Membrane Active Peptides Remove Surface Adsorbed Protein Corona From Extracellular Vesicles of Red Blood Cells

Priyanka Singh; Imola Cs Szigyártó; Maria Ricci; Ferenc Zsila; Tünde Juhász; Judith Mihály; Szilvia Bősze; Éva Bulyáki; József Kardos; Diána Kitka; Zoltán Varga; Tamás Beke-Somfai

doi:10.3389/fchem.2020.00703

Membrane Active Peptides Remove Surface Adsorbed Protein Corona From Extracellular Vesicles of Red Blood Cells

Priyanka Singh, Imola Cs Szigyártó, Maria Ricci, Ferenc Zsila, Tünde Juhász, Judith Mihály, Szilvia Bősze, Éva Bulyáki, József Kardos, Diána Kitka, Zoltán Varga, Tamás Beke-Somfai

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

15 Scopus citations

Abstract

Besides the outstanding potential in biomedical applications, extracellular vesicles (EVs) are also promising candidates to expand our knowledge on interactions between vesicular surface proteins and small-molecules which exert biomembrane-related functions. Here we provide mechanistic details on interactions between membrane active peptides with antimicrobial effect (MAPs) and red blood cell derived EVs (REVs) and we demonstrate that they have the capacity to remove members of the protein corona from REVs even at lower than 5 μM concentrations. In case of REVs, the Soret-band arising from the membrane associated hemoglobins allowed to follow the detachment process by flow-Linear Dichroism (flow-LD). Further on, the significant change on the vesicle surfaces was confirmed by transmission electron microscopy (TEM). Since membrane active peptides, such as melittin have the affinity to disrupt vesicles, a combination of techniques, fluorescent antibody labeling, microfluidic resistive pulse sensing, and flow-LD were employed to distinguish between membrane destruction and surface protein detachment. The removal of protein corona members is a newly identified role for the investigated peptides, which indicates complexity of their in vivo function, but may also be exploited in synthetic and natural nanoparticle engineering. Furthermore, results also promote that EVs can be used as improved model systems for biophysical studies providing insight to areas with so far limited knowledge.

Original language	English (US)
Article number	703
Journal	Frontiers in Chemistry
Volume	8
DOIs	https://doi.org/10.3389/fchem.2020.00703
State	Published - Aug 11 2020
Externally published	Yes

Bibliographical note

Funding Information:
The authors gratefully acknowledge Ter?z Kiss for assisting FF-TEM measurements. Funding. This work was funded by the Momentum Programme [LP2016-2 (TB-S)] of the Hungarian Academy of Sciences, by the National Competitiveness and Excellence Program (NVKP_16-1-2016-0007), of the National Research, Development and Innovation Office, NKFIH, Hungary and the GINOP grant (BIONANO_GINOP-2.3.2-15-2016-00017). ZV was supported by the J?nos Bolyai Research Fellowship and from the National Research, Development and Innovation Office under grant number PD121326. This work was completed in the ELTE Thematic Excellence Programme (Szint+) supported by the Hungarian Ministry for Innovation and Technology.

Funding Information:
This work was funded by the Momentum Programme [LP2016-2 (TB-S)] of the Hungarian Academy of Sciences, by the National Competitiveness and Excellence Program (NVKP_16-1-2016-0007), of the National Research, Development and Innovation Office, NKFIH, Hungary and the GINOP grant (BIONANO_GINOP-2.3.2-15-2016-00017). ZV was supported by the János Bolyai Research Fellowship and from the National Research, Development and Innovation Office under grant number PD121326. This work was completed in the ELTE Thematic Excellence Programme (Szint+) supported by the Hungarian Ministry for Innovation and Technology.

Publisher Copyright:
© Copyright © 2020 Singh, Szigyártó, Ricci, Zsila, Juhász, Mihály, Bősze, Bulyáki, Kardos, Kitka, Varga and Beke-Somfai.

