Pentagamavunone-1 suppresses MYCN-positive HuH-7 Cancer Cell Growth via Mitotic Arrest in vitro
Keywords:
PGV-1, hepatocellular carcinoma, HuH-7, mitotic arrest, MYCN
Abstract
High expression of MYCN is usually found in progressive liver cancer. The present study investigated the potential effects of Pentagamavunone-1 (PGV-1) against the MYCN-positive human hepatocellular carcinoma (HCC) cell line in vitro based on the cellular physiology. The MYCN-positive cell line, HuH-7, was employed as a cell model in this study. The cytotoxic effect of PGV-1 was observed using the trypan blue exclusion method while its alterations to the cell cycle and level of intracellular reactive oxygen species (ROS) were determined through flow cytometry. Further, the cellular morphology of the cells was presented with Hoechst and X-gal staining whilst the expression of MYCN was detected by Western blot. The results demonstrated that PGV-1 was cytotoxic to HuH-7 cells with GI50 of 0.36 μM, much lower than sorafenib and peretinoin which had GI50 of 2.07 and 45.6 μM, respectively. PGV-1 inhibited the growth of HuH-7 cells in a dose-dependent manner, even after removal of the drug. Flow cytometry analysis confirmed that the cycle of HuH-7 cells appeared to arrest in the G2/M phase and intracellular ROS levels were increased. Moreover, the Hoechst staining showed chromosomal condensation in the mitotic phase, particularly in prometaphase. The X-gal staining confirmed that the PGV-1-treated cells undergo senescence. PGV-1 also decreased MYCN expression in HuH-7 cells. All these findings imply that PGV-1 is a potential agent to inhibit MYCN-positive liver cancer cells via mitotic arrest.
References
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Chen, X., Yang, G., Guo, X., Zhang, J., Sun, W., Liu, D., Wang, H., & Liu, S. (2022). DJ-1/FGFR-1 Signaling Pathway Contributes to Sorafenib Resistance in Hepatocellular Carcinoma. Oxidative Medicine and Cellular Longevity, 2022, 2543220. https://doi.org/10.1155/2022/2543220
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Fukuyama, K., Asagiri, M., Sugimoto, M., Tsushima, H., Seo, S., Taura, K., Uemoto, S., & Iwaisako, K. (2021). Gene expression profiles of liver cancer cell lines reveal two hepatocyte-like and fibroblast-like clusters. PLoS ONE, 16(2 February), 1–17. https://doi.org/10.1371/journal.pone.0245939
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Hasbiyani, N. A., Wulandari, F., Nugroho, E. P., Hermawan, A., & Meiyanto, E. (2021). Bioinformatics Analysis Confirms the Target Protein Underlying Mitotic Catastrophe of 4T1 Cells under Combinatorial Treatment of PGV-1 and Galangin. In Scientia Pharmaceutica (Vol. 89, Issue 3). https://doi.org/10.3390/scipharm89030038
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Larasati, Y. A., Yoneda-Kato, N., Nakamae, I., Yokoyama, T., Meiyanto, E., & Kato, J.-Y. (2018). Curcumin targets multiple enzymes involved in the ROS metabolic pathway to suppress tumor cell growth. Scientific Reports, 8(1), 2039. https://doi.org/10.1038/s41598-018-20179-6
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Meiyanto, E., Novitasari, D., Utomo, R. Y., Susidarti, R. A., & Meiyanto, E. (2022). Bioinformatic and Molecular Interaction Studies Uncover That CCA-1.1 and PGV-1 Differentially Target Mitotic Regulatory Protein and Have a Synergistic Effect against Leukemia Cells. Indonesian Journal of Pharmacy, 33(2), 225–233.
