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Journal ArticleDOI

Thaulin-1: The first antimicrobial peptide isolated from the skin of a Patagonian frog Pleurodema thaul (Anura: Leptodactylidae: Leiuperinae) with activity against Escherichia coli.

20 Mar 2017-Gene (Elsevier)-Vol. 605, pp 70-80

TL;DR: Patagonia's biodiversity has been explored from many points of view, however, skin secretions of native amphibians have not been evaluated for antimicrobial peptide research until now and the first peptides described for amphibians of the Pleurodema genus are described.

AbstractPatagonia's biodiversity has been explored from many points of view, however, skin secretions of native amphibians have not been evaluated for antimicrobial peptide research until now. In this sense, Pleurodema thaul is the first amphibian specie to be studied from this large region of South America. Analysis of cDNA-encoding peptide in skin samples allowed identification of four new antimicrobial peptides. The predicted mature peptides were synthesized and all of them showed weak or null antimicrobial activity against Klebsiella pneumoniae, Staphylococcus aureus and Escherichia coli with the exception of thaulin-1, a cationic 26-residue linear, amphipathic, Gly- and Leu-rich peptide with moderate antimicrobial activity against E. coli (MIC of 24.7μM). AFM and SPR studies suggested a preferential interaction between these peptides and bacterial membranes. Cytotoxicity assays showed that thaulin peptides had minimal effects at MIC concentrations towards human and animal cells. These are the first peptides described for amphibians of the Pleurodema genus. These findings highlight the potential of the Patagonian region's unexplored biodiversity as a source for new molecule discovery.

Topics: Antimicrobial peptides (60%), Pleurodema (54%), Pleurodema thaul (53%), Antimicrobial (50%)

Summary (1 min read)

Introduction

  • The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form.
  • B IPCSH – CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Bvd. Brown 2915.

INTRODUCCTION

  • During the last decades there has been a rapid increase in the number of antimicrobial peptides (AMPs) described, with more than 1017 active peptides derived from amphibians (antimicrobial peptide database, APD).
  • Figure 1. (A) Pleurodema thaul distribution from the International Union for Conservation of Nature (IUCN).
  • (B) Collection site area (photo by S. Polcowñuk, used with permission).

RESULTS AND DISCUSSION

  • Preproregions (signal peptide and acidic region boxed white and black respectively) and variable domain (boxed gray) that correspond to mature peptide are AC CE PT ED M AN US CR IP T signaled.
  • It is noteworthy that the highest similarity belongs to membrane proteins described in Gram-negative microorganisms.
  • Synthetic purified and quantified thaulin-1 and Gly-thaulin- 1 peptides showed identical minimal inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) values (Table 4), demonstrating that the mechanism of action is mainly bactericide, not involving a significant inhibitory stage.

CONCLUSIONS

  • This work reports the first four peptides identified from the skin of the Patagonian frog P. thaul.
  • Sequences were analyzed using the Lasergene sequence analysis software (DNASTAR, Inc.).
  • All tests were performed in triplicate and according to CLSI (2012).
  • Cultures of BMDM were supplemented with the different concentrations of the test compounds for 24h.
  • Peptides were tested at different concentrations (15.62–500 µg/mL) according to Bignami [Bignami, 1993] with modifications.

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Accepted Manuscript
Thaulin-1: The first antimicrobial peptide isolated from the skin
of a Patagonian frog Pleurodema thaul (Anura: Leptodactylidae:
Leiuperinae) with activity against Escherichia coli
Mariela M. Marani, Luis O. Perez, Alyne Rodrigues de Araujo,
Alexandra Plácido, Carla F. Sousa, Patrick Veras Quelemes,
Mayara Oliveira, Ana G. Gomes-Alves, Mariana Pueta, Paula
Gameiro, Ana M. Tomás, Cristina Delerue-Matos, Peter Eaton,
Silvia A. Camperi, Néstor G. Basso, Jose Roberto de Souza de
Almeida Leite
PII: S0378-1119(16)31020-4
DOI: doi: 10.1016/j.gene.2016.12.020
Reference: GENE 41718
To appear in: Gene
Received date: 13 October 2016
Revised date: 19 November 2016
Accepted date: 20 December 2016
Please cite this article as: Mariela M. Marani, Luis O. Perez, Alyne Rodrigues de Araujo,
Alexandra Plácido, Carla F. Sousa, Patrick Veras Quelemes, Mayara Oliveira, Ana G.
Gomes-Alves, Mariana Pueta, Paula Gameiro, Ana M. Tomás, Cristina Delerue-Matos,
Peter Eaton, Silvia A. Camperi, Néstor G. Basso, Jose Roberto de Souza de Almeida Leite
, Thaulin-1: The first antimicrobial peptide isolated from the skin of a Patagonian frog
Pleurodema thaul (Anura: Leptodactylidae: Leiuperinae) with activity against Escherichia
coli. The address for the corresponding author was captured as affiliation for all authors.
Please check if appropriate. Gene(2016), doi: 10.1016/j.gene.2016.12.020
This is a PDF file of an unedited manuscript that has been accepted for publication. As
a service to our customers we are providing this early version of the manuscript. The
manuscript will undergo copyediting, typesetting, and review of the resulting proof before
it is published in its final form. Please note that during the production process errors may
be discovered which could affect the content, and all legal disclaimers that apply to the
journal pertain.

