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SMARCE1 promotes neuroblastoma tumorigenesis through assisting MYCN-mediated transcriptional activation

Oncogene volume 41, pages 4295–4306 (2022)Cite this article

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Abstract

SMARCE1 gene, encoding a core subunit of SWI/SNF chromatin remodeling complex, is situated on chromosome 17q21-ter region that is frequently gained in neuroblastoma. However, its role in the tumorigenesis remains unknown. Here, we showed that high expression of SMARCE1 was associated with poor prognosis of patients with neuroblastoma, especially those with MYCN amplification. Knockdown of SMARCE1 reduced proliferation, colony formation, and tumorigenicity of neuroblastoma cells. Mechanistically, SMARCE1 directly interacted with MYCN, which was necessary for MYCN-mediated transcriptional activation of downstream target genes including PLK1, ODC1, and E2F2. Overexpression of PLK1, ODC1 or E2F2 significantly reversed the inhibiting effect of SMARCE1 knockdown on the proliferation, colony formation, and tumorigenicity of MYCN-amplified neuroblastoma cells. Moreover, we revealed that MYCN directly regulated SMARCE1 transcription through binding to a non-canonical E-box of SMARCE1 promoter, thus enhancing SMARCE1-MYCN cooperativity. These findings establish SMARCE1 is a critical oncogenic factor in neuroblastoma and provide a new potential target for treatment of neuroblastoma with 17q21-ter gain and MYCN amplification.

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Fig. 1: High SMARCE1 expression associates with 17q21-ter gain, MYCN-amplification, and poor patient prognosis in neuroblastoma.
Fig. 2: SMARCE1 affects the proliferation and tumorigenicity of neuroblastoma cells.
Fig. 3: MYCN directly upregulates SMARCE1 expression by binding to the SMARCE1 promoter.
Fig. 4: SMARCE1 forms a protein complex with MYCN.
Fig. 5: SMARCE1 induces the expression of the MYCN target genes PLK1, ODC1 and E2F2.
Fig. 6: SMARCE1 and MYCN form co-activators that regulates PLK1, ODC1 and E2F2 transcription.
Fig. 7: SMARCE1 promotes neuroblastoma progression via regulating PLK1, ODC1 and E2F2 expression.

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Data availability

All of the data and material in this paper are available when requested. We obtained several other publicly available ChIP-seq datasets (GSM2113542, GSM2214113, GSM2113529, GSM2113526 and ENCSR157TCS) for analysis. We also obtained 88 human Neuroblastoma samples dataset (GSE16476) for analysis (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi; https://www.encodeproject.org/).

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Acknowledgements

This research was supported by the Natural Science Foundation of Chongqing (cstc2019jcyj-zdxmX0033, cstc2022ycjh-bgzxm0145), the pilot program of Southwest University (SWU-XDZD22006).

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Authors and Affiliations

  1. State Key Laboratory of Silkworm Genome Biology, Southwest University, Chongqing, 400716, China

    Xiaosong Hu, Ruochen Liu, Jianbing Hou, Wen Peng, Sicheng Wan, Minghao Xu, Yongsen Li, Guanghui Zhang & Hongjuan Cui

  2. Cancer Center, Medical Research Institute, Southwest University, Chongqing, 400716, China

    Xiaosong Hu, Ruochen Liu, Jianbing Hou, Wen Peng, Sicheng Wan, Minghao Xu, Yongsen Li, Guanghui Zhang & Hongjuan Cui

  3. Department of Neurosurgery, Children’s Hospital of Chongqing Medical University, Chongqing, 400014, China

    Xuan Zhai & Ping Liang

  4. Chongqing Key Laboratory of Pediatrics, Chongqing, 400010, China

    Xuan Zhai & Ping Liang

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  1. Xiaosong Hu
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Contributions

HC, PL and XH conceived and designed the experiments. XH, JH, WP, SW, YL, GZ and XZ performed the experiments, collected the data. XH, RL and MX analyzed the data and prepared the figures. XH and HC wrote the manuscript. All the authors read and approved the final manuscript.

Corresponding authors

Correspondence to Ping Liang or Hongjuan Cui.

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Competing interests

The authors declare no competing interests.

Ethical approval

All experiments involving cancer patients’ samples were obtained from Chaoying Biotechnology Co., Ltd. (Henan, China), and the studies were approved by the Medical Ethics Committee of Tongxu County People’s Hospital of Henan Province. All of the patients were informed consent.

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Supplementary information

Supplementary figure legends

The primers in this study

Supplementary Figure 1. High SMARCE1 expression associates with poor patient prognosis in neuroblastoma

41388_2022_2428_MOESM4_ESM.jpg

Supplementary Figure 2. SMARCE1 is required for the colony-formation ability and proper cell cycle progression of MYCN-amplified neuroblastoma cells

Supplementary Figure 3. MYCN regulates the expression of SMARCE1

Supplementary Figure 4. SMARCE1 interacts with MYCN

Supplementary Figure 5. SMARCE1 regulates the expression of PLK1, ODC1 and E2F2

41388_2022_2428_MOESM8_ESM.jpg

Supplementary Figure 6. SMARCE1 cooperate with MYCN to transcriptionally regulates the expression of PLK1, ODC1 and E2F2

41388_2022_2428_MOESM9_ESM.jpg

Supplementary Figure 7. The MYCN-SMARCE1 interaction is an important factor that regulates PLK1 expression and cell proliferation.

41388_2022_2428_MOESM10_ESM.jpg

Supplementary Figure 8. Analysis of the correlation between MYCN and SMARCE1 expression levels in several MYCN-amplified or overexpressed cancers

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Hu, X., Liu, R., Hou, J. et al. SMARCE1 promotes neuroblastoma tumorigenesis through assisting MYCN-mediated transcriptional activation. Oncogene 41, 4295–4306 (2022). https://doi.org/10.1038/s41388-022-02428-1

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