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Schinus terebinthifolia leaf lectin (SteLL) is an immunomodulatory agent by altering cytokine release by mice splenocytes

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Abstract

Schinus terebinthifolia leaf lectin (SteLL) was reported to be an antimicrobial and antitumor agent. In this work, we evaluated the immunomodulatory activity of SteLL on mice splenocytes and also determined its native molecular mass and putative sequence similarities with plant proteins. The effects of SteLL (12.5 μg/mL) on viability, cytosolic Ca2+ concentration ([Ca2+]cyt), cytosolic and mitochondrial levels of reactive oxygen species (ROS), and mitochondrial transmembrane potential (ΔΨm) of mice splenocytes were determined. In addition, the culture supernatants were collected for quantification of interleukins (IL), tumor necrosis factor (TNF), interferon-gamma (IFN-γ) and nitric oxide (NO). SteLL showed a native molecular mass of 12.4 kDa and tandem mass spectrometry (MS/MS) ions search revealed similarities with adenosine triphosphate (ATP) synthase and F1-ATPase from plants (4% and 6% coverage, respectively). SteLL was not toxic to splenocytes, did not alter the [Ca2+]cyt and ROS levels, and slightly reduced ΔΨm. The presence of SteLL stimulated the cells to release pro-inflammatory cytokines (IL-17A, TNF-α, IFN-γ and IL-2) and also of IL-4, an anti-inflammatory cytokine that can prevent exacerbated inflammation. SteLL induced decrease in the secretion of NO. In conclusion, SteLL has biotechnological potential as an immunomodulator agent for use in studies employing cultures of immune cells. In addition, the anti-infectious and antitumor properties of the leaves may involve the immunomodulation property of SteLL.

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Abbreviations

ΔΨm:

Mitochondrial transmembrane potential

[Ca2+]cyt :

Cytosolic Ca2+ concentration

AnnV:

Annexin V

ATP:

Adenosine triphosphate

CBA:

Cytometric bead array

CXCL:

Chemokine (C-X-C motif) ligand

ESI-QUAD-TOF:

Electrospray ionization quadrupole time-of-flight

FITC:

Fluorescein isothiocyanate

HA:

Hemagglutinating activity

HSP70:

70-kDa heat shock proteins

IC50 :

Concentrations that reduced cell viability to 50%)

IFN-γ:

Interferon-gamma

IL:

Interleukin

JAK/STAT:

Janus kinases/signal transducer and activator of transcription proteins

MIP-1α:

Macrophage inflammatory protein 1α

MS/MS:

Tandem mass spectrometry

NO:

Nitric oxide (NO)

PBS:

Phosphate buffered saline

PI:

Propidium iodide

ROS:

Reactive oxygen species

SDS-PAGE:

Polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulphate

SteLL:

Schinus terebinthifolia leaf lectin

Th:

T helper

TNF:

Tumor necrosis factor

UFPE:

Universidade Federal de Pernambuco

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Acknowledgements

The authors express their gratitude to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; 408789/2016-6) for research grants and fellowships (RBZ, PMGP and THN) as well as to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance Code 001) and Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE; APQ-0108-2.08/14; APQ-0661-2.08/15) for financial support. The authors thank the Núcleo de Plataformas Tecnológicas of the Instituto Aggeu Magalhães, Fundação Oswaldo Cruz (FIOCRUZ Pernambuco). We thank Ana Lucia Oliveira Carvalho and Augusto Vieira for technical assistance with mass spectrometry analysis.

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Authors and Affiliations

  1. Departamento de Morfologia e Fisiologia Animal, Universidade Federal Rural de Pernambuco, Recife, Brazil

    Ardilles Juan Carlos Alves dos Santos & Emmanuel Viana Pontual

  2. Departamento de Antibióticos, Centro de Biociências, Universidade Federal de Pernambuco, Recife, Brazil

    Bárbara Rafaela da Silva Barros, Lethícia Maria de Souza Aguiar & Cristiane Moutinho Lagos de Melo

  3. Departamento de Bioquímica, Centro de Biociências, Universidade Federal de Pernambuco, Recife, Brazil

    Leydianne Leite de Siqueira Patriota, Thâmarah de Albuquerque Lima, Patrícia Maria Guedes Paiva & Thiago Henrique Napoleão

  4. Instituto de Bioquímica Médica Leopoldo de Meis, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Russolina Benedeta Zingali

Authors
  1. Ardilles Juan Carlos Alves dos Santos
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  2. Bárbara Rafaela da Silva Barros
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  3. Lethícia Maria de Souza Aguiar
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  7. Patrícia Maria Guedes Paiva
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  8. Thiago Henrique Napoleão
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  9. Cristiane Moutinho Lagos de Melo
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  10. Emmanuel Viana Pontual
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Correspondence to Emmanuel Viana Pontual.

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dos Santos, A.J.C.A., da Silva Barros, B.R., de Souza Aguiar, L.M. et al. Schinus terebinthifolia leaf lectin (SteLL) is an immunomodulatory agent by altering cytokine release by mice splenocytes. 3 Biotech 10, 144 (2020). https://doi.org/10.1007/s13205-020-2137-2

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