Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma

Head and neck squamous cell carcinoma (HNSCC) usually has a poor prognosis and is associated with a high mortality rate. Its etiology is mainly the result from long-term exposure to either alcohol, tobacco or human papillomavirus (HPV) infection or a combination of these insults. However, HNSCC pati...

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Main Authors: Lingzhang Meng, Heming Lu, Yueyong Li, Jingjie Zhao, Siyuan He, Zechen Wang, Jiajia Shen, Huixian Huang, Jinru Xiao, Suren Rao Sooranna, Jian Song
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.1013542/full
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author Lingzhang Meng
Lingzhang Meng
Heming Lu
Heming Lu
Yueyong Li
Jingjie Zhao
Siyuan He
Zechen Wang
Jiajia Shen
Huixian Huang
Huixian Huang
Jinru Xiao
Suren Rao Sooranna
Jian Song
Jian Song
author_facet Lingzhang Meng
Lingzhang Meng
Heming Lu
Heming Lu
Yueyong Li
Jingjie Zhao
Siyuan He
Zechen Wang
Jiajia Shen
Huixian Huang
Huixian Huang
Jinru Xiao
Suren Rao Sooranna
Jian Song
Jian Song
author_sort Lingzhang Meng
collection DOAJ
description Head and neck squamous cell carcinoma (HNSCC) usually has a poor prognosis and is associated with a high mortality rate. Its etiology is mainly the result from long-term exposure to either alcohol, tobacco or human papillomavirus (HPV) infection or a combination of these insults. However, HNSCC patients with HPV have been found to show a survival advantage over those without the virus, but the mechanism that confers this advantage is unclear. Due to the large number of HPV-independent HNSCC cases, there is a possibility that the difference in prognosis between HPV-positive (HPV+) and negative (HPV-) patients is due to different carcinogens. To clarify this, we used scRNA data and viral tracking methods in order to identify HPV+ and HPV- cells in the tumour tissues of patients infected with HPV. By comparing HPV+ and HPV- malignant cells, we found a higher level of tumour stemness in HPV- tumour cells. Using tumour stemness-related genes, we established a six-gene prognostic signature that was used to divide the patients into low- and high-risk groups. It was found that HPV patients who were at low-risk of contracting HNSCC had a higher number of CD8+ T-cells as well as a higher expression of immune checkpoint molecules. Correspondingly, we found that HPV+ tumour cells expressed higher levels of CCL4, and these were highly correlated with CD8+ T cells infiltration and immune checkpoint molecules. These data suggest that the stemness features of tumour cells are not only associated with the prognostic risk, but that it could also affect the immune cell interactions and associated signalling pathways.
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spelling doaj.art-09cf746ffa5e40cf85f3e6e4cde2d4e42022-12-22T03:39:59ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-11-011310.3389/fimmu.2022.10135421013542Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinomaLingzhang Meng0Lingzhang Meng1Heming Lu2Heming Lu3Yueyong Li4Jingjie Zhao5Siyuan He6Zechen Wang7Jiajia Shen8Huixian Huang9Huixian Huang10Jinru Xiao11Suren Rao Sooranna12Jian Song13Jian Song14Institute of Cardiovascular Sciences, Guangxi Academy of Medical Sciences, Nanning, ChinaCenter for Systemic Inflammation Research (CSIR), School of Preclinical Medicine, Youjiang Medical University for Nationalities, Baise, ChinaSecond Division of Department of Radiation Oncology, Guangxi Academy of Medical Sciences, Nanning, ChinaSecond Division of Department of Radiation Oncology, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, ChinaDepartment of Interventive Medicine, The Affiliated Hospital of Youjiang Medical University for Nationalities, Baise, ChinaLife Science and Clinical Research Center, Affiliated Hospital of Youjiang Medical University for Nationalities, Baise, ChinaCenter for Systemic Inflammation Research (CSIR), School of Preclinical Medicine, Youjiang Medical University for Nationalities, Baise, ChinaCenter for Systemic Inflammation Research (CSIR), School of Preclinical Medicine, Youjiang Medical University for Nationalities, Baise, ChinaCenter for Systemic Inflammation Research (CSIR), School of Preclinical Medicine, Youjiang Medical University for Nationalities, Baise, ChinaSecond Division of Department of Radiation Oncology, Guangxi Academy of Medical Sciences, Nanning, ChinaSecond Division of Department of Radiation Oncology, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, ChinaGraduate School, Guangxi University of Chinese Medicine, Nanning, ChinaDepartment of Metabolism, Digestion and Reproduction, Imperial College London, Chelsea & Westminster Hospital, London, United KingdomInstitute of Cardiovascular Sciences, Guangxi Academy of Medical Sciences, Nanning, ChinaCenter for Systemic Inflammation Research (CSIR), School of Preclinical Medicine, Youjiang Medical University for Nationalities, Baise, ChinaHead and neck squamous cell carcinoma (HNSCC) usually has a poor prognosis and is associated with a high mortality rate. Its etiology is mainly the result from long-term exposure to either alcohol, tobacco or human papillomavirus (HPV) infection or a combination of these insults. However, HNSCC patients with HPV have been found to show a survival advantage over those without the virus, but the mechanism that confers this advantage is unclear. Due to the large number of HPV-independent HNSCC cases, there is a possibility that the difference in prognosis between HPV-positive (HPV+) and negative (HPV-) patients is due to different carcinogens. To clarify this, we used scRNA data and viral tracking methods in order to identify HPV+ and HPV- cells in the tumour tissues of patients infected with HPV. By comparing HPV+ and HPV- malignant cells, we found a higher level of tumour stemness in HPV- tumour cells. Using tumour stemness-related genes, we established a six-gene prognostic signature that was used to divide the patients into low- and high-risk groups. It was found that HPV patients who were at low-risk of contracting HNSCC had a higher number of CD8+ T-cells as well as a higher expression of immune checkpoint molecules. Correspondingly, we found that HPV+ tumour cells expressed higher levels of CCL4, and these were highly correlated with CD8+ T cells infiltration and immune checkpoint molecules. These data suggest that the stemness features of tumour cells are not only associated with the prognostic risk, but that it could also affect the immune cell interactions and associated signalling pathways.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1013542/fullhuman papillomavirussingle cell transcriptomichead and neck squamous cell carcinomatumour stemnesstumour infiltrating immune cellsimmune checkpoint genes
spellingShingle Lingzhang Meng
Lingzhang Meng
Heming Lu
Heming Lu
Yueyong Li
Jingjie Zhao
Siyuan He
Zechen Wang
Jiajia Shen
Huixian Huang
Huixian Huang
Jinru Xiao
Suren Rao Sooranna
Jian Song
Jian Song
Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma
Frontiers in Immunology
human papillomavirus
single cell transcriptomic
head and neck squamous cell carcinoma
tumour stemness
tumour infiltrating immune cells
immune checkpoint genes
title Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma
title_full Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma
title_fullStr Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma
title_full_unstemmed Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma
title_short Human papillomavirus infection can alter the level of tumour stemness and T cell infiltration in patients with head and neck squamous cell carcinoma
title_sort human papillomavirus infection can alter the level of tumour stemness and t cell infiltration in patients with head and neck squamous cell carcinoma
topic human papillomavirus
single cell transcriptomic
head and neck squamous cell carcinoma
tumour stemness
tumour infiltrating immune cells
immune checkpoint genes
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.1013542/full
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