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New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies

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A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Cellular Pathology".

Deadline for manuscript submissions: closed (30 June 2023) | Viewed by 23453

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Prof. Dr. Julia Bar

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Department of Immunopathology and Molecular Biology, Wroclaw Medical University, Wroclaw, Poland
Interests: stem cell biology; regenerative medicine; immunopathology; molecular biology; cancer stem cells biology
Special Issues, Collections and Topics in MDPI journals

Dr. Nina Zidar

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Guest Editor

Institute of Pathology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia
Interests: epithelial-mesenchymal transition; colorectal carcinoma; precancerosis and carcinoma of the head and neck; inflammatory bowel disease; organ fibrosis
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Dr. Piotr Cierpikowski

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Guest Editor

Department of Maxillofacial Surgery, The Ludwik Rydygier Specialist Hospital, Krakow, Poland
Interests: head and neck cancer; maxillofacial surgery; prognostic biomarkers; cancer biology; immunohistochemistry
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Head and neck cancer is a heterogenous malignancy with high mortality and increasing incidence worldwide. Late diagnosis, rapid tumor growth, poor response to radiochemotherapy and early local recurrence are still key challenges in modern treatment. Growing evidence suggests that the highly aggressive behaviour of head and neck cancer may be an effect of cancer stem cells and abnormalities in the signaling pathways associated with them. Despite recent advances in therapeutic strategies, the 5-year survival rate has remained the same in the last decades at about 50%. For this reason, further studies elucidating head and neck cancer biology are urgently required to improve the survival of patients.

We are delighted to present this Special Issue of Cells that is focused on the latest advances and future trends in the diagnosis, prognosis and treatment of head and neck cancer. This Special Issue will present original research articles as well as up-to-date review papers that show cellular and molecular mechanisms of head and neck cancer and, in particular, new specific biomarkers or potential therapy targets that may allow us to better stratify the prognosis of patients and improve their clinical outcome. We would like to encourage head and neck cancer researchers around the world to submit their manuscripts to this Special Issue.

Prof. Dr. Julia Bar
Dr. Nina Zidar
Dr. Piotr Cierpikowski
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cells is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

head and neck cancer
oral cancer
biomarker
prognosis
carcinogenesis
oral premalignant lesions
cancer stem cells
signaling pathways
molecular targeted therapy

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Related Special Issue

New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies II in Cells (1 article)

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Research

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20 pages, 4861 KiB

Open AccessArticle

The Effect of Xevinapant Combined with Ionizing Radiation on HNSCC and Normal Tissue Cells and the Impact of Xevinapant on Its Targeted Proteins cIAP1 and XIAP

by Julia Fleischmann, Laura S. Hildebrand, Lukas Kuhlmann, Rainer Fietkau and Luitpold V. Distel

Cells 2023, 12(12), 1653; https://doi.org/10.3390/cells12121653 - 17 Jun 2023

Cited by 2 | Viewed by 2261

Abstract

The poor prognosis of HNSCC is partly due to treatment resistance. The SMAC mimetic Xevinapant is a promising new approach to targeted cancer therapy. Xevinapant inhibits cIAP1/2 and XIAP, leading to apoptosis, necroptosis and inhibition of prosurvival signaling. Combining Xevinapant with IR could improve therapeutic potential. The effect of Xevinapant in combination with IR on HNSCC and healthy tissue cells was investigated. Cell growth, cell death, clonogenic survival and DNA double-strand breaks (DSBs) were studied, and intracellular cIAP1 and XIAP levels were evaluated. Xevinapant had cytostatic and cytotoxic, as well as radiosensitizing, effects on the malignant cells, while healthy tissue cells were less affected. Apoptotic and necrotic cell death was particularly affected, but the increase in residual DSBs and the reduced survival implied an additional effect of Xevinapant on DNA damage repair and other cell inactivation mechanisms. cIAP1 and XIAP levels varied for each cell line and were affected by Xevinapant and IR treatment. There was an association between higher IAP levels and increased cell death. Xevinapant appears to be a potent new drug for HNSCC therapy, especially in combination with IR. IAP levels could be an indicator for impaired DNA damage repair and increased susceptibility to cellular stress. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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14 pages, 4038 KiB

