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Molecular and Cellular Microbiology (MCM)  |  Bioactive Compounds and Functional Foods

Efficacy of Jasminum subtriplinerve Extract against 7,12-Dimethylbenz[a]anthracene-Induced Cancer in Mice

Phan Hong Minh1,2, Pham Thi Van Anh2, Bui Thanh Tung1, Ho My Dung1, Tran Thi Thu Trang6, Pham Thi Hong Nhung1, Nguyen Thi Hang3, Nguyen Thi Minh Nguyet4, Nguyen Viet Phong5, Le Ba Vinh5*, and Mai Phuong Thanh2*

1University of Medicine and Pharmacy, Vietnam National University, Hanoi, Vietnam
2Department of Pharmacology, Hanoi Medical University, Hanoi, Vietnam
3National Institute of Medical Materials (NIMM), Hanoi, 11022, Vietnam
4Vinmec- VinUni Institute of Immunology, Vinmec Healthcare System, Hanoi, Vietnam
5Institute of Marine Biochemistry, Vietnam Academy of Science and Technology, Hanoi, Vietnam
6Hanoi University Pharmacy, Hanoi, Vietnam

Correspondence to:
Vinh Le Ba,        vinhrooney@gmail.com
Received: July 24, 2024; Revised: September 3, 2024; Accepted: September 3, 2024

J. Microbiol. Biotechnol. 2024; 34(11): 2173-2183

Published November 28, 2024 https://doi.org/10.4014/jmb.2407.07045

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Jasminum subtriplinerve Blume tea is a traditional Vietnamese medicine used to treat impetigo, menstruation issues, and painful menstrual hematometra. Previous studies have shown that extracts and isolated compounds from J. subtriplinerve possess diverse pharmacological properties, such as antioxidant, antibacterial, and antidiabetic effects. However, their potential anticancer effects and underlying mechanisms of action have not been clear. Here, we examined the effects of J. subtriplinerve extracts against three human cancer cell lines. We also conducted in vivo analyses using a mouse model of 7,12-dimethylbenz[a]anthracene-induced breast cancer, including an investigation of changes in histological sections. The effect of the J. subtriplinerve ethyl acetate fraction on cytokine levels (IL-2, PGE2, TNF-α) in serum was determined using ELISA kits. Results showed that the ethyl acetate (EtOAc) fraction had the highest anti-proliferative activity (IC50 = 13.7 mg/ml) against the breast cancer (MCF-7) cell line, while the butanol (BuOH) and water fractions did not show any anticancer effects. Additionally, the EtOAc fraction at a dose of 14.4 mg/kg was able to elevate IL-2 levels and suppress the expression of PGE2 in the serum of mice. A remarkable decrease in the percentage of death and tumor incidence in mice was achieved following treatment with the EtOAc fraction at a dose of 14.4mg/kg. No abnormal parameters in blood were observed in the J. subtriplinerve treatment groups. These results suggest that J. subtriplinerve, when used as tea or a functional food, is nontoxic and has clear chemopreventive effects against breast cancer.

