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A prognostic marker LTBP1 is associated with epithelial mesenchymal transition and can promote the progression of gastric cancer

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Abstract

LTBP1 is closely related to TGF-β1 function as an essential component, which was unclear in gastric cancer (GC). Harbin Medical University (HMU)-GC cohort and The Cancer Genome Atlas (TCGA) dataset were combined to form a training cohort to calculate the connection between LTBP1 mRNA expression, prognosis and clinicopathological features. The training cohort was also used to verify the biological function of LTBP1 and its relationship with immune microenvironment and chemosensitivity. In the tissue microarrays (TMAs), immunohistochemical (IHC) staining was performed to observe LTBP1 protein expression. The correlation between LTBP1 protein expression level and prognosis was also analyzed, and a nomogram model was constructed. Western blotting (WB) was used in cell lines to assess LTBP1 expression. Transwell assays and CCK-8 were employed to assess LTBP1's biological roles. In compared to normal gastric tissues, LTBP1 expression was upregulated in GC tissues, and high expression was linked to a bad prognosis for GC patients. Based on a gene enrichment analysis, LTBP1 was primarily enriched in the TGF-β and EMT signaling pathways. Furthermore, high expression of LTBP1 in the tumor microenvironment was positively correlated with an immunosuppressive response. We also found that LTBP1 expression (p = 0.006) and metastatic lymph node ratio (p = 0.044) were independent prognostic risk factors for GC patients. The prognostic model combining LTBP1 expression and lymph node metastasis ratio reliably predicted the prognosis of GC patients. In vitro proliferation and invasion of MKN-45 GC cells were inhibited and their viability was decreased by LTBP1 knockout. LTBP1 plays an essential role in the development and progression of GC, and is a potential prognostic biomarker and therapeutic target for GC.

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Data availability

Harbin Medical University (HMU)- gastric cancer (GC) cohort were stored in the Gene Expression Omnibus (GEO) repository (GSE184336 and GSE179252). Patients’ data were saved in the Gastric Cancer Information Management System v1.2 of Harbin Medical University Cancer Hospital (Copyright No.2013SR087424, http: www. sgihmu.com).

Abbreviations

GC:

Gastric cancer

HMU:

Harbin medical university

TCGA:

The cancer genome atlas

WB:

Western blotting

IHC:

Immunohistochemical

CAFs:

Cancer-associated fibroblasts

GEO:

Gene expression omnibus

STAD:

Stomach adenocarcinoma

DEGs:

Differentially expressed genes

FDR:

False discovery rate

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

GSEA:

Gene set enrichment analysis

NES:

Normalized enrichment score

NOM:

Nominal

PPI:

Protein-protein interaction

STRING:

Search tool for retrieving interacting genes

TMAs:

Tissue microarrays

DAB:

Diaminobenzidine

GES:

Gastric epithelial cell line

BCA:

Biochemical Acid

SDS-PAGE:

Sodium dodecyl sulfate–polyacrylamide gels

CI:

Confidence interval

BP:

Biological processes

CC:

Cellular components

MF:

Molecular functions

TME:

Tumor microenvironment

ROC:

Receiver operating characteristic curve

AUC:

Area under receiver operating characteristic curve

DCA:

Decision curve analysis

GBMLGG:

Glioma

LGG:

Brain lower grade glioma

ACC:

Adrenocortical carcinoma

KIRP:

Kedney renal papillary cell carcinoma

BLCA:

Bladder urothelial carcinoma

CHOL:

Cholangiocarcinoma

HNSC:

Neck squamous cell carcinoma

KICH:

Kidney chromophobe

PAAD:

Pancreatic cancer

KIPAN:

Pan-kidney cohort

BRCA:

Breast invasive carcinoma

MSI:

Microsatellite instability

TMB:

Tumor mutation burden

LAML:

Acute myeloid leukemia

MESO:

Mesothelioma

PAAD:

Pancreatic adenocarcinoma

ESCC:

Esophageal squamous cell carcinoma

GBM:

Glioblastoma

Treg:

Regulatory T cells

TGCT:

Testicular germ cell tumors

VEGFR2:

Vascular endothelial growth factor receptor 2

BMI:

Body mass index

INFa:

Expanding growth and a distinct border with the surrounding tissue

INFc:

Infiltrating growth and an indistinct border with the surrounding tissue

INFb:

In-between INFa and INFc

CEA:

Carcinoembryonic antigen

CA19-9:

Carbohydrate antigen 19–9

CA72-4:

Carbohydrate antigen 72–4

HER2:

Human Epidermal Growth Factor Receptor 2

IQR:

Interquartile range

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Acknowledgements

Not applicable

Funding

This work was partially supported by the Natural Science Foundation of Inner Mongolia Autonomous Region: 2022QR08003. This work was supported by Heilongjiang Provincial Leading Talent EchelonReserve Leader 

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Author notes

  1. Xinju Jiang, Shengjie Yin, Xin Yin These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Pathology, Basic Medical Science College, Harbin Medical University, Harbin, Heilongjiang, China

    Xinju Jiang, Shuo Yang, Xiulan Bian & Lei Zhang

  2. Department of Medical Oncology, Municipal Hospital of Chifeng, Chifeng, Inner Mongolia Autonomous Region, China

    Shengjie Yin

  3. Department of Gastroenterological Surgery, Harbin Medical University Cancer Hospital, Harbin Medical University, Harbin, Heilongjiang, China

    Xin Yin, Yufei Wang, Tianyi Fang & Yingwei Xue

  4. Department of Colorectal and Anal Surgery, Chifeng Municipal Hospital, Chifeng Clinical Medical School of Inner Mongolia Medical University, Chifeng, Inner Mongolia Autonomous Region, China

    Guoli Li

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  1. Xinju Jiang
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Contributions

XJ, SY and XY jointly completed the writing of the manuscript, YW and TF completed the immunochemistry experiment and drew the picture, XJ and SY were responsible for the editing of the picture, LZ, XB, YX and YW participated in the review of the article and put forward suggestions for revision.

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Correspondence to Lei Zhang.

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The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee from Harbin Medical University Cancer Hospital, China (Approval Number: SHGC-1029). Informed consent was obtained from all subjects involved in the study.

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Jiang, X., Yin, S., Yin, X. et al. A prognostic marker LTBP1 is associated with epithelial mesenchymal transition and can promote the progression of gastric cancer. Funct Integr Genomics 24, 30 (2024). https://doi.org/10.1007/s10142-024-01311-4

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