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Glycoconjugate Journal

, Volume 34, Issue 1, pp 127–138 | Cite as

Catfish rhamnose-binding lectin induces G0/1 cell cycle arrest in Burkitt’s lymphoma cells via membrane surface Gb3

  • Shigeki Sugawara
  • Changhun Im
  • Tasuku Kawano
  • Takeo Tatsuta
  • Yasuhiro Koide
  • Daiki Yamamoto
  • Yasuhiro Ozeki
  • Kazuo Nitta
  • Masahiro Hosono
Original Article

Abstract

Silurus asotus egg lectin (SAL), an α-galactoside-binding protein isolated from the eggs of catfish, is a member of the rhamnose-binding lectin family that binds to Gb3 glycan (Galα1–4Galβ1–4Glc). We have previously demonstrated that SAL reduces the proliferation of Gb3-expressing Burkitt’s lymphoma Raji cells and confirm here that it does not reduce their viability, indicating that unlike other lectins, it is not cytotoxic. The aim of this study was to determine the signal transduction mechanism(s) underlying this novel SAL/Gb3 binding-mediated effect profile. SAL/Gb3 interaction arrested the cell cycle through increasing the G0/1 phase population of Raji cells. SAL suppressed the transcription of cell cycle-related factors such as c-MYC, cyclin D3, and cyclin-dependent protein kinase (CDK)-4. Conversely, the CDK inhibitors p21 and p27 were elevated by treatment with SAL. In particular, the production of p27 in response to SAL treatment increased steadily, whereas p21 production was maximal at 12 h and lower at 24 h. Activation of Ras-MEK-ERK pathway led to an increase in expression of p21. Notably, treatment of Raji cells with anti-Gb3 mAb alone did not produce the above effects. Taken together, our findings suggest that Gb3 on the Raji cell surface interacts with SAL to trigger sequential GDP-Ras phosphorylation, Ras-MEK-ERK pathway activation, p21 production, and cell cycle arrest at the G0/1 phase.

Keywords

Cell cycle arrest Extracellular signal-regulated kinase Globotriaosylceramide p21 SUEL/rhamnose-binding lectin 

Abbreviations

BrdU

Bromodeoxy uridine

CCND3

Cyclin D3

CDK

Cyclin-dependent protein kinase

ERK

Extracellular signal-regulated kinase

FBS

Fetal bovine serum

FITC

Fluorescein isothiocyanate

Gb3

Galα1–4Galβ1–4Glc-Cer

GDP

Guanosine diphosphate

GEM

Glycosphingolipid-enriched microdomains

GTP

Guanosine triphosphate

GSL

Glycosphingolipid

mAb

Monoclonal antibody

JNK

c-Jun N-terminal kinase

MAPK

Mitogen-activated protein kinase

MEK

MAPK/ERK kinase

PVDF

Polyvinylidene difluoride

qRT-PCR

Quantitative reverse transcription-polymerase chain reaction

SAL

Silurus asotus egg lectin

SDS-PAGE

Sodium dodecyl sulfate-polyacrylamide gel electrophoresis

SUEL

Sea urchin egg lectin

Notes

Acknowledgments

This study was supported by the “Academic Frontier” Project for Private Universities and the “Strategic Project to Support the Formation of Research Bases at Private Universities (SENRYAKU)” from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan. We would like to thank Editage (www.editage.jp) for English language editing.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10719_2016_9739_MOESM1_ESM.docx (665 kb)
ESM 1 (DOCX 665 kb)

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Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Division of Cell Recognition Study, Institute of Molecular Biomembrane and GlycobiologyTohoku Medical and Pharmaceutical UniversitySendaiJapan
  2. 2.Laboratory of Glycobiology and Marine Biochemistry, Department of Life and Environmental System Science, Graduate School of NanoBio SciencesYokohama City UniversityYokohamaJapan

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