Keywords

Jasminium subtriplinerve Blume, breast cancer, DMBA, IL-2

Graphical Abstract


References

  1. Zhang J, Wu Y, Li Y, Li S, Liu J, Yang X, et al. 2024. Natural products and derivatives for breast cancer treatment: from drug discovery to molecular mechanism. Phytomedicine 155600.
    Pubmed
  2. Li M, Duan Y, Wang Y, Chen L, Abdelrahim ME, Yan J. 2024. The effect of Green green tea consumption on body mass index, lipoprotein, liver enzymes, and liver cancer: an updated systemic review incorporating a meta-analysis. Crit. Rev. Food Sci. Nutr. 64: 1043-1051.
    Pubmed
  3. Bray F, Laversanne M, Weiderpass E, Soerjomataram I. 2021. The ever‐increasing importance of cancer as a leading cause of premature death worldwide. Cancer 127: 3029-3030.
    Pubmed
  4. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. 2021. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer J. Clin. 71: 209-249.
    Pubmed
  5. Debela DT, Muzazu SG, Heraro KD, Ndalama MT, Mesele BW, Haile DC, et al. 2021. New approaches and procedures for cancer treatment: current perspectives. SAGE Open Med. 9: 20503121211034366.
    Pubmed PMC
  6. Khazir J, Mir BA, Pilcher L, Riley DL. 2014. Role of plants in anticancer drug discovery. Phytochem. Lett. 7: 173-181.
  7. Hue Ngan D, Hoai HTC, Mai Huong L, Hansen PE, Vang O. 2008. Bioactivities and chemical constituents of a Vietnamese medicinal plant Che Vang, Jasminum subtriplinerve Blume (Oleaceae). Nat. Prod. Res. 22: 942-949.
    Pubmed
  8. Vang APDO. 2005. Bioactivities and chemical constituents of a Vietnamese medicinal plant Jasminum subtriplinerve Blume (Che Vang). Department of Chemistry and Life Science, Roskilde University.
  9. Dai DN, Thang TD, Ogunwande IA, Lawal OA. 2016. Study on essential oils from the leaves of two Vietnamese plants: Jasminum subtriplinerve CL Blume and Vitex quinata (Lour) FN Williams. Nat. Prod. Res. 30: 860-864.
    Pubmed
  10. Huong NTH, Cu NKQ, Quy TV, Zidorn C, Ganzera M, Stuppner H. 2008. A new phenylpropanoid glycoside from Jasminum subtriplinerve blume. J. Asian Nat. Prod. Res. 10: 1035-1038.
    Pubmed
  11. Thang Hoang D, Hien Truong TT, Viet Duc N, Anh Hoang LT, Do TT, Vinh LB, et al. 2021. Hepatoprotective effects of extract of Helicteres hirsuta Lour. on liver fibrosis induced by carbon tetrachloride in rats. Appl. Sci. 11: 8758.
  12. Vinh LB, Nguyet NTM, Yang SY, Kim JH, Thanh NV, Cuong NX, et al. 2019. Cytotoxic triterpene saponins from the mangrove Aegiceras corniculatum. Nat. Prod. Res. 33: 628-634.
    Pubmed
  13. Vinh LB, Han YK, Park SY, Kim YJ, Phong NV, Kim E, et al. 2023. Identification of triterpenoid saponin inhibitors of interleukin (IL)33 signaling from the roots of Astragalus membranaceus. J. Funct. Foods 101: 105418.
  14. Han YK, Vinh LB, Nam M-h, Lee KY. 2023. Identification of compounds using HPLC-QTOF-MS online antioxidant activity mapping from aerial parts of Ligularia stenocephala. Appl. Biol. Chem. 66: 53.
  15. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
    Pubmed
  16. Rashidi M, Ziai SA, Moini ZT, Khalilnezhad A, Jamshidi H, Amani D. 2016. Umbelliprenin is potentially toxic against the HT29, CT26, MCF-7, 4T1, A172, and GL26 cell lines, potentially harmful against bone marrow-derived stem cells, and non-toxic against peripheral blood mononuclear cells. Iran. Red Crescent Med. J. 18: e35167.
    Pubmed PMC
  17. Augustine D, Rao RS, Anbu J, Chidambara MKN. 2017. In vitro antiproliferative effect of earthworm coelomic fluid of Eudrilus eugeniae, Eisenia foetida, and Perionyx excavatus on squamous cell carcinoma-9 cell line: a pilot study. Pharmacog. Res. 9: S61-S66.
    Pubmed PMC
  18. Karimi B, Ashrafi M, Shomali T, Yektaseresht A. 2019. Therapeutic effect of simvastatin on DMBA‐induced breast cancer in mice. Fundam. Clin. Pharmacol. 33: 84-93.
    Pubmed
  19. Duyen NT, Vinh LB, Phong NV, Khoi NM, Long PQ, Hien TT, et al. 2022. Steroid glycosides isolated from Paris polyphylla var. chinensis aerial parts and paris saponin II induces G1/S-phase MCF-7 cell cycle arrest. Carbohydr. Res. 519: 108613.
    Pubmed
  20. Edmondson JM, Armstrong LS, Martinez AO. 1988. A rapid and simple MTT-based spectrophotometric assay for determining drug sensitivity in monolayer cultures. J. Tissue Culture Methods. 11: 15-17.
  21. Stiborová M, Černá V, Moserová M, Mrízová I, Arlt VM, Frei E. 2014. The anticancer drug ellipticine activated with cytochrome P450 mediates DNA damage determining its pharmacological efficiencies: studies with rats, hepatic cytochrome P450 reductase null (HRN™) mice and pure enzymes. Int. J. Mol. Sci. 16: 284-306.
    Pubmed PMC
  22. Schreiber RD, Old LJ, Smyth MJ. 2011. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331: 1565-1570.
    Pubmed
  23. Paul W. 1999. Fundamental immunology 4th edition.
  24. Stauber DJ, Debler EW, Horton PA, Smith KA, Wilson IA. 2006. Crystal structure of the IL-2 signaling complex: paradigm for a heterotrimeric cytokine receptor. Proc. Natl. Acad. Sci. USA 103: 2788-2793.
    Pubmed PMC
  25. Massari F, Santoni M, Ciccarese C, Santini D. 2015. The immunocheckpoints in modern oncology: the next 15 years. Expert. Opin. Biol. Ther. 15: 917-921.
    Pubmed
  26. Pels E. 2015. Comparison of saliva interleukin-2 concentration to the condition of gums in children with acute lymphoblastic leukaemia during anti-tumour treatment. Cancer Chemother. Pharmacol. 76: 205-210.
    Pubmed PMC
  27. Finetti F, Travelli C, Ercoli J, Colombo G, Buoso E, Trabalzini L. 2020. Prostaglandin E2 and cancer: insight into tumor progression and immunity. Biology (Basel) 9: 434.
    Pubmed PMC
  28. Kunhachan P, Banchonglikitkul C, Kajsongkram T, Khayungarnnawee A, Leelamanit W. 2012. Chemical composition, toxicity and vasodilatation effect of the flowers extract of Jasminum sambac (L.) Ait.“G. Duke of Tuscany”. Evid. Based Complement. Alternative Med. 2012: 471312.
    Pubmed PMC
  29. Budin SB, Siti Nor Ain SM, Omar B, Taib IS, Hidayatulfathi O. 2012. Acute and subacute oral toxicity of Litsea elliptica Blume essential oil in rats. J. Zhejiang Univ. Sci. B 13: 783-790.
    Pubmed PMC
  30. Henn JG, Steffens L, de Moura Sperotto ND, de Souza Ponce B, Veríssimo RM, Boaretto FBM, et al. 2019. Toxicological evaluation of a standardized hydroethanolic extract from leaves of Plantago australis and its major compound, verbascoside. J. Ethnopharmacol. 229: 145-156.
    Pubmed
  31. Harbeck N, Penault-Llorca F, Cortes J, Gnant M, Houssami N, Poortmans P, et al. 2019. Breast cancer. Nat. Rev. Dis. Primers. 5: 1-31.
    Pubmed
  32. Hermawan A, Putri H. 2018. Current report of natural product development against breast cancer stem cells. Int. J. Biochem. Cell Biol. 104: 114-132.
    Pubmed

