PARP16/ARTD15 is a novel endoplasmic-reticulum-associated mono-ADP-ribosyltransferase that interacts with, and modifies karyopherin-ß1

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Di Paola, Simone ^a   Micaroni, Massimo ^a,b   Di Tullio, Giuseppe ^a   Buccione, Roberto ^a   Di Girolamo, Maria ^a  

^a Consorzio Mario Negri Sud ^*  (Italy)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN BETA; KARYOPHERIN BETA1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN ARTD15; PROTEIN PARP16; PROTEINASE; UNCLASSIFIED DRUG; ARTD15 PROTEIN, HUMAN;

ARTICLE; CELL LYSATE; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ELECTRON MICROSCOPY; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PROTEASE PROTECTION ASSAY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

ADP RIBOSE TRANSFERASES; BETA KARYOPHERINS; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MASS SPECTROMETRY; MICROSCOPY, ELECTRON; NUCLEAR ENVELOPE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN STRUCTURE, TERTIARY;

EID: 84862233980     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037352     Document Type: Article

References (72)

1. Corda D, Di Girolamo M, (2003) Functional aspects of protein mono-ADP-ribosylation. Embo J 22: 1953 1958.
2. Di Girolamo M, Dani N, Stilla A, Corda D, (2005) Physiological relevance of the endogenous mono(ADP-ribosyl)ation of cellular proteins. Febs J 272: 4565 4575.
3. Seman M, Adriouch S, Haag F, Koch-Nolte F, (2004) Ecto-ADP-ribosyltransferases (ARTs): emerging actors in cell communication and signaling. Curr Med Chem 11: 857 872.
4. Krueger KM, Barbieri JT, (1995) The family of bacterial ADP-ribosylating exotoxins. Clin Microbiol Rev 8: 34 47.
5. Deng Q, Barbieri JT, (2008) Molecular mechanisms of the cytotoxicity of ADP-ribosylating toxins. Annu Rev Microbiol 62: 271 288.
6. Moss J, Zolkiewska A, Okazaki I, (1997) ADP-ribosylarginine hydrolases and ADP-ribosyltransferases. Partners in ADP-ribosylation cycles. Adv Exp Med Biol 419: 25 33.
7. Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F, (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci.
8. Domenighini M, Magagnoli C, Pizza M, Rappuoli R, (1994) Common features of the NAD-binding and catalytic site of ADP- ribosylating toxins. Mol Microbiol 14: 41 50.
9. Glowacki G, Braren R, Firner K, Nissen M, Kuhl M, (2002) The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci 11: 1657 1670.
10. Seman M, Adriouch S, Scheuplein F, Krebs C, Freese D, (2003) NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 19: 571 582.
11. Paone G, Wada A, Stevens LA, Matin A, Hirayama T, (2002) ADP ribosylation of human neutrophil peptide-1 regulates its biological properties. Proc Natl Acad Sci U S A 99: 8231 8235.
12. Zolkiewska A, Moss J, (1993) Integrin alpha 7 as substrate for a glycosylphosphatidylinositol- anchored ADP-ribosyltransferase on the surface of skeletal muscle cells. J Biol Chem 268: 25273 25276.
13. Leno GH, Ledford BE, (1989) ADP-ribosylation of the 78-kDa glucose-regulated protein during nutritional stress. Eur J Biochem 186: 205 211.
14. Lupi R, Corda D, Di Girolamo M, (2000) Endogenous ADP-ribosylation of the G protein beta subunit prevents the inhibition of type 1 adenylyl cyclase. J Biol Chem 275: 9418 9424.
15. Herrero-Yraola A, Bakhit SM, Franke P, Weise C, Schweiger M, (2001) Regulation of glutamate dehydrogenase by reversible ADP-ribosylation in mitochondria. Embo J 20: 2404 2412.
16. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 126: 941 954.
17. Tanner KG, Landry J, Sternglanz R, Denu JM, (2000) Silent information regulator 2 family of NAD- dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc Natl Acad Sci U S A 97: 14178 14182.
18. Frye RA, (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 273: 793 798.
19. Ame JC, Spenlehauer C, de Murcia G, (2004) The PARP superfamily. Bioessays 26: 882 893.
20. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, (2005) In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 6: 139.
21. D'Amours D, Desnoyers S, D'Silva I, Poirier GG, (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342 (Pt 2): 249 268.
22. Schreiber V, Dantzer F, Ame JC, de Murcia G, (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7: 517 528.
23. Hassa PO, Hottiger MO, (2008) The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci 13: 3046 3082.
24. Boehler C, Dantzer F, (2011) PARP-3, a DNA-dependent PARP with emerging roles in double-strand break repair and mitotic progression. Cell Cycle 10: 1023 1024.
25. Chang P, Coughlin M, Mitchison TJ, (2005) Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 7: 1133 1139.
26. Raval-Fernandes S, Kickhoefer VA, Kitchen C, Rome LH, (2005) Increased susceptibility of vault poly(ADP-ribose) polymerase-deficient mice to carcinogen-induced tumorigenesis. Cancer Res 65: 8846 8852.
27. Schreiber V, Ame JC, Dolle P, Schultz I, Rinaldi B, (2002) Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem 277: 23028 23036.
28. Kickhoefer VA, Siva AC, Kedersha NL, Inman EM, Ruland C, (1999) The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol 146: 917 928.
29. Kleine H, Poreba E, Lesniewicz K, Hassa PO, Hottiger MO, (2008) Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol Cell 32: 57 69.
30. Kerns JA, Emerman M, Malik HS, (2008) Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. PLoS Genet 4: e21.
31. Ma Q, Baldwin KT, Renzelli AJ, McDaniel A, Dong L, (2001) TCDD-inducible poly(ADP-ribose) polymerase: a novel response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Biophys Res Commun 289: 499 506.
32. Aguiar RC, Takeyama K, He C, Kreinbrink K, Shipp MA, (2005) B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J Biol Chem 280: 33756 33765.
33. Goenka S, Boothby M, (2006) Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc Natl Acad Sci U S A 103: 4210 4215.
34. Chou HY, Chou HT, Lee SC, (2006) CDK-dependent activation of poly(ADP-ribose) polymerase member 10 (PARP10). J Biol Chem 281: 15201 15207.
35. Yu M, Schreek S, Cerni C, Schamberger C, Lesniewicz K, (2005) PARP-10, a novel Myc-interacting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 24: 1982 1993.
36. Gorlich D, Prehn S, Laskey RA, Hartmann E, (1994) Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79: 767 778.
37. Fried H, Kutay U, (2003) Nucleocytoplasmic transport: taking an inventory. Cell Mol Life Sci 60: 1659 1688.
38. Conti E, Izaurralde E, (2001) Nucleocytoplasmic transport enters the atomic age. Curr Opin Cell Biol 13: 310 319.
39. Cingolani G, Petosa C, Weis K, Muller CW, (1999) Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399: 221 229.
40. Gorlich D, Kostka S, Kraft R, Dingwall C, Laskey RA, (1995) Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr Biol 5: 383 392.
41. Gorlich D, Laskey RA, (1995) Roles of importin in nuclear protein import. Cold Spring Harb Symp Quant Biol 60: 695 699.
42. Nachury MV, Maresca TJ, Salmon WC, Waterman-Storer CM, Heald R, (2001) Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 104: 95 106.
43. Wiese C, Wilde A, Moore MS, Adam SA, Merdes A, (2001) Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 291: 653 656.
44. Merdes A, Ramyar K, Vechio JD, Cleveland DW, (1996) A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87: 447 458.
45. Wittmann T, Wilm M, Karsenti E, Vernos I, (2000) TPX2, A novel xenopus MAP involved in spindle pole organization. J Cell Biol 149: 1405 1418.
46. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ 2nd, et al (1991) SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 266: 19599 19610.
47. Loesberg C, van Rooij H, Smets LA, (1990) Meta-iodobenzylguanidine (MIBG), a novel high-affinity substrate for cholera toxin that interferes with cellular mono(ADP-ribosylation). Biochim Biophys Acta 1037: 92 99.
