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Published in: Journal of Translational Medicine 1/2023

Open Access 01-12-2023 | Research

Multi-omics characterization of a scoring system to quantify hypoxia patterns in patients with head and neck squamous cell carcinoma

Authors: Cong Peng, Huiping Ye, Zhengyang li, Xiaofeng Duan, Wen Yang, Zhuguang Yi

Published in: Journal of Translational Medicine | Issue 1/2023

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Abstract

Background

The 5-year survival rate of patients with head and neck squamous cell carcinoma (HNSCC) remains  < 50%. Hypoxia patterns are a hallmark of HNSCC that are associated with its occurrence and progression. However, the precise role of hypoxia during HNSCC, such as the relationship between hypoxia, tumor immune landscape and cell communication orchestration remains largely unknown. The current study integrated data from bulk and single-cell RNA sequencing analyses to define the relationship between hypoxia and HNSCC.

Methods

A scoring system named the hypoxia score (HS) was constructed based on hypoxia-related genes (HRGs) expression. The predictive value of HS response for patient outcomes and different treatments was evaluated. Single-cell datasets and cell communication were utilized to rule out cell populations which hypoxia targeted on.

Results

The survival outcomes, immune/Estimate scores, responses to targeted inhibitors, and chemotherapeutic, and immunotherapy responses were distinct between a high HS group and a low HS group (all P < 0.05). Single-cell datasets showed different distributions of HS in immune cell populations (P < 0.05). Furthermore, HLA-DPA1/CD4 axis was identified as a unique interaction between CD4 + T Conv and pDC cells.

