Autoencoder-based multimodal prediction of non-small cell lung cancer survival.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
22 09 2023
Historique:
received: 18 04 2023
accepted: 09 09 2023
medline: 25 9 2023
pubmed: 22 9 2023
entrez: 22 9 2023
Statut: epublish

Résumé

The ability to accurately predict non-small cell lung cancer (NSCLC) patient survival is crucial for informing physician decision-making, and the increasing availability of multi-omics data offers the promise of enhancing prognosis predictions. We present a multimodal integration approach that leverages microRNA, mRNA, DNA methylation, long non-coding RNA (lncRNA) and clinical data to predict NSCLC survival and identify patient subtypes, utilizing denoising autoencoders for data compression and integration. Survival performance for patients with lung adenocarcinoma (LUAD) and squamous cell carcinoma (LUSC) was compared across modality combinations and data integration methods. Using The Cancer Genome Atlas data, our results demonstrate that survival prediction models combining multiple modalities outperform single modality models. The highest performance was achieved with a combination of only two modalities, lncRNA and clinical, at concordance indices (C-indices) of 0.69 ± 0.03 for LUAD and 0.62 ± 0.03 for LUSC. Models utilizing all five modalities achieved mean C-indices of 0.67 ± 0.04 and 0.63 ± 0.02 for LUAD and LUSC, respectively, while the best individual modality performance reached C-indices of 0.64 ± 0.03 for LUAD and 0.59 ± 0.03 for LUSC. Analysis of biological differences revealed two distinct survival subtypes with over 900 differentially expressed transcripts.

Identifiants

pubmed: 37737469
doi: 10.1038/s41598-023-42365-x
pii: 10.1038/s41598-023-42365-x
pmc: PMC10517020
doi:

Substances chimiques

RNA, Long Noncoding 0
MicroRNAs 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

15761

Informations de copyright

© 2023. Springer Nature Limited.

