Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue
Abstract The 5-year survival rate for patients with oral squamous cell carcinomas (SCC), including tongue SCC, has not significantly improved over the last several decades. Oral potentially malignant disorders (OPMD), including oral dysplasias, are oral epithelial disorders that can develop into ora...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Springer
2023-02-01
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| Series: | Discover Oncology |
| Subjects: | |
| Online Access: | https://doi.org/10.1007/s12672-023-00629-y |
| _version_ | 1797864329796648960 |
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| author | Tuo Zhang David Kutler Theresa Scognamiglio Lorraine J. Gudas Xiao-Han Tang |
| author_facet | Tuo Zhang David Kutler Theresa Scognamiglio Lorraine J. Gudas Xiao-Han Tang |
| author_sort | Tuo Zhang |
| collection | DOAJ |
| description | Abstract The 5-year survival rate for patients with oral squamous cell carcinomas (SCC), including tongue SCC, has not significantly improved over the last several decades. Oral potentially malignant disorders (OPMD), including oral dysplasias, are oral epithelial disorders that can develop into oral SCCs. To identify molecular characteristics that might predict conversion of OPMDs to SCCs and guide treatment plans, we performed global transcriptomic analysis of human tongue OPMD (n = 9) and tongue SCC (n = 11) samples with paired normal margin tissue from patients treated at Weill Cornell Medicine. Compared to margin tissue, SCCs showed more transcript changes than OPMDs. OPMDs and SCCs shared some altered transcripts, but these changes were generally greater in SCCs than OPMDs. Both OPMDs and SCCs showed altered signaling pathways related to cell migration, basement membrane disruption, and metastasis. We suggest that OPMDs are on the path toward malignant transformation. Based on patterns of gene expression, both OPMD and tongue SCC samples can be categorized into subclasses (mesenchymal, classical, basal, and atypical) similar to those seen in human head and neck SCC (HNSCC). These subclasses of OPMDs have the potential to be used to stratify patient prognoses and therapeutic options for tongue OPMDs. Lastly, we identified a gene set (ELF5; RPTN; IGSF10; CRMP1; HTR3A) whose transcript changes have the power to classify OPMDs and SCCs and developed a Firth logistic regression model using the changes in these transcripts relative to paired normal tissue to validate pathological diagnosis and potentially predict the likelihood of an OPMD developing into SCC, as data sets become available. |
| first_indexed | 2024-04-09T22:50:04Z |
| format | Article |
| id | doaj.art-0fe8597c77f845b591ad5ae29a7fcb03 |
| institution | Directory Open Access Journal |
| issn | 2730-6011 |
| language | English |
| last_indexed | 2024-04-09T22:50:04Z |
| publishDate | 2023-02-01 |
| publisher | Springer |
| record_format | Article |
| series | Discover Oncology |
| spelling | doaj.art-0fe8597c77f845b591ad5ae29a7fcb032023-03-22T11:39:29ZengSpringerDiscover Oncology2730-60112023-02-0114111310.1007/s12672-023-00629-yTranscriptomic analysis predicts the risk of progression of premalignant lesions in human tongueTuo Zhang0David Kutler1Theresa Scognamiglio2Lorraine J. Gudas3Xiao-Han Tang4Genomics Resources Core Facility, Weill Cornell Medical College of Cornell UniversityDivision of Head and Neck Surgery in the Department of Otolaryngology at New York Presbyterian Hospital/Weill Cornell Medical CenterDivision of Anatomic Pathology, New York Presbyterian Hospital, Department of Pathology and Laboratory Medicine, Weill Cornell Medical College of Cornell UniversityDepartment of Pharmacology, Weill Cornell Medical College of Cornell UniversityDepartment of Pharmacology, Weill Cornell Medical College of Cornell UniversityAbstract The 5-year survival rate for patients with oral squamous cell carcinomas (SCC), including tongue SCC, has not significantly improved over the last several decades. Oral potentially malignant disorders (OPMD), including oral dysplasias, are oral epithelial disorders that can develop into oral SCCs. To identify molecular characteristics that might predict conversion of OPMDs to SCCs and guide treatment plans, we performed global transcriptomic analysis of human tongue OPMD (n = 9) and tongue SCC (n = 11) samples with paired normal margin tissue from patients treated at Weill Cornell Medicine. Compared to margin tissue, SCCs showed more transcript changes than OPMDs. OPMDs and SCCs shared some altered transcripts, but these changes were generally greater in SCCs than OPMDs. Both OPMDs and SCCs showed altered signaling pathways related to cell migration, basement membrane disruption, and metastasis. We suggest that OPMDs are on the path toward malignant transformation. Based on patterns of gene expression, both OPMD and tongue SCC samples can be categorized into subclasses (mesenchymal, classical, basal, and atypical) similar to those seen in human head and neck SCC (HNSCC). These subclasses of OPMDs have the potential to be used to stratify patient prognoses and therapeutic options for tongue OPMDs. Lastly, we identified a gene set (ELF5; RPTN; IGSF10; CRMP1; HTR3A) whose transcript changes have the power to classify OPMDs and SCCs and developed a Firth logistic regression model using the changes in these transcripts relative to paired normal tissue to validate pathological diagnosis and potentially predict the likelihood of an OPMD developing into SCC, as data sets become available.https://doi.org/10.1007/s12672-023-00629-yTongue squamous cell carcinomasOral potentially malignant disordersRNA-seqFirth logistic regression |
| spellingShingle | Tuo Zhang David Kutler Theresa Scognamiglio Lorraine J. Gudas Xiao-Han Tang Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue Discover Oncology Tongue squamous cell carcinomas Oral potentially malignant disorders RNA-seq Firth logistic regression |
| title | Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue |
| title_full | Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue |
| title_fullStr | Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue |
| title_full_unstemmed | Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue |
| title_short | Transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue |
| title_sort | transcriptomic analysis predicts the risk of progression of premalignant lesions in human tongue |
| topic | Tongue squamous cell carcinomas Oral potentially malignant disorders RNA-seq Firth logistic regression |
| url | https://doi.org/10.1007/s12672-023-00629-y |
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