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  3. Osteoblasts are induced into cancer-associated osteoblasts to promote tumor progression in head and neck squamous cell carcinoma

Osteoblasts are induced into cancer-associated osteoblasts to promote tumor progression in head and neck squamous cell carcinoma

  • Biochim Biophys Acta Mol Basis Dis. 2024 Oct;1870(7):167439. doi: 10.1016/j.bbadis.2024.167439.
Yaqi Chen 1,  Xianglong Zheng 2,  Wenrui Shi 3,  Chenghui Lu 4,  Yu Qiu 5,  Lisong Lin 6
Affiliations

Affiliations

  • 1 Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Fujian Medical University, Fuzhou 350005, China; School and Hospital of Stomatology, Fujian Medical University, Fuzhou 350002, China; Fujian Key Laboratory of Oral Diseases, School and Hospital of Stomatology, Fujian Medical University, Fuzhou 350004, China; Department of Oral and Maxillofacial Surgery, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou 350212, China. Electronic address: fzchenyaqi@fjmu.edu.cn.
  • 2 Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Fujian Medical University, Fuzhou 350005, China; Department of Oral and Maxillofacial Surgery, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou 350212, China.
  • 3 Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Fujian Medical University, Fuzhou 350005, China; School and Hospital of Stomatology, Fujian Medical University, Fuzhou 350002, China; Fujian Key Laboratory of Oral Diseases, School and Hospital of Stomatology, Fujian Medical University, Fuzhou 350004, China; Department of Oral and Maxillofacial Surgery, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou 350212, China. Electronic address: kqswr@fjmu.edu.cn.
  • 4 School and Hospital of Stomatology, Fujian Medical University, Fuzhou 350002, China.
  • 5 Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Fujian Medical University, Fuzhou 350005, China; Department of Oral and Maxillofacial Surgery, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou 350212, China. Electronic address: qy97@163.com.
  • 6 Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Fujian Medical University, Fuzhou 350005, China; School and Hospital of Stomatology, Fujian Medical University, Fuzhou 350002, China; Department of Oral and Maxillofacial Surgery, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou 350212, China. Electronic address: fjmudrlls@hotmail.com.
PMID: 39074625 DOI: 10.1016/j.bbadis.2024.167439
Abstract

Bone invasion by head and neck squamous cell carcinoma (HNSCC) significantly impacts tumor staging, treatment choice, prognosis, and quality of life. While HNSCC is known to cause osteolytic bone invasion, we found that specific HNSCC subtypes can induce osteogenic bone destruction at the tumor-bone interface. This destruction mode significantly correlated with reduced patient survival rates and increased neck lymph node metastasis. Further in vivo and in vitro experiments indicated that HNSCC cells triggered abnormal phenotypic changes in osteoblasts to remodel the tumor-bone microenvironment, facilitating tumor lymphatic metastasis. Through transcriptome analysis, we identified three genes-osteopontin (SPP1), chemokine (C-X-C motif) ligand 1 (CXCL1), and matrix metalloprotein (MMP)9 (MMP9) linked to a poorer prognosis. We discovered osteoblasts with abnormal phenotypes at the tumor-bone interface exhibiting high SPP1, MMP9, and CXCL1 expressions. Based on these characteristics, we identified this osteoblast subpopulation as "cancer-associated osteoblasts (CAOs)." HNSCC cells activated the TNF-α/NF-κB signaling pathway in osteoblasts, transforming them into "CAOs." These CAOs significantly contributed to the progression of tumor-induced bone invasion, facilitating Cancer growth and metastasis. We first provided clinical data and in vivo and in vitro evidence that HNSCC cells can promote tumor progression by manipulating osteoblasts into "CAOs" in the bone invasion.

Keywords

Bone invasion; Cellular interaction; HNSCC; Tumor-bone microenvironment.

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