Skip to main content

Advertisement

SpringerLink
Log in

Detection of glycidic receptors in microalgae using glycodendrons as probes: a new tool for studies on cell surface interactions

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Cell recognition, adhesion, and internalization are involved in infectious, reproductive, and inflammatory processes and are generally mediated by interactions between molecules located in the cell membrane and the extracellular matrix. These processes can decrease proliferation rates and they are well known for bacteria, fungi, and animals, but there is a lack of knowledge regarding autotrophic cells. Carbohydrates and proteins (e.g., lectins) are important molecules for cell interactions and information about these molecules is essential to better understand many biological phenomena in uni- or multicellular organisms. Most studies focus on the identification of the carbohydrates present on the cell surface by using labeled lectins. Alternatively, here we present a pioneer research performed by using three different labeled carbohydrates in a multivalent presentation (glycodendrons) to detect the presence of carbohydrate receptors (e.g., lectins) on cell surfaces of 12 algal species. The goal of this study was to detect some specificity in these molecular interactions, but in a reverse way in comparison to that commonly described in the literature. We tested trivalent molecules containing residuals of D-mannose, L-fucose, or N-acetyl-galactosamine to identify their bindings with the corresponding lectins expressed on cell surfaces. We envisage that our new approach could be an alternative tool for taxonomic and physiological studies on microalgae or even on other groups of organisms. Based on our results, the receptors found in the cell surface of the algal species tend to differ in composition, quantity, and distribution. The differences were mainly species-specific, since no patterns were identified at higher taxonomic level. Moreover, like lectins, labeled carbohydrates were proved to be a reliable tool for the study of cell surface composition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguilera A, González-Gil S (2001) Lectin analysis of surface saccharides during the cell cycle in four dinoflagellate species. J Exp Mar Biol Ecol 256:149–166

    Article  CAS  PubMed  Google Scholar 

  • Brandley GK, Schnaar R (1986) Cell surface carbohydrate in cell recognition and response. J Leukoc Biol 40:97–111

    Article  CAS  PubMed  Google Scholar 

  • Carmichael WW, Bent PE (1981) Hemagglutination method for detection of freshwater cyanobacteria (blue-green algae) toxins. Appl Environ Microbiol 41:1383–1388

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho ES, Choi BD, Cho YC, Kim TJ, Kim HG (2001) Discrimination of three highly toxic Alexandrium tamarense (Dinophyceae) isolates using FITC-conjugated lectin probes. J Plankton Res 23:89–96

    Article  CAS  Google Scholar 

  • Clarke AE, Wilson IA (eds) (1988) Carbohydrate-protein interaction. Curr Top Microbiol Immunol, vol. 139. Springer, Berlin

  • Cloninger MJ (2002) Biological applications of dendrimers. Curr Opin Chem Biol 6:742–748

    Article  CAS  PubMed  Google Scholar 

  • Costas E, Aguilera A, Gonzalez-Gil S, López-Rodas V (1993) Contact inhibition: also a control for cell proliferation in unicellular algae? Biol Bull 184:1–5

    Article  CAS  PubMed  Google Scholar 

  • Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E, Green BR (1999) A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J Mol Evol 48:59–68

    Article  CAS  PubMed  Google Scholar 

  • East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta 1572:364–386

    Article  CAS  PubMed  Google Scholar 

  • Espinosa PE, Perrigault M, Ward EJ, Shumway ES, Allam B (2010) Microalgal cell surface carbohydrate as recognition sites for particle sorting in suspension-feeding bivalves. Biol Bull 218:75–86

    Article  CAS  PubMed  Google Scholar 

  • Esquenazi D, de Souza W, Alviano CS, Rozental S (2003) The role of surface carbohydrates on the interaction of microconidia of Trichophyton mentagrophytes with epithelial cells. FEMS Immunol Med Microbiol 35:113–123

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TB, Kwon DS, Torensma R, Van Vliet SJ, Van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littam DR, Figdor CG, Van Kook Y (2000) DC-SIGN, a dendritic cell-specific HIV-1 binding protein that enhances trans-infection of T cells. Cell 100:587–597

    Article  CAS  PubMed  Google Scholar 

  • Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517

    Article  CAS  PubMed  Google Scholar 

  • Guillard RRL, Lorenzen CJ (1972) Yellow-green algae with chlorrophyllide c. J Phycol 8:10–14

