Abstract
The tradeoff between cost and efficiency is omnipresent in organisms. Specifically, how the evolutionary force shapes the tradeoff between biosynthetic cost and translation efficiency remains unclear. In the cancer community, whether the adjustment of cost-efficiency tradeoff acts as a strategy to facilitate tumor proliferation and contributes to oncogenesis is uninvestigated. To address this issue, we retrieved the gene expression profile in various cancer types and the matched normal samples from The Cancer Genome Atlas (TCGA). We found that the highly expressed genes in cancers generally have higher tAI/nitro ratios than those in normal samples. This is possibly caused by the higher tAI/nitro ratios observed in oncogenes than tumor suppressor genes (TSG). Furthermore, in the cancer samples, derived mutations in oncogenes usually lead to higher tAI/nitro ratios, while those mutations in TSG lead to lower tAI/nitro. For a special case of kidney cancer, we investigated several crucial genes in tumor samples versus normal samples, and discovered that the changes in tAI/nitro ratios are correlated with the changes in translation level. Our study for the first time revealed the optimization of cost-efficiency tradeoff in cancers. The cost-efficiency dilemma is optimized by the tumor cells, and is possibly beneficial for the translation and production of oncogenes, and eventually contributes to proliferation and oncogenesis. Our findings could provide novel perspectives in depicting the cancer genomes and might help unravel the cancer evolution.
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Data availability
All data used in our study are public data, which has been mentioned in the Materials and methods section. The reference genome sequences: UCSC genome browser web site. The cancer data: TCGA (The Cancer Gene Atlas). The tRNA data: genomic tRNA database website (http://gtrnadb.ucsc.edu). The oncogenes and tumor suppressor genes: The Cancer Gene Census website (CGC, https://cancer.sanger.ac.uk/census/).
Abbreviations
- ACC:
-
Adrenocortical carcinoma
- BLCA:
-
Bladder urothelial carcinoma
- LGG:
-
Brain lower-grade glioma
- BRCA:
-
Breast invasive carcinoma
- CESC:
-
Cervical squamous cell carcinoma and endocervical adenocarcinoma
- CHOL:
-
Cholangiocarcinoma
- COAD:
-
Colon adenocarcinoma
- ESCA:
-
Esophageal carcinoma
- GBM:
-
Glioblastoma multiforme
- HNSC:
-
Head and neck squamous cell carcinoma
- KICH:
-
Kidney chromophobe
- KIRC:
-
Kidney renal clear cell carcinoma
- KIRP:
-
Kidney renal papillary cell carcinoma
- LAML:
-
Acute myeloid leukemia
- LIHC:
-
Liver hepatocellular carcinoma
- LUAD:
-
Lung adenocarcinoma
- LUSC:
-
Lung squamous cell carcinoma
- DLBC:
-
Lymphoid neoplasm diffuse large B cell lymphoma
- OV:
-
Ovarian serous cystadenocarcinoma
- PAAD:
-
Pancreatic adenocarcinoma
- PCPG:
-
Pheochromocytoma and paraganglioma
- PRAD:
-
Prostate adenocarcinoma
- SARC:
-
Sarcoma
- SKCM:
-
Skin cutaneous melanoma
- STAD:
-
Stomach adenocarcinoma
- TGCT:
-
Testicular germ cell tumors
- THYM:
-
Thymoma
- THCA:
-
Thyroid carcinoma
- UCS:
-
Uterine carcinosarcoma
- UCEC:
-
Uterine corpus endometrial carcinoma
- UVM:
-
Uveal melanoma
- NGS:
-
Next generation sequencing
- mRNA:
-
Messenger RNA
- CDS:
-
Coding sequence
- UTR:
-
Untranslated region
- RPF:
-
Ribosome protected fragment
- CAI:
-
Codon adaptation index
- tRNA:
-
Transfer RNA
- tAI:
-
TRNA adaptation index
- Onc:
-
Oncogene
- TSG:
-
Tumor suppressor gene
- RPKM:
-
Reads per kilobase per million mapped reads
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The corresponding author WL designed and supervised this research. All authors contributed to the big data analyses. All authors contributed to writing this article.
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Zhao, S., Song, S., Qi, Q. et al. Cost-efficiency tradeoff is optimized in various cancer types revealed by genome-wide analysis. Mol Genet Genomics 296, 369–378 (2021). https://doi.org/10.1007/s00438-020-01747-w
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DOI: https://doi.org/10.1007/s00438-020-01747-w