Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata

Giovanna Morán-Marcillo; Verónica Sánchez Hinojosa; Nina Espinosa de los Monteros-Silva; Ailín Blasco-Zúñiga; Miryan Rivera; Renato E. Naranjo; José Rafael Almeida; Lei Wang; Mei Zhou; Tianbao Chen; Chris Shaw; Carolina Proaño-Bolaños

doi:10.1016/j.jprot.2022.104633

Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata

Giovanna Morán-Marcillo, Verónica Sánchez Hinojosa, Nina Espinosa de los Monteros-Silva, Ailín Blasco-Zúñiga, Miryan Rivera, Renato E. Naranjo, José Rafael Almeida, Lei Wang, Mei Zhou, Tianbao Chen, Chris Shaw, Carolina Proaño-Bolaños^*

^*Corresponding author for this work

Faculty of Exact and Natural Sciences

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

The Imbabura treefrog (Boana picturata) is an underexplored source of bioactive peptides. The combination of molecular cloning and mass spectrometry allowed us to identify three new peptide families, named “Picturins” (PTR), “Pictuseptins” (PTS), and “Boanins” (BNS). PTR is composed of three 25-mer peptides, characterized by the N-terminal sequence: GVFKDALKQ and the C-terminal sequence: AANALKPK. The sequences of PTR-1, −2 and − 3 are highly conserved only showing two divergent sites: (L/F) in position 10 and (K/Q) in position 17. PTS gathers six peptides. PTS -1, −2 and − 4 have 22 amino acid residues in length, while PTS -3, −5 and − 6 are composed of 26 residues. Whereas BNS are four 28–37 mer peptides, showing two conserved regions: the N-terminal sequence FLGAL and the C-terminal sequence KALNP. PTR-1 to 3 and PTS -1 to −3 were chemically synthetized and their antimicrobial and haemolytic activity was assessed. PTR displayed moderate activity against Escherichia coli (MIC 24.80 to 48.95 μM), while PTS showed a broad antimicrobial and antifungal effect. PTS-1 was the most active peptide against E. coli (6.8 μM) followed by PTS-3 (11.7 μM) and PTS-2 (14.24 μM). These peptides also showed low haemolytic activity, pointing to a favorable selectivity. Overall, new unique non-hemolytic and cationic peptide sequences were characterized that could be valuable for the next-generation of anti-infective drugs. Future functional studies should explore the pharmacological potential of Boanins to include them as antimicrobial scaffolds. Biological significance: Nature-inspired solutions have shown their importance mainly for the development of the pharmaceutical industry. Frog skin peptides are excellent examples of the biomedical potential of naturally evolved molecules for specific targets, including multi-resistant bacteria. The characterization of new chemical entities from poorly studied skin secretions of Ecuadorian biodiversity, such as B. picturata, represents an unprecedented opportunity to identify candidates to tackle global concerns, for instance, antibiotic resistance.

Original language	English
Article number	104633
Journal	Journal of Proteomics
Volume	264
DOIs	https://doi.org/10.1016/j.jprot.2022.104633
State	Published - 30 Jul 2022