  • Hori K, Ogata T, Kamiya H, Mimuro M (1996) Lectin-like compounds and lectin receptors in marine microalgae: hemagglutination and reactivity with purified lectins. J Phycol 32:783–790

    Article  CAS  Google Scholar 

  • Imam SH, Bard RF, Tosteson TR (1984) Specificity of marine microbial surface interactions. Appl Environ Microbiol 48:833–839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kane RS (2010) Thermodynamics of multivalent interactions: influence of the linker. Langmuir 26:8636–8640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang S, Suresh A, Kim YC (2017) A highly efficient cell penetrating peptide pVEC-mediated protein delivery system into microalgae. Algal Res 24:360–367

    Article  Google Scholar 

  • Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B 365:729–748

    Article  CAS  Google Scholar 

  • Kehr JC, Zilliges Y, Springer A, Disney MD, Ratner DD, Bouchier C, Seeberger PH, de Marsac NT, Dittmann E (2006) A Mannan binding lectin is involved in cell-cell attachment in a toxic strain of Microcystis aeruginosa. Mol Microbiol 59:893–906

    Article  CAS  PubMed  Google Scholar 

  • Khowala S, Verma D, Banik SP (2008) Biomolecules: introduction, structure and function/carbohydrates. Drug Dev Biotechnol Indian Inst Chem Biol :2–93

  • Kikkeri R, Kamena F, Gupta T, Hossain LH, Boonyarattanakalin S, Gorodyska G, Beurer E, Coullerez G, Textor M, Seeberger PH (2010) Ru(II) glycodendrimers as probes to study lectin-carbohydrate interactions and electrochemically measure monosaccharide and oligosaccharide concentrations. Langmuir 26:1520–1523

    Article  CAS  PubMed  Google Scholar 

  • Kim GH, Yoon M, west JA, Klochkova TA, Kim SH (2007) Possible surface carbohydrates involved in signaling during conjugation process in Zygnema cruciatum monitored with fluorescein isothiocyanate-lectins (Zygnemataceae, Chlorophyta). Phycol Res 55:135–142

    Article  CAS  Google Scholar 

  • Kleene R, Schachner M (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5:195–208

    Article  CAS  PubMed  Google Scholar 

  • Knox JP (1992) Molecular probes of the plant cell surface. Protoplasma 167:1–9

    Article  CAS  Google Scholar 

  • Kolb HC, Finn MG, Sharpless KB (2001) Click chemistry: diverse chemical function from a few good reactions. Angew Chem Int Ed Eng 40:2004–2021

    Article  CAS  Google Scholar 

  • Kosaka T, Heizmann CW (1989) Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res 483:158–163

    Article  CAS  PubMed  Google Scholar 

  • Kremp A, Anderson DM (2004) Lectin binding patterns of Scrippsiella lachrymosa (Dinophyceae) in relation to cyst formation and nutrient conditions. J Exp Mar Biol Ecol 307:165–181

    Article  CAS  Google Scholar 

  • Kresse H, Schönherr E (2001) Proteoglycans of the extracellular matrix and growth control. J Cell Physiol 189:266–274

    Article  CAS  PubMed  Google Scholar 

  • Kushchayev SV, Sankar T, Eggink LL, Kushchayeva YS, Wiener PC, Hoober JK, Eschbacher J, Liu R, Shi FD, Abdelwahab MG, Scheck AC, Preul MC (2012) Monocyte galactose/N-acetylgalactosamine-specific C-type lectin receptor stimulant immunotherapy of an experimental glioma. Part 1: stimulatory effects on blood monocytes and monocyte-derived cells of the brain. Cancer Manag Res 4:309–323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lasky LA (1991) Lectin cell adhesion molecules (LEC-CAMs): a new family of cell adhesion proteins involved with inflammation. J Cell Biochem 45:139–146

    Article  CAS  PubMed  Google Scholar 

  • Lee YC, Lee RT (1995) Carbohydrate-protein interactions: basis of glycobiology. Acc Chem Res 28:321–327

    Article  CAS  Google Scholar 

  • Li H, Wie L, Fang P, Yang P (2014) Recent advances in the fabrication and detection of lectin microarrays and their application in glycobiology analysis. Anal Methods 6:2003–2014

    Article  CAS  Google Scholar 

  • Mammen M, Choi SK, Whitesides GM (1998) Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors. Angew Chem Int Ed 37:2754–2794

