Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context

Summary: Background: Noninvasive in vivo cell tracking is valuable in understanding the mechanisms that enhance anti-cancer immunity. We have recently developed a new method called phototruncation-assisted cell tracking (PACT), that uses photoconvertible cell tracking technology to detect in vivo c...

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Main Authors: Hiroshi Fukushima, Aki Furusawa, Seiichiro Takao, Siddharth S. Matikonda, Makoto Kano, Shuhei Okuyama, Hiroshi Yamamoto, Peter L. Choyke, Martin J. Schnermann, Hisataka Kobayashi
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396424000859
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author Hiroshi Fukushima
Aki Furusawa
Seiichiro Takao
Siddharth S. Matikonda
Makoto Kano
Shuhei Okuyama
Hiroshi Yamamoto
Peter L. Choyke
Martin J. Schnermann
Hisataka Kobayashi
author_facet Hiroshi Fukushima
Aki Furusawa
Seiichiro Takao
Siddharth S. Matikonda
Makoto Kano
Shuhei Okuyama
Hiroshi Yamamoto
Peter L. Choyke
Martin J. Schnermann
Hisataka Kobayashi
author_sort Hiroshi Fukushima
collection DOAJ
description Summary: Background: Noninvasive in vivo cell tracking is valuable in understanding the mechanisms that enhance anti-cancer immunity. We have recently developed a new method called phototruncation-assisted cell tracking (PACT), that uses photoconvertible cell tracking technology to detect in vivo cell migration. This method has the advantages of not requiring genetic engineering of cells and employing tissue-penetrant near-infrared light. Methods: We applied PACT to monitor the migration of immune cells between a tumour and its tumour-draining lymph node (TDLN) after near-infrared photoimmunotherapy (NIR-PIT). Findings: PACT showed a significant increase in the migration of dendritic cells (DCs) and macrophages from the tumour to the TDLN immediately after NIR-PIT. This migration by NIR-PIT was abrogated by inhibiting the sphingosine-1-phosphate pathway or Gαi signaling. These results were corroborated by intranodal immune cell profiles at two days post-treatment; NIR-PIT significantly induced DC maturation and increased and activated the CD8+ T cell population in the TDLN. Furthermore, PACT revealed that NIR-PIT significantly enhanced the migration of CD8+ T cells from the TDLN to the tumour four days post-treatment, which was consistent with the immunohistochemical assessment of tumour-infiltrating lymphocytes and tumour regression. Interpretation: Immune cells dramatically migrated between the tumour and TDLN following NIR-PIT, indicating its potential as an immune-stimulating therapy. Also, PACT is potentially applicable to a wide range of immunological research. Funding: This work was supported by the Intramural Research Program of the National Institutes of Health, National Cancer Institute, Centre for Cancer Research (grant number: ZIA BC011513 and ZIA BC011506).
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spelling doaj.art-1f65c025b2264b8093f63a4ce5821a252024-04-11T04:41:25ZengElsevierEBioMedicine2352-39642024-04-01102105050Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in contextHiroshi Fukushima0Aki Furusawa1Seiichiro Takao2Siddharth S. Matikonda3Makoto Kano4Shuhei Okuyama5Hiroshi Yamamoto6Peter L. Choyke7Martin J. Schnermann8Hisataka Kobayashi9Molecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAChemical Biology Laboratory, Centre for Cancer Research, National Cancer Institute, NIH, Frederick, MD, 21702, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USAChemical Biology Laboratory, Centre for Cancer Research, National Cancer Institute, NIH, Frederick, MD, 21702, USAMolecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, Bethesda, MD, 20892, USA; Corresponding author. Molecular Imaging Branch, Centre for Cancer Research, National Cancer Institute, NIH, 10 Centre Drive, Bethesda, MD, 20892, USA.Summary: Background: Noninvasive in vivo cell tracking is valuable in understanding the mechanisms that enhance anti-cancer immunity. We have recently developed a new method called phototruncation-assisted cell tracking (PACT), that uses photoconvertible cell tracking technology to detect in vivo cell migration. This method has the advantages of not requiring genetic engineering of cells and employing tissue-penetrant near-infrared light. Methods: We applied PACT to monitor the migration of immune cells between a tumour and its tumour-draining lymph node (TDLN) after near-infrared photoimmunotherapy (NIR-PIT). Findings: PACT showed a significant increase in the migration of dendritic cells (DCs) and macrophages from the tumour to the TDLN immediately after NIR-PIT. This migration by NIR-PIT was abrogated by inhibiting the sphingosine-1-phosphate pathway or Gαi signaling. These results were corroborated by intranodal immune cell profiles at two days post-treatment; NIR-PIT significantly induced DC maturation and increased and activated the CD8+ T cell population in the TDLN. Furthermore, PACT revealed that NIR-PIT significantly enhanced the migration of CD8+ T cells from the TDLN to the tumour four days post-treatment, which was consistent with the immunohistochemical assessment of tumour-infiltrating lymphocytes and tumour regression. Interpretation: Immune cells dramatically migrated between the tumour and TDLN following NIR-PIT, indicating its potential as an immune-stimulating therapy. Also, PACT is potentially applicable to a wide range of immunological research. Funding: This work was supported by the Intramural Research Program of the National Institutes of Health, National Cancer Institute, Centre for Cancer Research (grant number: ZIA BC011513 and ZIA BC011506).http://www.sciencedirect.com/science/article/pii/S2352396424000859CyanineImmune cell migrationNear-infrared photoimmunotherapyPhototruncationTumour-draining lymph node
spellingShingle Hiroshi Fukushima
Aki Furusawa
Seiichiro Takao
Siddharth S. Matikonda
Makoto Kano
Shuhei Okuyama
Hiroshi Yamamoto
Peter L. Choyke
Martin J. Schnermann
Hisataka Kobayashi
Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context
EBioMedicine
Cyanine
Immune cell migration
Near-infrared photoimmunotherapy
Phototruncation
Tumour-draining lymph node
title Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context
title_full Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context
title_fullStr Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context
title_full_unstemmed Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context
title_short Phototruncation cell tracking with near-infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsResearch in context
title_sort phototruncation cell tracking with near infrared photoimmunotherapy using heptamethine cyanine dye to visualise migratory dynamics of immune cellsresearch in context
topic Cyanine
Immune cell migration
Near-infrared photoimmunotherapy
Phototruncation
Tumour-draining lymph node
url http://www.sciencedirect.com/science/article/pii/S2352396424000859
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