Molecular and Cellular Biochemistry

, Volume 320, Issue 1–2, pp 93–100 | Cite as

Glycosylphosphatidylinositol-anchored arginine-specific ADP-ribosyltransferase7.1 (Art7.1) on chicken B cells: the possible role of Art7 in B cell receptor signalling and proliferation

  • Masaharu Terashima
  • Mai Takahashi
  • Makoto Shimoyama
  • Yoshinori Tanigawa
  • Takeshi Urano
  • Mikako Tsuchiya


Arginine-specific ADP-ribosyltransferase (Art) catalyzes the mono-ADP-ribosylation, in which it transfers a single ADP-ribose moiety of NAD to the arginine residue(s) of target proteins, and may regulate the function of the proteins or peptides in cellular processes. In vertebrates, Art family is consisted of seven members (Arts1–7), and these Arts are distributed among various tissues except B lymphocytes. Previously, we described molecular cloning, characterization and distribution of glycosylphosphatidylinositol (GPI)-anchored Arts, Art7.1 and Art7.2 (formerly, we referred as cgArt1 and cgArt2, respectively) in chicken tissues (Terashima et al (2005) Biochem J 389:853–861). Here, we demonstrate for the first time that Art7.1 was predominantly expressed on the surface of B cells from the bursa of Fabricius as a GPI-anchored form, as well as on T cells from the thymocytes. Furthermore, we show that the expression of Art7.1 molecules on B cells could modulate the B cell receptor (BCR) signalling and direct the B cell fate to maturation. Thus, our present observation sheds light on the Art molecule expressed on B cells and its possible functional role in BCR signalling.