Meiyanto, E., Putri, D. D. P., Susidarti, R. A., Murwanti, R., Sardjiman, Fitriasari, A., Husnaa, U., Purnomo, H., & Kawaichi, M. (2014). Curcumin and its analogues (PGV-0 and PGV-1) enhance sensitivity of resistant MCF-7 cells to doxorubicin through inhibition of HER2 and NF-kB activation. Asian Pacific Journal of Cancer Prevention: APJCP, 15(1), 179–184. https://doi.org/10.7314/apjcp.2014.15.1.179
Meiyanto, E., Putri, H., Arum Larasati, Y., Yudi Utomo, R., Istighfari Jenie, R., Ikawati, M., Lestari, B., Yoneda-Kato, N., Nakamae, I., Kawaichi, M., & Kato, J.-Y. (2019). Anti-proliferative and Anti-metastatic Potential of Curcumin Analogue, Pentagamavunon-1 (PGV-1), Toward Highly Metastatic Breast Cancer Cells in Correlation with ROS Generation. Advanced Pharmaceutical Bulletin, 9(3), 445–452. https://doi.org/10.15171/apb.2019.053
Meiyanto, E., Septisetyani, E. P., Larasati, Y. A., & Kawaichi, M. (2018). Curcumin Analog Pentagamavunon-1 (PGV-1) Sensitizes Widr Cells to 5-Fluorouracil through Inhibition of NF-κB Activation. Asian Pacific Journal of Cancer Prevention: APJCP, 19(1), 49–56. https://doi.org/10.22034/APJCP.2018.19.1.49
Moordiani, Novitasari, D., Susidarti, R. A., Ikawati, M., Kato, J. Y., & Meiyanto, E. (2023). Curcumin Analogs PGV-1 and CCA-1.1 Induce Cell Cycle Arrest in Human Hepatocellular Carcinoma Cells with Overexpressed MYCN. Indonesian Biomedical Journal, 15(2), 141–149. https://doi.org/10.18585/inabj.v15i2.2147
Musyayyadah, H., Wulandari, F., Nangimi, A. F., Dewi, A., Ikawati, M., & Meiyanto, E. (2021). The Growth Suppression Activity of Diosmin and PGV-1 Co-Treatment on 4T1 Breast Cancer Targets Mitotic Regulatory Proteins. 22, 2929–2938. https://doi.org/10.31557/APJCP.2021.22.9.2929
Novitasari, D., Jenie, R. I., Wulandari, F., Utomo, R. Y., Putri, D. D. P., Kato, J.-Y., & Meiyanto, E. (2021a). A Curcumin-like structure (CCA-1.1) induces permanent mitotic arrest (Senescence) on Triple-negative breast cancer (TNBC) cells, 4T1. Research Journal of Pharmacy and Technology, 14(8), 4375–82. https://doi.org/10.52711/0974-360X.2021.00760
Novitasari, D., Jenie, R. I., Wulandari, F., Utomo, R. Y., Putri, D. D. P., Kato, J., & Meiyanto, E. (2021b). No TitleCurcumin-like structure (CCA-1.1) induces permanent mitotic arrest (Senescence) on Triple-negative breast cancer (TNBC) cells, 4T1. Research Journal of Pharmacy and Technology, 14(8), 4375–4382. https://doi.org/doi: 10.52711/0974-360X.2021.00760
Novitasari, D., Kato, J. ya, Ikawati, M., Putri, D. D. P., Wulandari, F., Widyarini, S., Zulfin, U. M., Salsabila, D. U., & Meiyanto, E. (2023). PGV-1 permanently arrests HepG2 cells in M phase and inhibits DMH-induced liver carcinogenesis in rats. Journal of Applied Pharmaceutical Science, 13(8), 204–211. https://doi.org/10.7324/JAPS.2023.131550
Okuno, M., Newhook, T. E., Joechle, K., Kawaguchi, Y., Bellis, M. De, Tzeng, C. D., Chun, Y. S., Aloia, T. A., Shindoh, J., Kaseb, A. O., & Vauthey, J. (2020). Characteristics of atypical large well-differentiated hepatocellular carcinoma: a speci fi c subtype of hepatocellular carcinoma? International Hepato-Pancreato-Biliary Association, 22(4), 545–552. https://doi.org/10.1016/j.hpb.2019.08.012
Qin, X.-Y., Su, T., Yu, W., & Kojima, S. (2020). Lipid desaturation-associated endoplasmic reticulum stress regulates MYCN gene expression in hepatocellular carcinoma cells. Cell Death & Disease, 11(1), 66. https://doi.org/10.1038/s41419-020-2257-y
Qin, X.-Y., Suzuki, H., Honda, M., Okada, H., Kaneko, S., Inoue, I., Ebisui, E., Hashimoto, K., Carninci, P., Kanki, K., Tatsukawa, H., Ishibashi, N., Masaki, T., Matsuura, T., Kagechika, H., Toriguchi, K., Hatano, E., Shirakami, Y., Shiota, G., … Kojima, S. (2018). Prevention of hepatocellular carcinoma by targeting MYCN-positive liver cancer stem cells with acyclic retinoid. Proceedings of the National Academy of Sciences of the United States of America, 115(19), 4969–4974. https://doi.org/10.1073/pnas.1802279115
Reksohadiprodjo, M. S., Timmerman, H., Sardjiman, Margono, S. A., Martono, S., Sugiyanto, Hakim, L., Nurlaila, Hakim, A. R., Puspitasari, I., Nurrochmad, A., Purwantiningsih, Oetari, & Yuwono, T. (2003). Derivatives of benzylidene cyclohexanone, benzylidene cyclopentanone, and benzylidene acetone, and therapeutic uses thereof (Patent No. US20030092772A1). United States.