Open AccessArticle

ATM Inhibition-Induced ISG15/IFI27/OASL Is Correlated with Immunotherapy Response and Inflamed Immunophenotype

by Chi-Han Huang, Yun-Cian Huang, Jun-Kai Xu, Si-Yun Chen, Lu-Chia Tseng, Jau-Ling Huang and Chang-Shen Lin

Cells 2023, 12(9), 1288; https://doi.org/10.3390/cells12091288 - 30 Apr 2023

Cited by 5 | Viewed by 2231

Abstract

Immune checkpoint blockade (ICB) therapy can improve the survival of cancer patients with a high tumor mutation burden (TMB-H) or deficiency in DNA mismatch repair (dMMR) in their tumors. However, most cancer patients without TMB-H and dMMR do not benefit from ICB therapy. The inhibition of ATM can increase DNA damage and activate the interferon response, thus modulating the tumor immune microenvironment (TIME) and the efficacy of ICB therapy. In this study, we showed that ATM inhibition activated interferon signaling and induced interferon-stimulated genes (ISGs) in cisplatin-resistant and parent cancer cells. The ISGs induced by ATM inhibition were correlated with survival in cancer patients who received ICB therapy. In oral cancer, high expressions of ISG15, IFI27, and OASL were associated with low expressions of ATM, the activation of inflamed immune pathways, and increased tumor-infiltrating scores of CD8+ T, natural killer, and dendritic cells. The high expressions of ISG15, IFI27, and OASL were also correlated with complete remission in patients with cervical cancer treated with cisplatin. These results suggest that ATM inhibition can induce the interferon response and inflamed TIME, which may benefit ICB therapy. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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23 pages, 8292 KiB

Open AccessArticle

Molecular Signature of Long Non-Coding RNA Associated with Areca Nut-Induced Head and Neck Cancer

by Hung-Han Huang, Guo-Rung You, Shang-Ju Tang, Joseph T. Chang and Ann-Joy Cheng

Cells 2023, 12(6), 873; https://doi.org/10.3390/cells12060873 - 11 Mar 2023

Cited by 4 | Viewed by 2075

Abstract

The areca nut is a high-risk carcinogen for head and neck cancer (HNC) patients in Southeast Asia. The underlying molecular mechanism of areca nut-induced HNC remains unclear, especially regarding the role of long non-coding RNA (lncRNA). This study employed a systemic strategy to identify lncRNA signatures related to areca nut-induced HNC. In total, 84 cancer-related lncRNAs were identified. Using a PCR array method, 28 lncRNAs were identified as being dysregulated in HNC cells treated with areca nut (17 upregulated and 11 downregulated). Using bioinformatics analysis of The Cancer Genome Atlas Head-Neck Squamous Cell Carcinoma (TCGA-HNSC) dataset, 45 lncRNAs were differentially expressed in tumor tissues from HNC patients (39 over- and 6 under-expressions). The integrated evaluation showed 10 lncRNAs dysregulated by the areca nut and altered expression in patients, suggesting that these panel molecules participate in areca nut-induced HNC. Five oncogenic (LUCAT1, MIR31HG, UCA1, HIF1A-AS2, and SUMO1P3) and tumor-suppressive (LINC00312) lncRNAs were independently validated, and three key molecules were further examined. Pathway prediction revealed that LUCAT1, UCA1, and MIR31HG modulate multiple oncogenic mechanisms, including stress response and cellular motility. Clinical assessment showed that these lncRNAs exhibited biomarker potentials in diagnosis (area under the curve = 0.815 for LUCAT1) and a worse prognosis (both p < 0.05, survival analysis). Cellular studies further demonstrated that MIR31HG facilitates areca nut-induced cancer progression, as silencing this molecule attenuated arecoline-induced invasion ability in HNC cells. This study identified lncRNA signatures that play a role in areca nut-induced HNC. These molecules may be further applied in risk assessment, diagnosis, prognosis, and therapeutics for areca nut-associated malignancies. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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18 pages, 4939 KiB

Open AccessArticle

Blocking EREG/GPX4 Sensitizes Head and Neck Cancer to Cetuximab through Ferroptosis Induction

by Aude Jehl, Ombline Conrad, Mickaël Burgy, Sophie Foppolo, Romain Vauchelles, Carole Ronzani, Nelly Etienne-Selloum, Marie-Pierre Chenard, Aurélien Danic, Thomas Dourlhes, Claire Thibault, Philippe Schultz, Monique Dontenwill and Sophie Martin

