Skip to main content
Top
Published in: BMC Cancer 1/2023

Open Access 01-12-2023 | Hepatocellular Carcinoma | Research

Characterization of a novel peptide mined from the Red Sea brine pools and modified to enhance its anticancer activity

Authors: Youssef T. Abdou, Sheri M. Saleeb, Khaled M. A. Abdel-Raouf, Mohamed Allam, Mustafa Adel, Asma Amleh

Published in: BMC Cancer | Issue 1/2023

Login to get access

Abstract

Drug resistance is a major cause of the inefficacy of conventional cancer therapies, and often accompanied by severe side effects. Thus, there is an urgent need to develop novel drugs with low cytotoxicity, high selectivity and minimal acquired chemical resistance. Peptide-based drugs (less than 0.5 kDa) have emerged as a potential approach to address these issues due to their high specificity and potent anticancer activity. In this study, we developed a support vector machine model (SVM) to detect the potential anticancer properties of novel peptides by scanning the American University in Cairo (AUC) Red Sea metagenomics library. We identified a novel 37-mer antimicrobial peptide through SVM pipeline analysis and characterized its anticancer potential through in silico cross-examination. The peptide sequence was further modified to enhance its anticancer activity, analyzed for gene ontology, and subsequently synthesized. To evaluate the anticancer properties of the modified 37-mer peptide, we assessed its effect on the viability and morphology of SNU449, HepG2, SKOV3, and HeLa cells, using an MTT assay. Additionally, we evaluated the migration capabilities of SNU449 and SKOV3 cells using a scratch-wound healing assay. The targeted selectivity of the modified peptide was examined by evaluating its hemolytic activity on human erythrocytes. Treatment with the peptide significantly reduced cell viability and had a critical impact on the morphology of hepatocellular carcinoma (SNU449 and HepG2), and ovarian cancer (SKOV3) cells, with a marginal effect on cervical cancer cell lines (HeLa). The viability of a human fibroblast cell line (1Br-hTERT) was also significantly reduced by peptide treatment, as were the proliferation and migration abilities of SNU449 and SKOV3 cells. The annexin V assay revealed programmed cell death (apoptosis) as one of the potential cellular death pathways in SNU449 cells upon peptide treatment. Finally, the peptide exhibited antimicrobial effects on both gram-positive and gram-negative bacterial strains. The findings presented here suggest the potential of our novel peptide as a potent anticancer and antimicrobial agent.
Appendix
Available only for authorised users
Literature
2.
go back to reference Craik DJ, Fairlie DP, Liras S, Price D. The future of peptide-based drugs. Chem Biol Drug Des. 2013;81(1):136–47.CrossRefPubMed Craik DJ, Fairlie DP, Liras S, Price D. The future of peptide-based drugs. Chem Biol Drug Des. 2013;81(1):136–47.CrossRefPubMed
3.
go back to reference Coussens NP, Braisted JC, Peryea T, Sittampalam GS, Simeonov A, Hall MD. Small-molecule screens: a gateway to cancer therapeutic agents with case studies of food and drug administration-approved drugs. Pharmacol Rev. 2017;69(4):479–96.CrossRefPubMedPubMedCentral Coussens NP, Braisted JC, Peryea T, Sittampalam GS, Simeonov A, Hall MD. Small-molecule screens: a gateway to cancer therapeutic agents with case studies of food and drug administration-approved drugs. Pharmacol Rev. 2017;69(4):479–96.CrossRefPubMedPubMedCentral
4.
go back to reference Felício MR, Silva ON, Gonçalves S, Santos NC, Franco OL. Peptides with dual antimicrobial and anticancer activities. Front Chem. 2017;5(February):1–9. Felício MR, Silva ON, Gonçalves S, Santos NC, Franco OL. Peptides with dual antimicrobial and anticancer activities. Front Chem. 2017;5(February):1–9.
5.
go back to reference Schweizer F. Cationic amphiphilic peptides with cancer-selective toxicity. Eur J Pharmacol. 2009;625(1–3):190–4.CrossRefPubMed Schweizer F. Cationic amphiphilic peptides with cancer-selective toxicity. Eur J Pharmacol. 2009;625(1–3):190–4.CrossRefPubMed
7.
