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Molecular cloning, expression pattern, and phylogenetic analysis of a tetraspanin CD82-like molecule in lamprey Lampetra japonica

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Abstract

CD82, a member of the tetraspanins, is originally identified as an accessory molecule in T cell activation, and it participates in the formation of immune synapse both in T cells and antigen-presenting cells of jawed vertebrates. In the present study, a CD82 homologous complementary DNA (cDNA) sequence is identified in the lamprey Lampetra japonica. The open reading frame of this sequence is 801 bp long and encodes a 266-amino acid protein. The multialignment of this sequence with several typical CD82s and CD37s of jawed vertebrates shows that it also possesses their conserved four transmembrane domains and a six-cysteine motif Cys-Cys-Gly…Cys-Ser-Cys…Cys…Cys, which is a characteristic motif of CD82 and CD37 vertebrate tetraspanin sequences. Since it is close to CD82s in sequence similarity, we name it as Lja-CD82-like. From the distribution profile of the conserved motifs of CD82-like, CD82, and CD37 molecules from molluscas to mammals, it seems that the CD82s and CD37s evolved from a common ancestral gene through a gene duplication event to their modern forms by a short insertion or substitution approaches. The phylogenetic analysis indicated that CD82 and CD37 molecules of jawed vertebrates originated from a common ancestral gene which is close to agnathan CD82-like and evolved into two distinct paralogous groups maybe after the divergence of jawed and jawless vertebrates. An expression vector with trigger factor (TF) was constructed to ensure that Lja-CD82-like express in prokaryotic expression host. The expressions of Lja-CD82-like messenger RNA (mRNA) and protein in immune-related tissues of lamprey were detected by real-time quantitative polymerase chain reaction and western blotting. Results showed that the mRNA and the protein levels of Lja-CD82-like were significantly upregulated in lymphocyte-like cells, gills, and supraneural myeloid bodies after stimulation with mixed antigens, respectively. Our data provided a foundation for the further study of Lja-CD82-like and its role in immune response process of jawless vertebrates.

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References

  • Amemiya CT, Saha NR, Zapata A (2007) Evolution and development of immunological structures in the lamprey. Curr Opin Immunol 19(5):535–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Artavanis-Tsakonas K, Kasperkovitz PV, Papa E, Cardenas ML, Khan NS, Van der Veen AG, Ploegh HL, Vyas JM (2011) The tetraspanin CD82 is specifically recruited to fungal and bacterial phagosomes prior to acidification. Infect Immun 79(3):1098–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajoghli B, Guo P, Aghaallaei N, Hirano M, Strohmeier C, McCurley N, Bockman DE, Schorpp M, Cooper MD, Boehm T (2011) A thymus candidate in lampreys. Nature 470(7332):90–94

    Article  CAS  PubMed  Google Scholar 

  • Bassani S, Cingolani LA (2012) Tetraspains: interactions and interplay with integrins. Int J Biochem Cell Biol 44:703–708

    Article  CAS  PubMed  Google Scholar 

  • Berditchevski F, Odintsova E (2007) Tetraspanins as regulators of protein trafficking. Traffic 8(2):89–96

    Article  CAS  PubMed  Google Scholar 

  • Boucheix C, Rubinstein E (2001) Tetraspanins. Cell Mol Life Sci 58(9):1189–1205

    Article  CAS  PubMed  Google Scholar 

  • Charrin S, Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E (2009) Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 420:133–154

    Article  CAS  PubMed  Google Scholar 

  • Charrin S, Jouannet S, Boucheix C, Rubinstein E (2014) Tetraspanins at a glance. J Cell Sci 127(Pt 17):3641–3648

    Article  CAS  PubMed  Google Scholar 

  • Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124(4):815–822

    Article  CAS  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(1):486–491

    Article  CAS  PubMed  Google Scholar 

  • Dong JT, Lamb PW, Rinker-Schaeffer CW, Vukanovic J, Ichikawa T, Isaacs JT, Barrett JC (1995) KAI 1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 268(5212):884–886