Bibliographical note

Publisher Copyright:
© 2022

Funding

This research was funded by (1) SENESCYT through a scholarship to C.P.-B, (2) THE NATURAL DRUG DISCOVERY GROUP of QUB, and (3) The PONTIFICIA UNIVERSIDAD CATÓLICA DEL ECUADOR, project code QINV0046-IINV529010100.Carolina Proaño-Bolaños received a scholarship from the Ecuadorian Secretariat of Science and Technology (SENESCYT). This research was funded by the Natural Drug Discovery Group, School of Pharmacy, Queen's University Belfast (QUB), the Pontificia Universidad Católica del Ecuador project code QINV0046-IINV529010100, Centro de Investigación para la Salud en América Latina-CISeAL, and SENESCYT. The latter also supported field work to CPB. The collection and rearing of frogs in Ecuador were done under permits of Ministerio del Ambiente of Ecuador (currently Ministerio de Ambiente Agua y Transición Ecológica -MAATE) 001-13 IC-FAU-DNB/MA, 003-11 IC-FAU-DNB/MA, and 005-15 IC-FAU-DNB/MA (issued to the Centro Jambatu de Investigación y Conservación de Anfibios). Exportation of skin secretion samples was done under exportation permits 003-13-EXP-CI-FAU-DNB/MA and 2015-003-FO-DPAP-MA. This research was done under the framework contract for genetic resources access between MAE and IKIAM (MAE-DNB-CM-2016-0051). Furthermore, it is part of the project “Conservation of Ecuadorian amphibian diversity and sustainable use of its genetic resources,” which involved MAE, Universidad Regional Amazónica Ikiam, Queen's University Belfast, and Centro Jambatu, and the help of the Global Environmental Facility (GEF) and “Programa de las Naciones Unidas para el Desarrollo” (PNUD). We thank the kind donation of bacterial and fungal strains by Sonia Zapata (USFQ) and Jorge Reyes (INSPI). We also thank Fernando Valdivieso, Berenice Benavides, and Miguel Angel Llumiquinga for their help with MIC experiments. Elicio E. Tapia aided in collecting specimens in Esmeraldas province. Finally, we are grateful to Catriona Arlow, who helped with the language reviews of the first draft of this manuscript, and Luis A. Coloma who provided the frog picture used in the graphical abstract. Carolina Proaño-Bolaños received a scholarship from the Ecuadorian Secretariat of Science and Technology (SENESCYT). This research was funded by the Natural Drug Discovery Group , School of Pharmacy, Queen's University Belfast (QUB), the Pontificia Universidad Católica del Ecuador project code QINV0046-IINV529010100, Centro de Investigación para la Salud en América Latina-CISeAL, and SENESCYT. The latter also supported field work to CPB. The collection and rearing of frogs in Ecuador were done under permits of Ministerio del Ambiente of Ecuador (currently Ministerio de Ambiente Agua y Transición Ecológica -MAATE) 001-13 IC-FAU-DNB/MA, 003-11 IC-FAU-DNB/MA, and 005-15 IC-FAU-DNB/MA (issued to the Centro Jambatu de Investigación y Conservación de Anfibios). Exportation of skin secretion samples was done under exportation permits 003-13-EXP-CI-FAU-DNB/MA and 2015-003-FO-DPAP-MA. This research was done under the framework contract for genetic resources access between MAE and IKIAM (MAE-DNB-CM-2016-0051). Furthermore, it is part of the project “Conservation of Ecuadorian amphibian diversity and sustainable use of its genetic resources,” which involved MAE, Universidad Regional Amazónica Ikiam, Queen's University Belfast, and Centro Jambatu, and the help of the Global Environmental Facility (GEF) and “Programa de las Naciones Unidas para el Desarrollo” (PNUD). We thank the kind donation of bacterial and fungal strains by Sonia Zapata (USFQ) and Jorge Reyes (INSPI). We also thank Fernando Valdivieso, Berenice Benavides, and Miguel Angel Llumiquinga for their help with MIC experiments. Elicio E. Tapia aided in collecting specimens in Esmeraldas province. Finally, we are grateful to Catriona Arlow, who helped with the language reviews of the first draft of this manuscript, and Luis A. Coloma who provided the frog picture used in the graphical abstract.

Funders	Funder number
Centro de Investigación para la Salud en América Latina-CISeAL
Ecuadorian Secretariat of Science and Technology
Ministerio del Ambiente
Natural Drug Discovery Group
Sonia Zapata
Universidad Regional Amazónica Ikiam
United Nations Development Programme
Ministerio del Ambiente, Agua y Transición Ecológica	003-13-EXP-CI-FAU-DNB/MA, 005-15 IC-FAU-DNB/MA, 2015-003-FO-DPAP-MA, 003-11 IC-FAU-DNB/MA, MAE-DNB-CM-2016-0051, 001-13 IC-FAU-DNB/MA
Queen's University Belfast
Secretaría de Educación Superior, Ciencia, Tecnología e Innovación
Universidad San Francisco de Quito
Pontifical Catholic University of Ecuador

Keywords

Antibacterial
Antifungal
Frog skin secretion
Peptidomics
Synthetic peptides

Access to Document

10.1016/j.jprot.2022.104633

Cite this

Morán-Marcillo, G., Sánchez Hinojosa, V., de los Monteros-Silva, N. E., Blasco-Zúñiga, A., Rivera, M., Naranjo, R. E., Almeida, J. R., Wang, L., Zhou, M., Chen, T., Shaw, C., & Proaño-Bolaños, C. (2022). Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata. Journal of Proteomics, 264, Article 104633. https://doi.org/10.1016/j.jprot.2022.104633

