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For whom the bell tolls? DING proteins in health and disease

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Abstract

DING proteins, identified mainly by their eponymous N-terminal sequences, are ubiquitous in living organisms. Amongst bacteria, they are common in pseudomonads, and have been characterised with respect to genetics and structure. They form part of a wider family of phosphate-binding proteins, with emerging roles in phosphate acquisition and pathogenicity. Many DING proteins have been isolated in eukaryotes, in which they have been associated with very diverse biological activities, often in the context of possible signalling roles. Disease states in which DING proteins have been implicated include rheumatoid arthritis, lithiasis, atherosclerosis, some tumours and tumour-associated cachexia, and bacterial and viral adherence. Complete genetic and structural characterisation of eukaryotic DING genes and proteins is still lacking, though the phosphate-binding site seems to be conserved. Whether as bacterial proteins related to bacterial pathogenicity, or as eukaryotic components of biochemical signalling systems, DING proteins require further study.

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References

  1. Berna A, Bernier F, Scott K, Stuhlmuller B (2002) Ring up the curtain on DING proteins. FEBS Lett 524:6–10

    Article  PubMed  CAS  Google Scholar 

  2. Berna A, Bernier F, Chabrière E, Perera T, Scott K (2008) DING proteins; novel members of a prokaryotic phosphate-binding protein superfamily which extends into the eukaryotic kingdom. Int J Biochem Cell Biol 40:170–175

    Article  PubMed  CAS  Google Scholar 

  3. Zhang XX, Scott K, Meffin R, Rainey PB (2007) Genetic characterization of psp encoding the DING protein in Pseudomonas fluorescens SBW25. BMC Microbiol 7:114

    Article  PubMed  CAS  Google Scholar 

  4. Scott K, Wu L (2005) Functional properties of a recombinant bacterial DING protein: comparison with a homologous human protein. Biochim Biophys Acta 1744:234–244

    Article  PubMed  CAS  Google Scholar 

  5. Ahn S, Moniot S, Elias M, Chabrière E, Kim D, Scott K (2007) Structure–function relationships in a bacterial DING protein. FEBS Lett 581:3455–3460

    Article  PubMed  CAS  Google Scholar 

  6. Boos W, Lucht JM (1996) Periplasmic binding protein-dependent ABC transporters. In: Neidhart FC, Curtiss R, Ingraham JL, Lin ECC, Low KB, Magasanik B (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 2nd edn. American Society for Microbiology, Washington, pp 1175–1209

    Google Scholar 

  7. Luecke H, Quiocho FA (1990) High specificity of a phosphate transport protein determined by hydrogen bonds. Nature 347:402–406

    Article  PubMed  CAS  Google Scholar 

  8. Tan AS, Worobec EA (1993) Isolation and characterization of two immunochemically distinct alkaline phosphatases from Pseudomonas aeruginosa. FEMS Microbiol Lett 106:281–286

    Article  PubMed  CAS  Google Scholar 

  9. Ball G, Durand E, Lazdunski A, Filloux A (2002) A novel type II secretion system in Pseudomonas aeruginosa. Mol Microbiol 43:475–485

    Article  PubMed  CAS  Google Scholar 

  10. Jones HE, Holland IB, Campbell AK (2002) Direct measurement of free Ca(2+) shows different regulation of Ca(2+) between the periplasm and the cytosol of Escherichia coli. Cell Calcium 32:183–192

    Article  PubMed  CAS  Google Scholar 

  11. Zaborina O, Holbrook C, Chen Y, Long J, Zaborin A, Morozova I, Fernandez H, Wang Y, Turner JR, Alverdy JC (2008) Structure–function aspects of PstS in multi-drug-resistant Pseudomonas aeruginosa. PLoS Pathog 4:e43

    Article  PubMed  CAS  Google Scholar 

  12. Mattick JS, Whitchurch CB, Alm RA (1996) The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa—a review. Gene 179:147–155

    Article  PubMed  Google Scholar 

  13. Vallet I, Diggle SP, Stacey RP, Camara M, Ventre I, Lory S, Lazdunski A, Williams P, Filloux A (2004) Biofilm formation in Pseudomonas aeruginosa: fimbrial cup gene clusters are controlled by the transcriptional regulator MvaT. J Bacteriol 186:2880–2890

