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The Tripartite Motif

Structure and Function
  • Lucia Micale
  • Evelyne Chaignat
  • Carmela Fusco
  • Alexandre Reymond
  • Giuseppe Merla
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 770)

Abstract

The TRIM/RBCC proteins belong to a family whom members are involved in a variety of cellular processes such as apoptosis and cell cycle regulation. These proteins are defined by the presence of a tripartite motif composed of three zinc-binding domains, a RING finger, one or two B-box motifs, a coiled-coil region and a highly variable C-terminal region. Interestingly, the preserved order of the tripartite motif from the N-to the C-terminal end of the protein and the highly conserved overall architecture of this motif throughout evolution suggest that common biochemical functions may underline their assorted cellular roles.

Here we present the structure and the proposed function of each TRIM domain including the highly variable C-terminal domain.

Keywords

Familial Mediterranean Fever Ring Finger Ring Domain High Molecular Weight Complex Spry Domain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Cao T, Borden KL, Freemont PS et al. Involvement of the rfp tripartite motif in protein-protein interactions and subcellular distribution. J Cell Sci 1997; 110(Pt 14): 1563–1571.PubMedGoogle Scholar
  2. 2.
    Peng H, Feldman I, Rauscher FJ et al. Hetero-oligomerization among the TIF family of RBCC/TRIM domain-containingnuclear cofactors: a potentialmechanism for regulating the switch between coactivation and corepression. J Mol Biol 2002; 320(3):629–644.PubMedCrossRefGoogle Scholar
  3. 3.
    Short KM, Cox TC. Subclassification of the RBCC/TRIM superfamily reveals a novel motif necessary for microtubule binding. J Biol Chem 2006; 281(13):8970–8980.PubMedCrossRefGoogle Scholar
  4. 4.
    Slack FJ, Ruvkun G. A novel repeat domain that is often associated with RING finger and B-box motifs. Trends Biochem Sci 1998; 23(12):474–475.PubMedCrossRefGoogle Scholar
  5. 5.
    Reymond A, Meroni G, Fantozzi A et al. The tripartite motif family identifies cell compartments. EMBO J 2001;20(9):2140–2151.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Borden KL, Martin SR, O’Reilly NJ et al. Characterisation of a novel cysteine/histidine-rich metal binding domain from Xenopus nuclear factor XNF7. FEBS Lett 1993; 335(2):255–260.PubMedCrossRefGoogle Scholar
  7. 7.
    Strausberg RL, Feingold EA, Grouse LH et al. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci USA 2002; 99(26):16899–16903.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Miyamoto K, Nakamura N, Kashiwagi M et al. RING finger, B-box and coiled-coil (RBCC)protein expression in branchial epithelial cells of Japanese eel, Anguilla japonica. Eur J Biochem 2002; 269(24):6152–6161.PubMedCrossRefGoogle Scholar
  9. 9.
    Meroni G, Diez-Roux G. TRIM/RBCC, a novel class of’ single protein RING finger’ E3 ubiquitin ligases. Bioessays 2005; 27(11):1147–1157.PubMedCrossRefGoogle Scholar
  10. 10.
    Nisole S, Stoye JP, Saib A. TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 2005; 3(10):799–808.PubMedCrossRefGoogle Scholar
  11. 11.
    de The H, Lavau C, Marchio A et al. The PML-RAR alpha fusion mRNA generated by thet (15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 1991; 66(4): 675–684.PubMedCrossRefGoogle Scholar
  12. 12.
    Goddard AD, Borrow J, Freemont PS et al. Characterization of a zinc finger gene disrupted by the t(l5; 17) in acute promyelocytic leukemia. Science 1991; 254(5036):1371–1374.PubMedCrossRefGoogle Scholar
  13. 13.
    Kakizuka A, Miller WH, Jr., Umesono K et al. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML. Cell 1991; 66(4):663–674.PubMedCrossRefGoogle Scholar
  14. 14.
    Takahashi M, Buma Y, Iwamoto T et al. Cloning and expression of the ret proto-oncogene encoding a tyrosine kinase with two potential transmembrane domains. Oncogene 1988; 3(5):571–578.PubMedGoogle Scholar
  15. 15.
    Goff SP. Host factors exploited by retroviruses. Nat Rev Microbiol 2007; 5(4):253–263.PubMedCrossRefGoogle Scholar
  16. 16.
    Bieniasz PD. Intrinsic immunity: a front-line defense against viral attack. Nat Immunol 2004; 5(11): 1109–1115.PubMedCrossRefGoogle Scholar
  17. 17.