ACCEPTED MANUSCRIPT
1
Thaulin-1: the first antimicrobial peptide isolated from the skin of a Patagonian frog
Pleurodema thaul (Anura: Leptodactylidae: Leiuperinae) with activity against
Escherichia coli
Mariela M. Marani
*a
, Luis O. Perez
b
, Alyne Rodrigues de Araujo
c
, Alexandra Plácido
d
,
Carla F. Sousa
e
, Patrick Veras Quelemes
c
, Mayara Oliveira
f
, Ana G. Gomes-Alves
g,h,i
,
Mariana Pueta
j
, Paula Gameiro
e
, Ana M. Tomás
g,h,k
, Cristina Delerue-Matos
d
, Peter
Eaton
c,e
, Silvia A. Camperi
l
, Néstor G. Basso
m
, Jose Roberto de Souza de Almeida Leite
c,e,f
a
IPEEC CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Bvd.
Brown 2915. Puerto Madryn, Argentina; mmarani@cenpat-conicet.gob.ar.
b
IPCSH CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Bvd.
Brown 2915. Puerto Madryn, Argentina; orlandoperez@cenpat-conicet.gob.ar.
c
BIOTEC UFPI, Núcleo de Pesquisa em Biodiversidade e Biotecnologia, Campus de
Parnaíba, Universidade Federal do Piauí, Parnaíba, Brazil; alyne.rdearaujo@gmail.com;
pquelemes@gmail.com; peter.eaton@fc.up.pt; jrleite@pq.cnpq.br.
d
REQUIMTE LAQV, Instituto Superior de Engenharia do Instituto Politécnico do Porto,
Rua Dr. António Bernardino de Almeida, 431, 4200-072, Porto, Portugal;
alexandra.placido@gmail.com; cmm@isep.ipp.pt.
e
REQUIMTE UCIBIO, Departamento de Química e Bioquímica, Faculdade de Ciências,
Universidade do Porto, Rua do Campo Alegre, 687, Porto 4169-007, Portugal;
cfilipams@gmail.com; agsantos@fc.up.pt; peter.eaton@fc.up.pt
ACCEPTED MANUSCRIPT

ACCEPTED MANUSCRIPT
2
f
NMT, Núcleo de Medicina Tropical, Programa de Pós-Graduação em Medicina Tropical,
Universidade de Brasília, Brasília, DF, Brazil. mayaragco@gmail.com.
g
Instituto de Investigação e Inovação em Saúde, Universidade do Porto, 4200 Porto,
Portugal; georgina.alves@ibmc.up.pt; atomas@ibmc.up.pt.
h
IBMC, Instituto de Biologia Molecular e Celular, Universidade do Porto, 4150-180 Porto,
Portugal; georgina.alves@ibmc.up.pt; atomas@ibmc.up.pt.
i
CEB, Centro de Engenharia Biológica, Universidade do Minho, Campus de Gualtar,
4710-057, Braga, Portugal; georgina.alves@ibmc.up.pt
j
INIBIOMA, Instituto de Investigación en Biodiversidad y Medio Ambiente CONICET
UNComa, Departamento de Biología General, Universidad Nacional del Comahue,
Quintral 1250. San Carlos de Bariloche, Argentina; mpueta@gmail.com.
k
ICBAS Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, 4050-313
Porto, Portugal; atomas@ibmc.up.pt.
l
Instituto NANOBIOTEC, UBA-CONICET, Cátedra de Biotecnología, Facultad de
Farmacia y Bioquímica, Universidad de Buenos Aires, Junín 956. Buenos Aires, Argentina;
scamperi@ffyb.uba.ar.
m
IDEAus CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Bvd.
Brown 2915. Puerto Madryn, Argentina; nbasso@cenpat-conicet.gob.ar.
*Corresponding author at: IPEECCONICET, Laboratorio de Bioprospección y
Aplicaciones Biotecnológicas de Péptidos (BIAPEP), Bvd. Brown 2915, CP U9120ACD,
Puerto Madryn, Chubut, Argentina. Tel.: +54 280 4883184; fax: +54 280 4883543
E-mail address: mmarani@cenpat-conicet.gob.ar (M.M. Marani)
ACCEPTED MANUSCRIPT