Références

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. 71, 209–249 (2021).
pubmed: 33538338
Lee, B. et al. DeepBTS: Prediction of recurrence-free survival of non-small cell lung cancer using a time-binned deep neural network. Sci. Rep. 10, 1952 (2020).
pubmed: 32029785 pmcid: 7005286
Wang, J. et al. SurvNet: A novel deep neural network for lung cancer survival analysis with missing values. Front. Oncol. https://doi.org/10.3389/fonc.2020.588990 (2021).
doi: 10.3389/fonc.2020.588990 pubmed: 35769548 pmcid: 8739965
Sun, Z., Wigle, D. A. & Yang, P. Non-overlapping and non-cell-type-specific gene expression signatures predict lung cancer survival. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 26, 877–883 (2008).
Zou, X., Hu, Z., Huang, C. & Chang, J. A seven-gene signature with close immune correlation was identified for survival prediction of lung adenocarcinoma. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 26, e924269-1-e924269-18 (2020).
Zhu, W., Xie, L., Han, J. & Guo, X. The application of deep learning in cancer prognosis prediction. Cancers 12, 603 (2020).
pubmed: 32150991 pmcid: 7139576
Cheerla, A. & Gevaert, O. Deep learning with multimodal representation for pancancer prognosis prediction. Bioinformatics 35, i446–i454 (2019).
pubmed: 31510656 pmcid: 6612862
Vale-Silva, L. A. & Rohr, K. Long-term cancer survival prediction using multimodal deep learning. Sci. Rep. 11, 13505 (2021).
pubmed: 34188098 pmcid: 8242026
Lai, Y.-H. et al. Overall survival prediction of non-small cell lung cancer by integrating microarray and clinical data with deep learning. Sci. Rep. 10, 4679 (2020).
pubmed: 32170141 pmcid: 7069964
Takahashi, S. et al. Predicting deep learning based multi-omics parallel integration survival subtypes in lung cancer using reverse phase protein array data. Biomolecules 10, 1460 (2020).
pubmed: 33086649 pmcid: 7603376
Asada, K. et al. Uncovering prognosis-related genes and pathways by multi-omics analysis in lung cancer. Biomolecules 10, 524 (2020).
pubmed: 32235589 pmcid: 7225957
Huang, S.-C., Pareek, A., Seyyedi, S., Banerjee, I. & Lungren, M. P. Fusion of medical imaging and electronic health records using deep learning: A systematic review and implementation guidelines. NPJ Digit. Med. 3, 1–9 (2020).
Picard, M., Scott-Boyer, M.-P., Bodein, A., Périn, O. & Droit, A. Integration strategies of multi-omics data for machine learning analysis. Comput. Struct. Biotechnol. J. 19, 3735–3746 (2021).
pubmed: 34285775 pmcid: 8258788
Lipkova, J. et al. Artificial intelligence for multimodal data integration in oncology. Cancer Cell 40, 1095–1110 (2022).
pubmed: 36220072
Alexe, G., Dalgin, G. S., Ganesan, S., Delisi, C. & Bhanot, G. Analysis of breast cancer progression using principal component analysis and clustering. J. Biosci. 32, 1027–1039 (2007).
pubmed: 17914245
Chaudhary, K., Poirion, O. B., Lu, L. & Garmire, L. X. Deep Learning based multi-omics integration robustly predicts survival in liver cancer. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 24, 1248–1259 (2018).
Baldi, P. Autoencoders, unsupervised learning and deep architectures. In Proceedings of the 2011 International Conference on Unsupervised and Transfer Learning workshop - Volume 27 37–50 (JMLR.org, 2011).
Wang, J. et al. Denoising autoencoder, a deep learning algorithm, aids the identification of a novel molecular signature of lung adenocarcinoma. Genom. Proteom. Bioinform. https://doi.org/10.1016/j.gpb.2019.02.003 (2020).
doi: 10.1016/j.gpb.2019.02.003
Chai, H. et al. Integrating multi-omics data through deep learning for accurate cancer prognosis prediction. Comput. Biol. Med. 134, 104481 (2021).
pubmed: 33989895
Vincent, P., Larochelle, H., Bengio, Y. & Manzagol, P.-A. Extracting and composing robust features with denoising autoencoders. In Proceedings of the 25th international conference on Machine learning - ICML ’08 1096–1103 (ACM Press, 2008). https://doi.org/10.1145/1390156.1390294
He, R. & Zuo, S. A robust 8-gene prognostic signature for early-stage non-small cell lung cancer. Front. Oncol. https://doi.org/10.3389/fonc.2019.00693 (2019).
doi: 10.3389/fonc.2019.00693 pubmed: 32083015 pmcid: 6930197
Rousseeuw, P. J. Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20, 53–65 (1987).
Stares, M. et al. Hypoalbuminaemia as a prognostic biomarker of first-line treatment resistance in metastatic non-small cell lung cancer. Front. Nutr. https://doi.org/10.3389/fnut.2021.734735 (2021).
doi: 10.3389/fnut.2021.734735 pubmed: 34660664 pmcid: 8517082
Bauer, A. K. et al. Targeted deletion of Nrf2 reduces urethane-induced lung tumor development in mice. PLoS One 6, e26590 (2011).
pubmed: 22039513 pmcid: 3198791
Ban, Y. et al. Radiation-activated secretory proteins of Scgb1a1+ club cells increase the efficacy of immune checkpoint blockade in lung cancer. Nat. Cancer 2, 919–931 (2021).
pubmed: 34917944 pmcid: 8670735
Qi, L. et al. Identification of lncRNAs associated with lung squamous cell carcinoma prognosis in the competitive endogenous RNA network. PeerJ 7, e7727 (2019).
pubmed: 31576252 pmcid: 6753923
Zhang, J., Ma, D., Kang, H., Zhao, J. & Yang, M. Long noncoding RNA LINC01287 promotes proliferation and inhibits apoptosis of lung adenocarcinoma cells via the miR-3529-5p/RNASEH2A axis under the competitive endogenous RNA pattern. Environ. Toxicol. 36, 2093–2104 (2021).
pubmed: 34254728
Ding, L. et al. A novel stromal lncRNA signature reprograms fibroblasts to promote the growth of oral squamous cell carcinoma via LncRNA-CAF/interleukin-33. Carcinogenesis 39, 397–406 (2018).
pubmed: 29346528