    Article  PubMed  CAS  Google Scholar 

  14. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131–147

    Article  PubMed  CAS  Google Scholar 

  15. Frisk A, Schurr JR, Wang G, Bertucci DC, Marrero L, Hwang SH, Hassett DJ, Schurr MJ (2004) Transcriptome analysis of Pseudomonas aeruginosa after interaction with human airway epithelial cells. Infect Immun 72:5433–5438

    Article  PubMed  CAS  Google Scholar 

  16. Kim D (2007) Microbial and eukaryotic origins of DING proteins. MSc thesis. University of Auckland

  17. Pantazaki AA, Tsolkas GP, Kyriakidis DA (2008) A DING phosphatase in Thermus thermophilus. Amino Acids 34:437–448

    Article  PubMed  CAS  Google Scholar 

  18. Henne A, Brüggemann H, Raasch C, Wiezer A, Hartsch T, Liesegang H, Johann A, Lienard T, Gohl O, Martinez-Arias R, Jacobi C, Starkuviene V, Schlenczeck S, Dencker S, Huber R, Klenk HP, Kramer W, Merkl R, Gottschalk G, Fritz HJ (2004) The genome sequence of the extreme thermophile Thermus thermophilus. Nat Biotechnol 22:547–553

    Article  PubMed  CAS  Google Scholar 

  19. Takayama G, Kosuge T, Maseda H, Nakamura A, Hoshino T (2004) Nucleotide sequence of the cryptic plasmid pTT8 from Thermus thermophilus HB8 and isolation and characterization of its high-copy-number mutant. Plasmid 51:227–237

    Article  PubMed  CAS  Google Scholar 

  20. Di Maro A, De Maio A, Castellano S, Parente A, Farina B, Faraone-Mennella MR (2008) The ADP-ribosylating thermozyme from Sulfolobus solfataricus is a DING protein. Biol Chem: S1431–S6730 [epub ahead of print]

  21. Moniot S, Elias M, Kim D, Scott K, Chabrière E (2007) Crystallization, diffraction data collection and preliminary crystallographic analysis of DING protein from Pseudomonas fluorescens. Acta Cryst F 63:590–592

    Article  CAS  Google Scholar 

  22. Morales R, Berna A, Carpentier P, Contreras-Martel C, Renault F, Nicodeme M, Chesne-Seck M-L, Bernier F, Dupuy J, Schaeffer C, Diemer H, Van-Dorsselaer A, Fontecilla-Camps JC, Masson P, Rochu P, Chabrière E (2006) Serendipitous discovery and X-ray structure of a human phosphate binding apolipoprotein. Structure 14:601–609

    Article  PubMed  CAS  Google Scholar 

  23. Diemer H, Elias M, Renault F, Rochu D, Contreras-Martel C, Schaeffer C, Van Dorsselaer A, Chabrière E (2008) Tandem use of X-ray crystallography and mass spectrometry to obtain ab initio the complete and exact amino acids sequence of HPBP, a human 38-kDa apolipoprotein. Proteins 71:1708–1720

    Article  PubMed  CAS  Google Scholar 

  24. Morales R, Berna A, Carpentier P, Contreras-Martel C, Renault F, Nicodeme M, Chesne-Seck ML, Bernier F, Dupuy J, Schaeffer C, Chabrière E (2007) Discovery and crystallographic structure of human apolipoprotein. Annal Pharma Franc 65:98–107

    CAS  Google Scholar 

  25. Felder CB, Graul RC, Lee AY, Merkle HP, Sadee W (1999) The Venus flytrap of periplasmic binding proteins: an ancient protein module present in multiple drug receptors. AAPS PharmSci 1:E2

    Article  PubMed  CAS  Google Scholar 

  26. Tam R, Saier MH (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57:320–346

    PubMed  CAS  Google Scholar 

  27. Wang Z, Luecke H, Yao N, Quiocho FA (1997) A low energy short hydrogen bond in very high resolution structures of protein receptor–phosphate complexes. Nat Struct Biol 4:519–522

    Article  PubMed  CAS  Google Scholar 

  28. Poole K, Hancock RE (1984) Phosphate transport in Pseudomonas aeruginosa. Involvement of a periplasmic phosphate-binding protein. Eur J Biochem 144:607–612