    Article  Google Scholar 

  • Martin-Cereceda M, Williams R, Guinea A, Novarino G (2007) An investigation of the fine structure, cell surface carbohydrates, and appeal of the diatom Extubocellulus sp. as prey for small flagellates. Protoplasma 232:69–78

    Article  CAS  PubMed  Google Scholar 

  • McClatchey AI, Yap AS (2012) Contact inhibition (of proliferation) redux. Curr Opin Cell Biol 24:685–694

    Article  CAS  PubMed  Google Scholar 

  • Ni Y, Wu J (2014) Far-red and near infrared BODIPY dyes: synthesis and applications for fluorescent pH probes and bio-imaging. Org Biomol Chem 12:3774–3791

    Article  CAS  PubMed  Google Scholar 

  • Ofek I, Beachey EH (1978) Mannose binding and epithelial cell adherence of Escherichia coli. Infect Immun 22:247–254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pannof JM, Priem B, Morvan H, Joset F (1988) Sulphated exopolysaccharides produced by two unicellular strains of cyanobacteria, Synechocystis PCC6803 and 6714. Arch Microbiol 150:558–563

    Article  Google Scholar 

  • Perrimon N, Bernfield M (2001) Cellular functions of proteoglycans - an overview. Semin Cell Dev Biol 12:65–67

    Article  CAS  PubMed  Google Scholar 

  • Praseptiangga D, Hirayama M, Hori K (2012) Purification, characterization, and cDNA cloning of a novel lectin from the green alga, Codium barbatum. Biosci Biotechnol Biochem 76:805–811

    Article  CAS  PubMed  Google Scholar 

  • Ramoino P (1997) Lectin-binding glycoconjugates in Paramecium primaurelia: changes with cellular age and starvation. Histochem Cell Biol 107:321–329

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro-Viana R, García-Vallejo JJ, Collado D, Pérez-Inestrosa E, Bloem K, Van Kooyk Y, Rojo J (2012) BODIPY-labeled DC-SIGN-targeting glycodendrons efficiently internalize and route to lysosomes in human dendritic cells. Biomacromolecules 13:3209–3219

    Article  CAS  PubMed  Google Scholar 

  • Roberts EC, Zubkov MV, Martin-Cereceda M, Novarino G, Wootton EC (2006) Cell surface lectin-binding glycoconjugates on marine planktonic protists. FEMS Microbiol Lett 265:202–207

    Article  CAS  PubMed  Google Scholar 

  • Rostovtsev VV, Green LG, Fokin VV, Sharpless KB (2002) A stepwise Huisgen cycloaddition process: copper(I)-catalyzed regioselective “ligation” of azides and terminal alkynes. Angew Chem Int Ed 41:2596–2599

    Article  CAS  Google Scholar 

  • Roy R, Shiao TC, Rittenhouse-Olson K (2013) Glycodendrimers: versatile tools for nanotechnology. Braz J Pharm Sci 49:85–108

    Article  CAS  Google Scholar 

  • Saifuddin M, Hart ML, Gewurz H, Zhang Y, Spear GT (2000) Interaction of mannose-binding lectin with primary isolates of human immunodeficiency virus type 1. J Gen Virol 81:949–955

    Article  CAS  PubMed  Google Scholar 

  • Sattin S, Daghetti A, Thépaut M, Berzi A, Sánchez-Navarro M, Tabarani G, Rojo J, Fieschi F, Clerici M, Bernardi A (2010) Inhibition of DC-SIGN-mediated HIV infection by a linear trimannoside mimic in a tetravalent presentation. ACS Chem Biol 5:301–312

    Article  CAS  PubMed  Google Scholar 

  • Schwartz W (1973) Lynn Margulis, origin of eukariotic cells: evidence and research implications for a theory of the origin and evolution of microbial, plant, and animal cells of the Precambrian Earth. J Basic Microbiol 13:186

    Google Scholar 

  • Sengbusch PV, Müller U (1983) Distribution of glyconconjugates at algal cell surfaces as monitored by FITC-conjugated lectins. Studies on selected species from Cyanophyta, Pyrrophyta, Raphidophyta, Euglenophyta, Chromophyta and Chlorophyta. Protoplasma 114:103–113

    Article  Google Scholar 

  • Sharon N, Lis H (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14:53R–62R