Suenaga, Y., Einvik, C., Takatori, A., & Zhu, Y. (2021). Editorial: Molecular Mechanisms and Treatment of MYCN-Driven Tumors. 11(November), 10–12. https://doi.org/10.3389/fonc.2021.803443
Suenaga, Y., Kaneko, Y., Matsumoto, D., Hossain, M. S., Ozaki, T., & Nakagawara, A. (2009). Positive auto-regulation of MYCN in human neuroblastoma. Biochemical and Biophysical Research Communications, 390(1), 21–26. https://doi.org/10.1016/j.bbrc.2009.09.044
Sung, H., Ferlay, J., Siegel, R. L., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2021). Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: A Cancer Journal for Clinicians, 71(3), 209–249. https://doi.org/10.3322/caac.21660
Wulandari, F., Ikawati, M., Kirihata, M., Kato, J. Y., & Meiyanto, E. (2021a). A new curcumin analog, CCA-1.1, induces cell death and cell cycle arrest in WiDr colon cancer cells via ROS generation. Journal of Applied Pharmaceutical Science, 11(9), 099–105. https://doi.org/10.7324/JAPS.2021.1101014
Wulandari, F., Ikawati, M., Kirihata, M., Kato, J. Y., & Meiyanto, E. (2021b). Curcumin Analogs, PGV-1 and CCA-1.1 Exhibit Anti-migratory Effects and Suppress MMP9 Expression on WiDr Cells. Indonesian Biomedical Journal, 13(3), 271–280. https://doi.org/10.18585/inabj.v13i3.1583
Wulandari, F., Ikawati, M., Widyarini, S., Kirihata, M., Novitasari, D., Kato, J-y., Meiyanto, E. (2023). Tumour‐suppressive effects of curcumin analogs CCA‐1.1 and Pentagamavunone‐1 in colon cancer: In vivo and in vitro studies. Journal of Advanced Pharmaceutical Technology & Research, 14(4), 317-324. https://doi.org/10.4103/JAPTR.JAPTR_315_23
Barone, G., Anderson, J., Pearson, A. D. J., Petrie, K., & Chesler, L. (2013). New strategies in neuroblastoma: Therapeutic targeting of MYCN and ALK. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 19(21), 5814–5821. https://doi.org/10.1158/1078-0432.CCR-13-0680
Chen, X., Yang, G., Guo, X., Zhang, J., Sun, W., Liu, D., Wang, H., & Liu, S. (2022). DJ-1/FGFR-1 Signaling Pathway Contributes to Sorafenib Resistance in Hepatocellular Carcinoma. Oxidative Medicine and Cellular Longevity, 2022, 2543220. https://doi.org/10.1155/2022/2543220
Eberherr, C., Beck, A., Vokuhl, C., Becker, K., Häberle, B., Von Schweinitz, D., & Kappler, R. (2019). Targeting excessive MYCN expression using MLN8237 and JQ1 impairs the growth of hepatoblastoma cells. International Journal of Oncology, 54(5), 1853–1863. https://doi.org/10.3892/ijo.2019.4741
Fukuyama, K., Asagiri, M., Sugimoto, M., Tsushima, H., Seo, S., Taura, K., Uemoto, S., & Iwaisako, K. (2021). Gene expression profiles of liver cancer cell lines reveal two hepatocyte-like and fibroblast-like clusters. PLoS ONE, 16(2 February), 1–17. https://doi.org/10.1371/journal.pone.0245939
Hanahan, D. (2022). Hallmarks of Cancer: New Dimensions. Cancer Discovery, 12(1), 31–46. https://doi.org/10.1158/2159-8290.CD-21-1059