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title = "Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata",

abstract = "The Imbabura treefrog (Boana picturata) is an underexplored source of bioactive peptides. The combination of molecular cloning and mass spectrometry allowed us to identify three new peptide families, named “Picturins” (PTR), “Pictuseptins” (PTS), and “Boanins” (BNS). PTR is composed of three 25-mer peptides, characterized by the N-terminal sequence: GVFKDALKQ and the C-terminal sequence: AANALKPK. The sequences of PTR-1, −2 and − 3 are highly conserved only showing two divergent sites: (L/F) in position 10 and (K/Q) in position 17. PTS gathers six peptides. PTS -1, −2 and − 4 have 22 amino acid residues in length, while PTS -3, −5 and − 6 are composed of 26 residues. Whereas BNS are four 28–37 mer peptides, showing two conserved regions: the N-terminal sequence FLGAL and the C-terminal sequence KALNP. PTR-1 to 3 and PTS -1 to −3 were chemically synthetized and their antimicrobial and haemolytic activity was assessed. PTR displayed moderate activity against Escherichia coli (MIC 24.80 to 48.95 μM), while PTS showed a broad antimicrobial and antifungal effect. PTS-1 was the most active peptide against E. coli (6.8 μM) followed by PTS-3 (11.7 μM) and PTS-2 (14.24 μM). These peptides also showed low haemolytic activity, pointing to a favorable selectivity. Overall, new unique non-hemolytic and cationic peptide sequences were characterized that could be valuable for the next-generation of anti-infective drugs. Future functional studies should explore the pharmacological potential of Boanins to include them as antimicrobial scaffolds. Biological significance: Nature-inspired solutions have shown their importance mainly for the development of the pharmaceutical industry. Frog skin peptides are excellent examples of the biomedical potential of naturally evolved molecules for specific targets, including multi-resistant bacteria. The characterization of new chemical entities from poorly studied skin secretions of Ecuadorian biodiversity, such as B. picturata, represents an unprecedented opportunity to identify candidates to tackle global concerns, for instance, antibiotic resistance.",

keywords = "Antibacterial, Antifungal, Frog skin secretion, Peptidomics, Synthetic peptides",

author = "Giovanna Mor{\'a}n-Marcillo and {S{\'a}nchez Hinojosa}, Ver{\'o}nica and {de los Monteros-Silva}, {Nina Espinosa} and Ail{\'i}n Blasco-Z{\'u}{\~n}iga and Miryan Rivera and Naranjo, {Renato E.} and Almeida, {Jos{\'e} Rafael} and Lei Wang and Mei Zhou and Tianbao Chen and Chris Shaw and Carolina Proa{\~n}o-Bola{\~n}os",

note = "Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = jul,

day = "30",

doi = "10.1016/j.jprot.2022.104633",

language = "English",

volume = "264",

journal = "Journal of Proteomics",

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Morán-Marcillo, G, Sánchez Hinojosa, V, de los Monteros-Silva, NE, Blasco-Zúñiga, A, Rivera, M, Naranjo, RE, Almeida, JR, Wang, L, Zhou, M, Chen, T, Shaw, C & Proaño-Bolaños, C 2022, 'Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata', Journal of Proteomics, vol. 264, 104633. https://doi.org/10.1016/j.jprot.2022.104633

TY - JOUR

T1 - Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata

AU - Morán-Marcillo, Giovanna

AU - Sánchez Hinojosa, Verónica

AU - de los Monteros-Silva, Nina Espinosa

AU - Blasco-Zúñiga, Ailín

AU - Rivera, Miryan

AU - Naranjo, Renato E.

