Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells

Süleyman İlhan; Çisil Çamlı Pulat

doi:10.17776/csj.829358

EN

Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells

Abstract

In the present study, biogenic silver nanoparticles (PL-AgNPs) were synthesized by using Piper longum (PL) dried fruit extract and investigated the effect of PL-AgNPs on angiogenesis and signal transduction pathway of hypoxia-inducible factor alpha (HIF-1α)/vascular endothelial growth factor (VEGF) on human prostate cancer cells. The prepared PL-AgNPs were characterized by ultraviolet-visible (UV-vis) spectroscopy, scanning electron microscopy (SEM), energy-dispersive X-ray spectroscopy (EDX) and dynamic light scattering (DLS) analysis. Potential cytotoxic and anti-angiogenic effects of PL-AgNPs were evaluated on PC-3 and DU-145 prostate cancer cells. Cytotoxicity was evaluated by MTT assay. The anti-angiogenic effect was investigated via a cell migration assay. Protein and mRNA levels of key angiogenesis related molecules such as VEGF and HIF-1α were evaluated via ELISA and qRT-PCR assays. UV-vis spectroscopy showed an absorbance peak at 450 nm confirming the PL-AgNPs synthesis. Various characterization techniques revealed that the average size of synthesized PL-AgNPs was below 100 nm. The cytotoxic effect was elevated in a concentration-dependent manner (p˂0.05). The biosynthesized PL-AgNPs inhibited cell migration and reduced the levels of both protein and mRNA levels of VEGF and HIF-1α in prostate cancer cells (p˂0.05). Results revealed that the PL extract with AgNO3 nanoparticles may be a potential candidate for developing novel anticancer and antiangiogenic compounds for prostate cancer.

Keywords

Silver nanoparticles, prostate cancer, VEGF, Piper longum, HIF-1α

References

[1] Bray F., Ferlay J., Soerjomataram I., Siegel R.L., Torre L.A., Jemal A., Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries, CA. Cancer J. Clin., 68(6) (2018) 394–424
[2] Paduch R., The role of lymphangiogenesis and angiogenesis in tumor metastasis, Cell. Oncol., 39(5) (2016) 397-410
[3] Ahn G.O., Seita J., Hong B.J., Kim Y.E., Bok S., Lee C.J., et al., Transcriptional activation of hypoxia-inducible factor-1 (HIF-1) in myeloid cells promotes angiogenesis through VEGF and S100A8, Proc. Natl. Acad. Sci. U. S. A., 11(7) (2014) 2698-2703.
[4] Cragg G.M., Newman D.J., Natural products: A continuing source of novel drug leads, Biochim. Biophys. Acta - Gen. Subj., 1830(6) (2013) 3670-3695.
[5] Ahmad N., Fazal H., Abbasi B.H., Farooq S., Ali M., Khan M.A., Biological role of Piper nigrum L. (Black pepper): A review, Asian Pac. J. Trop. Biomed., 2012(1) (2012) 1945–1953
[6] Liu H.-L., Luo R., Chen X.-Q., Ba Y.-Y., Zheng L., Guo W.-W., et al., Identification and simultaneous quantification of five alkaloids in Piper longum L. by HPLC–ESI-MSn and UFLC–ESI-MS/MS and their application to Piper nigrum L., Food Chem., 177 (2015) 191–196
[7] Kumar S., Kamboj J., Suman, Sharma S., Overview for Various Aspects of the Health Benefits of Piper Longum Linn. Fruit, J. Acupunct. Meridian Stud., 4(2) (2011) 134–140
[8] Justin Packia Jacob S., Finub J.S., Narayanan A., Synthesis of silver nanoparticles using Piper longum leaf extracts and its cytotoxic activity against Hep-2 cell line, Colloids Surfaces B Biointerfaces, 91(1) (2012) 212–214.
[9] Sunila E.S., Kuttan G., Immunomodulatory and antitumor activity of Piper longum Linn. and piperine, J. Ethnopharmacol., 90(2-3) (2004) 339-346.
[10] Sruthi D., John Zachariah T., In vitro antioxidant activity and cytotoxicity of sequential extracts from selected black pepper (Piper nigrum L.) varieties and Piper species, Int. Food Res. J., 24(1) (2017) 75-85.