Hanahan, D., & Weinberg, R. A. (2011). Hallmarks of cancer: The next generation. Cell, 144(5), 646–674. https://doi.org/10.1016/j.cell.2011.02.013
Hasbiyani, N. A., Wulandari, F., Nugroho, E. P., Hermawan, A., & Meiyanto, E. (2021). Bioinformatics Analysis Confirms the Target Protein Underlying Mitotic Catastrophe of 4T1 Cells under Combinatorial Treatment of PGV-1 and Galangin. In Scientia Pharmaceutica (Vol. 89, Issue 3). https://doi.org/10.3390/scipharm89030038
Huang, M., & Weiss, W. A. (2013). Neuroblastoma and MYCN. Cold Spring Harbor Perspectives in Medicine, 3(10), a014415. https://doi.org/10.1101/cshperspect.a014415
Keating, G. M. (2017). Sorafenib: A Review in Hepatocellular Carcinoma. Targeted Oncology, 12(2), 243–253. https://doi.org/10.1007/s11523-017-0484-7
Kress, T. R., Sabò, A., & Amati, B. (2015). MYC: connecting selective transcriptional control to global RNA production. Nature Reviews Cancer, 15(10), 593–607. https://doi.org/10.1038/nrc3984
Larasati, Y. A., Yoneda-Kato, N., Nakamae, I., Yokoyama, T., Meiyanto, E., & Kato, J.-Y. (2018). Curcumin targets multiple enzymes involved in the ROS metabolic pathway to suppress tumor cell growth. Scientific Reports, 8(1), 2039. https://doi.org/10.1038/s41598-018-20179-6
Lestari, B., Nakamae, I., Yoneda-Kato, N., Morimoto, T., Kanaya, S., Yokoyama, T., Shionyu, M., Shirai, T., Meiyanto, E., & Kato, J. (2019). Pentagamavunon-1 (PGV-1) inhibits ROS metabolic enzymes and suppresses tumor cell growth by inducing M phase (prometaphase) arrest and cell senescence. Scientific Reports, 9(1), 14867. https://doi.org/10.1038/s41598-019-51244-3
Liu, R., Shi, P., Wang, Z., Yuan, C., & Cui, H. (2021). Molecular Mechanisms of MYCN Dysregulation in Cancers. In Frontiers in Oncology (Vol. 10, pp. 1–12). https://doi.org/https://doi.org/10.3389/fonc.2020.625332
Llovet, J. M., Kelley, R. K., Villanueva, A., Singal, A. G., Pikarsky, E., Roayaie, S., Lencioni, R., Koike, K., Zucman-Rossi, J., & Finn, R. S. (2021). Hepatocellular carcinoma. Nature Reviews. Disease Primers, 7(1), 6. https://doi.org/10.1038/s41572-020-00240-3
Meiyanto, E., Husnaa, U., Kastian, R. F., Putri, H., Larasati, Y. A., Khumaira, A., Pamungkas, D. D. P., Jenie, R. I., Kawaichi, M., Lestari, B., Yokoyama, T., & Kato, J.-Y. (2021). The Target Differences of Anti-Tumorigenesis Potential of Curcumin and its Analogues Against HER-2 Positive and Triple-Negative Breast Cancer Cells. Advanced Pharmaceutical Bulletin, 11(1), 188–196. https://doi.org/10.34172/apb.2021.020
Meiyanto, E., Novitasari, D., Utomo, R. Y., Susidarti, R. A., & Meiyanto, E. (2022). Bioinformatic and Molecular Interaction Studies Uncover That CCA-1.1 and PGV-1 Differentially Target Mitotic Regulatory Protein and Have a Synergistic Effect against Leukemia Cells. Indonesian Journal of Pharmacy, 33(2), 225–233.