AU - Almeida, José Rafael

AU - Wang, Lei

AU - Zhou, Mei

AU - Chen, Tianbao

AU - Shaw, Chris

AU - Proaño-Bolaños, Carolina

PY - 2022/7/30

Y1 - 2022/7/30

N2 - The Imbabura treefrog (Boana picturata) is an underexplored source of bioactive peptides. The combination of molecular cloning and mass spectrometry allowed us to identify three new peptide families, named “Picturins” (PTR), “Pictuseptins” (PTS), and “Boanins” (BNS). PTR is composed of three 25-mer peptides, characterized by the N-terminal sequence: GVFKDALKQ and the C-terminal sequence: AANALKPK. The sequences of PTR-1, −2 and − 3 are highly conserved only showing two divergent sites: (L/F) in position 10 and (K/Q) in position 17. PTS gathers six peptides. PTS -1, −2 and − 4 have 22 amino acid residues in length, while PTS -3, −5 and − 6 are composed of 26 residues. Whereas BNS are four 28–37 mer peptides, showing two conserved regions: the N-terminal sequence FLGAL and the C-terminal sequence KALNP. PTR-1 to 3 and PTS -1 to −3 were chemically synthetized and their antimicrobial and haemolytic activity was assessed. PTR displayed moderate activity against Escherichia coli (MIC 24.80 to 48.95 μM), while PTS showed a broad antimicrobial and antifungal effect. PTS-1 was the most active peptide against E. coli (6.8 μM) followed by PTS-3 (11.7 μM) and PTS-2 (14.24 μM). These peptides also showed low haemolytic activity, pointing to a favorable selectivity. Overall, new unique non-hemolytic and cationic peptide sequences were characterized that could be valuable for the next-generation of anti-infective drugs. Future functional studies should explore the pharmacological potential of Boanins to include them as antimicrobial scaffolds. Biological significance: Nature-inspired solutions have shown their importance mainly for the development of the pharmaceutical industry. Frog skin peptides are excellent examples of the biomedical potential of naturally evolved molecules for specific targets, including multi-resistant bacteria. The characterization of new chemical entities from poorly studied skin secretions of Ecuadorian biodiversity, such as B. picturata, represents an unprecedented opportunity to identify candidates to tackle global concerns, for instance, antibiotic resistance.

AB - The Imbabura treefrog (Boana picturata) is an underexplored source of bioactive peptides. The combination of molecular cloning and mass spectrometry allowed us to identify three new peptide families, named “Picturins” (PTR), “Pictuseptins” (PTS), and “Boanins” (BNS). PTR is composed of three 25-mer peptides, characterized by the N-terminal sequence: GVFKDALKQ and the C-terminal sequence: AANALKPK. The sequences of PTR-1, −2 and − 3 are highly conserved only showing two divergent sites: (L/F) in position 10 and (K/Q) in position 17. PTS gathers six peptides. PTS -1, −2 and − 4 have 22 amino acid residues in length, while PTS -3, −5 and − 6 are composed of 26 residues. Whereas BNS are four 28–37 mer peptides, showing two conserved regions: the N-terminal sequence FLGAL and the C-terminal sequence KALNP. PTR-1 to 3 and PTS -1 to −3 were chemically synthetized and their antimicrobial and haemolytic activity was assessed. PTR displayed moderate activity against Escherichia coli (MIC 24.80 to 48.95 μM), while PTS showed a broad antimicrobial and antifungal effect. PTS-1 was the most active peptide against E. coli (6.8 μM) followed by PTS-3 (11.7 μM) and PTS-2 (14.24 μM). These peptides also showed low haemolytic activity, pointing to a favorable selectivity. Overall, new unique non-hemolytic and cationic peptide sequences were characterized that could be valuable for the next-generation of anti-infective drugs. Future functional studies should explore the pharmacological potential of Boanins to include them as antimicrobial scaffolds. Biological significance: Nature-inspired solutions have shown their importance mainly for the development of the pharmaceutical industry. Frog skin peptides are excellent examples of the biomedical potential of naturally evolved molecules for specific targets, including multi-resistant bacteria. The characterization of new chemical entities from poorly studied skin secretions of Ecuadorian biodiversity, such as B. picturata, represents an unprecedented opportunity to identify candidates to tackle global concerns, for instance, antibiotic resistance.

KW - Antibacterial

KW - Antifungal

KW - Frog skin secretion

KW - Peptidomics

KW - Synthetic peptides

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DO - 10.1016/j.jprot.2022.104633

M3 - Article

C2 - 35640793

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SN - 1874-3919

VL - 264

JO - Journal of Proteomics

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ER -

Picturins and Pictuseptins, two novel antimicrobial peptide families from the skin secretions of the Chachi treefrog, Boana picturata

Abstract

Bibliographical note

Funding

Keywords

Access to Document

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