Keywords

antimicrobial peptide
biomembrane
extracellular vesicles
liposome
protein corona

Publisher link

10.3389/fchem.2020.00703

Find It

Find It at U of M Libraries

Cite this

@article{6ed8e2ba6c364d28ab8e5ce719e01eff,

title = "Membrane Active Peptides Remove Surface Adsorbed Protein Corona From Extracellular Vesicles of Red Blood Cells",

abstract = "Besides the outstanding potential in biomedical applications, extracellular vesicles (EVs) are also promising candidates to expand our knowledge on interactions between vesicular surface proteins and small-molecules which exert biomembrane-related functions. Here we provide mechanistic details on interactions between membrane active peptides with antimicrobial effect (MAPs) and red blood cell derived EVs (REVs) and we demonstrate that they have the capacity to remove members of the protein corona from REVs even at lower than 5 μM concentrations. In case of REVs, the Soret-band arising from the membrane associated hemoglobins allowed to follow the detachment process by flow-Linear Dichroism (flow-LD). Further on, the significant change on the vesicle surfaces was confirmed by transmission electron microscopy (TEM). Since membrane active peptides, such as melittin have the affinity to disrupt vesicles, a combination of techniques, fluorescent antibody labeling, microfluidic resistive pulse sensing, and flow-LD were employed to distinguish between membrane destruction and surface protein detachment. The removal of protein corona members is a newly identified role for the investigated peptides, which indicates complexity of their in vivo function, but may also be exploited in synthetic and natural nanoparticle engineering. Furthermore, results also promote that EVs can be used as improved model systems for biophysical studies providing insight to areas with so far limited knowledge.",

keywords = "antimicrobial peptide, biomembrane, extracellular vesicles, liposome, protein corona",

author = "Priyanka Singh and Szigy{\'a}rt{\'o}, {Imola Cs} and Maria Ricci and Ferenc Zsila and T{\"u}nde Juh{\'a}sz and Judith Mih{\'a}ly and Szilvia B{\H o}sze and {\'E}va Buly{\'a}ki and J{\'o}zsef Kardos and Di{\'a}na Kitka and Zolt{\'a}n Varga and Tam{\'a}s Beke-Somfai",

note = "Funding Information: The authors gratefully acknowledge Ter?z Kiss for assisting FF-TEM measurements. Funding. This work was funded by the Momentum Programme [LP2016-2 (TB-S)] of the Hungarian Academy of Sciences, by the National Competitiveness and Excellence Program (NVKP_16-1-2016-0007), of the National Research, Development and Innovation Office, NKFIH, Hungary and the GINOP grant (BIONANO_GINOP-2.3.2-15-2016-00017). ZV was supported by the J?nos Bolyai Research Fellowship and from the National Research, Development and Innovation Office under grant number PD121326. This work was completed in the ELTE Thematic Excellence Programme (Szint+) supported by the Hungarian Ministry for Innovation and Technology. Funding Information: This work was funded by the Momentum Programme [LP2016-2 (TB-S)] of the Hungarian Academy of Sciences, by the National Competitiveness and Excellence Program (NVKP_16-1-2016-0007), of the National Research, Development and Innovation Office, NKFIH, Hungary and the GINOP grant (BIONANO_GINOP-2.3.2-15-2016-00017). ZV was supported by the J{\'a}nos Bolyai Research Fellowship and from the National Research, Development and Innovation Office under grant number PD121326. This work was completed in the ELTE Thematic Excellence Programme (Szint+) supported by the Hungarian Ministry for Innovation and Technology. Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2020 Singh, Szigy{\'a}rt{\'o}, Ricci, Zsila, Juh{\'a}sz, Mih{\'a}ly, B{\H o}sze, Buly{\'a}ki, Kardos, Kitka, Varga and Beke-Somfai.",

year = "2020",

month = aug,

day = "11",

doi = "10.3389/fchem.2020.00703",

language = "English (US)",

volume = "8",

journal = "Frontiers in Chemistry",

issn = "2296-2646",

publisher = "Frontiers Media SA",

}

TY - JOUR

T1 - Membrane Active Peptides Remove Surface Adsorbed Protein Corona From Extracellular Vesicles of Red Blood Cells

