Skip to main content
SpringerLink
Log in

Tetraspanins in Lower Eukaryotes

  • Chapter
  • First Online:
Tetraspanins

Part of the book series: Proteins and Cell Regulation ((PROR,volume 9))

Abstract

Tetraspanins are widely distributed among metazoan phyla. Recent progress in various genome projects have enabled us to carry out a comparative analysis of tetraspanins and their relative in lower eukaryotes including unicellular organisms (e.g. Amoeba and Encephalitozoon). The functions of tetraspanins in lower eukaryotes are largely unknown, but recent comprehensive genetic analyses have provided us with some clues for the roles played by these proteins in these organisms. Here we overview tetraspanin proteins in lower eukaryotes and plants and describe what is known about their specific functions in the context of organ development and differentiation. We also review recent data describing physiological regulators of tetraspanins and their involvement in processes related to parasitism.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allaoui A, Botteaux A, Dumont JE, Hoste C, De Deken X (2009) Dual oxidases and hydrogen peroxide in a complex dialogue between host mucosae and bacteria. Trends Mol Med 15:571–579

    Article  PubMed  CAS  Google Scholar 

  • Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313

    Article  PubMed  CAS  Google Scholar 

  • Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP et al (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352–358

    Article  PubMed  CAS  Google Scholar 

  • Blaxter M, Bird D (1997) Parasitic nematodes. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 851–878

    Google Scholar 

  • Braschi S, Borges WC, Wilson RA (2006) Proteomic analysis of the schistosome tegument and its surface membranes. Mem Inst Oswaldo Cruz 101(Suppl 1):205–212

    Article  PubMed  CAS  Google Scholar 

  • Brun S, Malagnac F, Bidard F, Lalucque H, Silar P (2009) Functions and regulation of the Nox family in the filamentous fungus Podospora anserina: a new role in cellulose degradation. Mol Microbiol 74:480–496

    Article  PubMed  CAS  Google Scholar 

  • Chávez V, Mohri-Shiomi A, Garsin DA (2009) Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect Immun 77:4983–4989

    Article  PubMed  Google Scholar 

  • Chiu W-H, Chandler J, Cnops G, Van Lijsebettens M, Werr W (2007) Mutations in the tornado2 gene affect cellular decisions in the peripheral zone of the shoot apical meristem of Arabidopsis thaliana. Plant Mol Biol 63:731–744

    Article  PubMed  CAS  Google Scholar 

  • Clergeot PH, Gourgues M, Cots J, Laurans F, Latorse MP et al (2001) PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea. Proc Natl Acad Sci U S A 98:6963–6968

    Article  PubMed  CAS  Google Scholar 

  • Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M et al (2000) Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root. Development 127:3385–3394

    PubMed  CAS  Google Scholar 

  • Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H et al (2006) The tornado1 and tornado2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell 18:852–866

    Article  PubMed  CAS  Google Scholar 

  • Consortium CeS (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018

    Article  Google Scholar 

  • Davern KM, Wright MD, Herrmann VR, Mitchell GF (1991) Further characterisation of the Schistosoma japonicum protein Sj23, a target antigen of an immunodiagnostic monoclonal antibody. Mol Biochem Parasitol 48:67–75

    Article  PubMed  CAS  Google Scholar 

  • De Deken X, Wang D, Many MC, Costagliola S, Libert F et al (2000) Cloning of two human ­thyroid cDNAs encoding new members of the NADPH oxidase family. J Biol Chem 275:23227–23233

    Article  PubMed  Google Scholar 

  • Desalle R, Mares R, Garcia-España A (2010) Evolution of cysteine patterns in the large extracellular loop of tetraspanins from animals, fungi, plants and single-celled eukaryotes. Mol Phylogenet Evol 56:486–491

    Article  PubMed  CAS  Google Scholar 

  • Donkó A, Péterfi Z, Sum A, Leto T, Geiszt M (2005) Dual oxidases. Philos Trans R Soc Lond B Biol Sci 360:2301–2308

    Article  PubMed  Google Scholar 

  • Dunn CD, Sulis ML, Ferrando AA, Greenwald I (2010) A conserved tetraspanin subfamily promotes Notch signaling in Caenorhabditis elegans and in human cells. Proc Natl Acad Sci USA 107:5907–5912

    Article  PubMed  CAS  Google Scholar 

  • Dupuy C, Ohayon R, Valent A, Noël-Hudson MS, Dème D et al (1999) Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cDNAs. J Biol Chem 274:37265–37269

