Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis

Abstract Background Lymphatic metastasis is the major challenge in the treatment of penile cancer. The prognosis of individuals with lymphatic metastasis is extremely poor. Therefore, early identification of disease progression and lymphatic metastasis is an urgent task for researchers in penile can...

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Main Authors: Da‐Ming Xu, Xiao‐Yu Zhuang, Hua‐Li Ma, Zai‐Shang Li, Li‐Chao Wei, Jun‐Hang Luo, Hui Han
Format: Article
Language:English
Published: Wiley 2024-07-01
Series:Cancer Medicine
Subjects:
Online Access:https://doi.org/10.1002/cam4.70025
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author Da‐Ming Xu
Xiao‐Yu Zhuang
Hua‐Li Ma
Zai‐Shang Li
Li‐Chao Wei
Jun‐Hang Luo
Hui Han
author_facet Da‐Ming Xu
Xiao‐Yu Zhuang
Hua‐Li Ma
Zai‐Shang Li
Li‐Chao Wei
Jun‐Hang Luo
Hui Han
author_sort Da‐Ming Xu
collection DOAJ
description Abstract Background Lymphatic metastasis is the major challenge in the treatment of penile cancer. The prognosis of individuals with lymphatic metastasis is extremely poor. Therefore, early identification of disease progression and lymphatic metastasis is an urgent task for researchers in penile cancer worldwide. Methods In this study, using single‐cell RNA sequencing, an immune landscape was established for the cancer ecosystem based on 46,861 cells from six patients with penile cancer (four with lymphatic metastasis [stage IV] and two without lymphatic metastasis [stage I]). Using bulk RNA sequencing, the discrepancy between the cancers and their respective metastatic lymph nodes was depicted based on seven patients with penile cancer. Results The interaction between epithelial cells, fibroblasts, and endothelial cells, and the functional cooperation among invasion, epithelial‐mesenchymal transition, and angiogenesis were found to be important landscapes in the penile cancer ecosystem, playing important roles in progression of cancer and lymph node metastasis. Conclusions This study is the first to investigate the altered tumor microenvironment heterogeneity of penile cancer as it evolves from non‐lymphatic to lymphatic metastasis and provides insights into the mechanisms underlying malignant progression, the premetastatic niche, and lymphatic metastasis in penile cancer.
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spelling doaj-art-cfb38915d1f84f3fb6f3348e6906b9972025-08-20T01:58:16ZengWileyCancer Medicine2045-76342024-07-011314n/an/a10.1002/cam4.70025Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasisDa‐Ming Xu0Xiao‐Yu Zhuang1Hua‐Li Ma2Zai‐Shang Li3Li‐Chao Wei4Jun‐Hang Luo5Hui Han6State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer Sun Yat‐sen University Cancer Center Guangzhou P. R. ChinaDepartment of Anesthesiology Second Affiliated Hospital of Shantou University Medical College Shantou P. R. ChinaState Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer Sun Yat‐sen University Cancer Center Guangzhou P. R. ChinaDepartment of Urology, Shenzhen People's Hospital The Second Clinic Medical College of Jinan University Shenzhen P. R. ChinaState Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer Sun Yat‐sen University Cancer Center Guangzhou P. R. ChinaDepartment of Urology, First Affiliated Hospital Sun Yat‐sen University Guangzhou P. R. ChinaState Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer Sun Yat‐sen University Cancer Center Guangzhou P. R. ChinaAbstract Background Lymphatic metastasis is the major challenge in the treatment of penile cancer. The prognosis of individuals with lymphatic metastasis is extremely poor. Therefore, early identification of disease progression and lymphatic metastasis is an urgent task for researchers in penile cancer worldwide. Methods In this study, using single‐cell RNA sequencing, an immune landscape was established for the cancer ecosystem based on 46,861 cells from six patients with penile cancer (four with lymphatic metastasis [stage IV] and two without lymphatic metastasis [stage I]). Using bulk RNA sequencing, the discrepancy between the cancers and their respective metastatic lymph nodes was depicted based on seven patients with penile cancer. Results The interaction between epithelial cells, fibroblasts, and endothelial cells, and the functional cooperation among invasion, epithelial‐mesenchymal transition, and angiogenesis were found to be important landscapes in the penile cancer ecosystem, playing important roles in progression of cancer and lymph node metastasis. Conclusions This study is the first to investigate the altered tumor microenvironment heterogeneity of penile cancer as it evolves from non‐lymphatic to lymphatic metastasis and provides insights into the mechanisms underlying malignant progression, the premetastatic niche, and lymphatic metastasis in penile cancer.https://doi.org/10.1002/cam4.70025lymphatic metastasismalignant progressionpenile cancerpremetastatic nichetumor microenvironment
spellingShingle Da‐Ming Xu
Xiao‐Yu Zhuang
Hua‐Li Ma
Zai‐Shang Li
Li‐Chao Wei
Jun‐Hang Luo
Hui Han
Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis
Cancer Medicine
lymphatic metastasis
malignant progression
penile cancer
premetastatic niche
tumor microenvironment
title Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis
title_full Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis
title_fullStr Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis
title_full_unstemmed Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis
title_short Altered tumor microenvironment heterogeneity of penile cancer during progression from non‐lymphatic to lymphatic metastasis
title_sort altered tumor microenvironment heterogeneity of penile cancer during progression from non lymphatic to lymphatic metastasis
topic lymphatic metastasis
malignant progression
penile cancer
premetastatic niche
tumor microenvironment
url https://doi.org/10.1002/cam4.70025
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