go back to reference Dai SX, Li WX, Han FF, Guo YC, Zheng JJ, Liu JQ, et al. In silico identification of anti-cancer compounds and plants from traditional Chinese medicine database. Sci Rep. 2016;6:25462.CrossRefPubMedPubMedCentral Dai SX, Li WX, Han FF, Guo YC, Zheng JJ, Liu JQ, et al. In silico identification of anti-cancer compounds and plants from traditional Chinese medicine database. Sci Rep. 2016;6:25462.CrossRefPubMedPubMedCentral
8.
go back to reference McKeown STW, Lundy FT, Nelson J, Lockhart D, Irwin CR, Cowan CG, et al. The cytotoxic effects of human neutrophil peptide-1 (HNP1) and lactoferrin on oral squamous cell carcinoma (OSCC) in vitro. Oral Oncol. 2006;42(7):685–90.CrossRefPubMed McKeown STW, Lundy FT, Nelson J, Lockhart D, Irwin CR, Cowan CG, et al. The cytotoxic effects of human neutrophil peptide-1 (HNP1) and lactoferrin on oral squamous cell carcinoma (OSCC) in vitro. Oral Oncol. 2006;42(7):685–90.CrossRefPubMed
11.
go back to reference Papo N, Shai Y. Cellular and Molecular Life Sciences Visions & Reflections Host defense peptides as new weapons in cancer treatment. Cell Mol Life Sci. 2005;62:784–90.CrossRefPubMed Papo N, Shai Y. Cellular and Molecular Life Sciences Visions & Reflections Host defense peptides as new weapons in cancer treatment. Cell Mol Life Sci. 2005;62:784–90.CrossRefPubMed
12.
go back to reference Tyagi A, Kapoor P, Kumar R, Chaudhary K, Gautam A, Raghava GPS. In silico models for designing and discovering novel anticancer peptides. Sci Rep. 2013;3:2984.CrossRefPubMedPubMedCentral Tyagi A, Kapoor P, Kumar R, Chaudhary K, Gautam A, Raghava GPS. In silico models for designing and discovering novel anticancer peptides. Sci Rep. 2013;3:2984.CrossRefPubMedPubMedCentral
15.
go back to reference Adel M, Elbehery AHA, Aziz SK, Aziz RK, Grossart HP, Siam R. Viruses-to-mobile genetic elements skew in the deep Atlantis II brine pool sediments. Sci Rep. 2016;6(July):1–9. Adel M, Elbehery AHA, Aziz SK, Aziz RK, Grossart HP, Siam R. Viruses-to-mobile genetic elements skew in the deep Atlantis II brine pool sediments. Sci Rep. 2016;6(July):1–9.
16.
go back to reference Huse SM, Huber JA, Morrison HG, Sogin ML, Welch DM. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 2007;8(7):1–9.CrossRef Huse SM, Huber JA, Morrison HG, Sogin ML, Welch DM. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 2007;8(7):1–9.CrossRef
18.
go back to reference Gomez-Alvarez V, Teal TK, Schmidt TM. Systematic artifacts in metagenomes from complex microbial communities. ISME J. 2009;3(11):1314–7.CrossRefPubMed Gomez-Alvarez V, Teal TK, Schmidt TM. Systematic artifacts in metagenomes from complex microbial communities. ISME J. 2009;3(11):1314–7.CrossRefPubMed
19.
go back to reference Wang G, Li X, Wang Z. APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res. 2009;37(Database issue):D933–7.CrossRefPubMed Wang G, Li X, Wang Z. APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res. 2009;37(Database issue):D933–7.CrossRefPubMed
23.
go back to reference Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: The protein families database. Nucleic Acids Res. 2014;42(Database issue):D222–30.CrossRefPubMed Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: The protein families database. Nucleic Acids Res. 2014;42(Database issue):D222–30.CrossRefPubMed
24.
go back to reference Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.CrossRefPubMed Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.CrossRefPubMed
25.
go back to reference Waghu FH, Gopi L, Barai RS, Ramteke P, Nizami B, Idicula-Thomas S. CAMP: Collection of sequences and structures of antimicrobial peptides. Nucleic Acids Res. 2014;42(Database issue):D1154–8. Waghu FH, Gopi L, Barai RS, Ramteke P, Nizami B, Idicula-Thomas S. CAMP: Collection of sequences and structures of antimicrobial peptides. Nucleic Acids Res. 2014;42(Database issue):D1154–8.
26.
go back to reference Novković M, Simunić J, Bojović V, Tossi A, Juretić D. DADP: The database of anuran defense peptides. Bioinformatics. 2012;28(10):1406–7.CrossRefPubMed Novković M, Simunić J, Bojović V, Tossi A, Juretić D. DADP: The database of anuran defense peptides. Bioinformatics. 2012;28(10):1406–7.CrossRefPubMed
27.
28.
