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Cost-efficiency tradeoff is optimized in various cancer types revealed by genome-wide analysis

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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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Acknowledgements

We thank our colleagues in other departments that have given us precious suggestions and help.

Funding

This work was not supported by funding.

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Authors and Affiliations

  1. Department of Oncological Radiotherapy, Affiliated Hospital of Medical College Qingdao University, Shandong, China

    Shufen Zhao, Shanai Song, Qi Qi & Wei Lei

Authors
  1. Shufen Zhao
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  2. Shanai Song
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  3. Qi Qi
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  4. Wei Lei
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Contributions

The corresponding author WL designed and supervised this research. All authors contributed to the big data analyses. All authors contributed to writing this article.

Corresponding author

Correspondence to Wei Lei.

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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

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