[11] Kumar S., Arya P., Mukherjee C., Singh B.K., Singh N., Parmar V.S., et al., Novel Aromatic Ester from Piper longum and Its Analogues Inhibit Expression of Cell Adhesion Molecules on Endothelial Cells †, Biochemistry, 44(48) (2005) 15944–15952.
[12] Natarajan K.S., Narasimhan M., Shanmugasundaram K.R., Shanmugasundaram E.R.B., Antioxidant activity of a salt–spice–herbal mixture against free radical induction, J. Ethnopharmacol., 105 (2006) 76–83.
[13] Priya N.., Kumari S., Research Article Antiviral Activities and Cytotoxicity Assay of Seed Extracts of Piper longum and Piper nigrum on Human Cell Lines, Int. J. Pharm. Sci. Rev. Res., 44 (2017) 197–202
[14] Pradeep C.R., Kuttan G., Effect of piperine on the inhibition of lung metastasis induced B16F-10 melanoma cells in mice., Clin. Exp. Metastasis, 19 (2002) 703–708.
[15] Li S., Lei Y., Jia Y., Li N., Wink M., Ma Y., Piperine, a piperidine alkaloid from Piper nigrum re-sensitizes P-gp, MRP1 and BCRP dependent multidrug resistant cancer cells, Phytomedicine, 19(1) (2011) 83–87.
[16] Lee W., Kim K.-Y., Yu S.-N., Kim S.-H., Chun S.-S., Ji J.-H., et al., Pipernonaline from Piper longum Linn. induces ROS-mediated apoptosis in human prostate cancer PC-3 cells, Biochem. Biophys. Res. Commun., 430(1) (2013) 406–412.
[17] Bezerra D.P., Pessoa C., Moraes M.O. de, Alencar N.M.N. de, Mesquita R.O., Lima M.W., et al., In vivo growth inhibition of sarcoma 180 by piperlonguminine, an alkaloid amide from the Piper species, J. Appl. Toxicol., 28 (2008) 599–607
[18] Patra J.K., Das G., Fraceto L.F., Campos E.V.R., Rodriguez-Torres M. del P., Acosta-Torres L.S., et al., Nano based drug delivery systems: recent developments and future prospects, J. Nanobiotechnology, 16 (2018) 1-33.
[19] Chandran S.P., Chaudhary M., Pasricha R., Ahmad A., Sastry M., Synthesis of Gold Nanotriangles and Silver Nanoparticles Using Aloe vera Plant Extract, Biotechnol. Prog., 22 (2006) 577–583
[20] Sathishkumar M., Sneha K., Won S.W., Cho C.-W., Kim S., Yun Y.-S., Cinnamon zeylanicum bark extract and powder mediated green synthesis of nano-crystalline silver particles and its bactericidal activity, Colloids Surfaces B Biointerfaces, 73 (2009) 332–338.
[21] McNamara K., Tofail S.A.M., Nanoparticles in biomedical applications, Adv. Phys. X, 2 (2017) 54–88
[22] Siddiqi K.S., Husen A., Rao R.A.K., A review on biosynthesis of silver nanoparticles and their biocidal properties, J. Nanobiotechnology, 16(1) (2018) 14.
[23] Saifuddin N., Wong C.W., Yasumira A.A.N., Rapid Biosynthesis of Silver Nanoparticles Using Culture Supernatant of Bacteria with Microwave Irradiation, E-Journal Chem., 6 (2009) 61–70.
[24] Kowshik M., Ashtaputre S., Kharrazi S., Vogel W., Urban J., Kulkarni S.K., et al., Extracellular synthesis of silver nanoparticles by a silver-tolerant yeast strain MKY3, Nanotechnology, 14 (2003) 95–100.
[25] Marslin G., Siram K., Maqbool Q., Selvakesavan R., Kruszka D., Kachlicki P., et al., Secondary Metabolites in the Green Synthesis of Metallic Nanoparticles, Materials (Basel).,11(6) (2018) 1-25.
[26] Rajesh R.W., Jaya L.R., Niranjan K.S., Vijay D.M., Sahebrao B.K., Phytosynthesis of Silver Nanoparticle Using Gliricidia sepium (Jacq.), Curr. Nanosci., 5(1) (2009) 112-117.
[27] Golovine K. V., Makhov P.B., Teper E., Kutikov A., Canter D., Uzzo R.G., et al., Piperlongumine induces rapid depletion of the androgen receptor in human prostate cancer cells, Prostate, 73 (2013) 23–30.
[28] Shin J.-M., Jeong Y.-J., Cho H.-J., Park K.-K., Chung I.-K., Lee I.-K., et al., Melittin Suppresses HIF-1α/VEGF Expression through Inhibition of ERK and mTOR/p70S6K Pathway in Human Cervical Carcinoma Cells, PLoS One, 8(7) (2013) e69380
[29] Hosseini H., Rajabibazl M., Ebrahimizadeh W., Dehbidi G.R., Inhibiting angiogenesis with human single-chain variable fragment antibody targeting VEGF, Microvasc. Res., 97 (2015) 13–18.
[30] Ferrara N., Gerber H.-P., LeCouter J., The biology of VEGF and its receptors, Nat. Med., 9 (2003) 669–676
[31] Semenza G.L., Targeting HIF-1 for cancer therapy, Nat. Rev. Cancer, 3 (2003) 721–732.

