Skip to main content
Log in

The chicken SLAM family

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The signaling lymphocytic activation molecule (SLAM) family of receptors is critically involved in the immune regulation of lymphocytes but has only been detected in mammals, with one member being present in Xenopus. Here, we describe the identification, cloning, and analysis of the chicken homologues to the mammalian SLAMF1 (CD150), SLAMF2 (CD48), and SLAMF4 (CD244, 2B4). Two additional chicken SLAM genes were identified and designated SLAMF3like and SLAM5like in order to stress that those two receptors have no clear mammalian counterpart but share some features with mammalian SLAMF3 and SLAMF5, respectively. Three of the chicken SLAM genes are located on chromosome 25, whereas two are currently not yet assigned. The mammalian and chicken receptors share a common structure with a V-like domain that lacks conserved cysteine residues and a C2-type Ig domain with four cysteines forming two disulfide bonds. Chicken SLAMF2, like its mammalian counterpart, lacks a transmembrane and cytoplasmic domain and thus represents a glycosyl-phosphatidyl-inositol-anchored protein. The cytoplasmic tails of SLAMF1 and SLAMF4 display two and four conserved immunoreceptor tyrosine-based switch motifs (ITSMs), respectively, whereas both chicken SLAMF3like and SLAMF5like have only a single ITSM. We have also identified the chicken homologues of the SLAM-associated protein family of adaptors (SAP), SAP and EAT-2. Chicken SAP shares about 70 % identity with mammalian SAP, and chicken EAT-2 is homologous to mouse EAT-2, whereas human EAT-2 is much shorter. The characterization of the chicken SLAM family of receptors and the SAP adaptors demonstrates the phylogenetic conservation of this family, in particular, its signaling capacities.

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

Access this article

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

GPI:

glycosyl-phosphatidyl-inositol

SLAM:

signaling lymphocytic activation molecule

SAP:

SLAM-associated protein family of adaptors

ITSM:

immunoreceptor tyrosine-based switch motif

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    Article  PubMed  Google Scholar 

  • Boles KS, Stepp SE, Bennett M, Kumar V, Mathew PA (2001) 2B4 (CD244) and CS1: novel members of the CD2 subset of the immunoglobulin superfamily molecules expressed on natural killer cells and other leukocytes. Immunol Rev 181:234–249

    Article  PubMed  CAS  Google Scholar 

  • Cannons JL, Tangye SG, Schwartzberg PL (2011) SLAM family receptors and SAP adaptors in immunity. Annu Rev Immunol 29:665–705

    Article  PubMed  CAS  Google Scholar 

  • Colonna M (1997) Specificity and function of immunoglobulin superfamily NK cell inhibitory and stimulatory receptors. Immunol Rev 155:127–133

    Article  PubMed  CAS  Google Scholar 

  • Daeron M, Jaeger S, Du Pasquier L, Vivier E (2008) Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol Rev 224:11–43

    Article  PubMed  CAS  Google Scholar 

  • Dong Z, Davidson D, Perez-Quintero LA, Kurosaki T, Swat W, Veillette A (2012) The adaptor SAP controls NK cell activation by regulating the enzymes Vav-1 and SHIP-1 and by enhancing conjugates with target cells. Immunity 36:974–985

    Article  PubMed  CAS  Google Scholar 

  • Göbel TW, Bolliger L (1998) The chicken TCR ζ-chain restores the function of a mouse T cell hybridoma. J Immunol 160:1552–1554

    PubMed  Google Scholar 

  • Göbel TW, Chen CH, Cooper MD (1996a) Avian natural killer cells. Curr Top Microbiol Immunol 212:107–117

    Article  PubMed  Google Scholar 

  • Göbel TW, Chen CH, Cooper MD (1996b) Expression of an avian CD6 candidate is restricted to αβ T cells, splenic CD8+ γδ T cells and embryonic natural killer cells. Eur J Immunol 26:1743–1747

    Article  PubMed  Google Scholar 

  • Guselnikov SV, Laktionov PP, Najakshin AM, Baranov KO, Taranin AV (2011) Expansion and diversification of the signaling capabilities of the CD2/SLAM family in Xenopodinae amphibians. Immunogenet 63:679–689

    Article  CAS  Google Scholar 

  • Kageyama R, Cannons JL, Zhao F, Yusuf I, Lao C, Locci M, Schwartzberg PL, Crotty S (2012) The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development. Immunity 36:986–1002

    Article  PubMed  CAS  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305

    Article  PubMed  CAS  Google Scholar 

  • Long EO (1999) Regulation of immune responses through inhibitory receptors. Annu Rev Immunol 17:875–904