    Sokolskaja E, Luban J. Cyclophilin, TRIM5 and innate immunity to HIV-1. Curr Opin Microbiol 2006; 9(4):404–408.PubMedCrossRefGoogle Scholar
  18. 18.
    Balci-Peynircioglu B, Waite AL, Hu C et al. Pyrin, product of the MEFV locus, interacts with the proapoptotic protein, Siva. J Cell Physiol 2008.Google Scholar
  19. 19.
    Doganc T, Yuksel Konuk BE, Alpan N et al. A novel mutation in TRIM37 is associated with mulibrey nanism in a Turkish boy. Clin Dysmorphol 2007; 16(3):173–176.PubMedCrossRefGoogle Scholar
  20. 20.
    Hamalainen RH, Avela K, Lambert JA et al. Novel mutations in the TRIM37 gene in Mulibrey Nanism. Hum Mutat 2004; 23(5): 522.PubMedCrossRefGoogle Scholar
  21. 21.
    Kallijarvi J, Avela K, Lipsanen-Nyman M et al. The TRIM37 gene encodes a peroxisomal RING-B-box-coiled-coil protein: classification of mulibrey nanism as a new peroxisomal disorder. Am J Hum Genet 2002; 70(5):1215–1228.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Saccone V, Palmieri M, Passamano L et al. Mutations that impair interaction properties of TRIM32 associated with limb-girdle muscular dystrophy 2H. Hum Mutat 2008; 29(2):240–247.PubMedCrossRefGoogle Scholar
  23. 23.
    Short KM, Hopwood B, Yi Z et al. MID1 and MID2 homo and heterodimerise to tether the rapamycin-sensitive PP2A regulatory subunit, alpha 4, to microtubules: implications for the clinical variability of X-linked Opitz GBBB syndrome and other developmental disorders. BMC Cell Biol 2002; 3:1.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Torok M, Etkin LD. Two B or not two B? Overview of the rapidly expanding B-box family of proteins. Differentiation 2001; 67(3):63–71.PubMedCrossRefGoogle Scholar
  25. 25.
    Freemont PS. RING for destruction? Curr Biol 2000; 10(2):R84–87.PubMedCrossRefGoogle Scholar
  26. 26.
    Barlow PN, Luisi B, Milner A et al. Structure of the C3HC4 domain by 1H-nuclear magnetic resonance spectroscopy. Anew structural class of zinc-finger. J Mol Biol 1994; 237(2):201–211.PubMedCrossRefGoogle Scholar
  27. 27.
    Borden KL, Boddy MN, Lally J et al. The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncoprotein PML. EMBO J 1995; 14(7):1532–1541.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem 2009; 78:399–434.CrossRefPubMedGoogle Scholar
  29. 29.
    Bellon SF, Rodgers KK, Schatz DG et al. Crystal structure of the RAG1 dimerization domain reveals multiple zinc-binding motifs including a novel zinc binuclear cluster. Nat Struct Biol 1997; 4(7): 586–591.PubMedCrossRefGoogle Scholar
  30. 30.
    Brzovic PS, Meza JE, King MC et al. BRCA1 RING domain cancer-predisposing mutations. Structural consequences and effects on protein-protein interactions. J Biol Chem 2001; 276(44): 41399–41406.PubMedCrossRefGoogle Scholar
  31. 31.
    Kentsis A, Gordon RE, Borden KL. Control of biochemical reactions through supramolecular RING domain self-assembly. Proc Natl Acad Sci USA 2002; 99(24): 15404–15409.PubMedCrossRefGoogle Scholar
  32. 32.
    Kentsis A, Gordon RE, Borden KL. Self-assembly properties of a model RING domain. Proc Natl Acad Sci USA 2002; 99(2):667–672.PubMedCrossRefGoogle Scholar
  33. 33.
    Joazeiro CA, Weissman AM. RING finger proteins: mediators of ubiquitin ligase activity. Cell 2000; 102(5):549–552.PubMedCrossRefGoogle Scholar
  34. 34.
    Li X, Sodroski J. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J Virol 2008; 82(23): 11495–11502.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82(2):373–428.PubMedCrossRefGoogle Scholar
  36. 36.
    Koegl M, Hoppe T, Schlenker S et al. A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 1999; 96(5):635–644.PubMedCrossRefGoogle Scholar
  37. 37.
    Zheng N, Wang P, Jeffrey PD et al. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 2000; 102(4):533–539.PubMedCrossRefGoogle Scholar
  38. 38.