Cells 2023, 12(5), 733; https://doi.org/10.3390/cells12050733 - 24 Feb 2023

Cited by 8 | Viewed by 2679

Abstract

(1) Background: Epiregulin (EREG) is a ligand of EGFR and ErB4 involved in the development and the progression of various cancers including head and neck squamous cell carcinoma (HNSCC). Its overexpression in HNSCC is correlated with short overall survival and progression-free survival but predictive of tumors responding to anti-EGFR therapies. Besides tumor cells, macrophages and cancer-associated fibroblasts shed EREG in the tumor microenvironment to support tumor progression and to promote therapy resistance. Although EREG seems to be an interesting therapeutic target, no study has been conducted so far on the consequences of EREG invalidation regarding the behavior and response of HNSCC to anti-EGFR therapies and, more specifically, to cetuximab (CTX); (2) Methods: EREG was silenced in various HNSCC cell lines. The resulting phenotype (growth, clonogenic survival, apoptosis, metabolism, ferroptosis) was assessed in the absence or presence of CTX. The data were confirmed in patient-derived tumoroids; (3) Results: Here, we show that EREG invalidation sensitizes cells to CTX. This is illustrated by the reduction in cell survival, the alteration of cell metabolism associated with mitochondrial dysfunction and the initiation of ferroptosis characterized by lipid peroxidation, iron accumulation and the loss of GPX4. Combining ferroptosis inducers (RSL3 and metformin) with CTX drastically reduces the survival of HNSCC cells but also HNSCC patient-derived tumoroids; (4) Conclusions: The loss of EREG might be considered in clinical settings as a predictive biomarker for patients that might undergo ferroptosis in response to CTX and that might benefit the most from the combination of ferroptosis inducers and CTX. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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11 pages, 448 KiB

Open AccessCommunication

An Inflammatory Signature to Predict the Clinical Benefit of First-Line Cetuximab Plus Platinum-Based Chemotherapy in Recurrent/Metastatic Head and Neck Cancer

by Stefano Cavalieri, Mara Serena Serafini, Andrea Carenzo, Silvana Canevari, Deborah Lenoci, Federico Pistore, Rosalba Miceli, Stefania Vecchio, Daris Ferrari, Cecilia Moro, Andrea Sponghini, Alessia Caldara, Maria Cossu Rocca, Simona Secondino, Gabriella Moretti, Nerina Denaro, Francesco Caponigro, Emanuela Vaccher, Gaetana Rinaldi, Francesco Ferraù, Paolo Bossi, Lisa Licitra and Loris De Cecco Show full author list Hide full author list

Cells 2022, 11(19), 3176; https://doi.org/10.3390/cells11193176 - 10 Oct 2022

Viewed by 1962

Abstract

Epidermal growth factor receptor (EGFR) pathway has been shown to play a crucial role in several inflammatory conditions and host immune-inflammation status is related to tumor prognosis. This study aims to evaluate the prognostic significance of a four-gene inflammatory signature in recurrent/metastatic (R/M) head and neck squamous cell carcinoma (HNSCC) patients treated with the EGFR inhibitor cetuximab plus chemotherapy. The inflammatory signature was assessed on 123 R/M HNSCC patients, enrolled in the multicenter trial B490 receiving first-line cetuximab plus platinum-based chemotherapy. The primary endpoint of the study was progression free survival (PFS), while secondary endpoints were overall survival (OS) and objective response rate (ORR). The patient population was subdivided into 3 groups according to the signature score groups. The four-genes-signature proved a significant prognostic value, resulting in a median PFS of 9.2 months in patients with high vs. 6.2 months for intermediate vs. 3.9 months for low values (p = 0.0016). The same findings were confirmed for OS, with median time of 18.4, 13.4, and 7.5 months for high, intermediate, and low values of the score, respectively (p = 0.0001). When ORR was considered, the signature was significantly higher in responders than in non-responders (p = 0.0092), reaching an area under the curve (AUC) of 0.65 (95% CI: 0.55–0.75). Our findings highlight the role of inflammation in the response to cetuximab and chemotherapy in R/M-HNSCC and may have translational implications for improving treatment selection. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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14 pages, 5144 KiB