go back to reference Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera - A visualization system for exploratory research and analysis. J Comput Chem. 2004;25(13):1605–12.CrossRefPubMed Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera - A visualization system for exploratory research and analysis. J Comput Chem. 2004;25(13):1605–12.CrossRefPubMed
29.
go back to reference Mathur D, Singh S, Mehta A, Agrawal P, Raghava GPS. In silico approaches for predicting the half-life of natural and modified peptides in blood. PLoS ONE. 2018;13(6):1–10.CrossRef Mathur D, Singh S, Mehta A, Agrawal P, Raghava GPS. In silico approaches for predicting the half-life of natural and modified peptides in blood. PLoS ONE. 2018;13(6):1–10.CrossRef
30.
go back to reference Elbaz NM, Ziko L, Siam R, Mamdouh W. Core-shell silver/polymeric nanoparticles-based combinatorial therapy against breast cancer In-vitro. Sci Rep. 2016;6:30729.CrossRefPubMedPubMedCentral Elbaz NM, Ziko L, Siam R, Mamdouh W. Core-shell silver/polymeric nanoparticles-based combinatorial therapy against breast cancer In-vitro. Sci Rep. 2016;6:30729.CrossRefPubMedPubMedCentral
31.
go back to reference Ziko L, Saqr AHA, Ouf A, Gimpel M, Aziz RK, Neubauer P, et al. Antibacterial and anticancer activities of orphan biosynthetic gene clusters from Atlantis II Red Sea brine pool. Microb Cell Fact. 2019;18(1):56.CrossRefPubMedPubMedCentral Ziko L, Saqr AHA, Ouf A, Gimpel M, Aziz RK, Neubauer P, et al. Antibacterial and anticancer activities of orphan biosynthetic gene clusters from Atlantis II Red Sea brine pool. Microb Cell Fact. 2019;18(1):56.CrossRefPubMedPubMedCentral
35.
go back to reference Gomes-Porras M, Cárdenas-Salas J, Álvarez-Escolá C. Somatostatin analogs in clinical practice: a review. Int J Mol Sci. 2020;21(5):1–27.CrossRef Gomes-Porras M, Cárdenas-Salas J, Álvarez-Escolá C. Somatostatin analogs in clinical practice: a review. Int J Mol Sci. 2020;21(5):1–27.CrossRef
36.
go back to reference Pons F, Varela M, Llovet JM. Staging systems in hepatocellular carcinoma. Vol. 7, HPB. 2005. Pons F, Varela M, Llovet JM. Staging systems in hepatocellular carcinoma. Vol. 7, HPB. 2005.
38.
go back to reference Psyrri A, Gkotzamanidou M, Papaxoinis G, Krikoni L, Economopoulou P, Kotsantis I, et al. The DNA damage response network in the treatment of head and neck squamous cell carcinoma. ESMO Open. 2021;6(2):100075.CrossRefPubMedPubMedCentral Psyrri A, Gkotzamanidou M, Papaxoinis G, Krikoni L, Economopoulou P, Kotsantis I, et al. The DNA damage response network in the treatment of head and neck squamous cell carcinoma. ESMO Open. 2021;6(2):100075.CrossRefPubMedPubMedCentral
40.
go back to reference Schutte B, Nuydens R, Geerts H, Ramaekers F. Annexin V binding assay as a tool to measure apoptosis in differentiated neuronal cells. J Neurosci Methods. 1998;86(1):63–9.CrossRefPubMed Schutte B, Nuydens R, Geerts H, Ramaekers F. Annexin V binding assay as a tool to measure apoptosis in differentiated neuronal cells. J Neurosci Methods. 1998;86(1):63–9.CrossRefPubMed
43.
go back to reference Stathopoulos GP, Boulikas T, Vougiouka M, Deliconstantinos G, Rigatos S, Darli E, et al. Pharmacokinetics and adverse reactions of a new liposomal cisplatin (Lipoplatin): phase I study. Oncol Rep. 2005;13(4):589–95.PubMed Stathopoulos GP, Boulikas T, Vougiouka M, Deliconstantinos G, Rigatos S, Darli E, et al. Pharmacokinetics and adverse reactions of a new liposomal cisplatin (Lipoplatin): phase I study. Oncol Rep. 2005;13(4):589–95.PubMed
44.
go back to reference Emelianova AA, Kuzmin DV, Panteleev PV, Sorokin M, Buzdin AA, Ovchinnikova TV. Anticancer activity of the goat antimicrobial peptide ChMAP-28. Front Pharmacol. 2018;9(December):1–11. Emelianova AA, Kuzmin DV, Panteleev PV, Sorokin M, Buzdin AA, Ovchinnikova TV. Anticancer activity of the goat antimicrobial peptide ChMAP-28. Front Pharmacol. 2018;9(December):1–11.
Metadata
Title
Characterization of a novel peptide mined from the Red Sea brine pools and modified to enhance its anticancer activity
Authors
Youssef T. Abdou
Sheri M. Saleeb
Khaled M. A. Abdel-Raouf
Mohamed Allam
Mustafa Adel
Asma Amleh
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2023
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-023-11045-4

Other articles of this Issue 1/2023

BMC Cancer 1/2023 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine