs could greatly improve the delivery within dense biological tissues, increase efficiency of intracellular gold uptake, and specificity of GNP formation within cancer cells. These attributes in combination with safe clinical application of gold salts make this process a viable strategy for clinical translation. Here, the first summary of the current knowledge related to GNP biomineralization in mammalian cells is provided along with critical assessment of potential biomedical applications of this newly emergent field.

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Endocytosis-driven gold nanoparticle fractal rearrangement in cells and its influence on photothermal conversion

Abstract: Cellular endocytosis and intracellular trafficking of nanoparticles induce dynamic rearrangements that profoundly modifies the nanoparticle physical properties and governs their biological outcomes when activated by external fields. The precise structure,...

Cited by 12 publications

References 71 publications

Tumor-Selective Immune-Active Mild Hyperthermia Associated with Chemotherapy in Colon Peritoneal Metastasis by Photoactivation of Fluorouracil–Gold Nanoparticle Complexes

Tumor-Selective Immune-Active Mild Hyperthermia Associated with Chemotherapy in Colon Peritoneal Metastasis by Photoactivation of Fluorouracil–Gold Nanoparticle Complexes

Poroelastic Attributes: A Real-time Determinant Membrane Nanorheology for Receptor Dependent Endocytosis of Targeted Gold Nanoparticles

Prospecting Cellular Gold Nanoparticle Biomineralization as a Viable Alternative to Prefabricated Gold Nanoparticles

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