    Article  PubMed  CAS  Google Scholar 

  • Neulen ML, Göbel TW (2012) Identification of a chicken CLEC-2 homologue, an activating C-type lectin expressed by thrombocytes. Immunogenet 64:389–397

    Article  CAS  Google Scholar 

  • Nimmerjahn F, Ravetch JV (2008) Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8:34–47

    Article  PubMed  CAS  Google Scholar 

  • Odorizzi PM, Wherry EJ (2012) Inhibitory receptors on lymphocytes: insights from infections. J Immunol 188:2957–2965

    Article  PubMed  CAS  Google Scholar 

  • Ravetch JV, Lanier LL (2000) Immune inhibitory receptors. Science 290:84–89

    Article  PubMed  CAS  Google Scholar 

  • Reth M (1989) Antigen receptor tail clue. Nature 338:383–384

    Article  PubMed  CAS  Google Scholar 

  • Rhee I, Veillette A (2012) Protein tyrosine phosphatases in lymphocyte activation and autoimmunity. Nat Immunol 13:439–447

    Article  PubMed  CAS  Google Scholar 

  • Rogers SL, Viertlboeck BC, Göbel TW, Kaufman J (2008) Avian NK activities, cells and receptors. Semin Immunol 20:353–360

    Article  PubMed  CAS  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95:5857–5864

    Article  PubMed  CAS  Google Scholar 

  • Shlapatska LM, Mikhalap SV, Berdova AG, Zelensky OM, Yun TJ, Nichols KE, Clark EA, Sidorenko SP (2001) CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J Immunol 166:5480–5487

    PubMed  CAS  Google Scholar 

  • Sidorenko SP, Clark EA (2003) The dual-function CD150 receptor subfamily: the viral attraction. Nat Immunol 4:19–24

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Veillette A (2010) SLAM-family receptors: immune regulators with or without SAP-family adaptors. Cold Spring Harb. Perspect Biol 2:1–15

    Google Scholar 

  • Viertlboeck BC, Göbel TW (2007) Chicken thrombocytes express the CD51/CD61 integrin. Vet Immunol Immunopathol 119:137–141

    Article  PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Göbel TW (2011) The chicken leukocyte receptor cluster. Vet Immunol Immunopathol 144:1–10

    Article  PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Crooijmans RP, Groenen MA, Göbel TW (2004) Chicken Ig-like receptor B2, a member of a multigene family, is mainly expressed on B lymphocytes, recruits both Src homology 2 domain containing protein tyrosine phosphatase (SHP)-1 and SHP-2, and inhibits proliferation. J Immunol 173:7385–7393

    PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Habermann FA, Schmitt R, Groenen MA, Du Pasquier L, Göbel TW (2005) The chicken leukocyte receptor complex: a highly diverse multigene family encoding at least six structurally distinct receptor types. J Immunol 175:385–393

    PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Schmitt R, Göbel TW (2006) The chicken immunoregulatory receptor families SIRP, TREM, and CMRF35/CD300L. Immunogenet 58:180–190

    Article  CAS  Google Scholar 

  • Viertlboeck BC, Schweinsberg S, Hanczaruk MA, Schmitt R, Du Pasquier L, Herberg FW, Göbel TW (2007) The chicken leukocyte receptor complex encodes a primordial, activating, high-affinity IgY Fc receptor. Proc Natl Acad Sci U S A 104:11718–11723

    Article  PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Hanczaruk MA, Schmitt FC, Schmitt R, Göbel TW (2008) Characterization of the chicken CD200 receptor family. Mol Immunol 45:2097–2105

    Article  PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Schmitt R, Hanczaruk MA, Crooijmans RP, Groenen MA, Göbel TW (2009) A novel activating chicken IgY FcR is related to leukocyte receptor complex (LRC) genes but is located on a chromosomal region distinct from the LRC and FcR gene clusters. J Immunol 182:1533–1540

    Article  PubMed  CAS  Google Scholar 

  • Zhao F, Cannons JL, Dutta M, Griffiths GM, Schwartzberg PL (2012) Positive and negative signaling through SLAM receptors regulate synapse organization and thresholds of cytolysis. Immunity 36:1003–1016

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Yao S, Chen L (2011) Cell surface signaling molecules in the control of immune responses: a tide model. Immunity 34:466–478

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Deutsche Forschungsgemeinschaft DFG GO489/5-1 grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas W. Göbel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(JPEG 267 kb)

High resolution image file (TIFF 1108 kb)

ESM 2

(DOC 56 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Straub, C., Viertlboeck, B.C. & Göbel, T.W. The chicken SLAM family. Immunogenetics 65, 63–73 (2013). https://doi.org/10.1007/s00251-012-0657-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-012-0657-6

Keywords

Navigation