Kim, J. S. et al. MiR-34a and miR-34b/c have distinct effects on the suppression of lung adenocarcinomas. Exp. Mol. Med. 51, 1–10 (2019).
pubmed: 31827074 pmcid: 6881327
Wan, N. & Zheng, J. MicroRNA-891a-5p is a novel biomarker for non-small cell lung cancer and targets HOXA5 to regulate tumor cell biological function. Oncol. Lett. 22, 1–10 (2021).
Powrózek, T., Krawczyk, P., Kucharczyk, T. & Milanowski, J. Septin 9 promoter region methylation in free circulating DNA—Potential role in noninvasive diagnosis of lung cancer: preliminary report. Med. Oncol. Northwood Lond. Engl. 31, 917 (2014).
Shen, N. et al. Hypermethylation of the SEPT9 gene suggests significantly poor prognosis in cancer patients: A systematic review and meta-analysis. Front. Genet. https://doi.org/10.3389/fgene.2019.00887 (2019).
doi: 10.3389/fgene.2019.00887 pubmed: 32117415 pmcid: 6928056
Wang, H., Wei, C., Pan, P., Yuan, F. & Cheng, J. Identification of a methylomics-associated nomogram for predicting overall survival of stage I-II lung adenocarcinoma. Sci. Rep. 11, 9938 (2021).
pubmed: 33976305 pmcid: 8113535
Liu, B., Chen, Y. & Yang, J. LncRNAs are altered in lung squamous cell carcinoma and lung adenocarcinoma. Oncotarget 8, 24275–24291 (2016).
pmcid: 5421846
Yu, Y. & Ren, K. Five long non-coding RNAs establish a prognostic nomogram and construct a competing endogenous RNA network in the progression of non-small cell lung cancer. BMC Cancer 21, 457 (2021).
pubmed: 33892664 pmcid: 8067646
Wulczyn, E. et al. Deep learning-based survival prediction for multiple cancer types using histopathology images. PLoS One https://doi.org/10.1371/journal.pone.0233678 (2020).
doi: 10.1371/journal.pone.0233678 pubmed: 32555646 pmcid: 7299324
Ma, B., Geng, Y., Meng, F., Yan, G. & Song, F. Identification of a sixteen-gene prognostic biomarker for lung adenocarcinoma using a machine learning method. J. Cancer 11, 1288–1298 (2020).
pubmed: 31956375 pmcid: 6959071
Li, Y. et al. A large cohort study identifying a novel prognosis prediction model for lung adenocarcinoma through machine learning strategies. BMC Cancer 19, 886 (2019).
pubmed: 31488089 pmcid: 6729062
Lee, T.-Y., Huang, K.-Y., Chuang, C.-H., Lee, C.-Y. & Chang, T.-H. Incorporating deep learning and multi-omics autoencoding for analysis of lung adenocarcinoma prognostication. Comput. Biol. Chem. 87, 107277 (2020).
pubmed: 32512487
Tomczak, K., Czerwińska, P. & Wiznerowicz, M. The cancer genome atlas (TCGA): An immeasurable source of knowledge. Contemp. Oncol. 19, A68–A77 (2015).
Li, Y. et al. Pan-cancer characterization of immune-related lncRNAs identifies potential oncogenic biomarkers. Nat. Commun. 11, 1000 (2020).
pubmed: 32081859 pmcid: 7035327
Pratella, D., Ait-El-Mkadem Saadi, S., Bannwarth, S., Paquis-Fluckinger, V. & Bottini, S. A survey of autoencoder algorithms to pave the diagnosis of rare diseases. Int. J. Mol. Sci. 22, 10891 (2021).
pubmed: 34639231 pmcid: 8509321
Spooner, A. et al. A comparison of machine learning methods for survival analysis of high-dimensional clinical data for dementia prediction. Sci. Rep. 10, 20410 (2020).
pubmed: 33230128 pmcid: 7683682
Du, P. et al. Comparison of beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinform. 11, 587 (2010).
Brentnall, A. R. & Cuzick, J. Use of the concordance index for predictors of censored survival data. Stat. Methods Med. Res. 27, 2359–2373 (2018).
pubmed: 27920368
Pan, Q., Wang, L., Zhang, H., Liang, C. & Li, B. Identification of a 5-gene signature predicting progression and prognosis of clear cell renal cell carcinoma. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 25, 4401–4413 (2019).
Zhou, Q., Chen, Q., Chen, X. & Hao, L. Bioinformatics analysis to screen DNA methylation-driven genes for prognosis of patients with bladder cancer. Transl. Androl. Urol. 10, 3604–3619 (2021).
pubmed: 34733656 pmcid: 8511533
Li, W. et al. Identification and validation of a prognostic lncRNA signature for hepatocellular carcinoma. Front. Oncol. 10, 780 (2020).
pubmed: 32587825 pmcid: 7298074
Lou, Y. et al. Gene microarray analysis of lncRNA and mRNA expression profiles in patients with high-grade ovarian serous cancer. Int. J. Mol. Med. 42, 91–104 (2018).
pubmed: 29577163 pmcid: 5979786
Yan, Z., Hong, S., Song, Y. & Bi, M. microR-4449 promotes colorectal cancer cell proliferation via regulation of SOCS3 and activation of STAT3 signaling. Cancer Manag. Res. 13, 3029–3039 (2021).
pubmed: 33854373 pmcid: 8039016
Lin, T.-C. et al. MicroRNA-184 deregulated by the MicroRNA-21 promotes tumor malignancy and poor outcomes in non-small cell lung cancer via targeting CDC25A and c-Myc. Ann. Surg. Oncol. 22(Suppl 3), S1532-1539 (2015).
pubmed: 25990966
Pastor, M. D. et al. Identification of proteomic signatures associated with lung cancer and COPD. J. Proteom. 89, 227–237 (2013).
Soulières, D. et al. PTPRF expression as a potential prognostic/predictive marker for treatment with Erlotinib in non-small-cell lung cancer. J. Thorac. Oncol. 10, 1364–1369 (2015).
pubmed: 26291013
Vallejo-Díaz, J. et al. Targeted depletion of PIK3R2 induces regression of lung squamous cell carcinoma. Oncotarget 7, 85063–85078 (2016).
pubmed: 27835880 pmcid: 5356720

Auteurs

Jacob G Ellen (JG)

Institute of Health Informatics, University College London, London, UK. jellen@hms.harvard.edu.

Etai Jacob (E)

AstraZeneca, Oncology Data Science, Waltham, MA, USA.

Nikos Nikolaou (N)

AstraZeneca, Oncology Data Science, Waltham, MA, USA.

Natasha Markuzon (N)

AstraZeneca, Oncology Data Science, Waltham, MA, USA. natasha.markuzon@astrazeneca.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH