Skip to main content
SpringerLink
Log in

Molecular cloning, expression pattern, and molecular evolution of the spleen tyrosine kinase in lamprey, Lampetra japonica

  • Short Communication
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Spleen tyrosine kinase (Syk), a member of Syk family of cytoplasmic non-receptor tyrosine kinases, is a key component of B cell receptor signaling and regulates multiple physiological functions of B lymphocytes in vertebrates. In the current study, a Syk homologue was identified in the lamprey Lampetra japonica (Lj-Syk). The cDNA fragment of Lj-Syk contains a 1953-bp open reading frame which encodes 651 amino acids, a 12-bp fragment of 5′-untranslated region, and a 1029-bp 3′-untranslated region. The same as vertebrate's Syks, Lj-Syk protein also contains a tyrosine kinase catalytic domain which functions as its kinase activity center and two Src homology 2 (SH2) domains which are the targets when Syk is recruited by phosphorylated immunoreceptor tyrosine-based activation motif. It is revealed by multiple sequence alignment that the tyrosine kinase catalytic domain and two SH2 domains are conserved throughout the Syk gene family in vertebrates. The evolutionary dynamics of Syks were analyzed by MEME software using conserved motifs as markers. Among 19 conserved motifs elicited from 22 Syks or Syk-like proteins, 12 motifs that locate at N-terminal, two tandem SH2, Inter SH2, and Tyrkc domains are conserved in Syks from jawless to jawed vertebrates. From the absence and existence of the other seven motifs, it can be concluded that the primary Syk gene evolved to modern functional gene through short insertion and deletion strategy in their gene sequence rather than gene duplication. The expression of lamprey Syk was examined by real-time quantitative PCR and Western blot methods in leukocyte cells, gills, supraneural myeloid bodies, kidneys, and hearts of lampreys before and after the animals were stimulated with lipopolysaccharide (LPS). The transcriptional level of lamprey Syk was upregulated in gill, kidney, heart, and leukocyte cells, and the protein expression level is upregulated in leukocyte cells and supraneural myeloid bodies after stimulated with LPS. It could be deduced that Lj-Syk may play a crucial role in immune response of the jawless vertebrates.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Abbreviations

Syk:

Spleen tyrosine kinase

Lj-Syk:

Syk of Lampetra japonica

EST:

Expressed Sequence Tags

RACE:

Rapid amplification of cDNA ends

LPS:

Lipopolysaccharide

qPCR:

Real-time quantitative PCR detecting system

ITAM:

Immunoreceptor tyrosine-based activation motif

References

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fütterer K, Wong J, Grucza RA, Chan AC, Waksman G (1998) Structural basis for Syk tyrosine kinase ubiquity in signal transduction pathways revealed by the crystal structure of its regulatory SH2 domains bound to a dually phosphorylated ITAM peptide. J Mol Biol 281(3):523–537

    Article  PubMed  Google Scholar 

  • Feng G, Wang X (2014) Role of spleen tyrosine kinase in the pathogenesis of chronic lymphocytic leukemia. Leuk Lymphoma 0: 1-7

  • Forey PL, Janvier P (1993) Agnathans and the origin of jawed vertebrates. Nature 361:129–134

    Article  Google Scholar 

  • Guo P, Hirano M, Herrin BR, Li JX, Yu CL (2009) Dual nature of the adaptive immune system in lampreys. Nature 459:796–801

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Haruta C, Suzuki T, Kasahara M (2006) Variable domains in hagfish: NICIR is a polymorphic multigene family expressed preferentially in leukocytes and is related to lamprey TCR-like. Immunogenetics 58(2–3):216–25

    Article  CAS  PubMed  Google Scholar 

  • Kurosaki T, Shinohara H, Baba Y (2010) B cell signaling and fate decision. Annu Rev Immunol 28:21–55

    Article  CAS  PubMed  Google Scholar 

  • Lee YG, Chain BM, Cho JY (2009) Distinct role of spleen tyrosine kinase in the early phosphorylation of inhibitor of KBa via activation of the phosphoinositide-3-kinase and Akt pathways. Int J Biochem Cell Biol 41(4):811–821

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Yankee TM, Hu J, Asai DJ, Harrison ML, Geahlen RL (2001) Visualization of Syk-antigen receptor interactions using green fluorescent protein: differential roles for Syk and Lyn in the regulation of receptor capping and internalization. J Immunol 166(3):1507–1516

    Article  CAS  PubMed  Google Scholar 

  • Martin F, Gisela Z, Anne CA et al (1995) Molecule characterization of the murine Syk protein tyrosine kinase cDNA, transcripts and protein. Biochem Biophys Res Commun 213:273–281

    Article  Google Scholar 

  • Mócsai A, Ruland J, Tybulewicz VL (2010) The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 10(6):387–402

    Article  PubMed  Google Scholar 

  • Ohtsuka M, Arase H, Takeuchi A, Yamasaki S, Shiina R, Suenaga T, Sakurai D, Yokosuka T, Arase N, Iwashima M, Kitamura T, Moriya H, Saito T (2004) NFAM1, an immunoreceptor tyrosine-based activation motif-bearing molecule that regulates B cell development and signaling. Proc Natl Acad Sci U S A 101(21):8126–8131

    Article  PubMed Central  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 430:174–180

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Saha NR, Kasamatsu J et al (2005) Variable lymphocyte receptors in hagfish. Proc Natl Acad Sci 102:9224–9229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stewart ZA, Pietenpol JA (2001) Syk: a new player in the field of breast cancer. Breast Cancer Res 3:5–7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taniguchi T, Kobayashi T, Kondo J (1991) Molecular cloning of a porcine gene syk that encodes a 72-kDa protein-tyrosine kinase showing high susceptibility to proteolysis. J Biol Chem 266(24):15790–15796

    CAS  PubMed  Google Scholar 

  • Turner M, Sehweighoffer E, Colucei F et al (2000) Tyrosine kinase SYK: essential functions for immunoreceptor signaling. J lmmunol Today 2(3):148–154

    Article  Google Scholar 

  • Wang L, Duke L, Zhang PS, Arlinghaus RB, Symmans WF, Sahin A, Mendez R, Dai JL (2003) Alternative splicing disrupts a nuclear localization signal in spleen tyrosine kinase that is required for invasion suppression in breast cancer. Cancer Res 63:4724–4730

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from National Program on Key Basic Research Project (973 Program, Grant 2013CB835304), National Natural Science Foundation of China (Grant 31271323), and Natural Science Foundation of Liaoning Province of China (2014029203).

Author information

Authors and Affiliations

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

    Chang Liu, Peng Su, Ranran Li, Qiong Zhang, Ting Zhu, Xin Liu & Qingwei Li

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

    Chang Liu, Peng Su, Ranran Li, Qiong Zhang, Ting Zhu, Xin Liu & Qingwei Li

Authors
  1. Chang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peng Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ranran Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ting Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qingwei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xin Liu or Qingwei Li.

Additional information

Communicated by Matthias Hammerschmidt

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Su, P., Li, R. et al. Molecular cloning, expression pattern, and molecular evolution of the spleen tyrosine kinase in lamprey, Lampetra japonica . Dev Genes Evol 225, 113–120 (2015). https://doi.org/10.1007/s00427-015-0492-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-015-0492-5

Keywords

Search

Navigation