    Article  PubMed  CAS  Google Scholar 

  29. Renault F, Chabrière E, Andrieu JP, Dublet B, Masson P, Rochu D (2006) Tandem purification of two HDL-associated partner proteins in human plasma, paraoxonase (PON1) and phosphate binding protein (HPBP) using hydroxyapatite chromatography. J Chromatogr B 836:15–21

    Article  CAS  Google Scholar 

  30. Rochu D, Chabrière E, Elias M, Renault F, Clery-Barraud C, Masson P (2007) Stabilisation of active form of natural human PON1 requires HPBP. In: Mackness B, Mackness M, Aviram M, Paragh G (eds) The Paraoxonases: their role in disease development and xenobiotic metabolism. Springer, The Netherlands, pp 171–183

    Google Scholar 

  31. Rochu D, Chabrière E, Renault F, Elias M, Clery-Barraud C, Masson P (2007) Stabilization of the active form(s) of human paraoxonase by human phosphate-binding protein. Biochem Soc Trans 35:1616–1620

    Article  PubMed  CAS  Google Scholar 

  32. Rochu D, Renault F, Clery-Barraud C, Chabrière E, Masson P (2007) Stability of highly purified human paraoxonase (PON1): association with human phosphate binding protein (HPBP) is essential for preserving its active conformation(s). Biochim Biophys Acta 1774:874–883

    PubMed  CAS  Google Scholar 

  33. Rochu D, Renault F, Elias M, Hanne S, Cléry-Barraud C, Chabrière E, Masson P (2007) Functional states, storage and thermal stability of human paraoxonase: drawbacks, advantages and potential. Toxicology 233:226

    Article  CAS  Google Scholar 

  34. Wang Z, Choudhary A, Ledvina PS, Quiocho FA (1994) Fine tuning the specificity of the periplasmic phosphate transport receptor. Site-directed mutagenesis, ligand binding, and crystallographic studies. J Biol Chem 269:25091–25094

    PubMed  CAS  Google Scholar 

  35. Yao N, Ledvina PS, Choudhary A, Quiocho FA (1996) Modulation of a salt link does not affect binding of phosphate to its specific active transport receptor. Biochemistry 35:2079–2085

    Article  PubMed  CAS  Google Scholar 

  36. Darbinian-Sarkissian N, Darbinyan A, Otte J, Radhakrishnan S, Sawaya BE, Arzumanyan A, Chipitsyna G, Popov Y, Rappaport J, Amini S, Khalili K (2006) p27SJ, a novel protein in St John’s Wort, that suppresses expression of HIV-1 genome. Nat Gene Ther 13:288–295

    CAS  Google Scholar 

  37. Sebastian T, Johnson PF (2006) Stop and go: anti-proliferative and mitogenic functions of the transcription factor C/EBPbeta. Cell Cycle 5:953–957

    PubMed  CAS  Google Scholar 

  38. Weebadda WK, Hoover GJ, Hunter DB, Hayes MA (2001) Avian air sac and plasma proteins that bind surface polysaccharides of Escherichia coli O2. Comp Biochem Physiol B 130:299–312

    Article  PubMed  CAS  Google Scholar 

  39. Todorov PT, Wyke SM, Tisdale MJ (2007) Identification and characterization of a membrane receptor for proteolysis-inducing factor on skeletal muscle. Cancer Res 67:11419–11427

    Article  PubMed  CAS  Google Scholar 

  40. Belenky M, Prasain J, Kim H, Barnes S (2003) DING, a genistein target in human breast cancer: a protein without a gene. J Nutr 133:2497S–2501S

    PubMed  CAS  Google Scholar 

  41. Riah O, Dousset JC, Bofill-Cardona E, Courriere P (2000) Isolation and microsequencing of a novel cotinine receptor. Cell Mol Neurobiol 20:653–664

    Article  PubMed  CAS  Google Scholar 

  42. Kumar V, Yu S, Farell G, Toback FG, Lieske JC (2004) Renal epithelial cells constitutively produce a protein that blocks adhesion of crystals to their surface. Am J Physiol Renal Physiol 287:F373–F383