    Brzovic PS, Rajagopal P, Hoyt DW et al. Structure of a BRCA1-BARD1 heterodimeric RING-RING complex. Nat Struct Biol 2001; 8(10):833–837.PubMedCrossRefGoogle Scholar
  39. 39.
    Joazeiro CA, Hunter T. Biochemistry. Ubiquitination—more than two to tango. Science 2000; 289(5487):2061–2062.PubMedCrossRefGoogle Scholar
  40. 40.
    Hashizume R, Fukuda M, Maeda I et al. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J Biol Chem 2001; 276(18): 14537–14540.PubMedCrossRefGoogle Scholar
  41. 41.
    Wang H, Wang L, Erdjument-Bromage H et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004; 431(7010):873–878.PubMedCrossRefGoogle Scholar
  42. 42.
    Linares LK, Hengstermann A, Ciechanover A et al. HdmX stimulates Hdm2-mediated ubiquitination and degradation of p53. Proc Natl Acad Sci USA 2003; 100(21):12009–12014.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Micale L, Fusco C, Augello B et al. Williams-Beuren syndrome TRIM50 encodes an E3 ubiquitin ligase. Eur J Hum Genet 2008.Google Scholar
  44. 44.
    Kallijarvi J, Lahtinen U, Hamalainen R et al. TRIM37 defective in mulibrey nanism is a novel RING finger ubiquitin E3 ligase. Exp Cell Res 2005; 308(l):146–155.PubMedCrossRefGoogle Scholar
  45. 45.
    Massiah MA, Matts JA, Short KM et al. Solution structure of the MID1 B-box2 CHC(D/C)C(2)H(2) zinc-binding domain: insights into an evolutionarily conserved RING fold. J Mol Biol 2007; 369(1): 1–10.PubMedCrossRefGoogle Scholar
  46. 46.
    Massiah MA, Simmons BN, Short KM et al. Solution structure of the RBCC/TRIM B-box1 domain of human MID1: B-box with a RING. J Mol Biol 2006; 358(2):532–545.PubMedCrossRefGoogle Scholar
  47. 47.
    Borden KL, Lally JM, Martin SR et al. Novel topology of a zinc-binding domain from a protein involved in regulating early Xenopus development. EMBO J 1995; 14(23):5947–5956.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    De Falco F, Cainarca S, Andolfi G et al. X-linked Opitz syndrome: novel mutations in the MID1 gene and redefinition of the clinical spectrum. Am J Med Genet A 2003; 120(2):222–228.CrossRefGoogle Scholar
  49. 49.
    Schweiger S, Foerster J, Lehmann T et al. The Opitz syndrome gene product, MID1, associates with microtubules. Proc Natl Acad Sci USA 1999; 96(6):2794–2799.PubMedCrossRefGoogle Scholar
  50. 50.
    Lin RJ, Evans RM. Acquisition of oncogenic potential by RAR chimeras in acute promyelocytic leukemia through formation of homodimers. Mol Cell 2000; 5(5):821–830.PubMedCrossRefGoogle Scholar
  51. 51.
    Cainarca S, Messali S, Ballabio A et al. Functional characterization of the Opitz syndrome gene product (midin): evidence for homodimerization and association with microtubules throughout the cell cycle. Hum Mol Genet 1999; 8(8): 1387–1396.PubMedCrossRefGoogle Scholar
  52. 52.
    Cao T, Duprez E, Borden KL et al. Ret finger protein is a normal component of PML nuclear bodies and interacts directly with PML. J Cell Sci 1998; 111(Pt 10):1319–1329.PubMedGoogle Scholar
  53. 53.
    Buchner G, Montini E, Andolfi G et al. MID2, a homologue of the Opitz syndrome gene MID1: similarities in subcellular localization and differences in expression during development. Hum Mol Genet 1999; 8(8): 1397–1407.PubMedCrossRefGoogle Scholar
  54. 54.
    Grignani F, Gelmetti V, Fanelli M et al. Formation of PML/RAR alpha high molecular weight nuclear complexes through the PML coiled-coil region is essential for the PML/RAR alpha-mediated retinoic acid response. Oncogene 1999; 18(46):6313–6321.PubMedCrossRefGoogle Scholar
  55. 55.
    Borden KL, Freemont PS. The RING finger domain: a recent example of a sequence-structure family. Curr Opin Struct Biol 1996; 6(3):395–401.PubMedCrossRefGoogle Scholar
  56. 56.