    Article  PubMed  CAS  Google Scholar 

  • Edens WA, Sharling L, Cheng G, Shapira R, Kinkade JM et al (2001) Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol 154:879–891

    Article  PubMed  CAS  Google Scholar 

  • Egan MJ, Wang Z-Y, Jones MA, Smirnoff N, Talbot NJ (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci U S A 104:11772–11777

    Article  PubMed  CAS  Google Scholar 

  • Flores MV, Crawford KC, Pullin LM, Hall CJ, Crosier KE et al (2010) Dual oxidase in the intestinal epithelium of zebrafish larvae has anti-bacterial properties. Biochem Biophys Res Commun 400:164–168

    Article  PubMed  CAS  Google Scholar 

  • Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN (2002) Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci U S A 99:13663–13668

    Article  PubMed  CAS  Google Scholar 

  • Garcia-España A, Mares R, Sun T-T, Desalle R (2009) Intron evolution: testing hypotheses of intron evolution using the phylogenomics of tetraspanins. PLoS One 4:e4680

    Article  PubMed  Google Scholar 

  • Ghedin E, Wang S, Spiro D, Caler E, Zhao Q et al (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317:1756–1760

    Article  PubMed  CAS  Google Scholar 

  • Girin T, Sorefan K, Ostergaard L (2009) Meristematic sculpting in fruit development. J Exp Bot 60:1493–1502

    Article  PubMed  CAS  Google Scholar 

  • Gnanasekar M, Anand SB, Ramaswamy K (2008) Identification and cloning of a novel tetraspanin (TSP) homologue from Brugia malayi. DNA Seq 19:151–156

    PubMed  CAS  Google Scholar 

  • Gobert GN, Tran MH, Moertel L, Mulvenna J, Jones MK et al (2010) Transcriptional changes in Schistosoma mansoni during early schistosomula development and in the presence of erythrocytes. PLoS Negl Trop Dis 4:e600

    Article  PubMed  Google Scholar 

  • Gourgues M, Clergeot PH, Veneault C, Cots J, Sibuet S et al (2002) A new class of tetraspanins in fungi. Biochem Biophys Res Commun 297:1197–1204

    Article  PubMed  CAS  Google Scholar 

  • Gourgues M, Brunet-Simon A, Lebrun MH, Levis C (2004) The tetraspanin BcPls1 is required for appressorium-mediated penetration of Botrytis cinerea into host plant leaves. Mol Microbiol 51:619–629

    Article  PubMed  CAS  Google Scholar 

  • Grasberger H, Refetoff S (2006) Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent. J Biol Chem 281:18269–18272

    Article  PubMed  CAS  Google Scholar 

  • Grasberger H, De Deken X, Miot F, Pohlenz J, Refetoff S (2007) Missense mutations of dual oxidase 2 (DUOX2) implicated in congenital hypothyroidism have impaired trafficking in cells reconstituted with DUOX2 maturation factor. Mol Endocrinol 21:1408–1421

    Article  PubMed  CAS  Google Scholar 

  • Ha E-M, Oh C-T, Bae YS, Lee W-J (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310:847–850

    Article  PubMed  CAS  Google Scholar 

  • Hotez PJ, Bethony JM, Diemert DJ, Pearson M, Loukas A (2010) Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat Rev Microbiol 8:814–826

    Article  PubMed  CAS  Google Scholar 

  • Howard RJ, Ferrari MA, Roach DH, Money NP (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci U S A 88:11281–11284

    Article  PubMed  CAS  Google Scholar 

  • Huang S, Yuan S, Dong M, Su J, Yu C et al (2005) The phylogenetic analysis of tetraspanins ­projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86:674–684

    Article  PubMed  CAS  Google Scholar 

  • Johnstone IL (2000) Cuticle collagen genes. Expression in Caenorhabditis elegans. Trends Genet 16:21–27

    Article  PubMed  CAS  Google Scholar 

  • Kopan R, Ilagan MXG (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216–233

    Article  PubMed  CAS  Google Scholar 

  • Kopczynski CC, Davis GW, Goodman CS (1996) A neural tetraspanin, encoded by late bloomer, that facilitates synapse formation. Science 271:1867–1870