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Article

Research article

J. Microbiol. Biotechnol. 2024; 34(11): 2173-2183

Published online November 28, 2024 https://doi.org/10.4014/jmb.2407.07045

Copyright © The Korean Society for Microbiology and Biotechnology.

Efficacy of Jasminum subtriplinerve Extract against 7,12-Dimethylbenz[a]anthracene-Induced Cancer in Mice

Phan Hong Minh1,2, Pham Thi Van Anh2, Bui Thanh Tung1, Ho My Dung1, Tran Thi Thu Trang6, Pham Thi Hong Nhung1, Nguyen Thi Hang3, Nguyen Thi Minh Nguyet4, Nguyen Viet Phong5, Le Ba Vinh5*, and Mai Phuong Thanh2*

1University of Medicine and Pharmacy, Vietnam National University, Hanoi, Vietnam
2Department of Pharmacology, Hanoi Medical University, Hanoi, Vietnam
3National Institute of Medical Materials (NIMM), Hanoi, 11022, Vietnam
4Vinmec- VinUni Institute of Immunology, Vinmec Healthcare System, Hanoi, Vietnam
5Institute of Marine Biochemistry, Vietnam Academy of Science and Technology, Hanoi, Vietnam
6Hanoi University Pharmacy, Hanoi, Vietnam

Correspondence to:Vinh Le Ba,        vinhrooney@gmail.com

Received: July 24, 2024; Revised: September 3, 2024; Accepted: September 3, 2024

Abstract

Jasminum subtriplinerve Blume tea is a traditional Vietnamese medicine used to treat impetigo, menstruation issues, and painful menstrual hematometra. Previous studies have shown that extracts and isolated compounds from J. subtriplinerve possess diverse pharmacological properties, such as antioxidant, antibacterial, and antidiabetic effects. However, their potential anticancer effects and underlying mechanisms of action have not been clear. Here, we examined the effects of J. subtriplinerve extracts against three human cancer cell lines. We also conducted in vivo analyses using a mouse model of 7,12-dimethylbenz[a]anthracene-induced breast cancer, including an investigation of changes in histological sections. The effect of the J. subtriplinerve ethyl acetate fraction on cytokine levels (IL-2, PGE2, TNF-α) in serum was determined using ELISA kits. Results showed that the ethyl acetate (EtOAc) fraction had the highest anti-proliferative activity (IC50 = 13.7 mg/ml) against the breast cancer (MCF-7) cell line, while the butanol (BuOH) and water fractions did not show any anticancer effects. Additionally, the EtOAc fraction at a dose of 14.4 mg/kg was able to elevate IL-2 levels and suppress the expression of PGE2 in the serum of mice. A remarkable decrease in the percentage of death and tumor incidence in mice was achieved following treatment with the EtOAc fraction at a dose of 14.4mg/kg. No abnormal parameters in blood were observed in the J. subtriplinerve treatment groups. These results suggest that J. subtriplinerve, when used as tea or a functional food, is nontoxic and has clear chemopreventive effects against breast cancer.