Conclusions

Altogether, the quantification for hypoxia patterns is a potential biomarker for prognosis, individualized chemotherapeutic and immunotherapy strategies. The portrait of cell communication characteristics over the HNSCC ecosystem enhances the understanding of hypoxia patterns in HNSCC.
Appendix
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Literature
1.
go back to reference Sung H, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209-49. CrossRef Sung H, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209-49. CrossRef
2.
go back to reference Marur S, Forastiere AA. Head and Neck Squamous Cell Carcinoma: Update on Epidemiology, Diagnosis, and Treatment. Mayo Clin Proc. 2016;91(3):386-96. CrossRef Marur S, Forastiere AA. Head and Neck Squamous Cell Carcinoma: Update on Epidemiology, Diagnosis, and Treatment. Mayo Clin Proc. 2016;91(3):386-96. CrossRef
3.
go back to reference Kase S, Baburin A, Kuddu M, Innos K. Incidence and survival for head and neck cancers in Estonia, 1996–2016: a population-based study. Clin Epidemiol. 2021;13:149–59.CrossRef Kase S, Baburin A, Kuddu M, Innos K. Incidence and survival for head and neck cancers in Estonia, 1996–2016: a population-based study. Clin Epidemiol. 2021;13:149–59.CrossRef
4.
go back to reference Verdonck-de Leeuw IM, et al. The course of health-related quality of life in head and neck cancer patients treated with chemoradiation: a prospective cohort study. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2014;110:422–8.CrossRef Verdonck-de Leeuw IM, et al. The course of health-related quality of life in head and neck cancer patients treated with chemoradiation: a prospective cohort study. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2014;110:422–8.CrossRef
5.
go back to reference Osazuwa-Peters N, et al. Suicide risk among cancer survivors: head and neck versus other cancers. Cancer. 2018;124:4072–9.CrossRef Osazuwa-Peters N, et al. Suicide risk among cancer survivors: head and neck versus other cancers. Cancer. 2018;124:4072–9.CrossRef
6.
go back to reference Varadé J, Magadán S, González-Fernández Á. Human immunology and immunotherapy: main achievements and challenges. Cell Mol Immunol. 2021;18:805–28.CrossRef Varadé J, Magadán S, González-Fernández Á. Human immunology and immunotherapy: main achievements and challenges. Cell Mol Immunol. 2021;18:805–28.CrossRef
7.
go back to reference Johnson DE, et al. Head and neck squamous cell carcinoma. Nat Rev Dis Prim. 2020;6:92.CrossRef Johnson DE, et al. Head and neck squamous cell carcinoma. Nat Rev Dis Prim. 2020;6:92.CrossRef
8.
go back to reference Riera-Domingo C, et al. Immunity, hypoxia, and metabolism-the ménage à trois of cancer: implications for immunotherapy. Physiol Rev. 2020;100:1–102.CrossRef Riera-Domingo C, et al. Immunity, hypoxia, and metabolism-the ménage à trois of cancer: implications for immunotherapy. Physiol Rev. 2020;100:1–102.CrossRef
9.
go back to reference Elzakra N, Kim Y. HIF-1α metabolic pathways in human cancer. Adv Exp Med Biol. 2021;1280:243–60.CrossRef Elzakra N, Kim Y. HIF-1α metabolic pathways in human cancer. Adv Exp Med Biol. 2021;1280:243–60.CrossRef
10.
go back to reference Alsahafi E, et al. Clinical update on head and neck cancer: molecular biology and ongoing challenges. Cell Death Dis. 2019;10:540.CrossRef Alsahafi E, et al. Clinical update on head and neck cancer: molecular biology and ongoing challenges. Cell Death Dis. 2019;10:540.CrossRef
11.
go back to reference Mortezaee K, Majidpoor J. The impact of hypoxia on immune state in cancer. Life Sci. 2021;286:120057.CrossRef Mortezaee K, Majidpoor J. The impact of hypoxia on immune state in cancer. Life Sci. 2021;286:120057.CrossRef
12.
go back to reference Huan L, et al. Hypoxia induced LUCAT1/PTBP1 axis modulates cancer cell viability and chemotherapy response. Mol Cancer. 2020;19:11.CrossRef Huan L, et al. Hypoxia induced LUCAT1/PTBP1 axis modulates cancer cell viability and chemotherapy response. Mol Cancer. 2020;19:11.CrossRef
13.
go back to reference Wang Y-W, et al. A novel HIF1α-STIL-FOXM1 axis regulates tumor metastasis. J Biomed Sci. 2022;29:24.CrossRef Wang Y-W, et al. A novel HIF1α-STIL-FOXM1 axis regulates tumor metastasis. J Biomed Sci. 2022;29:24.CrossRef
14.