48. Dani N, Stilla A, Marchegiani A, Tamburro A, Till S, (2009) Combining affinity purification by ADP-ribose-binding macro domains with mass spectrometry to define the mammalian ADP-ribosyl proteome. Proc Natl Acad Sci U S A 106: 4243 4248.
49. Dani N, Mayo E, Stilla A, Marchegiani A, Di Paola S, (2011) Mono-ADP-ribosylation of the G Protein Dimer Is Modulated by Hormones and Inhibited by Arf6. J Biol Chem 286: 5995 6005.
50. Just I, Sehr P, Jung M, van Damme J, Puype M, (1995) ADP-ribosyltransferase type A from turkey erythrocytes modifies actin at Arg-95 and Arg-372. Biochemistry 34: 326 333.
51. Hsia JA, Tsai SC, Adamik R, Yost DA, Hewlett EL, (1985) Amino acid-specific ADP-ribosylation. Sensitivity to hydroxylamine of [cysteine(ADP-ribose)]protein and [arginine(ADP-ribose)]protein linkages. J Biol Chem 260: 16187 16191.
52. Payne DM, Jacobson EL, Moss J, Jacobson MK, (1985) Modification of proteins by mono(ADP-ribosylation) in vivo. Biochemistry 24: 7540 7549.
53. Cervantes-Laurean D, Loflin PT, Minter DE, Jacobson EL, Jacobson MK, (1995) Protein modification by ADP-ribose via acid-labile linkages. J Biol Chem 270: 7929 7936.
54. Panzeter PL, Althaus FR, (1990) High resolution size analysis of ADP-ribose polymers using modified DNA sequencing gels. Nucleic Acids Res 18: 2194.
55. Yates SP, Taylor PL, Jorgensen R, Ferraris D, Zhang J, (2005) Structure-function analysis of water-soluble inhibitors of the catalytic domain of exotoxin A from Pseudomonas aeruginosa. Biochem J 385: 667 675.
56. Hassa PO, Haenni SS, Elser M, Hottiger MO, (2006) Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev 70: 789 829.
57. Leung AK, Vyas S, Rood JE, Bhutkar A, Sharp PA, (2011) Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol Cell 42: 489 499.
58. Kalbfleisch T, Cambon A, Wattenberg BW, (2007) A bioinformatics approach to identifying tail-anchored proteins in the human genome. Traffic 8: 1687 1694.
59. Borgese N, Fasana E, (2011) Targeting pathways of C-tail-anchored proteins. Biochim Biophys Acta 1808: 937 946.
60. Harel A, Forbes DJ, (2004) Importin beta: conducting a much larger cellular symphony. Mol Cell 16: 319 330.
61. Zhong Y, Wang Y, Yang H, Ballar P, Lee JG, (2011) Importin Interacts with the Endoplasmic Reticulum-associated Degradation Machinery and Promotes Ubiquitination and Degradation of Mutant {alpha}1-Antitrypsin. J Biol Chem 286: 33921 33930.
62. Oka S, Kato J, Moss J, (2006) Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J Biol Chem 281: 705 713.
63. Ono T, Kasamatsu A, Oka S, Moss J, (2006) The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases. Proc Natl Acad Sci U S A 103: 16687 16691.
64. Terry LJ, Shows EB, Wente SR, (2007) Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318: 1412 1416.
65. Kanai M, Hanashiro K, Kim SH, Hanai S, Boulares AH, (2007) Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation. Nat Cell Biol 9: 1175 1183.
66. Kozlowski JM, Hart IR, Fidler IJ, Hanna N, (1984) A human melanoma line heterogeneous with respect to metastatic capacity in athymic nude mice. J Natl Cancer Inst 72: 913 917.
67. Stilla A, Di Paola S, Dani N, Krebs C, Arrizza A, (2011) Characterisation of a novel glycosylphosphatidylinositol-anchored mono-ADP-ribosyltransferase isoform in ovary cells. Eur J Cell Biol 90: 665 677.
68. Zhang J, (1997) Use of biotinylated NAD to label and purify ADP-ribosylated proteins. Methods Enzymol 280: 255 265.
69. Malanga M, Althaus FR, (2011) Noncovalent protein interaction with poly(ADP-ribose). Methods Mol Biol 780: 67 82.
70. Piron KJ, McMahon KK, (1990) Localization and partial characterization of ADP-ribosylation products in hearts from adult and neonatal rats. Biochem J 270: 591 597.
71. Polishchuk RS, Mironov AA, (2001) Correlative video light/electron microscopy. Curr Protoc Cell Biol Chapter 4: Unit 4 8.
72. Polishchuk VP, Tyvonchuk TP, Rengevich Ie V, Beketov GV, Budzanivskaia IG, (2000) [Use of atomic force microscopy to study the morphology and structure of viruses]. Mikrobiol Z 62: 40 43.