Keywords: Jasminium subtriplinerve Blume, breast cancer, DMBA, IL-2

References

  1. Zhang J, Wu Y, Li Y, Li S, Liu J, Yang X, et al. 2024. Natural products and derivatives for breast cancer treatment: from drug discovery to molecular mechanism. Phytomedicine 155600.
    Pubmed
  2. Li M, Duan Y, Wang Y, Chen L, Abdelrahim ME, Yan J. 2024. The effect of Green green tea consumption on body mass index, lipoprotein, liver enzymes, and liver cancer: an updated systemic review incorporating a meta-analysis. Crit. Rev. Food Sci. Nutr. 64: 1043-1051.
    Pubmed
  3. Bray F, Laversanne M, Weiderpass E, Soerjomataram I. 2021. The ever‐increasing importance of cancer as a leading cause of premature death worldwide. Cancer 127: 3029-3030.
    Pubmed
  4. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. 2021. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer J. Clin. 71: 209-249.
    Pubmed
  5. Debela DT, Muzazu SG, Heraro KD, Ndalama MT, Mesele BW, Haile DC, et al. 2021. New approaches and procedures for cancer treatment: current perspectives. SAGE Open Med. 9: 20503121211034366.
    Pubmed KoreaMed
  6. Khazir J, Mir BA, Pilcher L, Riley DL. 2014. Role of plants in anticancer drug discovery. Phytochem. Lett. 7: 173-181.
  7. Hue Ngan D, Hoai HTC, Mai Huong L, Hansen PE, Vang O. 2008. Bioactivities and chemical constituents of a Vietnamese medicinal plant Che Vang, Jasminum subtriplinerve Blume (Oleaceae). Nat. Prod. Res. 22: 942-949.
    Pubmed
  8. Vang APDO. 2005. Bioactivities and chemical constituents of a Vietnamese medicinal plant Jasminum subtriplinerve Blume (Che Vang). Department of Chemistry and Life Science, Roskilde University.
  9. Dai DN, Thang TD, Ogunwande IA, Lawal OA. 2016. Study on essential oils from the leaves of two Vietnamese plants: Jasminum subtriplinerve CL Blume and Vitex quinata (Lour) FN Williams. Nat. Prod. Res. 30: 860-864.
    Pubmed
  10. Huong NTH, Cu NKQ, Quy TV, Zidorn C, Ganzera M, Stuppner H. 2008. A new phenylpropanoid glycoside from Jasminum subtriplinerve blume. J. Asian Nat. Prod. Res. 10: 1035-1038.
    Pubmed
  11. Thang Hoang D, Hien Truong TT, Viet Duc N, Anh Hoang LT, Do TT, Vinh LB, et al. 2021. Hepatoprotective effects of extract of Helicteres hirsuta Lour. on liver fibrosis induced by carbon tetrachloride in rats. Appl. Sci. 11: 8758.
  12. Vinh LB, Nguyet NTM, Yang SY, Kim JH, Thanh NV, Cuong NX, et al. 2019. Cytotoxic triterpene saponins from the mangrove Aegiceras corniculatum. Nat. Prod. Res. 33: 628-634.
    Pubmed
  13. Vinh LB, Han YK, Park SY, Kim YJ, Phong NV, Kim E, et al. 2023. Identification of triterpenoid saponin inhibitors of interleukin (IL)33 signaling from the roots of Astragalus membranaceus. J. Funct. Foods 101: 105418.
  14. Han YK, Vinh LB, Nam M-h, Lee KY. 2023. Identification of compounds using HPLC-QTOF-MS online antioxidant activity mapping from aerial parts of Ligularia stenocephala. Appl. Biol. Chem. 66: 53.
  15. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
    Pubmed
  16. Rashidi M, Ziai SA, Moini ZT, Khalilnezhad A, Jamshidi H, Amani D. 2016. Umbelliprenin is potentially toxic against the HT29, CT26, MCF-7, 4T1, A172, and GL26 cell lines, potentially harmful against bone marrow-derived stem cells, and non-toxic against peripheral blood mononuclear cells. Iran. Red Crescent Med. J. 18: e35167.
    Pubmed KoreaMed