go back to reference Chen D, et al. Development and verification of the hypoxia- and immune-associated prognostic signature for pancreatic ductal adenocarcinoma. Front Immunol. 2021;12:728062.CrossRef Chen D, et al. Development and verification of the hypoxia- and immune-associated prognostic signature for pancreatic ductal adenocarcinoma. Front Immunol. 2021;12:728062.CrossRef
15.
go back to reference Feng X, et al. Hypoxia-induced acetylation of PAK1 enhances autophagy and promotes brain tumorigenesis via phosphorylating ATG5. Autophagy. 2021;17:723–42.CrossRef Feng X, et al. Hypoxia-induced acetylation of PAK1 enhances autophagy and promotes brain tumorigenesis via phosphorylating ATG5. Autophagy. 2021;17:723–42.CrossRef
16.
go back to reference Li S-R, Man Q-W, Liu B. Development and validation of a novel hypoxia-related signature for prognostic and immunogenic evaluation in head and neck squamous cell carcinoma. Front Oncol. 2022;12:1–19. Li S-R, Man Q-W, Liu B. Development and validation of a novel hypoxia-related signature for prognostic and immunogenic evaluation in head and neck squamous cell carcinoma. Front Oncol. 2022;12:1–19.
17.
go back to reference Korsunsky I, et al. Fast, sensitive and accurate integration of single-cell data with Harmony. Nat Methods. 2019;16:1289–96.CrossRef Korsunsky I, et al. Fast, sensitive and accurate integration of single-cell data with Harmony. Nat Methods. 2019;16:1289–96.CrossRef
18.
go back to reference Macosko EZ, et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell. 2015;161:1202–14.CrossRef Macosko EZ, et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell. 2015;161:1202–14.CrossRef
19.
go back to reference Zhang X, et al. Cell Marker: a manually curated resource of cell markers in human and mouse. Nucleic Acids Res. 2019;47:D721–8.CrossRef Zhang X, et al. Cell Marker: a manually curated resource of cell markers in human and mouse. Nucleic Acids Res. 2019;47:D721–8.CrossRef
20.
go back to reference Lambrechts D, et al. Phenotype molding of stromal cells in the lung tumor microenvironment. Nat Med. 2018;24:1277–89.CrossRef Lambrechts D, et al. Phenotype molding of stromal cells in the lung tumor microenvironment. Nat Med. 2018;24:1277–89.CrossRef
21.
go back to reference Mo Z, et al. Single-cell transcriptomics reveals the role of Macrophage-Naïve CD4 + T cell interaction in the immunosuppressive microenvironment of primary liver carcinoma. J Transl Med. 2022;20:466.CrossRef Mo Z, et al. Single-cell transcriptomics reveals the role of Macrophage-Naïve CD4 + T cell interaction in the immunosuppressive microenvironment of primary liver carcinoma. J Transl Med. 2022;20:466.CrossRef
22.
go back to reference Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics. 2010;26:1572–3.CrossRef Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics. 2010;26:1572–3.CrossRef
23.
go back to reference Hänzelmann S, Castelo R, Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics. 2013;14:7.CrossRef Hänzelmann S, Castelo R, Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics. 2013;14:7.CrossRef
24.
go back to reference Tang Y, Li C, Zhang YJ, Wu ZH. Ferroptosis-related long non-coding rna signature predicts the prognosis of head and neck squamous cell carcinoma. Int J Biol Sci. 2021;17:702–11.CrossRef Tang Y, Li C, Zhang YJ, Wu ZH. Ferroptosis-related long non-coding rna signature predicts the prognosis of head and neck squamous cell carcinoma. Int J Biol Sci. 2021;17:702–11.CrossRef
25.
go back to reference Tang Y, et al. Prognosis and dissection of immunosuppressive microenvironment in breast cancer based on fatty acid metabolism-related signature. Front Immunol. 2022;13:1–17. Tang Y, et al. Prognosis and dissection of immunosuppressive microenvironment in breast cancer based on fatty acid metabolism-related signature. Front Immunol. 2022;13:1–17.
26.
go back to reference Yoshihara K, et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat Commun. 2013;4:2612.CrossRef Yoshihara K, et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat Commun. 2013;4:2612.CrossRef
27.
go back to reference Li T, et al. TIMER: a web server for comprehensive analysis of tumor-infiltrating immune cells. Cancer Res. 2017;77:e108–10.CrossRef Li T, et al. TIMER: a web server for comprehensive analysis of tumor-infiltrating immune cells. Cancer Res. 2017;77:e108–10.CrossRef
28.
go back to reference Liu C-J, et al. GSCALite: a web server for gene set cancer analysis. Bioinformatics. 2018;34:3771–2.CrossRef Liu C-J, et al. GSCALite: a web server for gene set cancer analysis. Bioinformatics. 2018;34:3771–2.CrossRef