ADP-ribosyltransferase GPI-anchor B cells NAD DT40 cells 





B cell receptor


Extracellular signal-regulated kinase


Fluorescein isothiocyanate


Fluorescence-activated cell sorter




Hanks’ balanced salt solution


Phosphatidylinositol-specific phospholipase C


Phenylmethylsulfonyl fluoride


Water-soluble tetrazolium salt-1


  1. 1.
    Krueger KM, Barbieri JT (1995) The family of bacterial ADP-ribosylating exotoxins. Clin Microbiol Rev 8:34–47PubMedGoogle Scholar
  2. 2.
    Okazaki IJ, Moss J (1998) Glycosylphosphatidylinositol-anchored and secretory isoforms of mono-ADP-ribosyltransferases. J Biol Chem 273:23617–23620. doi: 10.1074/jbc.273.37.23617 CrossRefPubMedGoogle Scholar
  3. 3.
    Glowacki G, Braren R, Firner K, Nissen M, Kühl M, Reche P et al (2002) The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci 11:1657–1670. doi: 10.1110/ps.0200602 CrossRefPubMedGoogle Scholar
  4. 4.
    Corda D, Di Girolamo M (2003) Functional aspects of protein mono-ADP-ribosylation. EMBO J 22:1953–1958. doi: 10.1093/emboj/cdg209 CrossRefPubMedGoogle Scholar
  5. 5.
    Di Girolamo M, Dani N, Stilla A, Corda D (2005) Physiological relevance of the endogenous mono-ADP-ribosylation of cellular proteins. FEBS J 272:4565–4575. doi: 10.1111/j.1742-4658.2005.04876.x CrossRefPubMedGoogle Scholar
  6. 6.
    Mishima K, Terashima M, Obara S, Yamada K, Imai K, Shimoyama M (1991) Arginine-specific ADP-ribosyltransferase and its acceptor protein p33 in chicken polymorphonuclear cells: co-localization in the cell granules, partial characterization, and in situ mono-ADP-ribosylation. J Biochem 110:388–394PubMedGoogle Scholar
  7. 7.
    Tsuchiya M, Hara N, Yamada K, Osago H, Shimoyama M (1994) Cloning and expression of cDNA for arginine-specific ADP-ribosyltransferase from chicken bone marrow cells. J Biol Chem 269:27451–27457PubMedGoogle Scholar
  8. 8.
    Terashima M, Badruzzaman M, Tsuchiya M, Shimoyama M (1996) Exocytosis of arginine-specific ADP-ribosyltransferase and p33 induced by A23187 and calcium or serum-opsonized zymosan in chicken polymorphonuclear leukocytes. J Biochem 120:1209–1215PubMedGoogle Scholar
  9. 9.
    Davis T, Shall S (1995) Sequence of chicken erythroblast mono-ADP-ribosyltransferase-encoding gene and its upstream region. Gene 164:371–372. doi: 10.1016/0378-1119(95)00504-Y CrossRefPubMedGoogle Scholar
  10. 10.
    Terashima M, Osago H, Hara N, Tanigawa Y, Shimoyama M, Tsuchiya M (2005) Purification, characterization and molecular cloning of glycosylphosphatidylinositol-anchored arginine-specific ADP-ribosyltransferases from chicken. Biochem J 389:853–861. doi: 10.1042/BJ20042019 CrossRefPubMedGoogle Scholar
  11. 11.
    Adriouch S, Ohlrogge W, Haag F, Koch-Nolte F, Seman M (2001) Rapid induction of naive T cell apoptosis by ecto-nicotinamide adenine dinucleotide: requirement for mono-ADP-ribosyltransferase 2 and a downstream effector. J Immunol 167:196–203PubMedGoogle Scholar
  12. 12.
    Liu Z-X, Azhipa O, Okamoto S, Govindarajan S, Dennert G (2001) Extracellular nicotinamide adenine dinucleotide induces T cell apoptosis in vivo and in vitro. J Immunol 167:4942–4947PubMedGoogle Scholar
  13. 13.
    Okazaki IJ, Kim H-J, McElvaney G, Lesma E, Moss J (1996) Molecular characterization of a glycosylphosphatidylinositol-linked ADP-ribosyltransferase from lymphocytes. Blood 88:915–921PubMedGoogle Scholar
  14. 14.
    Wang J, Nemoto E, Kots AY, Kaslow HR, Dennert G (1994) Regulation of cytotoxic T cells by ecto-nicotinamide adenine dinucleotide (NAD) correlates with cell surface GPI-anchored/arginine ADP-ribosyltransferase. J Immunol 153:4048–4058PubMedGoogle Scholar
  15. 15.
    Okamoto S, Azhipa O, Yu Y, Russo E, Dennert G (1998) Expression of ADP-ribosyltransferase on normal T lymphocytes and effects of nicotinamide adenine dinucleotide on their function. J Immunol 160:4190–4198PubMedGoogle Scholar
  16. 16.
    Donnelly LE, Rendell NB, Murray S, Allport JR, Lo G, Kefalas P et al (1996) Arginine-specific mono-ADP-ribosyltransferase activity on the surface of human polymorphonuclear neutrophil leukocytes. Biochem J 315:635–641PubMedGoogle Scholar
  17. 17.
    Grahnert A, Friedrich M, Pfister M, Haag F, Koch-Nolte F, Hauschildt S (2002) Mono-ADP-ribosyltransferases in human monocytes: regulation by lipopolysaccharide. Biochem J 362:717–723. doi: 10.1042/0264-6021:3620717 CrossRefPubMedGoogle Scholar
  18. 18.