  17. Augustine D, Rao RS, Anbu J, Chidambara MKN. 2017. In vitro antiproliferative effect of earthworm coelomic fluid of Eudrilus eugeniae, Eisenia foetida, and Perionyx excavatus on squamous cell carcinoma-9 cell line: a pilot study. Pharmacog. Res. 9: S61-S66.
    Pubmed KoreaMed
  18. Karimi B, Ashrafi M, Shomali T, Yektaseresht A. 2019. Therapeutic effect of simvastatin on DMBA‐induced breast cancer in mice. Fundam. Clin. Pharmacol. 33: 84-93.
    Pubmed
  19. Duyen NT, Vinh LB, Phong NV, Khoi NM, Long PQ, Hien TT, et al. 2022. Steroid glycosides isolated from Paris polyphylla var. chinensis aerial parts and paris saponin II induces G1/S-phase MCF-7 cell cycle arrest. Carbohydr. Res. 519: 108613.
    Pubmed
  20. Edmondson JM, Armstrong LS, Martinez AO. 1988. A rapid and simple MTT-based spectrophotometric assay for determining drug sensitivity in monolayer cultures. J. Tissue Culture Methods. 11: 15-17.
  21. Stiborová M, Černá V, Moserová M, Mrízová I, Arlt VM, Frei E. 2014. The anticancer drug ellipticine activated with cytochrome P450 mediates DNA damage determining its pharmacological efficiencies: studies with rats, hepatic cytochrome P450 reductase null (HRN™) mice and pure enzymes. Int. J. Mol. Sci. 16: 284-306.
    Pubmed KoreaMed
  22. Schreiber RD, Old LJ, Smyth MJ. 2011. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331: 1565-1570.
    Pubmed
  23. Paul W. 1999. Fundamental immunology 4th edition.
  24. Stauber DJ, Debler EW, Horton PA, Smith KA, Wilson IA. 2006. Crystal structure of the IL-2 signaling complex: paradigm for a heterotrimeric cytokine receptor. Proc. Natl. Acad. Sci. USA 103: 2788-2793.
    Pubmed KoreaMed
  25. Massari F, Santoni M, Ciccarese C, Santini D. 2015. The immunocheckpoints in modern oncology: the next 15 years. Expert. Opin. Biol. Ther. 15: 917-921.
    Pubmed
  26. Pels E. 2015. Comparison of saliva interleukin-2 concentration to the condition of gums in children with acute lymphoblastic leukaemia during anti-tumour treatment. Cancer Chemother. Pharmacol. 76: 205-210.
    Pubmed KoreaMed
  27. Finetti F, Travelli C, Ercoli J, Colombo G, Buoso E, Trabalzini L. 2020. Prostaglandin E2 and cancer: insight into tumor progression and immunity. Biology (Basel) 9: 434.
    Pubmed KoreaMed
  28. Kunhachan P, Banchonglikitkul C, Kajsongkram T, Khayungarnnawee A, Leelamanit W. 2012. Chemical composition, toxicity and vasodilatation effect of the flowers extract of Jasminum sambac (L.) Ait.“G. Duke of Tuscany”. Evid. Based Complement. Alternative Med. 2012: 471312.
    Pubmed KoreaMed
  29. Budin SB, Siti Nor Ain SM, Omar B, Taib IS, Hidayatulfathi O. 2012. Acute and subacute oral toxicity of Litsea elliptica Blume essential oil in rats. J. Zhejiang Univ. Sci. B 13: 783-790.
    Pubmed KoreaMed
  30. Henn JG, Steffens L, de Moura Sperotto ND, de Souza Ponce B, Veríssimo RM, Boaretto FBM, et al. 2019. Toxicological evaluation of a standardized hydroethanolic extract from leaves of Plantago australis and its major compound, verbascoside. J. Ethnopharmacol. 229: 145-156.
    Pubmed
  31. Harbeck N, Penault-Llorca F, Cortes J, Gnant M, Houssami N, Poortmans P, et al. 2019. Breast cancer. Nat. Rev. Dis. Primers. 5: 1-31.
    Pubmed
  32. Hermawan A, Putri H. 2018. Current report of natural product development against breast cancer stem cells. Int. J. Biochem. Cell Biol. 104: 114-132.
    Pubmed