29.
go back to reference Geeleher P, Cox N, Huang RS. pRRophetic: an R package for prediction of clinical chemotherapeutic response from tumor gene expression levels. PLoS ONE. 2014;9:e107468.CrossRef Geeleher P, Cox N, Huang RS. pRRophetic: an R package for prediction of clinical chemotherapeutic response from tumor gene expression levels. PLoS ONE. 2014;9:e107468.CrossRef
30.
go back to reference Zhang H-C, et al. Identification and validation in a novel quantification system of ferroptosis patterns for the prediction of prognosis and immunotherapy response in left- and right-sided colon cancer. Front Immunol. 2022;13:1–16. Zhang H-C, et al. Identification and validation in a novel quantification system of ferroptosis patterns for the prediction of prognosis and immunotherapy response in left- and right-sided colon cancer. Front Immunol. 2022;13:1–16.
31.
go back to reference Jiang P, et al. Signatures of T cell dysfunction and exclusion predict cancer immunotherapy response. Nat Med. 2018;24:1550–8.CrossRef Jiang P, et al. Signatures of T cell dysfunction and exclusion predict cancer immunotherapy response. Nat Med. 2018;24:1550–8.CrossRef
32.
go back to reference Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.CrossRef Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.CrossRef
33.
go back to reference Yao Y, et al. CHCHD2 promotes hepatocellular carcinoma and indicates poor prognosis of hepatocellular carcinoma patients. J Cancer. 2019;10:6822–8.CrossRef Yao Y, et al. CHCHD2 promotes hepatocellular carcinoma and indicates poor prognosis of hepatocellular carcinoma patients. J Cancer. 2019;10:6822–8.CrossRef
34.
go back to reference Fu S, Chen X, Lo H-W, Lin J. Combined bazedoxifene and paclitaxel treatments inhibit cell viability, cell migration, colony formation, and tumor growth and induce apoptosis in breast cancer. Cancer Lett. 2019;448:11–9.CrossRef Fu S, Chen X, Lo H-W, Lin J. Combined bazedoxifene and paclitaxel treatments inhibit cell viability, cell migration, colony formation, and tumor growth and induce apoptosis in breast cancer. Cancer Lett. 2019;448:11–9.CrossRef
35.
go back to reference Mayakonda A, Lin D-C, Assenov Y, Plass C, Koeffler HP. Maftools: efficient and comprehensive analysis of somatic variants in cancer. Genome Res. 2018;28:1747–56.CrossRef Mayakonda A, Lin D-C, Assenov Y, Plass C, Koeffler HP. Maftools: efficient and comprehensive analysis of somatic variants in cancer. Genome Res. 2018;28:1747–56.CrossRef
36.
go back to reference Zhang H, Meltzer P, Davis S. RCircos: an R package for Circos 2D track plots. BMC Bioinformatics. 2013;14:244.CrossRef Zhang H, Meltzer P, Davis S. RCircos: an R package for Circos 2D track plots. BMC Bioinformatics. 2013;14:244.CrossRef
37.
go back to reference Krzywinska E, Stockmann C. Hypoxia metabolism and immune cell function. Biomedicines. 2018;6:56.CrossRef Krzywinska E, Stockmann C. Hypoxia metabolism and immune cell function. Biomedicines. 2018;6:56.CrossRef
38.
go back to reference Henze A-T, Mazzone M. The impact of hypoxia on tumor-associated macrophages. J Clin Invest. 2016;126:3672–9.CrossRef Henze A-T, Mazzone M. The impact of hypoxia on tumor-associated macrophages. J Clin Invest. 2016;126:3672–9.CrossRef
39.
go back to reference Troiano G, et al. Prognostic significance of CD68(+) and CD163(+) tumor associated macrophages in head and neck squamous cell carcinoma: a systematic review and meta-analysis. Oral Oncol. 2019;93:66–75.CrossRef Troiano G, et al. Prognostic significance of CD68(+) and CD163(+) tumor associated macrophages in head and neck squamous cell carcinoma: a systematic review and meta-analysis. Oral Oncol. 2019;93:66–75.CrossRef
40.
go back to reference Pylayeva-Gupta Y, Kelsey C, Mhatre VM, Ho JAL. The roles of mast cells in anticancer immunity Dyana. Bone. 2012;23:1–7. Pylayeva-Gupta Y, Kelsey C, Mhatre VM, Ho JAL. The roles of mast cells in anticancer immunity Dyana. Bone. 2012;23:1–7.
41.
go back to reference Manjili MH, Butler SE. Role of tregs in cancer dormancy or recurrence. Immunol Invest. 2016;45:759–66.CrossRef Manjili MH, Butler SE. Role of tregs in cancer dormancy or recurrence. Immunol Invest. 2016;45:759–66.CrossRef
42.