    Article  PubMed  CAS  Google Scholar 

  43. Chen Z, Franco CF, Baptista RP, Cabral JM, Coelho AV, Rodrigues CJ, Melo EP (2007) Purification and identification of cutinases from Colletotrichum kahawae and Colletotrichum gloeosporioides. Appl Microbiol Biotechnol 73:1306–1313

    Article  PubMed  CAS  Google Scholar 

  44. Bush D, Fritz H, Knight C, Mount J, Scott K (1998) A hirudin-sensitive, growth-related proteinase from human fibroblasts. Biol Chem 379:225–229

    Article  PubMed  CAS  Google Scholar 

  45. Lee DM, Weinblatt ME (2001) Rheumatoid arthritis. Lancet 358:903–911

    Article  PubMed  CAS  Google Scholar 

  46. Steiner G, Smolen J (2002) Autoantibodies in rheumatoid arthritis and their clinical significance. Arthritis Res 4(Suppl 2):S1–S5

    Article  PubMed  Google Scholar 

  47. Hain NA, Stuhlmuller B, Hahn GR, Kalden JR, Deutzmann R, Burmester GR (1996) Biochemical characterization and microsequencing of a 205-kDa synovial protein stimulatory for T cells and reactive with rheumatoid factor containing sera. J Immunol 157:1773–1780

    PubMed  CAS  Google Scholar 

  48. Blass S, Schumann F, Hain NA, Engel JM, Stuhlmuller B, Burmester GR (1999) p205 is a major target of autoreactive T cells in rheumatoid arthritis. Arthritis Rheum 42:971–980

    Article  PubMed  CAS  Google Scholar 

  49. Adams L, Davey S, Scott K (2002) The DING protein: an autocrine growth-stimulatory protein related to the human synovial stimulatory protein. Biochim Biophys Acta 1586:254–264

    PubMed  CAS  Google Scholar 

  50. Ross R (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362:801–809

    Article  PubMed  CAS  Google Scholar 

  51. Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. New Engl J Med 352:1685–1695

    Article  PubMed  CAS  Google Scholar 

  52. Mackness M, Mackness B (2004) Paraoxonase 1 and atherosclerosis: is the gene or the protein more important? Free Radic Biol Med 37:1317–1323

    Article  PubMed  CAS  Google Scholar 

  53. Shih DM, Gu L, Xia Y-R, Navab M, Li W-F, Hama S, Castellani LW, Furlong CE, Costa LG, Fogelman AM, Lusis AJ (1998) Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394:284–287

    Article  PubMed  CAS  Google Scholar 

  54. Aviram M, Rosenblat M (2004) Paraoxonases 1, 2, and 3, oxidative stress, and macrophage foam cell formation during atherosclerosis development. Free Radic Biol Med 37:1304–1316

    Article  PubMed  CAS  Google Scholar 

  55. Lamartiniere CA, Moore JB, Brown NM, Thompson R, Hardin MJ, Barnes S (1995) Genistein suppresses mammary cancer in rats. Carcinogenesis 16:2833–2840

    Article  PubMed  CAS  Google Scholar 

  56. Murrill WB, Brown NM, Zhang JX, Manzolillo PA, Barnes S, Lamartiniere CA (1996) Prepubertal genistein exposure suppresses mammary cancer and enhances gland differentiation in rats. Carcinogenesis 17:1451–1457

    Article  PubMed  CAS  Google Scholar 

  57. Naciff JM, Jump ML, Torontali SM, Carr GJ, Tiesman JP, Overmann GJ, Daston GP (2002) Gene expression profile induced by 17alpha-ethynyl estradiol, bisphenol A, and genistein in the developing female reproductive system of the rat. Toxicol Sci 68:184–199

    Article  PubMed  CAS  Google Scholar 

  58. Coe FL, Evan A, Worcester E (2005) Kidney stone disease. J Clin Invest 115:2598–2608

    Article  PubMed  CAS  Google Scholar 

  59. Gambaro G, Reis-Santos JM, Rao N (2004) Nephrolithiasis: why doesn’t our “learning” progress? Eur Urol 45:547–556

    Article  PubMed  Google Scholar 

  60. Argiles JM, Alvarez B, Lopez-Soriano FJ (1997) The metabolic basis of cancer cachexia. Med Res Rev 17:477–498

    Article  PubMed  CAS  Google Scholar 

  61. Tisdale MJ (2002) Cachexia in cancer patients. Nat Rev Cancer 2:862–871

    Article  PubMed  CAS  Google Scholar 

  62. Todorov P, Cariuk P, McDevitt T, Coles B, Fearon K, Tisdale M (1996) Characterization of a cancer cachectic factor. Nature 379:739–742

