Immune Signature-Based Subtypes of Cervical Squamous Cell Carcinoma Tightly Associated with Human Papillomavirus Type 16 Expression, Molecular Features, and Clinical Outcome

Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype of cervical cancer, cervical squamous cell carcinoma (CSCC), is poorly characterized regarding the association between its heterogeneity and...

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Published in:	Neoplasia (New York, N.Y.) Vol. 21; no. 6; pp. 591 - 601
Main Authors:	Lu, Xiaofan, Jiang, Liyun, Zhang, Liya, Zhu, Yue, Hu, Wenjun, Wang, Jiashuo, Ruan, Xinjia, Xu, Zhengbao, Meng, Xiaowei, Gao, Jun, Su, Xiaoping, Yan, Fangrong
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 01.06.2019 Elsevier
Subjects:	Adult Carcinoma, Squamous Cell - classification Carcinoma, Squamous Cell - genetics Carcinoma, Squamous Cell - pathology Carcinoma, Squamous Cell - virology Class I Phosphatidylinositol 3-Kinases - genetics DNA Methylation - genetics F-Box-WD Repeat-Containing Protein 7 - genetics Female Gene Expression Regulation, Neoplastic - genetics Human papillomavirus 16 - genetics Human papillomavirus 16 - pathogenicity Humans Kaplan-Meier Estimate Keratin-1 - genetics Middle Aged Mucin-4 - genetics Oncogene Proteins, Viral - genetics Papillomavirus E7 Proteins - genetics Papillomavirus Infections - genetics Papillomavirus Infections - immunology Papillomavirus Infections - pathology Papillomavirus Infections - virology Progression-Free Survival Repressor Proteins - genetics Signal Transduction - genetics Uterine Cervical Neoplasms - classification Uterine Cervical Neoplasms - genetics Uterine Cervical Neoplasms - pathology Uterine Cervical Neoplasms - virology ρ CGI CI GO GSEA HR CESC FPKM TCGA HPV CSCC FDR IC50
ISSN:	1476-5586, 1476-5586
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Abstract	Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype of cervical cancer, cervical squamous cell carcinoma (CSCC), is poorly characterized regarding the association between its heterogeneity and HPV oncoprotein expression. We filtered out 138 CSCC samples with infection of HPV16 only as the first step; then we compressed HPV16 E6/E7 expression as HPVpca and correlated HPVpca with the immunological profiling of CSCC based on supervised clustering to discover subtypes and to characterize the differences between subgroups in terms of the HPVpca level, pathway activity, epigenetic dysregulation, somatic mutation frequencies, and likelihood of responding to chemo/immunotherapies. Supervised clustering of immune signatures revealed two HPV16 subtypes (namely, HPV16-IMM and HPV16-KRT) that correlated with HPVpca and clinical outcomes. HPV16-KRT is characterized by elevated expression of genes in keratinization, biological oxidation, and Wnt signaling, whereas HPV16-IMM has a strong immune response and mesenchymal features. HPV16-IMM exhibited much more epigenetic silencing and significant mutation at FBXW7, while MUC4 and PIK3CA were mutated frequently for HPV16-KRT. We also imputed that HPV16-IMM is much more sensitive to chemo/immunotherapy than is HPV16-KRT. Our characterization tightly links the expression of HPV16 E6/E7 with biological and clinical outcomes of CSCC, providing valuable molecular-level information that points to decoding heterogeneity. Together, these results shed light on stratifications of CSCC infected by HPV16 and shall help to guide personalized management and treatment of patients.