    Article  CAS  PubMed  Google Scholar 

  • Smith EA, Thomas WD, Kiessling LL, Corn RM (2003) Surface plasmon resonance imaging studies of protein-carbohydrate interactions. J Am Chem Soc 125:6140–6148

    Article  CAS  PubMed  Google Scholar 

  • Spear GT, Zariffard MR, Xin J, Saifuddin M (2003) Inhibition of DC-SIGN-mediated trans infection of T-cells by mannose-binding lectin. Immunology 110:80–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tien CJ, Sigee DC, White KN (2005) Characterization of surface sugars on algal cells with fluorescein isothiocyanate-conjugated lectins. Protoplasma 225:225–233

    Article  CAS  PubMed  Google Scholar 

  • Tornøe CW, Christensen C, Meldal M (2002) Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper (I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J Organomet Chem 67:3057–3064

    Article  Google Scholar 

  • Varga N, Sutkeviciute I, Ribeiro-Viana R, Berzi A, Ramdasi R, Daghetti A, Vettorett G, Amara A, Clerici M, Rojo J, Fieschi F, Bernardi A (2014) A multivalent inhibitor of the DC-SIGN dependent uptake of HIV-1 and Dengue virus. Biomaterials 35:4175–4184

    Article  CAS  PubMed  Google Scholar 

  • Vivas M, Sacristán M, Legaz ME, Vicente C (2010) The cell recognition model in chlorolichens involving a fungal lectin binding to an algal ligand can be extended to cyanolichens. Plant Biol 12:615–621

    CAS  PubMed  Google Scholar 

  • Waite AM, Olson RJ, Dam HG, Passow U (1995) Sugar-containing compounds on the cell surfaces of marine diatoms measured using concanavalin A and flow cytometry. J Phycol 31:925–933

    Article  CAS  Google Scholar 

  • Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1993

    Article  CAS  PubMed  Google Scholar 

  • Wootton EC, Zubkov MV, Jones DH, Jones RH, Martel CM, Thornton CA, Roberts EC (2007) Biochemical prey recognition by planktonic protozoa. Environ Microbiol 9:216–222

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Jimbo M, Sakai R, Muramoto K, Kamiya H (1998) Purification and characterization of Microcystis aeruginosa (freshwater cyanobacterium) lectin. Comp Biochem Physiol B 119:593–597

    Article  CAS  PubMed  Google Scholar 

  • Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

C.C.F. and R.C.F. thank Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) for financial support. We also thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a Grant to C. Almeida. R.C.F thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-CsF) and Fundación Carolina for financial support. J.R. thanks Ministerio de Economía y Competitividad (MINECO) of Spain (project CTQ2014-52328-P) co-financed by European Regional Development Funds (ERDF) for financial support.

Author information

Authors and Affiliations

  1. Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida Antônio Carlos, 6627, Pampulha, Caixa Postal 486, Belo Horizonte, Minas Gerais, 31970-901, Brazil

    Cíntia de Almeida Gonçalves, Alessandra Giani & Cleber Cunha Figueredo

  2. Departamento de Química, Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, R. Diogo de Vasconcelos, 122, Pilar, Ouro Preto, 35400-000, Brazil

    Rute Cunha Figueiredo

  3. Departamento de Química Orgánica, Universidad de Málaga, 29071, Málaga, Spain

    Daniel Collado & Ezequiel Pérez-Inestrosa

  4. Centro de Nanomedicina y Biotecnología-BIONAND, Parque Tecnológico de Andalucía, 29590, Málaga, Spain

    Daniel Collado & Ezequiel Pérez-Inestrosa

  5. Glycosystems Laboratory, Instituto de Investigaciones Químicas (IIQ), CSIC – Universidad de Sevilla, 41092, Sevilla, Spain

    Javier Rojo

Authors
  1. Cíntia de Almeida Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rute Cunha Figueiredo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandra Giani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel Collado
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ezequiel Pérez-Inestrosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Javier Rojo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cleber Cunha Figueredo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cleber Cunha Figueredo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Almeida Gonçalves, C., Figueiredo, R.C., Giani, A. et al. Detection of glycidic receptors in microalgae using glycodendrons as probes: a new tool for studies on cell surface interactions. J Appl Phycol 31, 211–221 (2019). https://doi.org/10.1007/s10811-018-1555-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1555-6

Keywords

Search

Navigation