    Article  PubMed  CAS  Google Scholar 

  63. Lorite MJ, Smith HJ, Arnold JA, Morris A, Thompson MG, Tisdale MJ (2001) Activation of ATP-ubiquitin-dependent proteolysis in skeletal muscle in vivo and murine myoblasts in vitro by a proteolysis-inducing factor (PIF). Br J Cancer 85:297–302

    Article  PubMed  CAS  Google Scholar 

  64. Watchorn TM, Waddell I, Dowidar N, Ross JA (2001) Proteolysis-inducing factor regulates hepatic gene expression via the transcription factors NF-(kappa)B and STAT3. FASEB J 15:562–564

    PubMed  CAS  Google Scholar 

  65. Stewart GD, Skipworth RJ, Ross JA, Fearon K, Baracos VE (2008) The dermcidin gene in cancer: role in cachexia, carcinogenesis and tumour cell survival. Curr Opin Clin Nutr Metabol Care 11:208–213

    Article  CAS  Google Scholar 

  66. Mehta A, Lu X, Block T, Willis A, Dwek R, Tennant B, Blumberg B (2001) Synovial stimulatory protein fragments copurify with woodchuck hepatitis virus: implications for the etiology of arthritis in chronic hepatitis B virus infection. Arthritis Rheum 44:486–487

    Article  PubMed  CAS  Google Scholar 

  67. Snell T (1998) Chemical ecology of rotifers. Hydrobiology 387–388:267–276

    Article  Google Scholar 

  68. Snell T, Kubanek J, Carter W, Payne A, Kim J, Hicks M, Stelzer CP (2006) A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Mar Biol 149:763–773

    Article  CAS  Google Scholar 

  69. Khan SA, Khan SJ, Dorrington JH (1992) Interleukin-1 stimulates deoxyribonucleic acid synthesis in immature rat Leydig cells in vitro. Endocrinology 131:1853–1857

    Article  PubMed  CAS  Google Scholar 

  70. Hagiwara A, Hamada K, Hori S, Hirayama K (1994) Increased sexual reproduction in Brachionus plicatilis (Rotifera) with the addition of bacteria and rotifer extracts J. Exp Mar Biol Ecol 181:1–8

    Article  Google Scholar 

  71. Robertson D, Mitchell GP, Gilroy JS, Gerrish C, Bolwell GP, Slabas AR (1997) Differential extraction and protein sequencing reveals major differences in patterns of primary cell wall proteins from plants. J Biol Chem 272:15841–15848

    Article  PubMed  CAS  Google Scholar 

  72. Perera T, Berna A, Scott K, Lemaitre-Guillier C, Bernier F (2008) Proteins related to St. John’s Wort p27SJ, a suppressor of HIV-1 expression, are ubiquitous in plants. Phytochemistry 69:865–872

    Article  PubMed  CAS  Google Scholar 

  73. Bernier F, Berna A (2001) Germins and germin-like proteins: plant do-all proteins. But what do they do exactly? Plant Physiol Biochem 39:545–554

    Article  CAS  Google Scholar 

  74. Griffaut B, Debiton E, Madelmont JC, Maurizis JC, Ledoigt G (2007) Stressed Jerusalem artichoke tubers (Helianthus tuberosus L.) excrete a protein fraction with specific cytotoxicity on plant and animal tumour cell. Biochim Biophys Acta 1770:1324–1330

    PubMed  CAS  Google Scholar 

  75. Boonmee A, Reynolds CD, Sangvanich P (2007) Alpha-glucosidase inhibitor proteins from Sesbania grandiflora flowers. Planta Med 73:1197–1201

    Article  PubMed  CAS  Google Scholar 

  76. Khalili K, Sarkissian ND (2003) Antiproliferative protein from Hypericum perforatum and nucleic acids encoding the same. US Patent 60/376,996

  77. Darbinian N, Popov Y, Khalili K, Amini S (2008) Creation of a bi-directional protein transduction system for suppression of HIV-1 expression by p27SJ. Antiviral Res 79:136–141