AbstractList	Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype of cervical cancer, cervical squamous cell carcinoma (CSCC), is poorly characterized regarding the association between its heterogeneity and HPV oncoprotein expression. We filtered out 138 CSCC samples with infection of HPV16 only as the first step; then we compressed HPV16 E6/E7 expression as HPVpca and correlated HPVpca with the immunological profiling of CSCC based on supervised clustering to discover subtypes and to characterize the differences between subgroups in terms of the HPVpca level, pathway activity, epigenetic dysregulation, somatic mutation frequencies, and likelihood of responding to chemo/immunotherapies. Supervised clustering of immune signatures revealed two HPV16 subtypes (namely, HPV16-IMM and HPV16-KRT) that correlated with HPVpca and clinical outcomes. HPV16-KRT is characterized by elevated expression of genes in keratinization, biological oxidation, and Wnt signaling, whereas HPV16-IMM has a strong immune response and mesenchymal features. HPV16-IMM exhibited much more epigenetic silencing and significant mutation at FBXW7, while MUC4 and PIK3CA were mutated frequently for HPV16-KRT. We also imputed that HPV16-IMM is much more sensitive to chemo/immunotherapy than is HPV16-KRT. Our characterization tightly links the expression of HPV16 E6/E7 with biological and clinical outcomes of CSCC, providing valuable molecular-level information that points to decoding heterogeneity. Together, these results shed light on stratifications of CSCC infected by HPV16 and shall help to guide personalized management and treatment of patients. Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype of cervical cancer, cervical squamous cell carcinoma (CSCC), is poorly characterized regarding the association between its heterogeneity and HPV oncoprotein expression. We filtered out 138 CSCC samples with infection of HPV16 only as the first step; then we compressed HPV16 E6/E7 expression as HPVpca and correlated HPVpca with the immunological profiling of CSCC based on supervised clustering to discover subtypes and to characterize the differences between subgroups in terms of the HPVpca level, pathway activity, epigenetic dysregulation, somatic mutation frequencies, and likelihood of responding to chemo/immunotherapies. Supervised clustering of immune signatures revealed two HPV16 subtypes (namely, HPV16-IMM and HPV16-KRT) that correlated with HPVpca and clinical outcomes. HPV16-KRT is characterized by elevated expression of genes in keratinization, biological oxidation, and Wnt signaling, whereas HPV16-IMM has a strong immune response and mesenchymal features. HPV16-IMM exhibited much more epigenetic silencing and significant mutation at FBXW7, while MUC4 and PIK3CA were mutated frequently for HPV16-KRT. We also imputed that HPV16-IMM is much more sensitive to chemo/immunotherapy than is HPV16-KRT. Our characterization tightly links the expression of HPV16 E6/E7 with biological and clinical outcomes of CSCC, providing valuable molecular-level information that points to decoding heterogeneity. Together, these results shed light on stratifications of CSCC infected by HPV16 and shall help to guide personalized management and treatment of patients.Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype of cervical cancer, cervical squamous cell carcinoma (CSCC), is poorly characterized regarding the association between its heterogeneity and HPV oncoprotein expression. We filtered out 138 CSCC samples with infection of HPV16 only as the first step; then we compressed HPV16 E6/E7 expression as HPVpca and correlated HPVpca with the immunological profiling of CSCC based on supervised clustering to discover subtypes and to characterize the differences between subgroups in terms of the HPVpca level, pathway activity, epigenetic dysregulation, somatic mutation frequencies, and likelihood of responding to chemo/immunotherapies. Supervised clustering of immune signatures revealed two HPV16 subtypes (namely, HPV16-IMM and HPV16-KRT) that correlated with HPVpca and clinical outcomes. HPV16-KRT is characterized by elevated expression of genes in keratinization, biological oxidation, and Wnt signaling, whereas HPV16-IMM has a strong immune response and mesenchymal features. HPV16-IMM exhibited much more epigenetic silencing and significant mutation at FBXW7, while MUC4 and PIK3CA were mutated frequently for HPV16-KRT. We also imputed that HPV16-IMM is much more sensitive to chemo/immunotherapy than is HPV16-KRT. Our characterization tightly links the expression of HPV16 E6/E7 with biological and clinical outcomes of CSCC, providing valuable molecular-level information that points to decoding heterogeneity. Together, these results shed light on stratifications of CSCC infected by HPV16 and shall help to guide personalized management and treatment of patients. Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype of cervical cancer, cervical squamous cell carcinoma (CSCC), is poorly characterized regarding the association between its heterogeneity and HPV oncoprotein expression. We filtered out 138 CSCC samples with infection of HPV16 only as the first step; then we compressed HPV16 E6/E7 expression as HPV and correlated HPV with the immunological profiling of CSCC based on supervised clustering to discover subtypes and to characterize the differences between subgroups in terms of the HPV level, pathway activity, epigenetic dysregulation, somatic mutation frequencies, and likelihood of responding to chemo/immunotherapies. Supervised clustering of immune signatures revealed two HPV16 subtypes (namely, HPV16-IMM and HPV16-KRT) that correlated with HPV and clinical outcomes. HPV16-KRT is characterized by elevated expression of genes in keratinization, biological oxidation, and Wnt signaling, whereas HPV16-IMM has a strong immune response and mesenchymal features. HPV16-IMM exhibited much more epigenetic silencing and significant mutation at FBXW7, while MUC4 and PIK3CA were mutated frequently for HPV16-KRT. We also imputed that HPV16-IMM is much more sensitive to chemo/immunotherapy than is HPV16-KRT. Our characterization tightly links the expression of HPV16 E6/E7 with biological and clinical outcomes of CSCC, providing valuable molecular-level information that points to decoding heterogeneity. Together, these results shed light on stratifications of CSCC infected by HPV16 and shall help to guide personalized management and treatment of patients.