    Article  CAS  PubMed  Google Scholar 

  • Escola JM, Kleijmeer MJ, Stoorvogel W (1998) Selective enrichment of tetraspan proteins on the internal vesicals of muitivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273(32):20121–20127

    Article  CAS  PubMed  Google Scholar 

  • Garcia-España A, Chung PJ, Sarkar IN, Stiner E, Sun TT, Desalle R (2008) Appearance of new tetraspanin genes during vertebrate evolution. Genomics 91(4):326–334

    Article  PubMed  Google Scholar 

  • Guo P, Hirano M, Herrin BR, Li J, Yu C, Sadlonova A, Cooper MD (2009) Dual nature of the adaptive immune system in lampreys. Nature 459(7248):796–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemler ME (2008) Targeting of tetraspanin proteins-potential benefits and strategies. Nat Rev Drug Discov 7(9):747–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y, Xie X, Yu Y, Yu X, Chen S, Zhang S, Pontarotti P, Xu A (2005) The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 86(6):674–684

    Article  CAS  PubMed  Google Scholar 

  • Kropshofer H, Spindeldreher S, Röhn TA, Platania N, Grygar C, Daniel N, Wölpl A, Langen H, Horejsi V, Vogt AB (2001) Tetraspan microdomains distinct from lipid rafts enrich select peptide-MHC class II complexes. Nat Immunol 3(1):61–68

    Article  PubMed  Google Scholar 

  • Lebel-Binay S, Gil ML, Lagaudriere C, Miloux B, Marchiol-Fournigault C, Quillet-Mary A, Lopez M, Fradelizi D, Conjeaud H (1994) Further characterization of CD82/IA4 antigen (type III surface protein): An activation/differentiation marker of monoclear cells. Cell Immunol 154:468–483

    Article  CAS  PubMed  Google Scholar 

  • Lebel-Binay S, Laguadriere C, Fradelizi D, Conjeaud H (1995) CD82, member of the tetra-span-transmembrane protein family, is a costimulatory protein for T cell activation. J Immunol 155:101–110

    CAS  PubMed  Google Scholar 

  • Levy S, Shoham T (2005) The tetraspanin web modulates inmmune-signalling complexes. Nat Rev Immunol 5:136–148

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Liu X, Wu Y et al (2008) Separation and cytological character of peripheral blood lymphocytes in Japanese lamprey. Chin J Zool 43(1):82–87

    Google Scholar 

  • Miranti CK (2009) Controlling cell surface dynamics and signaling: how CD82/KAI1 suppresses metastasis? Cell Signal 21:196–211

    Article  CAS  PubMed  Google Scholar 

  • Odintsova E, Sugiure T, Berdichevski F (2000) Attenuation of EGF receptor signaling by a metastasis supressor, the tetraspanin CD82/KAI-1. Curr Biol 10:1009–1012

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Cooper MD (2006) The evolution of adaptive immunity. Annu Rev Immunol 24:497–518

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Amemiya CT, Ehrhardt GR, Ceitlin J, Gartland GL, Cooper MD (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430(6996):174–180

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Saha NR, Kasamatsu J, Suzuki T, Amemiya CT, Kasahara M, Cooper MD (2005) Variable lymphocyte receptors in hagfish. Proc Natl Acad Sci 102(26):9224–9229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saleh SM, Parhar RS, Al-Hejailan RS, Bakheet RH, Khaleel HS, Khalak HG, Halees AS, Zaidi MZ, Meyer BF, Yung GP, Seebach JD, Conca W, Khabar KS, Collison KS, Al-Mohanna FA (2013) Identification of the tetraspanin CD82 as a new barrier to xenotransplantation. J Immunol 193:2796–2805

    Article  Google Scholar 

  • Schwartz-Albiez R, Dörken B, Hofmann W, Moldenhauer G (1988) The B cell-associated CD37 antigen (gp40-52). Structure and subcellular expression of an extensively glycosylated glycoprotein. J Immunol 140(3):905–914