    Article  PubMed  CAS  Google Scholar 

  78. Homma J, Yamanaka R, Yajima N, Tsuchiya N, Genkai N, Sano M, Tanaka R (2006) Increased expression of CCAAT/enhancer binding protein beta correlates with prognosis in glioma patients. Oncol Rep 15:595–601

    PubMed  CAS  Google Scholar 

  79. Henderson AJ, Calame KL (1997) CCAAT/enhancer binding protein (C/EBP) sites are required for HIV-1 replication in primary macrophages but not CD4(+) T cells. Proc Natl Acad Sci USA 94:8714–8719

    Article  PubMed  CAS  Google Scholar 

  80. Berger EA, Murphy PM, Farber JM (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17:657–700

    Article  PubMed  CAS  Google Scholar 

  81. Mehta A, Zitzmann N, Rudd PM, Block TM, Dwek RA (1998) Alpha-glucosidase inhibitors as potential broad based anti-viral agents. FEBS Lett 430:17–22

    Article  PubMed  CAS  Google Scholar 

  82. Paulovicova E, Bystricky S, Machova E, Bujdakova H (2008) Immune responsiveness of a novel peptidoglycan conjugate prepared from surface Candida immunogens: mannan and CR3-related peptide. FEMS Lett 53:421–428

    CAS  Google Scholar 

  83. Du M, Zhao L, Li C, Zhao G, Hu X (2007) Purification and characterization of a novel fungi Se-containing protein from Se-enriched Ganoderma lucidum mushroom and its Se-dependent radical scavenging activity. Eur Food Res Technol 224:659–665

    Article  CAS  Google Scholar 

  84. Lewis AP, Crowther D (2005) DING proteins are from Pseudomonas. FEMS Microbiol Lett 252:215–222

    Article  PubMed  CAS  Google Scholar 

  85. Smith CD, Shu S, Mungall CJ, Karpen GH (2007) The release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316:1586–1591

    Article  PubMed  CAS  Google Scholar 

  86. Colgrove R, Japour A (1999) A combinatorial ledge: reverse transcriptase fidelity, total body viral burden, and the implications of multiple-drug HIV therapy for the evolution of antiviral resistance. Antiviral Res 41:45–56

    Article  PubMed  CAS  Google Scholar 

  87. Kim H, Peterson TG, Barnes S (1998) Mechanisms of action of the soy isoflavone genistein: emerging role for its effects via transforming growth factor beta signaling pathways. Am J Clin Nutr 68:1418S–1425S

    PubMed  CAS  Google Scholar 

  88. Scott K (2002) Is hirudin a potential therapeutic agent for arthritis? Ann Rheum Dis 61:561–562

    Article  PubMed  CAS  Google Scholar 

  89. Topol EJ (1996) A comparison of recombinant hirudin with heparin for the treatment of acute coronary syndromes. The Global Use of Strategies to Open Occluded Coronary Arteries (GUSTO) IIb Investigators. New Engl J Med 335:775–782

    Article  Google Scholar 

  90. Marty I, Peclat V, Kirdaite G, Salvi R, So A, Busso N (2001) Amelioration of collagen-induced arthritis by thrombin inhibition. J Clin Invest 107:631–640

    Article  PubMed  CAS  Google Scholar 

  91. Berna A, Scott K, Chabrière E, Bernier F (2009) The DING family of proteins: ubiquitous in eukaryotes, but where are the genes? Bioessays 31 (in press), due for publication May 09

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  1. Institut de Biologie Moléculaire des Plantes du CNRS, Institut de Botanique, Université de Strasbourg, 28 rue Goethe, 67083, Strasbourg Cedex, France

    Anne Berna & François Bernier

  2. Architecture et Fonction des Macromolécules Biologiques, CNRS, Université de la Méditerranée, 13288, Marseille, France

    Eric Chabrière & Mikael Elias

  3. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    Ken Scott & Andrew Suh

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  1. Anne Berna
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Correspondence to Ken Scott.

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Berna, A., Bernier, F., Chabrière, E. et al. For whom the bell tolls? DING proteins in health and disease. Cell. Mol. Life Sci. 66, 2205–2218 (2009). https://doi.org/10.1007/s00018-009-0006-6

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