journal article·2026-06-22Open access

Neuron‐Derived MIF Engages VCAM1 to Fuel a Self‐Amplifying CXCL8 Loop That Drives Perineural Invasion and Metastasis in Gastric Cancer

Xunjun Li, Zhongya Zhai, Haiyi Yu, Renjie Qiu, Fengyu Li, Luxi Xiao, Boxi Huang, Huiying Liu, Jiayong He, Bowen Cai, Jiawen Chen, Jiang Yu, Guoxin Li, Tao Chen

Abstract

ABSTRACT Background : Perineural invasion (PNI) is common in gastric cancer and predicts poor prognosis, but the molecular mechanisms underlying tumour–nerve crosstalk remain unclear. Methods : Transcriptomic data from TCGA and GEO were integrated to identify PNI regulators, with validation in surgical specimens. Mechanistic studies used tumor–neuron Transwell co‐culture, siRNA/lentiviral perturbation, Western blot, immunofluorescence, ELISA, co‐immunoprecipitation, and GST pull‐down. Functional effects were assessed via CCK‐8/Transwell assays, a sciatic nerve invasion xenograft model, and an orthotopic gastric cancer model with neuron‐specific MIF conditional knockout mice. Results : High CXCL8/VCAM1 expression correlates with poor overall survival, distant metastasis, and is upregulated in PNI‐positive tumours. Mechanistically, CXCL8 promotes neuronal MIF expression, while MIF directly binds VCAM1 and enhances tumour CXCL8 expression. VCAM1‐mediated CXCL8 upregulation drives tumour proliferation and invasion. In vivo, blocking CXCL8/VCAM1 or neuron‐specific MIF deletion reduces tumour growth and neural invasion. Conclusions : A MIF–VCAM1–CXCL8 positive‐feedback axis linking neural activity to gastric cancer progression and PNI is identified, providing prognostic biomarkers and actionable therapeutic targets.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Macrophage Migration Inhibitory Factor · Chemokine receptors and signaling · Immune cells in cancer

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of General Surgery & Guangdong Provincial Key Laboratory of Precision Medicine for Gastrointestinal Tumor Nanfang Hospital Southern Medical University Guangzhou Guangdong Province China

Department of Thyroid And Breast Surgery Shenzhen Hospital Southern Medical University Shenzhen Guangdong Province China

Cancer Center of Beijing Tsinghua Changgung Hospital School of Clinical Medicine Tsinghua Medicine Tsinghua University Beijing China

Department of Gastrointestinal and Hernia Surgery Ganzhou Hospital‐Nanfang Hospital Southern Medical University Ganzhou Jiangxi Province China

Funding

National Natural Science Foundation of China · Natural Science Foundation of Guangdong Province · Natural Science Foundation of Jiangxi Province

References (41)

