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Comprehensive pan-cancer analysis reveals CCDC58 as a carcinogenic factor related to immune infiltration

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Abstract

CCDC58, a member of the CCDC protein family, has been primarily associated with the malignant progression of hepatocellular carcinoma (HCC) and breast cancer, with limited research conducted on its involvement in other tumor types. We aimed to assess the significance of CCDC58 in pan-cancer. We utilized the TCGA, GTEx, and UALCAN databases to perform the differential expression of CCDC58 at both mRNA and protein levels. Prognostic value was evaluated through univariate Cox regression and Kaplan–Meier methods. Mutation and methylation analyses were conducted using the cBioPortal and SMART databases. We identified genes interacting with and correlated to CCDC58 through STRING and GEPIA2, respectively. Subsequently, we performed GO and KEGG enrichment analyses. To gain insights into the functional status of CCDC58 at the single-cell level, we utilized CancerSEA. We explored the correlation between CCDC58 and immune infiltration as well as immunotherapy using the ESTIMATE package, TIMER2.0, TISIDB, TIDE, TIMSO, and TCIA. We examined the relationship between CCDC58 and tumor heterogeneity, stemness, DNA methyltransferases, and MMR genes. Lastly, we constructed a nomogram based on CCDC58 in HCC and investigated its association with drug sensitivity. CCDC58 expression was significantly upregulated and correlated with poor prognosis across various tumor types. The mutation frequency of CCDC58 was found to be increased in 25 tumors. We observed a negative correlation between CCDC58 expression and the methylation sites in the majority of tumors. CCDC58 showed negative correlations with immune and stromal scores, as well as with NK T cells, Tregs, CAFs, endothelial cells, and immunomodulators. Its value in immunotherapy was comparable to that of tumor mutational burden. CCDC58 exhibited positive correlations with tumor heterogeneity, stemness, DNA methyltransferase genes, and MMR genes. In HCC, CCDC58 was identified as an independent risk factor and demonstrated potential associations with multiple drugs. CCDC58 demonstrates significant clinical value as a prognostic marker and indicator of immune response across various tumor types. Its comprehensive analysis provides insights into its potential implications in pan-cancer research.

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Data availability

The data are available from the corresponding author for reasonable requests.

Abbreviations

ACC:

Adrenocortical carcinoma

AUC:

Area under the curve

BLCA:

Bladder urothelial carcinoma

BP:

Biological process

BRCA:

Breast invasive carcinoma

CAFs:

Cancer-associated fibroblasts

CC:

Cellular component

CCDC58:

Coiled-coil domain containing 58

CESC:

Cervical squamous cell carcinoma and endocervical adenocarcinoma

CHOL:

Cholangiocarcinoma

CNA:

Copy number alteration

CNV:

Copy number variants

COAD:

Colon adenocarcinoma

COADREAD:

Colon adenocarcinoma/rectum adenocarcinoma

DFI:

Disease-free interval

DLBC:

Lymphoid neoplasm diffuse large B-cell lymphoma

DSS:

Disease-specific survival

ESCA:

Esophageal carcinoma

GBM:

Glioblastoma multiforme

GBMLGG:

Glioma

GO:

Gene ontology

GSEA:

Gene set enrichment analysis

HCC:

Hepatocellular carcinoma

HNSC:

Head and neck squamous cell carcinoma

HRD:

Homologous recombination deficiency

IC50:

Half-maximal inhibitory concentration

ICB:

Immune checkpoint blockade

IPS:

Immune phenotype scores

KEGG:

Kyoto encyclopedia of genes and genomes

KICH:

Kidney chromophobe

KIPAN:

Pan-kidney cohort (KICH + KIRC + KIRP)

KIRC:

Kidney renal clear cell carcinoma

KIRP:

Kidney renal papillary cell carcinoma

KM:

Kaplan–Meier

LAML:

Acute myeloid leukemia

LGG:

Brain lower grade glioma

LIHC:

Liver hepatocellular carcinoma

LOH:

Loss of heterozygosity

LUAD:

Lung adenocarcinoma

LUSC:

Lung squamous cell carcinoma

MATH:

Mutational and clonal intratumoral heterogeneity

MDSCs:

Myeloid-derived suppressor cells

MESO:

Mesothelioma

MF:

Molecular function

MMR:

Mismatch repair

MSI:

Microsatellite instability

NEO:

Neoantigen load

OS:

Overall survival

OV:

Ovarian serous cystadenocarcinoma

PAAD:

Pancreatic adenocarcinoma

PCPG:

Pheochromocytoma and paraganglioma

PFI:

Progression-free interval

PPI:

Protein–protein interaction

PRAD:

Prostate adenocarcinoma

READ:

Rectum adenocarcinoma

ROC:

Receiver operating characteristic

SARC:

Sarcoma

SKCM:

Skin cutaneous melanoma

SNV:

Single nucleotide variants

STAD:

Stomach adenocarcinoma

STES:

Stomach and esophageal carcinoma

TGCT:

Testicular germ cell tumors

THCA:

Thyroid carcinoma

THYM:

Thymoma

TILs:

Tumor-infiltrating lymphocytes

TMB:

Tumor mutational burden

TME:

Tumor microenvironment

TNBC:

Triple-negative breast cancer

UCEC:

Uterine corpus endometrial carcinoma

UCS:

Uterine carcinosarcoma

UVM:

Uveal melanoma

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  1. Huili Wu and Qing Geng have contributed equally to this study.

Authors and Affiliations

  1. Department of Endodontics, Zhonglou Hospital, Changzhou Hospital of Traditional Chinese Medicine, Changzhou, China

    Huili Wu

  2. School of Exercise and Health, Shanghai University of Sport, Shanghai, China

    Qing Geng

  3. Department of Pediatric Cardiology, Xinhua Hospital, Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Wenxiang Shi

  4. Department of General Surgery, Changzhou Hospital of Traditional Chinese Medicine, Changzhou, China

    Chenjie Qiu

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  1. Huili Wu
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HW, QG, WS, and CQ participated in the conception, design, acquisition of data, analysis, and interpretation. All authors participated in drafting the article and gave final approval.

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Wu, H., Geng, Q., Shi, W. et al. Comprehensive pan-cancer analysis reveals CCDC58 as a carcinogenic factor related to immune infiltration. Apoptosis 29, 536–555 (2024). https://doi.org/10.1007/s10495-023-01919-0

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