    Arai S, Itoh H, Kanda S, Endoh D, Hayashi M (2000) Effects of antioxidant on induction of apoptosis in bursal cells of Fabricius during in vitro cultivation. J Vet Med Sci 62:43–47. doi: 10.1292/jvms.62.43 CrossRefPubMedGoogle Scholar
  19. 19.
    Peters MA, Browning GF, Washington EA, Crabb BS, Kaiser P (2003) Embryonic age influences the capacity for cytokine induction in chicken thymocytes. Immunology 110:358–367. doi: 10.1046/j.1365-2567.2003.01744.x CrossRefPubMedGoogle Scholar
  20. 20.
    Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K (1996) A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol Pharm Bull 19:1518–1520PubMedGoogle Scholar
  21. 21.
    Kamiya Y, Ohta K, Kaneko Y (2005) Lidocaine-induced apoptosis and necrosis in U937 cells depending on its dosage. Biomed Res 26:231–239. doi: 10.2220/biomedres.26.231 CrossRefPubMedGoogle Scholar
  22. 22.
    Gauld SB, Dal Porto JM, Cambier JC (2002) B cell antigen receptor signalling: roles in cell development and disease. Science 296:1641–1642. doi: 10.1126/science.1071546 CrossRefPubMedGoogle Scholar
  23. 23.
    Harnett MM, Katz E, Ford CA (2005) Differential signalling during B-cell maturation. Immunol Lett 98:33–44. doi: 10.1016/j.imlet.2004.11.002 CrossRefPubMedGoogle Scholar
  24. 24.
    Koncz G, Bodor C, Kövesdi D, Gáti R, Sármay G (2002) BCR mediated signal transduction in immature and mature B cells. Immunol Lett 82:41–49. doi: 10.1016/S0165-2478(02)00017-2 CrossRefPubMedGoogle Scholar
  25. 25.
    Winding P, Berchtold MW (2001) The chicken B cell line DT40: a novel tool for gene disruption experiments. J Immunol Methods 249:1–16. doi: 10.1016/S0022-1759(00)00333-1 CrossRefPubMedGoogle Scholar
  26. 26.
    Koskela K, Kohonen P, Nieminen P, Buerstedde J-M, Lassila O (2003) Insight into lymphoid development by gene expression profiling of avian B cells. Immunogenetics 55:412–422. doi: 10.1007/s00251-003-0592-7 CrossRefPubMedGoogle Scholar
  27. 27.
    Chiu D, Ma K, Scott A, Duronio V (2005) Acute activation of Erk1/Erk2 and protein kinase B/akt proceed by independent pathways in multiple cell types. FEBS J 272:4372–4384. doi: 10.1111/j.1742-4658.2005.04850.x CrossRefPubMedGoogle Scholar
  28. 28.
    Jacob A, Cooney D, Pradhan M, Coggeshall KM (2002) Convergence of signalling pathway on the activation of ERK in B cells. J Biol Chem 277:23420–23426. doi: 10.1074/jbc.M202485200 CrossRefPubMedGoogle Scholar
  29. 29.
    Terashima M, Yamamori C, Shimoyama M, Tsuchiya M (1998) Suppression of cell adhesion and spreading activities of fibronectin by arginine-specific ADP-ribosyltransferase from chicken polymorphonuclear leukocytes. Biochim Biophys Acta 1404:299–304. doi: 10.1016/S0167-4889(98)00067-6 CrossRefPubMedGoogle Scholar
  30. 30.
    Terashima M, Hara N, Badruzzaman M, Shimoyama M, Tsuchiya M (1997) ADP-ribosylation of tuftsin suppresses its receptor-binding capacity and phagocytosis-stimulating activity to murine peritoneal macrophages. FEBS Lett 412:227–232. doi: 10.1016/S0014-5793(97)00784-9 CrossRefPubMedGoogle Scholar
  31. 31.
    Takata M, Homma Y, Kurosaki T (1995) Requirement of phospholipase C-γ2 activation in surface immunoglobulin M-induced B cell apoptosis. J Exp Med 182:907–914. doi: 10.1084/jem.182.4.907 CrossRefPubMedGoogle Scholar
  32. 32.
    Fearon DT, Carroll MC (2000) Regulation of B lymphocyte responses to foreign and self-antigens by the CD19/CD21 complex. Annu Rev Immunol 18:393–422. doi: 10.1146/annurev.immunol.18.1.393 CrossRefPubMedGoogle Scholar
  33. 33.
    Li X, Carter RH (1998) Convergence of CD19 and B cell antigen receptor signals at MEK1 in the ERK2 activation cascade. J Immunol 161:5901–5908PubMedGoogle Scholar
  34. 34.
    Bruzzone S, Moreschi I, Guida L, Usai C, Zocchi E, De Flora A (2006) Extracellular NAD+ regulates intracellular calcium levels and induces activation of human granulocytes. Biochem J 393:697–704. doi: 10.1042/BJ20051302 CrossRefPubMedGoogle Scholar
  35. 35.
    Gerth A, Nieber K, Oppenheimer NJ, Hauschildt S (2004) Extracellular NAD+ regulates intracellular free calcium concentration in human monocytes. Biochem J 382:849–856. doi: 10.1042/BJ20040979 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2008

Authors and Affiliations

  • Masaharu Terashima
    • 1
  • Mai Takahashi
    • 1
  • Makoto Shimoyama
    • 1
  • Yoshinori Tanigawa
    • 1
  • Takeshi Urano
    • 1
  • Mikako Tsuchiya
    • 1
  1. 1.Department of BiochemistryShimane University Faculty of MedicineIzumoJapan

Personalised recommendations