AU - Singh, Priyanka

AU - Szigyártó, Imola Cs

AU - Ricci, Maria

AU - Zsila, Ferenc

AU - Juhász, Tünde

AU - Mihály, Judith

AU - Bősze, Szilvia

AU - Bulyáki, Éva

AU - Kardos, József

AU - Kitka, Diána

AU - Varga, Zoltán

AU - Beke-Somfai, Tamás

N1 - Funding Information: The authors gratefully acknowledge Ter?z Kiss for assisting FF-TEM measurements. Funding. This work was funded by the Momentum Programme [LP2016-2 (TB-S)] of the Hungarian Academy of Sciences, by the National Competitiveness and Excellence Program (NVKP_16-1-2016-0007), of the National Research, Development and Innovation Office, NKFIH, Hungary and the GINOP grant (BIONANO_GINOP-2.3.2-15-2016-00017). ZV was supported by the J?nos Bolyai Research Fellowship and from the National Research, Development and Innovation Office under grant number PD121326. This work was completed in the ELTE Thematic Excellence Programme (Szint+) supported by the Hungarian Ministry for Innovation and Technology. Funding Information: This work was funded by the Momentum Programme [LP2016-2 (TB-S)] of the Hungarian Academy of Sciences, by the National Competitiveness and Excellence Program (NVKP_16-1-2016-0007), of the National Research, Development and Innovation Office, NKFIH, Hungary and the GINOP grant (BIONANO_GINOP-2.3.2-15-2016-00017). ZV was supported by the János Bolyai Research Fellowship and from the National Research, Development and Innovation Office under grant number PD121326. This work was completed in the ELTE Thematic Excellence Programme (Szint+) supported by the Hungarian Ministry for Innovation and Technology. Publisher Copyright: © Copyright © 2020 Singh, Szigyártó, Ricci, Zsila, Juhász, Mihály, Bősze, Bulyáki, Kardos, Kitka, Varga and Beke-Somfai.

PY - 2020/8/11

Y1 - 2020/8/11

N2 - Besides the outstanding potential in biomedical applications, extracellular vesicles (EVs) are also promising candidates to expand our knowledge on interactions between vesicular surface proteins and small-molecules which exert biomembrane-related functions. Here we provide mechanistic details on interactions between membrane active peptides with antimicrobial effect (MAPs) and red blood cell derived EVs (REVs) and we demonstrate that they have the capacity to remove members of the protein corona from REVs even at lower than 5 μM concentrations. In case of REVs, the Soret-band arising from the membrane associated hemoglobins allowed to follow the detachment process by flow-Linear Dichroism (flow-LD). Further on, the significant change on the vesicle surfaces was confirmed by transmission electron microscopy (TEM). Since membrane active peptides, such as melittin have the affinity to disrupt vesicles, a combination of techniques, fluorescent antibody labeling, microfluidic resistive pulse sensing, and flow-LD were employed to distinguish between membrane destruction and surface protein detachment. The removal of protein corona members is a newly identified role for the investigated peptides, which indicates complexity of their in vivo function, but may also be exploited in synthetic and natural nanoparticle engineering. Furthermore, results also promote that EVs can be used as improved model systems for biophysical studies providing insight to areas with so far limited knowledge.

AB - Besides the outstanding potential in biomedical applications, extracellular vesicles (EVs) are also promising candidates to expand our knowledge on interactions between vesicular surface proteins and small-molecules which exert biomembrane-related functions. Here we provide mechanistic details on interactions between membrane active peptides with antimicrobial effect (MAPs) and red blood cell derived EVs (REVs) and we demonstrate that they have the capacity to remove members of the protein corona from REVs even at lower than 5 μM concentrations. In case of REVs, the Soret-band arising from the membrane associated hemoglobins allowed to follow the detachment process by flow-Linear Dichroism (flow-LD). Further on, the significant change on the vesicle surfaces was confirmed by transmission electron microscopy (TEM). Since membrane active peptides, such as melittin have the affinity to disrupt vesicles, a combination of techniques, fluorescent antibody labeling, microfluidic resistive pulse sensing, and flow-LD were employed to distinguish between membrane destruction and surface protein detachment. The removal of protein corona members is a newly identified role for the investigated peptides, which indicates complexity of their in vivo function, but may also be exploited in synthetic and natural nanoparticle engineering. Furthermore, results also promote that EVs can be used as improved model systems for biophysical studies providing insight to areas with so far limited knowledge.

KW - antimicrobial peptide

KW - biomembrane

KW - extracellular vesicles

KW - liposome

KW - protein corona

UR - http://www.scopus.com/inward/record.url?scp=85090031066&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85090031066&partnerID=8YFLogxK

U2 - 10.3389/fchem.2020.00703

DO - 10.3389/fchem.2020.00703

M3 - Article

C2 - 32850685

AN - SCOPUS:85090031066

SN - 2296-2646

VL - 8

JO - Frontiers in Chemistry

JF - Frontiers in Chemistry

M1 - 703

ER -

Membrane Active Peptides Remove Surface Adsorbed Protein Corona From Extracellular Vesicles of Red Blood Cells

Abstract

Bibliographical note

Keywords

Publisher link

Find It

Other files and links

Fingerprint

Cite this