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3
ABSTRACT
Patagonia's biodiversity has been explored from many points of view, however, skin
secretions of native amphibians have not been evaluated for antimicrobial peptide research
until now. In this sense, Pleurodema thaul is the first amphibian specie to be studied from
this large region of South America. Analysis of cDNA-encoding peptide in skin samples
allowed identification of four new antimicrobial peptides. The predicted mature peptides
were synthesized and all of them showed weak or null antimicrobial activity against
Klebsiella pneumonia, Staphylococcus aureus and Escherichia coli with the exception of
thaulin-1, a cationic 26-residue linear, amphipathic, Gly- and Leu-rich peptide with
moderate antimicrobial activity against E. coli (MIC of 24.7 µM). AFM and SPR studies
suggested a preferential interaction between these peptides and bacterial membranes.
Cytotoxicity assays showed that thaulin peptides had minimal effects at MIC
concentrations towards human and animal cells. These are the first peptides described for
amphibians of the Pleurodema genus. These findings highlight the potential of the
Patagonian region’s unexplored biodiversity as a source for new molecule discovery.
Key words: Anura; Atomic Force Microscopy; cDNA; Circular Dichroism; Surface
Plasmon Resonance.
ACCEPTED MANUSCRIPT

ACCEPTED MANUSCRIPT
4
INTRODUCCTION
During the last decades there has been a rapid increase in the number of
antimicrobial peptides (AMPs) described, with more than 1017 active peptides derived
from amphibians (antimicrobial peptide database, APD). Most of these share common
characteristics: they are in general, cationic, amphipathic and with an α-helix secondary
structure, although some peptides with different characters such as negative charges [Harris
et al., 2009] or with different secondary structures [Wang & Zasloff, 2010] have
occasionally also been described. All AMPs are expressed as prepropeptides harboring a
conserved signal peptide, an acidic propiece and a highly variable domain encoding the
AMP itself [Amiche et al., 1999]. This last domain is so variable that the combination of
several of these peptides can form a distinctive marker for each amphibian specie [Jackway
et al., 2011]. However, within this variability, many peptides share common features such
that they have been classified into common peptide families, such as the brevinins
[Moricawa et al., 1992], caerin, dermasemptins [Amiche etal., 1999], esculetins [Simmaco
et al., 1993], magainins [Zasloff, 1987], ocellatins [Marani et al., 2015], temporins
[Mangoni et al., 2005], etc. Meanwhile, some peptides with totally novel structures, which
belong to no yet-described family have also been occasionally described (Leu rich
peptides).
AMPs are important functional molecules in the innate immune system and they
play defensive roles against external risk factors. However, besides antimicrobial activity,
multiple potential applications have been identified for AMPs such as anticancer [Oelkrug
et al., 2015; Wu et al., 2014; Gaspar et al., 2013; Chu et al., 2015], insecticidal [Smith et
ACCEPTED MANUSCRIPT

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"Thaulin-1: The first antimicrobial ..." refers background in this paper

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Frequently Asked Questions (2)
Q1. What contributions have the authors mentioned in the paper "Thaulin-1: the first antimicrobial peptide isolated from the skin of a patagonian frog pleurodema thaul (anura: leptodactylidae: leiuperinae) with activity against escherichia coli" ?

Please cite this article as: Mariela M. Marani, Luis O. Perez, Alyne Rodrigues de Araujo, Alexandra Plácido, Carla F. Sousa, Patrick Veras Quelemes, Mayara Oliveira, Ana G. Gomes-Alves, Mariana Pueta, Paula Gameiro, Ana M. Tomás, Cristina Delerue-Matos, Peter Eaton, Silvia A. Camperi, Néstor G. Basso, Jose Roberto de Souza de Almeida Leite, Thaulin-1: The first antimicrobial peptide isolated from the skin of a Patagonian frog Pleurodema thaul ( Anura: Leptodactylidae: Leiuperinae ) with activity against Escherichia coli. The address for the corresponding author was captured as affiliation for all authors. 

Further work will be performed to explore this application.