    Article  PubMed  CAS  Google Scholar 

  • Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181–189

    Article  PubMed  CAS  Google Scholar 

  • Lambou K, Tharreau D, Kohler A, Sirven C, Marguerettaz M et al (2008a) Fungi have three tetraspanin families with distinct functions. BMC Genomics 9:63

    Article  PubMed  Google Scholar 

  • Lambou K, Malagnac F, Barbisan C, Tharreau D, Lebrun M-H et al (2008b) The crucial role of the Pls1 tetraspanin during ascospore germination in Podospora anserina provides an example of the convergent evolution of morphogenetic processes in fungal plant pathogens and saprobes. Eukaryot Cell 7:1809–1818

    Article  PubMed  CAS  Google Scholar 

  • Loukas A, Tran M, Pearson MS (2007) Schistosome membrane proteins as vaccines. Int J Parasitol 37:257–263

    Article  PubMed  CAS  Google Scholar 

  • Luxen S, Noack D, Frausto M, Davanture S, Torbett BE et al (2009) Heterodimerization controls localization of Duox-DuoxA NADPH oxidases in airway cells. J Cell Sci 122:1238–1247

    Article  PubMed  CAS  Google Scholar 

  • Malagnac F, Lalucque H, Lepère G, Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:982–997

    Article  PubMed  CAS  Google Scholar 

  • Malagnac F, Bidard F, Lalucque H, Brun S, Lambou K et al (2008) Convergent evolution of morphogenetic processes in fungi: role of tetraspanins and NADPH oxidases 2 in plant pathogens and saprobes. Commun Integr Biol 1:180–181

    Article  PubMed  Google Scholar 

  • Miyazaki T, Müller U, Campbell KS (1997) Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81. EMBO J 16:4217–4225

    Article  PubMed  CAS  Google Scholar 

  • Morand S, Ueyama T, Tsujibe S, Saito N, Korzeniowska A et al (2009) Duox maturation factors form cell surface complexes with Duox affecting the specificity of reactive oxygen species generation. FASEB J 23:1205–1218

    Article  PubMed  CAS  Google Scholar 

  • Moribe H, Yochem J, Yamada H, Tabuse Y, Fujimoto T et al (2004) Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J Cell Sci 117:5209–5220

    Article  PubMed  CAS  Google Scholar 

  • Olmos E, Reiss B, Dekker K (2003) The ekeko mutant demonstrates a role for tetraspanin-like protein in plant development. Biochem Biophys Res Commun 310:1054–1061

    Article  PubMed  CAS  Google Scholar 

  • Page AP, Johnstone IL (2007) The cuticle. In: The C. elegans Research Community (ed) Wormbook. WormBook, doi:/10.1895/wormbook.1.7.1, http://www.wormbook.org

  • Segmüller N, Kokkelink L, Giesbert S, Odinius D, van Kan J et al (2008) NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol Plant Microbe Interact 21:808–819

    Article  PubMed  Google Scholar 

  • Sepulveda J, Tremblay JM, DeGnore JP, Skelly PJ, Shoemaker CB (2010) Schistosoma mansoni host-exposed surface antigens characterized by sera and recombinant antibodies from schistosomiasis-­resistant rats. Int J Parasitol 40:1407–1417

    Article  PubMed  CAS  Google Scholar 

  • Sinenko SA, Mathey-Prevot B (2004) Increased expression of Drosophila tetraspanin, Tsp68C, suppresses the abnormal proliferation of ytr-deficient and Ras/Raf-activated hemocytes. Oncogene 23:9120–9128

    Article  PubMed  CAS  Google Scholar 

  • Smyth D, Mcmanus DP, Smout MJ, Laha T, Zhang W et al (2003) Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infect Immun 71:2548–2554

    Article  PubMed  CAS  Google Scholar 

  • Sumimoto H (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J 275:3249–3277

    Article  PubMed  CAS  Google Scholar 

  • Tarrant JM, Groom J, Metcalf D, Li R, Borobokas B et al (2002) The absence of Tssc6, a member of the tetraspanin superfamily, does not affect lymphoid development but enhances in vitro T-cell proliferative responses. Mol Cell Biol 22:5006–5018

    Article  PubMed  CAS  Google Scholar 

  • Taylor MJ, Hoerauf A, Bockarie M (2010) Lymphatic filariasis and onchocerciasis. Lancet 376:1175–1185