    Urano T, Usui T, Takeda S et al. TRIM44 interacts with and stabilizes terf, a TRIM ubiquitin E3 ligase. Biochem Biophys Res Commun 2009; 383(2):263–268.PubMedCrossRefGoogle Scholar
  57. 57.
    Minucci S, Maccarana M, Cioce M et al. Oligomerization of RAR and AML1 transcription factors as a novel mechanism of oncogenic activation. Mol Cell 2000; 5(5):811–820.PubMedCrossRefGoogle Scholar
  58. 58.
    Vernet C, Boretto J, Mattei MG et al. Evolutionary study of multigenic families mapping close to the human MHC class I region. J Mol Evol 1993; 37(6):600–612.PubMedCrossRefGoogle Scholar
  59. 59.
    Orimo A, Yamagishi T, Tominaga N et al. Molecular cloning of testis-abundant finger Protein/Ring finger protein 23 (RNF23), a novel RING-B box-coiled coil-B30.2 protein on the class I region of the human MHC. Biochem Biophys Res Commun 2000; 276(1):45–51.PubMedCrossRefGoogle Scholar
  60. 60.
    Henry J, Ribouchon MT, Offer C et al. B30.2-like domain proteins: a growing family. Biochem Biophys Res Commun 1997; 235(1):162–165.PubMedCrossRefGoogle Scholar
  61. 61.
    Henry J, Mather IH, McDermott MF et al. B30.2-like domain proteins: update and new insights into a rapidly expanding family of proteins. Mol Biol Evol 1998; 15(12): 1696–1705.PubMedCrossRefGoogle Scholar
  62. 62.
    Ponting C, Schultz J, Bork P. SPRY domains in ryanodine receptors (Ca(2+)-release channels). Trends Biochem Sci 1997; 22(6):193–194.PubMedCrossRefGoogle Scholar
  63. 63.
    Rhodes DA, de Bono B, Trowsdale J. Relationship between SPRY and B30.2 protein domains. Evolution of a component of immune defence? Immunology 2005; 116(4):411–417.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Sawyer SL, Wu LI, Emerman M et al. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 2005; 102(8):2832–2837.PubMedCrossRefGoogle Scholar
  65. 65.
    Song B, Gold B, O’Huigin C et al. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J Virol 2005; 79(10):6111–6121.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Song B, Javanbakht H, Perron M et al. Retro virus restriction by TRIM5alpha variants from Old World and New World primates. J Virol 2005; 79(7):3930–3937.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Alexander WS, Starr R, Metcalf D et al. Suppressors of cytokine signaling (SOCS): negative regulators of signal transduction. J Leukoc Biol 1999; 66(4): 588–592.PubMedCrossRefGoogle Scholar
  68. 68.
    Hilton DJ, Richardson RT, Alexander WS et al. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci USA 1998; 95(1):114–119.PubMedCrossRefGoogle Scholar
  69. 69.
    Bleoo S, Sun X, Hendzel MJ et al. Association of human DEAD box protein DDX1 with a cleavage stimulation factor involved in 3’-end processing of preMRNA. Mol Biol Cell 2001; 12(10):3046–3059.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Schwarzmann N, Kunerth S, Weber K et al. Knock-down of the type 3 ryanodine receptor impairs sustained Ca2+ signaling via the T-cell receptor/CD3 complex. J Biol Chem 2002; 277(52):50636–50642.PubMedCrossRefGoogle Scholar
  71. 71.
    Rosa JL, Barbacid M. A giant protein that stimulates guanine nucleotide exchange on ARF1 and Rab proteins forms a cytosolic ternary complex with clathrin and Hsp70. Oncogene 1997; 15(1): 1–6.PubMedCrossRefGoogle Scholar
  72. 72.
    Adamson AL, Shearn A. Molecular genetic analysis of Drosophila ash2, a member of the trithorax group required for imaginai disc pattern formation. Genetics 1996; 144(2):621–633.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Roguev A, Schaft D, Shevchenko A et al. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 2001; 20(24):7137–7148.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Stremlau M, Owens CM, Perron MJ et al. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004; 427(6977):848–853.CrossRefPubMedGoogle Scholar
  75. 75.
    Goldschmidt V, Ciuffi A, Ortiz M et al. Antiretroviral activity of ancestral TRIM5alpha. J Virol 2008; 82(5):2089–2096.PubMedCrossRefGoogle Scholar
  76. 76.
    Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 2007; 131(1):46–57.PubMedCrossRefGoogle Scholar
  77. 77.