Show source-provided references
1. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries
2. Nerve‐tumor crosstalk in tumor microenvironment: From tumor initiation and progression to clinical implications10.1016/j.bbcan.2024.189121 ↗
3. Significance and mechanisms of perineural invasion in malignant tumors10.3389/fonc.2025.1572396 ↗
4. Influence of perineural invasion in predicting overall survival and disease‐free survival in patients With locally advanced gastric cancer10.1016/j.amjsurg.2016.05.022 ↗
5. Perineural invasion and associated pain in pancreatic cancer10.1038/nrc3131 ↗
6. Perineural invasion in cancer: A review of the literature
7. Prognostic significance of perineural invasion in patients With gastric cancer who underwent curative resection10.1245/s10434-010-1027-y ↗
8. Prognostic value of perineural invasion in gastric cancer: A systematic review and meta‐analysis10.1371/journal.pone.0088907 ↗
9. Mechanisms of Perineural Invasion10.1055/s-0036-1571835 ↗
10. The Chemokine (CCL2–CCR2) Signaling Axis Mediates Perineural Invasion10.1158/1541-7786.MCR-14-0303 ↗
11. Tumor‐ and Nerve‐Derived Axon Guidance Molecule Promotes Pancreatic Ductal Adenocarcinoma Progression and Metastasis Through Macrophage Reprogramming
12. Axon Guidance Molecules Promote Perineural Invasion and Metastasis of Orthotopic Pancreatic Tumors in Mice10.1053/j.gastro.2019.05.065 ↗
13. Autophagic Schwann cells promote perineural invasion mediated by the NGF/ATG7 paracrine pathway in pancreatic cancer10.1186/s13046-021-02198-w ↗
14. Neurotransmitter Receptor HTR2B Regulates Lipid Metabolism to Inhibit Ferroptosis in Gastric Cancer10.1158/0008-5472.CAN-23-1012 ↗
15. Neurodegeneration of local sympathetic inputs promotes colorectal cancer progression10.1016/j.canlet.2025.217817 ↗
16. Glutamate From nerve cells promotes perineural invasion in pancreatic cancer by regulating tumor glycolysis Through HK2 mRNA‐m6A modification10.1016/j.phrs.2022.106555 ↗
17. Harnessing cytokines and chemokines for cancer therapy10.1038/s41571-021-00588-9 ↗
18. CXCL12/CXCR4 facilitates perineural invasion via induction of the Twist/S100A4 axis in salivary adenoid cystic carcinoma10.1111/jcmm.16713 ↗
19. YAP1‐TEAD1 mediates the perineural invasion of prostate cancer cells induced by cancer‐associated fibroblasts10.1016/j.bbadis.2022.166540 ↗
20. CXCL8 and the peritoneal metastasis of ovarian and gastric cancer10.3389/fimmu.2023.1159061 ↗
21. Carbon monoxide releasing molecule‐2 ameliorates IL‐1β‐induced IL‐8 in human gastric cancer cells10.1016/j.tox.2016.07.003 ↗
22. Breast cancer metastasis: Putative therapeutic role of vascular cell adhesion molecule‐110.1007/s13402-017-0324-x ↗
23. IL‐17 and insulin/IGF1 enhance adhesion of prostate cancer cells to vascular endothelial cells Through CD44‐VCAM‐1 interaction10.1002/pros.22971 ↗
24. H3K18 lactylation‐mediated VCAM1 expression promotes gastric cancer progression and metastasis via AKT‐mTOR‐CXCL1 axis10.1016/j.bcp.2024.116120 ↗
25. Macrophage Migration Inhibitory Factor (MIF): Biological Activities and Relation With Cancer10.1007/s12253-016-0138-6 ↗
26. Mechanisms and effectors of MIF‐dependent promotion of tumourigenesis10.1016/j.cellsig.2003.07.002 ↗
27. An In Vivo Murine Sciatic Nerve Model of Perineural Invasion
28. Cross talk initiated by endothelial cells enhances migration and inhibits anoikis of squamous cell carcinoma cells Through STAT3/Akt/ERK signaling10.1593/neo.09266 ↗
29. The evolving tumor microenvironment: From cancer initiation to metastatic outgrowth10.1016/j.ccell.2023.02.016 ↗
30. Chemokine signaling in cancer: Implications on the tumor microenvironment and therapeutic targeting
31. Astragalus mongholicus Bunge and Curcuma aromatica Salisb. inhibits liver metastasis of colon cancer by regulating EMT via the CXCL8/CXCR2 axis and PI3K/AKT/mTOR signaling pathway10.1186/s13020-022-00641-4 ↗
32. CXCL8/CXCR2 signaling mediates bone marrow fibrosis and is a therapeutic target in myelofibrosis
33. The CXCL8‐CXCR1/2 pathways in cancer10.1016/j.cytogfr.2016.08.002 ↗
34. VCAM1 Promotes Tumor Cell Invasion and Metastasis by Inducing EMT and Transendothelial Migration in Colorectal Cancer10.3389/fonc.2020.01066 ↗
35. Association of VCAM‐1 overexpression With oncogenesis, tumor angiogenesis and metastasis of gastric carcinoma10.3748/wjg.v9.i7.1409 ↗
36. The role of macrophage inhibitory factor in tumorigenesis and central nervous system tumors
37. MIF‐ACKR3 causes irreversible fat loss by impairing adipogenesis in cancer cachexia10.1016/j.cmet.2025.01.018 ↗
38. Unlocking the Power of CXCR2 Inhibition to Overcome Gemcitabine Resistance in Pancreatic Cancer
39. Exploration of Pyrido[3,4‐d]pyrimidines as Antagonists of the Human Chemokine Receptor CXCR210.3390/molecules28052099 ↗
40. Discovery of new STAT3 inhibitors as anticancer agents using ligand‐receptor contact fingerprints and docking‐augmented machine learning10.1039/D2RA07007C ↗
41. Research progress of STAT3‐based dual inhibitors for cancer therapy10.1016/j.bmc.2023.117382 ↗