go back to reference Laska E, Meisner M, Wanderling J. A maximally selected test of symmetry about zero. Stat Med. 2012;31:3178–91.CrossRef Laska E, Meisner M, Wanderling J. A maximally selected test of symmetry about zero. Stat Med. 2012;31:3178–91.CrossRef
43.
go back to reference Fumet J-D, Truntzer C, Yarchoan M, Ghiringhelli F. Tumour mutational burden as a biomarker for immunotherapy: current data and emerging concepts. Eur J Cancer. 2020;131:40–50.CrossRef Fumet J-D, Truntzer C, Yarchoan M, Ghiringhelli F. Tumour mutational burden as a biomarker for immunotherapy: current data and emerging concepts. Eur J Cancer. 2020;131:40–50.CrossRef
44.
go back to reference Yin W, et al. Development and validation of a tumor mutation burden-related immune prognostic model for lower-grade glioma. Front Oncol. 2020;10:1409.CrossRef Yin W, et al. Development and validation of a tumor mutation burden-related immune prognostic model for lower-grade glioma. Front Oncol. 2020;10:1409.CrossRef
45.
go back to reference Eder T, et al. Interference of tumour mutational burden with outcome of patients with head and neck cancer treated with definitive chemoradiation: a multicentre retrospective study of the German Cancer Consortium Radiation Oncology Group. Eur J Cancer. 2019;116:67–76.CrossRef Eder T, et al. Interference of tumour mutational burden with outcome of patients with head and neck cancer treated with definitive chemoradiation: a multicentre retrospective study of the German Cancer Consortium Radiation Oncology Group. Eur J Cancer. 2019;116:67–76.CrossRef
46.
go back to reference Liu J, et al. Development of an oxidative phosphorylation-related and immune microenvironment prognostic signature in uterine corpus endometrial carcinoma. Front cell Dev Biol. 2021;9:753004.CrossRef Liu J, et al. Development of an oxidative phosphorylation-related and immune microenvironment prognostic signature in uterine corpus endometrial carcinoma. Front cell Dev Biol. 2021;9:753004.CrossRef
47.
go back to reference Yin X, Xia J, Sun Y, Zhang Z. CHCHD2 is a potential prognostic factor for NSCLC and is associated with HIF-1a expression. BMC Pulm Med. 2020;20:40.CrossRef Yin X, Xia J, Sun Y, Zhang Z. CHCHD2 is a potential prognostic factor for NSCLC and is associated with HIF-1a expression. BMC Pulm Med. 2020;20:40.CrossRef
48.
go back to reference Kindt N, Lechien JR, Nonclercq D, Laurent G, Saussez S. Involvement of CD74 in head and neck squamous cell carcinomas. J Cancer Res Clin Oncol. 2014;140:937–47.CrossRef Kindt N, Lechien JR, Nonclercq D, Laurent G, Saussez S. Involvement of CD74 in head and neck squamous cell carcinomas. J Cancer Res Clin Oncol. 2014;140:937–47.CrossRef
49.
go back to reference Zhu G, et al. HIF-α/MIF and NF-κB/IL-6 axes contribute to the recruitment of CD11b+Gr-1+ myeloid cells in hypoxic microenvironment of HNSCC. Neoplasia. 2014;16:168–79.CrossRef Zhu G, et al. HIF-α/MIF and NF-κB/IL-6 axes contribute to the recruitment of CD11b+Gr-1+ myeloid cells in hypoxic microenvironment of HNSCC. Neoplasia. 2014;16:168–79.CrossRef
50.
go back to reference Axelrod ML, Cook RS, Johnson DB, Balko JM. Biological consequences of MHC-II expression by tumor cells in cancer. Clin cancer Res. 2019;25:2392–402.CrossRef Axelrod ML, Cook RS, Johnson DB, Balko JM. Biological consequences of MHC-II expression by tumor cells in cancer. Clin cancer Res. 2019;25:2392–402.CrossRef
51.
go back to reference Accolla RS, Ramia E, Tedeschi A, Forlani G. CIITA-driven MHC class II expressing tumor cells as antigen presenting cell performers: toward the construction of an optimal anti-tumor vaccine. Front Immunol. 2019;10:1806.CrossRef Accolla RS, Ramia E, Tedeschi A, Forlani G. CIITA-driven MHC class II expressing tumor cells as antigen presenting cell performers: toward the construction of an optimal anti-tumor vaccine. Front Immunol. 2019;10:1806.CrossRef
52.
go back to reference He Y, et al. MHC class II expression in lung cancer. Lung Cancer. 2017;112:75–80.CrossRef He Y, et al. MHC class II expression in lung cancer. Lung Cancer. 2017;112:75–80.CrossRef
53.
go back to reference Schaafsma E, Fugle CM, Wang X, Cheng C. Pan-cancer association of HLA gene expression with cancer prognosis and immunotherapy efficacy. Br J Cancer. 2021;125:422–32.CrossRef Schaafsma E, Fugle CM, Wang X, Cheng C. Pan-cancer association of HLA gene expression with cancer prognosis and immunotherapy efficacy. Br J Cancer. 2021;125:422–32.CrossRef
54.