Meiyanto, E., Putri, D. D. P., Susidarti, R. A., Murwanti, R., Sardjiman, Fitriasari, A., Husnaa, U., Purnomo, H., & Kawaichi, M. (2014). Curcumin and its analogues (PGV-0 and PGV-1) enhance sensitivity of resistant MCF-7 cells to doxorubicin through inhibition of HER2 and NF-kB activation. Asian Pacific Journal of Cancer Prevention: APJCP, 15(1), 179–184. https://doi.org/10.7314/apjcp.2014.15.1.179
Meiyanto, E., Putri, H., Arum Larasati, Y., Yudi Utomo, R., Istighfari Jenie, R., Ikawati, M., Lestari, B., Yoneda-Kato, N., Nakamae, I., Kawaichi, M., & Kato, J.-Y. (2019). Anti-proliferative and Anti-metastatic Potential of Curcumin Analogue, Pentagamavunon-1 (PGV-1), Toward Highly Metastatic Breast Cancer Cells in Correlation with ROS Generation. Advanced Pharmaceutical Bulletin, 9(3), 445–452. https://doi.org/10.15171/apb.2019.053
Meiyanto, E., Septisetyani, E. P., Larasati, Y. A., & Kawaichi, M. (2018). Curcumin Analog Pentagamavunon-1 (PGV-1) Sensitizes Widr Cells to 5-Fluorouracil through Inhibition of NF-κB Activation. Asian Pacific Journal of Cancer Prevention: APJCP, 19(1), 49–56. https://doi.org/10.22034/APJCP.2018.19.1.49
Moordiani, Novitasari, D., Susidarti, R. A., Ikawati, M., Kato, J. Y., & Meiyanto, E. (2023). Curcumin Analogs PGV-1 and CCA-1.1 Induce Cell Cycle Arrest in Human Hepatocellular Carcinoma Cells with Overexpressed MYCN. Indonesian Biomedical Journal, 15(2), 141–149. https://doi.org/10.18585/inabj.v15i2.2147
Musyayyadah, H., Wulandari, F., Nangimi, A. F., Dewi, A., Ikawati, M., & Meiyanto, E. (2021). The Growth Suppression Activity of Diosmin and PGV-1 Co-Treatment on 4T1 Breast Cancer Targets Mitotic Regulatory Proteins. 22, 2929–2938. https://doi.org/10.31557/APJCP.2021.22.9.2929
Novitasari, D., Jenie, R. I., Wulandari, F., Utomo, R. Y., Putri, D. D. P., Kato, J.-Y., & Meiyanto, E. (2021a). A Curcumin-like structure (CCA-1.1) induces permanent mitotic arrest (Senescence) on Triple-negative breast cancer (TNBC) cells, 4T1. Research Journal of Pharmacy and Technology, 14(8), 4375–82. https://doi.org/10.52711/0974-360X.2021.00760
Novitasari, D., Jenie, R. I., Wulandari, F., Utomo, R. Y., Putri, D. D. P., Kato, J., & Meiyanto, E. (2021b). No TitleCurcumin-like structure (CCA-1.1) induces permanent mitotic arrest (Senescence) on Triple-negative breast cancer (TNBC) cells, 4T1. Research Journal of Pharmacy and Technology, 14(8), 4375–4382. https://doi.org/doi: 10.52711/0974-360X.2021.00760
Novitasari, D., Kato, J. ya, Ikawati, M., Putri, D. D. P., Wulandari, F., Widyarini, S., Zulfin, U. M., Salsabila, D. U., & Meiyanto, E. (2023). PGV-1 permanently arrests HepG2 cells in M phase and inhibits DMH-induced liver carcinogenesis in rats. Journal of Applied Pharmaceutical Science, 13(8), 204–211. https://doi.org/10.7324/JAPS.2023.131550
Okuno, M., Newhook, T. E., Joechle, K., Kawaguchi, Y., Bellis, M. De, Tzeng, C. D., Chun, Y. S., Aloia, T. A., Shindoh, J., Kaseb, A. O., & Vauthey, J. (2020). Characteristics of atypical large well-differentiated hepatocellular carcinoma: a speci fi c subtype of hepatocellular carcinoma? International Hepato-Pancreato-Biliary Association, 22(4), 545–552. https://doi.org/10.1016/j.hpb.2019.08.012
