Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types

ABSTRACT Background Metastasis is the major cause of cancer‐related mortality. The premetastatic niche is a promising target for its prevention. However, the generality and cellular dynamics in premetastatic niche formation have remained unclear. Aims This study aimed to elucidate the generality and...

Full description

Saved in:
Bibliographic Details
Main Authors: Shigeaki Sugiyama, Kanae Yumimoto, Keiichi I. Nakayama
Format: Article
Language:English
Published: Wiley 2025-01-01
Series:Cancer Medicine
Subjects:
Online Access:https://doi.org/10.1002/cam4.70557
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1841543393971273728
author Shigeaki Sugiyama
Kanae Yumimoto
Keiichi I. Nakayama
author_facet Shigeaki Sugiyama
Kanae Yumimoto
Keiichi I. Nakayama
author_sort Shigeaki Sugiyama
collection DOAJ
description ABSTRACT Background Metastasis is the major cause of cancer‐related mortality. The premetastatic niche is a promising target for its prevention. However, the generality and cellular dynamics in premetastatic niche formation have remained unclear. Aims This study aimed to elucidate the generality and cellular dynamics in premetastatic niche formation. Materials and Methods We performed comprehensive flow cytometric analysis of lung and peripheral immune cells at three time points (early premetastatic, late premetastatic, and micrometastatic phases) for mice with subcutaneous implants of three types of cancer cells (breast cancer, lung cancer, or melanoma cells). The immuno‐cell profiles were then used to predict the metastatic phase by machine learning. Results We found a common pattern of changes in both lung and peripheral immune cell profiles across the three cancer types, including a decrease in the proportion of eosinophils in the early premetastatic phase, an increase in that of regulatory T cells in the late premetastatic phase, and an increase in that of polymorphonuclear myeloid‐derived suppressor cells and a decrease in that of B cells in the micrometastatic phase. Machine learning using immune cell profiles could predict the metastatic phase with approximately 75% accuracy. Discussion Validation of our findings in humans will require data on the presence or absence of micrometastases in patients and the accumulation of comprehensive and temporal information on immune cells. In addition, blood proteins, extracellular vesicles, DNA, RNA, or metabolites may be useful for more accurate prediction. Conclusion The discovery of generalities in premetastatic niche formation allow prediction of metastatic phase and provide a basis for the development of methods for early detection and prevention of cancer metastasis in a cancer type‐independent manner.
format Article
id doaj-art-25b26120a0734e1787c44b60b91f70d4
institution Kabale University
issn 2045-7634
language English
publishDate 2025-01-01
publisher Wiley
record_format Article
series Cancer Medicine
spelling doaj-art-25b26120a0734e1787c44b60b91f70d42025-01-13T13:22:38ZengWileyCancer Medicine2045-76342025-01-01141n/an/a10.1002/cam4.70557Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer TypesShigeaki Sugiyama0Kanae Yumimoto1Keiichi I. Nakayama2Department of Molecular and Cellular Biology Medical Institute of Bioregulation, Kyushu University Fukuoka JapanDepartment of Molecular and Cellular Biology Medical Institute of Bioregulation, Kyushu University Fukuoka JapanDepartment of Molecular and Cellular Biology Medical Institute of Bioregulation, Kyushu University Fukuoka JapanABSTRACT Background Metastasis is the major cause of cancer‐related mortality. The premetastatic niche is a promising target for its prevention. However, the generality and cellular dynamics in premetastatic niche formation have remained unclear. Aims This study aimed to elucidate the generality and cellular dynamics in premetastatic niche formation. Materials and Methods We performed comprehensive flow cytometric analysis of lung and peripheral immune cells at three time points (early premetastatic, late premetastatic, and micrometastatic phases) for mice with subcutaneous implants of three types of cancer cells (breast cancer, lung cancer, or melanoma cells). The immuno‐cell profiles were then used to predict the metastatic phase by machine learning. Results We found a common pattern of changes in both lung and peripheral immune cell profiles across the three cancer types, including a decrease in the proportion of eosinophils in the early premetastatic phase, an increase in that of regulatory T cells in the late premetastatic phase, and an increase in that of polymorphonuclear myeloid‐derived suppressor cells and a decrease in that of B cells in the micrometastatic phase. Machine learning using immune cell profiles could predict the metastatic phase with approximately 75% accuracy. Discussion Validation of our findings in humans will require data on the presence or absence of micrometastases in patients and the accumulation of comprehensive and temporal information on immune cells. In addition, blood proteins, extracellular vesicles, DNA, RNA, or metabolites may be useful for more accurate prediction. Conclusion The discovery of generalities in premetastatic niche formation allow prediction of metastatic phase and provide a basis for the development of methods for early detection and prevention of cancer metastasis in a cancer type‐independent manner.https://doi.org/10.1002/cam4.70557diagnosismachine learningneoplasm metastasisprimary preventiontumor microenvironment
spellingShingle Shigeaki Sugiyama
Kanae Yumimoto
Keiichi I. Nakayama
Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types
Cancer Medicine
diagnosis
machine learning
neoplasm metastasis
primary prevention
tumor microenvironment
title Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types
title_full Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types
title_fullStr Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types
title_full_unstemmed Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types
title_short Immune Cell Profiling Reveals a Common Pattern in Premetastatic Niche Formation Across Various Cancer Types
title_sort immune cell profiling reveals a common pattern in premetastatic niche formation across various cancer types
topic diagnosis
machine learning
neoplasm metastasis
primary prevention
tumor microenvironment
url https://doi.org/10.1002/cam4.70557
work_keys_str_mv AT shigeakisugiyama immunecellprofilingrevealsacommonpatterninpremetastaticnicheformationacrossvariouscancertypes
AT kanaeyumimoto immunecellprofilingrevealsacommonpatterninpremetastaticnicheformationacrossvariouscancertypes
AT keiichiinakayama immunecellprofilingrevealsacommonpatterninpremetastaticnicheformationacrossvariouscancertypes