    Yap MW, Nisole S, Lynch C et al. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci USA 2004; 101(29):10786–10791.PubMedCrossRefGoogle Scholar
  78. 78.
    Zhang F, Hatziioannou T, Perez-Caballero D et al. Antiretroviral potential of human tripartite motif-5 and related proteins. Virology 2006; 353(2):396–409.PubMedCrossRefGoogle Scholar
  79. 79.
    Chelbi-Alix MK, Quignon F, Pelicano L et al. Resistanceto virus infection conferred by the interferon-induced promyelocytic leukemia protein. J Virol 1998; 72(2):1043–1051.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Everett RD, Rechter S, Papior P et al. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J Virol 2006; 80(16):7995–8005.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Tavalai N, Papior P, Rechter S et al. Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J Virol 2006; 80(16):8006–8018.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Fridell RA, Harding LS, Bogerd HP et al. Identification of a novel human zinc finger protein that specifically interacts with the activation domain of lentiviral Tat proteins. Virology 1995; 209(2):347–357.PubMedCrossRefGoogle Scholar
  83. 83.
    Tissot C, Mechti N. Molecular cloning of a new interferon-induced factor that represses human immunodeficiency virus type 1 long terminal repeat expression. J Biol Chem 1995;270(25):14891–14898.PubMedCrossRefGoogle Scholar
  84. 84.
    Sivaramakrishnan G, Sun Y, Rajmohan R et al. B30.2/SPRY domain in tripartite motif-containing 22 is essential for the formation of distinct nuclear bodies. FEBS Lett 2009; 583(12):2093–2099.PubMedCrossRefGoogle Scholar
  85. 85.
    Herr AM, Dressel R, Walter L. Different subcellular localisations of TRIM22 suggest species-specific function. Immunogenetics 2009; 61(4):271–280.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Spencer JA, Eliazer S, Ilaria RL Jr. et al. Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J Cell Biol 2000; 150(4):771–784.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Ohkawa N, Kokura K, Matsu-Ura T et al. Molecular cloning and characterization of neural activity-related RING finger protein (NARF): a new member of the RBCC family is a candidate for the partner of myosin V. J Neurochem 2001; 78(1):75–87.PubMedCrossRefGoogle Scholar
  88. 88.
    Balastik M, Ferraguti F, Pires-da Silva A et al. Deficiency in ubiquitin ligase TRIM2 causes accumulation of neurofilament light chain and neurodegeneration. Proc Natl Acad Sci USA 2008; 105(33): 12016–12021.PubMedCrossRefGoogle Scholar
  89. 89.
    Hammell CM, Lubin I, Boag PR et al. nhl-2 Modulates microRNA activity in Caenorhabditis elegans. Cell 2009; 136(5):926–938.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Schwamborn JC, Berezikov E, Knoblich JA. The TRIM-NHL protein TRIM32 activates micro RNAs and prevents self-renewal in mouse neural progenitors. Cell 2009; 136(5):913–925.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Haynes SR, Dollard C, Winston F et al. The bromodomain: a conserved sequence found in human, Drosophila and yeast proteins. Nucleic Acids Res 1992; 20(10):2603.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Tamkun JW, Deuring R, Scott MP et al. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 1992; 68(3):561–572.PubMedCrossRefGoogle Scholar
  93. 93.
    Moss J, Vaughan M. Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J Biol Chem 1995; 270(21):12327–12330.PubMedCrossRefGoogle Scholar
  94. 94.
    Holthuis JC, Burger KN. Sensing membrane curvature. Dev Cell 2003; 5(6):821–822.PubMedCrossRefGoogle Scholar
  95. 95.
    Nie Z, Hirsch DS, Randazzo PA. Arf and its many interactors. Curr Opin Cell Biol 2003; 15(4):396–404.PubMedCrossRefGoogle Scholar
  96. 96.
    Mishima K, Tsuchiya M, Nightingale MS et al. ARD 1, a 64-kDa guanine nucleotide-binding protein with a carboxyl-terminal ADP-ribosylation factor domain. J Biol Chem 1993; 268(12):8801–8807.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Lucia Micale
    • 1
  • Evelyne Chaignat
    • 2
  • Carmela Fusco
    • 1
  • Alexandre Reymond
    • 2
  • Giuseppe Merla
    • 1
  1. 1.Laboratory of Medical GeneticsIRCCS Casa Sollievo della SofferenzaSan Giovanni RotondoItaly
  2. 2.Center for Integrative GenomicsUniversity of LausanneLausanneSwitzerland

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