    Article  PubMed  Google Scholar 

  • Thein M, Winter A, Stepek G, Mccormack G, Stapleton G et al (2009) Combined extracellular matrix cross-linking activity of the peroxidase MLT-7 and the duox BLI-3 are critical for post-­embryonic viability in Caenorhabditis elegans. J Biol Chem 284:17549–17563

    Article  PubMed  CAS  Google Scholar 

  • Todres E, Nardi JB, Robertson HM (2000) The tetraspanin superfamily in insects. Insect Mol Biol 9:581–590

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson MG, Wright MD (1996) A new transmembrane 4 superfamily molecule in the nematode, Caenorhabditis elegans. J Mol Evol 43:312–314

    Article  PubMed  CAS  Google Scholar 

  • Tran MH, Pearson MS, Bethony JM, Smyth DJ, Jones MK et al (2006) Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nat Med 12:835–840

    Article  PubMed  CAS  Google Scholar 

  • Tran MH, Freitas TC, Cooper L, Gaze S, Gatton ML et al (2010) Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathog 6:e140

    Article  Google Scholar 

  • van Spriel AB, Puls KL, Sofi M, Pouniotis D, Hochrein H et al (2004) A regulatory role for CD37 in T cell proliferation. J Immunol 172:2953–2961

    PubMed  Google Scholar 

  • Veneault-Fourrey C, Parisot D, Gourgues M, Lauge R, Lebrun MH et al (2005) The tetraspanin gene ClPLS1 is essential for appressorium-mediated penetration of the fungal pathogen Colletotrichum lindemuthianum. Fungal Genet Biol 42:306–318

    Article  PubMed  CAS  Google Scholar 

  • Veneault-Fourrey C, Lambou K, Lebrun M-H (2006) Fungal Pls1 tetraspanins as key factors of penetration into host plants: a role in re-establishing polarized growth in the appressorium? FEMS Microbiol Lett 256:179–184

    Article  PubMed  CAS  Google Scholar 

  • Wakabayashi T, Craessaerts K, Bammens L, Bentahir M, Borgions F et al (2009) Analysis of the gamma-secretase interactome and validation of its association with tetraspanin-enriched microdomains. Nat Cell Biol 11:1340–1346

    Article  PubMed  CAS  Google Scholar 

  • World Health Organization (2009) Neglected tropical diseases, hidden successes, emerging opportunities. WHO Press, Geneva

    Google Scholar 

  • Wright MD, Henkle KJ, Mitchell GF (1990) An immunogenic Mr 23,000 integral membrane protein of Schistosoma mansoni worms that closely resembles a human tumor-associated antigen. J Immunol 144:3195–3200

    PubMed  CAS  Google Scholar 

  • Wright MD, Geary SM, Fitter S, Moseley GW, Lau L-M et al (2004) Characterization of mice lacking the tetraspanin superfamily member CD151. Mol Cell Biol 24:5978–5988

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Lee S-J, Suzuki E, Dugan KD, Stoddard A et al (2004) A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. EMBO J 23:811–822

    Article  PubMed  CAS  Google Scholar 

  • Xu D, Sharma C, Hemler ME (2009) Tetraspanin12 regulates ADAM10-dependent cleavage of amyloid precursor protein. FASEB J 23:3674–3681

    Article  PubMed  CAS  Google Scholar 

  • Yuan C, Y-j F, Li J, Y-f Y, L-l C et al (2010) Schistosoma japonicum: efficient and rapid purification of the tetraspanin extracellular loop 2, a potential protective antigen against schistosomiasis in mammalian. Exp Parasitol 126:456–461

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Kurume University School of Medicine, 67 Asahimachi, Kurume, Fukuoka, 830-0011, Japan

    Hiroki Moribe

  2. Department of Cell Biology, Research Institute for Microbial Diseases, Osaka University, 3-1 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Eisuke Mekada

Authors
  1. Hiroki Moribe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eisuke Mekada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroki Moribe .

Editor information

Editors and Affiliations

  1. , School of Cancer Sciences, University of Birmingham, Vincent Drive, Birmingham, B15 2TT, United Kingdom

    Fedor Berditchevski

  2. INSERM U1004, Av. Paul Vaillant Couturier 14, Villejuif, F-94807, France

    Eric Rubinstein

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Moribe, H., Mekada, E. (2013). Tetraspanins in Lower Eukaryotes. In: Berditchevski, F., Rubinstein, E. (eds) Tetraspanins. Proteins and Cell Regulation, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6070-7_8

Download citation

Publish with us

Policies and ethics

Search

Navigation