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Propionate-producing Veillonella parvula regulates the malignant properties of tumor cells of OSCC

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Abstract

Oral squamous cell carcinoma (OSCC), main head and neck squamous cell carcinomas (HNSCCs), remains a global health concern with unknown pathogenesis. Veillonella parvula NCTC11810 was observed to decrease in saliva microbiome of OSCC patients in this study and the aim was to detect the novel role of Veillonella parvula NCTC11810 in regulating the biological characteristics of OSCC through TROP2/PI3K/Akt pathway. Oral microbial community changes of OSCC patients were detected by 16S rDNA gene sequencing technology. CCK8 assay, Transwell assay, and Annexin V-FITC/PI staining were used for proliferation, invasion, and apoptosis analysis of OSCC cell lines. Expression of proteins were determined by Western blotting analysis. Veillonella parvula NCTC11810 showed decreased in saliva microbiome of TROP2 high-expressed OSCC patients. Culture supernatant of Veillonella parvula NCTC11810 promoted the apoptosis and inhibited the proliferation and invasion ability of HN6 cells, while sodium propionate (SP), the main metabolite of Veillonella parvula NCTC11810, played a similar role through the inhibition of TROP2/PI3K/Akt pathway. Studies above supported the proliferation-inhibiting, invasion-inhibiting, and apoptosis-promoting function of Veillonella parvula NCTC11810 in OSCC cells which provided new insights into oral microbiota and their metabolite as a therapeutic method for OSCC patients with TROP2 high expressing.

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Funding

This study was financially supported by the National Natural Science Foundation of China (81872426), the Nanjing Medical Science and Technology Development Fund (YKK21152), and the Science and Technology Development Fund of Nanjing Medical University (NMUB20210072).

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Authors and Affiliations

  1. Key Laboratory of Antibody Technique of National Health Commission, Jiangsu Province Engineering Research Center of Antibody Drug, School of Basic Medicine, Nanjing Medical University, 101 Longmian Road, Nanjing, 211166, Jiangsu, People’s Republic of China

    Xinxia Chang, Yufeng Chen, Daixun Cui, Yufei Wang & Xiao Zhang

  2. Department of Geriatrics, The Second Clinical Medical School, Nanjing Medical University, Nanjing, 210011, Jiangsu, People’s Republic of China

    Yingjia Zhou

  3. Department of Stomatology, Children’s Hospital of Nanjing Medical University, 72 Guangzhou Road, Nanjing, 210008, Jiangsu, People’s Republic of China

    Genxiong Tang

  4. School of Stomatology, Nanjing Medical University, Nanjing, 211166, Jiangsu, People’s Republic of China

    Yufei Wang

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  1. Xinxia Chang
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Correspondence to Xiao Zhang or Genxiong Tang.

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Supplementary Information

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12032_2023_1962_MOESM1_ESM.pdf

Supplementary file1 (PDF 102 KB)—The 16 S-V4 amplicon sequencing and nucleotide Blast program of clone 12 from Columbia blood plates. (A) The 16 SV4 amplicon sequence result of clone 12 picked out from Columbia blood plates; (B) The sequencing results showed that the nucleotide sequence presented a high percentage of similarity (99.71%) using the Nucleotide BLAST program with a peculiar microorganism Veillonella parvula NCTC11810

Supplementary file2 (PDF 45 KB)—The total apoptosis ratio of HOK and HN6 cells treated with SP; n=3, ****p<0.0001

12032_2023_1962_MOESM3_ESM.pdf

Supplementary file3 (PDF 485 KB)—The western blotting result of cleaved GSDMD expression level in HN6 cells; Supernatant: culture supernatant of Veillonella parvula NCTC11810-treated group; SP-Treated: sodium propionate-treated group; Heated-V.P.: Heat-inactivated Veillonella parvula NCTC11810-treated group; V.P.: Veillonella parvula NCTC11810-treated group

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Chang, X., Chen, Y., Cui, D. et al. Propionate-producing Veillonella parvula regulates the malignant properties of tumor cells of OSCC. Med Oncol 40, 98 (2023). https://doi.org/10.1007/s12032-023-01962-6

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