Qin, X.-Y., Su, T., Yu, W., & Kojima, S. (2020). Lipid desaturation-associated endoplasmic reticulum stress regulates MYCN gene expression in hepatocellular carcinoma cells. Cell Death & Disease, 11(1), 66. https://doi.org/10.1038/s41419-020-2257-y
Qin, X.-Y., Suzuki, H., Honda, M., Okada, H., Kaneko, S., Inoue, I., Ebisui, E., Hashimoto, K., Carninci, P., Kanki, K., Tatsukawa, H., Ishibashi, N., Masaki, T., Matsuura, T., Kagechika, H., Toriguchi, K., Hatano, E., Shirakami, Y., Shiota, G., … Kojima, S. (2018). Prevention of hepatocellular carcinoma by targeting MYCN-positive liver cancer stem cells with acyclic retinoid. Proceedings of the National Academy of Sciences of the United States of America, 115(19), 4969–4974. https://doi.org/10.1073/pnas.1802279115
Reksohadiprodjo, M. S., Timmerman, H., Sardjiman, Margono, S. A., Martono, S., Sugiyanto, Hakim, L., Nurlaila, Hakim, A. R., Puspitasari, I., Nurrochmad, A., Purwantiningsih, Oetari, & Yuwono, T. (2003). Derivatives of benzylidene cyclohexanone, benzylidene cyclopentanone, and benzylidene acetone, and therapeutic uses thereof (Patent No. US20030092772A1). United States.
Suenaga, Y., Einvik, C., Takatori, A., & Zhu, Y. (2021). Editorial: Molecular Mechanisms and Treatment of MYCN-Driven Tumors. 11(November), 10–12. https://doi.org/10.3389/fonc.2021.803443
Suenaga, Y., Kaneko, Y., Matsumoto, D., Hossain, M. S., Ozaki, T., & Nakagawara, A. (2009). Positive auto-regulation of MYCN in human neuroblastoma. Biochemical and Biophysical Research Communications, 390(1), 21–26. https://doi.org/10.1016/j.bbrc.2009.09.044
Sung, H., Ferlay, J., Siegel, R. L., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2021). Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: A Cancer Journal for Clinicians, 71(3), 209–249. https://doi.org/10.3322/caac.21660
Wulandari, F., Ikawati, M., Kirihata, M., Kato, J. Y., & Meiyanto, E. (2021a). A new curcumin analog, CCA-1.1, induces cell death and cell cycle arrest in WiDr colon cancer cells via ROS generation. Journal of Applied Pharmaceutical Science, 11(9), 099–105. https://doi.org/10.7324/JAPS.2021.1101014
Wulandari, F., Ikawati, M., Kirihata, M., Kato, J. Y., & Meiyanto, E. (2021b). Curcumin Analogs, PGV-1 and CCA-1.1 Exhibit Anti-migratory Effects and Suppress MMP9 Expression on WiDr Cells. Indonesian Biomedical Journal, 13(3), 271–280. https://doi.org/10.18585/inabj.v13i3.1583
Wulandari, F., Ikawati, M., Widyarini, S., Kirihata, M., Novitasari, D., Kato, J-y., Meiyanto, E. (2023). Tumour‐suppressive effects of curcumin analogs CCA‐1.1 and Pentagamavunone‐1 in colon cancer: In vivo and in vitro studies. Journal of Advanced Pharmaceutical Technology & Research, 14(4), 317-324. https://doi.org/10.4103/JAPTR.JAPTR_315_23
Published
2024-06-20
How to Cite
Meiyanto, E., Moordiani, M., Novitasari, D., Novitasari, D., Susidarti, R. A., Ikawati, M., Kato, J.-Y., Hippo, Y., & Suenaga, Y. (2024). Pentagamavunone-1 suppresses MYCN-positive HuH-7 Cancer Cell Growth via Mitotic Arrest in vitro. Indonesian Journal of Pharmacy. https://doi.org/10.22146/ijp.10610
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Research Article