go back to reference Oh DY, et al. Intratumoral CD4(+) T cells mediate anti-tumor cytotoxicity in human bladder cancer. Cell. 2020;181:1612-1625.e13.CrossRef Oh DY, et al. Intratumoral CD4(+) T cells mediate anti-tumor cytotoxicity in human bladder cancer. Cell. 2020;181:1612-1625.e13.CrossRef
55.
go back to reference Bi Q, et al. Predicted CD4(+) T cell infiltration levels could indicate better overall survival in sarcoma patients. J Int Med Res. 2021;49:300060520981539.CrossRef Bi Q, et al. Predicted CD4(+) T cell infiltration levels could indicate better overall survival in sarcoma patients. J Int Med Res. 2021;49:300060520981539.CrossRef
56.
go back to reference Wang H, Zheng L. Construction of a hypoxia-derived gene model to predict the prognosis and therapeutic response of head and neck squamous cell carcinoma. Sci Rep. 2022;12:1–11. Wang H, Zheng L. Construction of a hypoxia-derived gene model to predict the prognosis and therapeutic response of head and neck squamous cell carcinoma. Sci Rep. 2022;12:1–11.
57.
go back to reference Multhoff G, Vaupel P. Hypoxia compromises anti-cancer immune responses. Adv Exp Med Biol. 2020;1232:131–43.CrossRef Multhoff G, Vaupel P. Hypoxia compromises anti-cancer immune responses. Adv Exp Med Biol. 2020;1232:131–43.CrossRef
58.
go back to reference Zandberg DP, et al. Tumor hypoxia is associated with resistance to PD-1 blockade in squamous cell carcinoma of the head and neck. J Immunother cancer. 2021;9:e002088.CrossRef Zandberg DP, et al. Tumor hypoxia is associated with resistance to PD-1 blockade in squamous cell carcinoma of the head and neck. J Immunother cancer. 2021;9:e002088.CrossRef
59.
go back to reference Song C, et al. Hypoxia-targeting multifunctional nanoparticles for sensitized chemotherapy and phototherapy in head and neck squamous cell carcinoma. Int J Nanomedicine. 2020;15:347–61.CrossRef Song C, et al. Hypoxia-targeting multifunctional nanoparticles for sensitized chemotherapy and phototherapy in head and neck squamous cell carcinoma. Int J Nanomedicine. 2020;15:347–61.CrossRef
60.
go back to reference Wang Z, et al. Ferroptosis activation scoring model assists in chemotherapeutic agents’ selection and mediates cross-talk with immunocytes in malignant glioblastoma. Front Immunol. 2022;12:1–16.CrossRef Wang Z, et al. Ferroptosis activation scoring model assists in chemotherapeutic agents’ selection and mediates cross-talk with immunocytes in malignant glioblastoma. Front Immunol. 2022;12:1–16.CrossRef
61.
go back to reference Wang Z, et al. Multi-omics characterization of a glycerolipid metabolism-related gene enrichment score in colon cancer. Front Oncol. 2022;12:1–11. Wang Z, et al. Multi-omics characterization of a glycerolipid metabolism-related gene enrichment score in colon cancer. Front Oncol. 2022;12:1–11.
62.
go back to reference Lyu F, et al. Identification of ISG15 and ZFP36 as novel hypoxia- and immune-related gene signatures contributing to a new perspective for the treatment of prostate cancer by bioinformatics and experimental verification. J Transl Med. 2022;20:202.CrossRef Lyu F, et al. Identification of ISG15 and ZFP36 as novel hypoxia- and immune-related gene signatures contributing to a new perspective for the treatment of prostate cancer by bioinformatics and experimental verification. J Transl Med. 2022;20:202.CrossRef
63.
go back to reference Vasseur S, et al. DJ-1/PARK7 is an important mediator of hypoxia-induced cellular responses. Proc Natl Acad Sci U S A. 2009;106:1111–6.CrossRef Vasseur S, et al. DJ-1/PARK7 is an important mediator of hypoxia-induced cellular responses. Proc Natl Acad Sci U S A. 2009;106:1111–6.CrossRef
64.
go back to reference Ji Z-H, et al. Identification of immune-related biomarkers associated with tumorigenesis and prognosis in skin cutaneous melanoma. Am J Cancer Res. 2022;12:1727–39. Ji Z-H, et al. Identification of immune-related biomarkers associated with tumorigenesis and prognosis in skin cutaneous melanoma. Am J Cancer Res. 2022;12:1727–39.
Metadata
Title
Multi-omics characterization of a scoring system to quantify hypoxia patterns in patients with head and neck squamous cell carcinoma
Authors
Cong Peng
Huiping Ye
Zhengyang li
Xiaofeng Duan
Wen Yang
Zhuguang Yi
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2023
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-022-03869-8

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