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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

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Abstract

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.

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Abbreviations

Art:

ADP-ribosyltransferase

BCR:

B cell receptor

ERK:

Extracellular signal-regulated kinase

FITC:

Fluorescein isothiocyanate

FACS:

Fluorescence-activated cell sorter

GPI:

Glycosylphosphatidylinositol

HBSS:

Hanks’ balanced salt solution

PI-PLC:

Phosphatidylinositol-specific phospholipase C

PMSF:

Phenylmethylsulfonyl fluoride

WST-1:

Water-soluble tetrazolium salt-1

References

  1. Krueger KM, Barbieri JT (1995) The family of bacterial ADP-ribosylating exotoxins. Clin Microbiol Rev 8:34–47

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  4. Corda D, Di Girolamo M (2003) Functional aspects of protein mono-ADP-ribosylation. EMBO J 22:1953–1958. doi:10.1093/emboj/cdg209

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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 110:388–394

    CAS  PubMed  Google Scholar 

  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 269:27451–27457

    CAS  PubMed  Google Scholar 

  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 120:1209–1215

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 167:196–203

    CAS  PubMed  Google Scholar 

  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 167:4942–4947

    CAS  PubMed  Google Scholar 

  13. Okazaki IJ, Kim H-J, McElvaney G, Lesma E, Moss J (1996) Molecular characterization of a glycosylphosphatidylinositol-linked ADP-ribosyltransferase from lymphocytes. Blood 88:915–921

    CAS  PubMed  Google Scholar 

  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 153:4048–4058

    CAS  PubMed  Google Scholar 

  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 160:4190–4198

    CAS  PubMed  Google Scholar 

  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 315:635–641

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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 19:1518–1520

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  33. Li X, Carter RH (1998) Convergence of CD19 and B cell antigen receptor signals at MEK1 in the ERK2 activation cascade. J Immunol 161:5901–5908

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, Shimane University Faculty of Medicine, Izumo, 693-8501, Japan

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

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  1. Masaharu Terashima
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  2. Mai Takahashi
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  3. Makoto Shimoyama
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  4. Yoshinori Tanigawa
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Correspondence to Masaharu Terashima.

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Terashima, M., Takahashi, M., Shimoyama, M. et al. 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. Mol Cell Biochem 320, 93–100 (2009). https://doi.org/10.1007/s11010-008-9902-6

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