Open AccessArticle

Thyroid Hormone Induces Oral Cancer Growth via the PD-L1-Dependent Signaling Pathway

by Kuan-Wei Su, Hung-Yun Lin, Hsien-Chung Chiu, Shin-Yu Shen, Chun A. ChangOu, Dana R. Crawford, Yu-Chen S. H. Yang, Ya-Jung Shih, Zi-Lin Li, Haw-Ming Huang, Jaqueline Whang-Peng, Yih Ho and Kuan Wang

Cells 2022, 11(19), 3050; https://doi.org/10.3390/cells11193050 - 29 Sep 2022

Cited by 3 | Viewed by 2066

Abstract

Oral cancer is a fatal disease, and its incidence in Taiwan is increasing. Thyroid hormone as L-thyroxine (T₄) stimulates cancer cell proliferation via a receptor on integrin αvβ3 of plasma membranes. It also induces the expression of programmed death-ligand 1 (PD-L1) and cell proliferation in cancer cells. Thyroid hormone also activates β-catenin-dependent cell proliferation in cancer cells. However, the relationship between PD-L1 and cancer proliferation is not fully understood. In the current study, we investigated the role of inducible thyroid hormone-induced PD-L1-regulated gene expression and proliferation in oral cancer cells. Thyroxine bound to integrin αvβ3 to induce PD-L1 expressions via activation of ERK1/2 and signal transducer and activator of transcription 3 (STAT3). Inactivated STAT3 inhibited PD-L1 expression and nuclear PD-L1 accumulation. Inhibition of PD-L1 expression reduced β-catenin accumulation. Furthermore, nuclear PD-L1 formed a complex with nuclear proteins such as p300. Suppression PD-L1 expression by shRNA blocked not only expression of PD-L1 and β-catenin but also signal transduction, proliferative gene expressions, and cancer cell growth. In summary, thyroxine via integrin αvβ3 activated ERK1/2 and STAT3 to stimulate the PD-L1-dependent and β-catenin-related growth in oral cancer cells. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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Review

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29 pages, 2197 KiB

Open AccessReview

The Role of Hedgehog Signaling Pathway in Head and Neck Squamous Cell Carcinoma

by Piotr Cierpikowski, Anna Leszczyszyn and Julia Bar

Cells 2023, 12(16), 2083; https://doi.org/10.3390/cells12162083 - 17 Aug 2023

Cited by 8 | Viewed by 1682

Abstract

Head and neck squamous cell carcinoma (HNSCC) is the sixth leading malignancy worldwide, with a poor prognosis and limited treatment options. Molecularly targeted therapies for HNSCC are still lacking. However, recent reports provide novel insights about many molecular alterations in HNSCC that may be useful in future therapies. Therefore, it is necessary to identify new biomarkers that may provide a better prediction of the disease and promising targets for personalized therapy. The poor response of HNSCC to therapy is attributed to a small population of tumor cells called cancer stem cells (CSCs). Growing evidence indicates that the Hedgehog (HH) signaling pathway plays a crucial role in the development and maintenance of head and neck tissues. The HH pathway is normally involved in embryogenesis, stem cell renewal, and tissue regeneration. However, abnormal activation of the HH pathway is also associated with carcinogenesis and CSC regulation. Overactivation of the HH pathway was observed in several tumors, including basal cell carcinoma, that are successfully treated with HH inhibitors. However, clinical studies about HH pathways in HNSCC are still rare. In this review, we summarize the current knowledge and recent advances regarding the HH pathway in HNSCC and discuss its possible implications for prognosis and future therapy. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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27 pages, 996 KiB