Details

Primary Language

English

Subjects

Structural Biology

Journal Section

Research Article

Authors

Süleyman İlhan ^*
0000-0002-6584-3979
Türkiye

Çisil Çamlı Pulat
0000-0002-9641-7219
Türkiye

Publication Date

June 30, 2021

Submission Date

November 21, 2020

Acceptance Date

May 27, 2021

Published in Issue

Year 2021 Volume: 42 Number: 2

DOI

https://doi.org/10.17776/csj.829358

IZ

https://izlik.org/JA99YY52PA

APA

İlhan, S., & Çamlı Pulat, Ç. (2021). Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells. Cumhuriyet Science Journal, 42(2), 236-244. https://doi.org/10.17776/csj.829358

AMA

1.İlhan S, Çamlı Pulat Ç. Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells. CSJ. 2021;42(2):236-244. doi:10.17776/csj.829358

Chicago

İlhan, Süleyman, and Çisil Çamlı Pulat. 2021. “Biogenic Silver Nanoparticles Synthesized from Piper Longum Fruit Extract Inhibit HIF-1α VEGF Mediated Angiogenesis in Prostate Cancer Cells”. Cumhuriyet Science Journal 42 (2): 236-44. https://doi.org/10.17776/csj.829358.

EndNote

İlhan S, Çamlı Pulat Ç (June 1, 2021) Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells. Cumhuriyet Science Journal 42 2 236–244.

IEEE

[1]S. İlhan and Ç. Çamlı Pulat, “Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells”, CSJ, vol. 42, no. 2, pp. 236–244, June 2021, doi: 10.17776/csj.829358.

ISNAD

İlhan, Süleyman - Çamlı Pulat, Çisil. “Biogenic Silver Nanoparticles Synthesized from Piper Longum Fruit Extract Inhibit HIF-1α VEGF Mediated Angiogenesis in Prostate Cancer Cells”. Cumhuriyet Science Journal 42/2 (June 1, 2021): 236-244. https://doi.org/10.17776/csj.829358.

JAMA

1.İlhan S, Çamlı Pulat Ç. Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells. CSJ. 2021;42:236–244.

MLA

İlhan, Süleyman, and Çisil Çamlı Pulat. “Biogenic Silver Nanoparticles Synthesized from Piper Longum Fruit Extract Inhibit HIF-1α VEGF Mediated Angiogenesis in Prostate Cancer Cells”. Cumhuriyet Science Journal, vol. 42, no. 2, June 2021, pp. 236-44, doi:10.17776/csj.829358.

Vancouver

1.Süleyman İlhan, Çisil Çamlı Pulat. Biogenic silver nanoparticles synthesized from Piper longum fruit extract inhibit HIF-1α/VEGF mediated angiogenesis in prostate cancer cells. CSJ. 2021 Jun. 1;42(2):236-44. doi:10.17776/csj.829358

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