    CAS  PubMed  Google Scholar 

  • Seigneuret M, Delaguillaumie A, Lagaudriere-Gesbert C, Conjeaud H (2001) Structure of the tetraspain main extracellular domain: a partially conserved fold with a structurally variable domain insertion. J Biol Chem 276(43):40055–40064

    Article  CAS  PubMed  Google Scholar 

  • Shibagaki N, Hanada K, Yamaguchi S, Yamashita H, Shimada S, Hamada H (1998) Functional analysis of CD82 in the early phase of T cell activation: roles in cell adhesion and signal transduction. Eur J Immunol 28:1125–1133

    Article  CAS  PubMed  Google Scholar 

  • Shibagaki N, Hanada K, Yamashita H, Shimada S, Hamada H (1999) Overexpression of CD82 on human T cells enhances LFA-1/ICAM-1-mediated cell-cell adhesion: functional association between CD82 and LFA-1 in T cell activation. Eur J Immunol 29:4081–4091

    Article  CAS  PubMed  Google Scholar 

  • Sridhar SC, Miranti CK (2006) Tetraspanin KAI1/CD82 suppresses invasion by inhubiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene 25:2367–2378

    Article  CAS  PubMed  Google Scholar 

  • Stipp CS, Kolesnikova TV, Hemler ME (2003) Functional domains in tetraspanin proteins. Trends Biochem Sci 28(2):106–112

    Article  CAS  PubMed  Google Scholar 

  • Takahashi M, Sugiure T, Abe M, Lshii K, Shirasuna K (2007) Regulation of c-Met signaling by the tetraspanin KAI-1/CD82 affects cancer cell migration. Int J Cancer 121:1919–1929

    Article  CAS  PubMed  Google Scholar 

  • Tarrant JM, Robb L, Spriel AB, Wright MD (2003) Tetraspanins: molecular organisers of the leukocyto surface. Trends Immunol 24:610–617

    Article  CAS  PubMed  Google Scholar 

  • Termini CM, Cotter ML, Marjon KD, Buranda T, Lidke A, Gillette JM (2014) The membrane scaffold CD82 regulates cell adhesion by altering α4 integrin stability and molecular density. Mol Biol Cell 25:1560–1573

    Article  PubMed  PubMed Central  Google Scholar 

  • Van den Ent F, Lowe J (2006) RF: cloning: a restriction-free method for inserting target gengs into plasmid. J Biochem Biophys Methods 67(1):67–74

    Article  PubMed  Google Scholar 

  • Xu C, Zhang YH, Thangavel M, Richardson MM, Liu L, Zhou B, Zheng Y, Ostrom RS, Zhang XA (2009) CD82 endocytosis and cholesterol-dependent reorganization of tetraspanin webs and lipid rafts. FASEB J 23:3273–3288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yien CT, Weissman AM (2011) Dissecting the diverse functions of the metastasis suppressor CD82/KAI1. FEBS Lett 585(20):3166–3173

    Article  Google Scholar 

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Authors and Affiliations

  1. College of Life Science, Liaoning Normal University, Dalian, 116029, China

    Xiaoping Zhang, Xueying Song, Peng Su, Meng Gou, Hao Wang, Xin Liu & Qingwei Li

  2. Lamprey Research Center, Liaoning Normal University, Dalian, 116029, China

    Xiaoping Zhang, Xueying Song, Peng Su, Meng Gou, Hao Wang, Xin Liu & Qingwei Li

Authors
  1. Xiaoping Zhang
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  2. Xueying Song
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  3. Peng Su
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  4. Meng Gou
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  5. Hao Wang
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  6. Xin Liu
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  7. Qingwei Li
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Correspondence to Xin Liu or Qingwei Li.

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Communicated by Matthias Hammerschmidt

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Zhang, X., Song, X., Su, P. et al. Molecular cloning, expression pattern, and phylogenetic analysis of a tetraspanin CD82-like molecule in lamprey Lampetra japonica . Dev Genes Evol 226, 87–98 (2016). https://doi.org/10.1007/s00427-016-0530-y

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