Open AccessReview

RNA-Based Liquid Biopsy in Head and Neck Cancer

by Jacek Kabzinski, Aleksandra Kucharska-Lusina and Ireneusz Majsterek

Cells 2023, 12(14), 1916; https://doi.org/10.3390/cells12141916 - 23 Jul 2023

Cited by 7 | Viewed by 1887

Abstract

Head and neck cancer (HNC) is a prevalent and diverse group of malignancies with substantial morbidity and mortality rates. Early detection and monitoring of HNC are crucial for improving patient outcomes. Liquid biopsy, a non-invasive diagnostic approach, has emerged as a promising tool for cancer detection and monitoring. In this article, we review the application of RNA-based liquid biopsy in HNC. Various types of RNA, including messenger RNA (mRNA), microRNA (miRNA), long non-coding RNA (lncRNA), small nuclear RNA (snRNA), small nucleolar RNA (snoRNA), circular RNA (circRNA) and PIWI-interacting RNA (piRNA), are explored as potential biomarkers in HNC liquid-based diagnostics. The roles of RNAs in HNC diagnosis, metastasis, tumor resistance to radio and chemotherapy, and overall prognosis are discussed. RNA-based liquid biopsy holds great promise for the early detection, prognosis, and personalized treatment of HNC. Further research and validation are necessary to translate these findings into clinical practice and improve patient outcomes. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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14 pages, 671 KiB

Open AccessReview

Human β-Defensins in Diagnosis of Head and Neck Cancers

by Jenna Kompuinen, Mutlu Keskin, Dogukan Yilmaz, Mervi Gürsoy and Ulvi Kahraman Gürsoy

Cells 2023, 12(6), 830; https://doi.org/10.3390/cells12060830 - 7 Mar 2023

Cited by 3 | Viewed by 2020

Abstract

Head and neck cancers are malignant growths with high death rates, which makes the early diagnosis of the affected patients of utmost importance. Over 90% of oral cavity cancers come from squamous cells, and the tongue, oral cavity, and salivary glands are the most common locations for oral squamous cell carcinoma lesions. Human β-defensins (hBDs), which are mainly produced by epithelial cells, are cationic peptides with a wide antimicrobial spectrum. In addition to their role in antimicrobial defense, these peptides also take part in the regulation of the immune response. Recent studies produced evidence that these small antimicrobial peptides are related to the gene and protein expression profiles of tumors. While the suppression of hBDs is a common finding in head and neck cancer studies, opposite findings were also presented. In the present narrative review, the aim will be to discuss the changes in the hBD expression profile during the onset and progression of head and neck cancers. The final aim will be to discuss the use of hBDs as diagnostic markers of head and neck cancers. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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16 pages, 1703 KiB

Open AccessSystematic Review

Systematic Review of Roles of Arecoline and Arecoline N-Oxide in Oral Cancer and Strategies to Block Carcinogenesis

by Albert Min-Shan Ko, Hung-Pin Tu and Ying-Chin Ko

Cells 2023, 12(8), 1208; https://doi.org/10.3390/cells12081208 - 21 Apr 2023

Cited by 16 | Viewed by 2799

Abstract

Betel quid and areca nut are complex mixture carcinogens, but little is known about whether their derived single-agent arecoline or arecoline N-oxide (ANO) is carcinogenic, and the underlying mechanisms remain unclear. In this systematic review, we analyzed recent studies on the roles of arecoline and ANO in cancer and strategies to block carcinogenesis. In the oral cavity, flavin-containing monooxygenase 3 oxidizes arecoline to ANO, and both alkaloids conjugate with N-acetylcysteine to form mercapturic acid compounds, which are excreted in urine, reducing arecoline and ANO toxicity. However, detoxification may not be complete. Arecoline and ANO upregulated protein expression in oral cancer tissue from areca nut users compared to expression levels in adjacent normal tissue, suggesting a causal relationship between these compounds and oral cancer. Sublingual fibrosis, hyperplasia, and oral leukoplakia were diagnosed in mice subjected to oral mucosal smearing of ANO. ANO is more cytotoxic and genotoxic than arecoline. During carcinogenesis and metastasis, these compounds increase the expression of epithelial–mesenchymal transition (EMT) inducers such as reactive oxygen species, transforming growth factor-β1, Notch receptor-1, and inflammatory cytokines, and they activate EMT-related proteins. Arecoline-induced epigenetic markers such as sirtuin-1 hypermethylation, low protein expression of miR-22, and miR-886-3-p accelerate oral cancer progression. Antioxidants and targeted inhibitors of the EMT inducers used reduce the risk of oral cancer development and progression. Our review findings substantiate the association of arecoline and ANO with oral cancer. Both of these single compounds are likely carcinogenic to humans, and their mechanisms and pathways of carcinogenesis are useful indicators for cancer therapy and prognosis. Full article

(This article belongs to the Special Issue New Trends and Advances in Diagnosis and Prognosis of Head and Neck Cancer from Carcinogenesis to Future Molecular Targeted Therapies)

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