Author	Ruan, Xinjia Meng, Xiaowei Hu, Wenjun Yan, Fangrong Zhu, Yue Xu, Zhengbao Lu, Xiaofan Wang, Jiashuo Jiang, Liyun Zhang, Liya Gao, Jun Su, Xiaoping
Author_xml	– sequence: 1 givenname: Xiaofan surname: Lu fullname: Lu, Xiaofan organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 2 givenname: Liyun surname: Jiang fullname: Jiang, Liyun organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 3 givenname: Liya surname: Zhang fullname: Zhang, Liya organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 4 givenname: Yue surname: Zhu fullname: Zhu, Yue organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 5 givenname: Wenjun surname: Hu fullname: Hu, Wenjun organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 6 givenname: Jiashuo surname: Wang fullname: Wang, Jiashuo organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 7 givenname: Xinjia surname: Ruan fullname: Ruan, Xinjia organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 8 givenname: Zhengbao surname: Xu fullname: Xu, Zhengbao organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 9 givenname: Xiaowei surname: Meng fullname: Meng, Xiaowei organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 10 givenname: Jun surname: Gao fullname: Gao, Jun organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China – sequence: 11 givenname: Xiaoping surname: Su fullname: Su, Xiaoping email: xsu1@mdanderson.org organization: Department of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX – sequence: 12 givenname: Fangrong surname: Yan fullname: Yan, Fangrong email: f.r.yan@163.com organization: Research Center of Biostatistics and Computational Pharmacy, China Pharmaceutical University, Nanjing, PR, China
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PublicationTitle	Neoplasia (New York, N.Y.)
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Publisher	Elsevier Inc Elsevier
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10.1016/j.neo.2019.04.003_bb0225 article-title: Integrated molecular analysis of tumour biopsies on sequential CTLA-4 and PD-1 blockade reveals markers of response and resistance publication-title: Sci Transl Med doi: 10.1126/scitranslmed.aah3560 – volume: 29 start-page: 266 year: 2012 ident: 10.1016/j.neo.2019.04.003_bb0110 article-title: VirusSeq: software to identify viruses and their integration sites using next-generation sequencing of human cancer tissue publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts665 – volume: 37 start-page: 319 year: 2005 ident: 10.1016/j.neo.2019.04.003_bb0045 article-title: The role of HPV E6 and E7 oncoproteins in HPV-associated cervical carcinogenesis publication-title: Cancer Res Treat doi: 10.4143/crt.2005.37.6.319 – volume: 6 start-page: 1279 year: 2014 ident: 10.1016/j.neo.2019.04.003_bb0210 article-title: Epithelial-mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer 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Snippet	Substantial heterogeneity exists within cervical cancer that is generally infected by human papillomavirus (HPV). However, the most common histological subtype...
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SubjectTerms	Adult Carcinoma, Squamous Cell - classification Carcinoma, Squamous Cell - genetics Carcinoma, Squamous Cell - pathology Carcinoma, Squamous Cell - virology Class I Phosphatidylinositol 3-Kinases - genetics DNA Methylation - genetics F-Box-WD Repeat-Containing Protein 7 - genetics Female Gene Expression Regulation, Neoplastic - genetics Human papillomavirus 16 - genetics Human papillomavirus 16 - pathogenicity Humans Kaplan-Meier Estimate Keratin-1 - genetics Middle Aged Mucin-4 - genetics Oncogene Proteins, Viral - genetics Papillomavirus E7 Proteins - genetics Papillomavirus Infections - genetics Papillomavirus Infections - immunology Papillomavirus Infections - pathology Papillomavirus Infections - virology Progression-Free Survival Repressor Proteins - genetics Signal Transduction - genetics Uterine Cervical Neoplasms - classification Uterine Cervical Neoplasms - genetics Uterine Cervical Neoplasms - pathology Uterine Cervical Neoplasms - virology
Title	Immune Signature-Based Subtypes of Cervical Squamous Cell Carcinoma Tightly Associated with Human Papillomavirus Type 16 Expression, Molecular Features, and Clinical Outcome
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