LEDGF/p75 proteins with alternative chromatin tethers are functional HIV-1 cofactors

PLoS Pathogens

Volumn 5, Issue 7, 2009, Pages

  Meehan, Anne M ^a   Saenz, Dyana T ^a   Morrison, James H ^a   Garcia Rivera, Jose A ^b   Peretz, Mary ^a   Llano, Manuel ^b   Poeschla, Eric M ^a  

^a Mayo Clinic   (United States)

^b UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DIMER; GREEN FLUORESCENT PROTEIN; HISTONE H2A; HISTONE H2B; INTEGRASE BINDING PROTEIN; LENS EPITHELIUM DERIVED GROWTH FACTOR; PROTEIN P75; UNCLASSIFIED DRUG; VIRUS PROTEIN; ANTIVIRUS AGENT; DNA BINDING PROTEIN; HISTONE; HYBRID PROTEIN; INTEGRASE; LATENCY ASSOCIATED NUCLEAR ANTIGEN; LATENCY-ASSOCIATED NUCLEAR ANTIGEN; NUCLEAR PROTEIN; PEPTIDE FRAGMENT; PROTEASOME; PSIP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSCRIPTION FACTOR; VIRUS ANTIGEN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHIMERA; CHROMATIN; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS 1; LUPUS ERYTHEMATOSUS CELL TEST; MOLECULAR MECHANICS; MOUSE; MUTANT; NONHUMAN; NUCLEOSOME; PROTEIN DOMAIN; RETROVIRUS; RNA INTERFERENCE; SARCOMA VIRUS; VIRUS INFECTION; VIRUS MUTANT; ANIMAL; CELL CULTURE; CELL LINE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; VIROLOGY; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, VIRAL; ANTIVIRAL AGENTS; BASE SEQUENCE; CELL LINE; CELLS, CULTURED; CHROMATIN; DNA-BINDING PROTEINS; GREEN FLUORESCENT PROTEINS; HISTONES; HIV INFECTIONS; HIV INTEGRASE; HIV-1; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; VIRUS REPLICATION;

EID: 70049090961     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000522     Document Type: Article

References (71)

1. Craigie R (2001) HIV integrase, a brief overview from chemistry to therapeutics. J Biol Chem 276: 23213-23216. (Pubitemid 37410700)
2. Brown PO (1999) Integration. In: Coffin JM, Hughes SH, Varmus HE, eds. Retroviruses. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press. pp 161-203.
3. Engelman A (2003) The roles of cellular factors in retroviral integration. Curr Top Microbiol Immunol 281: 209-238. (Pubitemid 36950687)
4. Cherepanov P, Maertens G, Proost P, Devreese B, Van Beeumen J, et al. (2003) HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J Biol Chem 278: 372-381. (Pubitemid 36043586)
5. Emiliani S, Mousnier A, Busschots K, Maroun M, Van Maele B, et al. (2005) Integrase mutants defective for interaction with LEDGF/p75 are impaired in chromosome tethering and HIV-1 replication. J Biol Chem 280: 25517-25523. (Pubitemid 40962257)
6. Ciuffi A, Llano M, Poeschla E, Hoffmann C, Leipzig J, et al. (2005) A role for LEDGF/p75 in targeting HIV DNA integration. Nature Medicine 11: 1287-1289. (Pubitemid 41752906)
7. Llano M, Saenz DT, Meehan A, Wongthida P, Peretz M, et al. (2006) An Essential Role for LEDGF/p75 in HIV Integration. Science 314: 461-464. (Pubitemid 44628966)
8. De Rijck J, Vandekerckhove L, Gijsbers R, Hombrouck A, Hendrix J, et al. (2006) Overexpression of the lens epithelium-derived growth factor/p75 integrase binding domain inhibits human immunodeficiency virus replication. J Virol 80: 11498-11509. (Pubitemid 44788865)
9. Vandekerckhove L, Christ F, Van Maele B, De Rijck J, Gijsbers R, et al. (2006) Transient and stable knockdown of the integrase cofactor LEDGF/p75 reveals its role in the replication cycle of human immunodeficiency virus. J Virol 80: 1886-1896. (Pubitemid 43228728)
10. Cherepanov P (2007) LEDGF/p75 interacts with divergent lentiviral integrases and modulates their enzymatic activity in vitro. Nucleic Acids Res 35: 113-124.
11. Hombrouck A, De Rijck J, Hendrix J, Vandekerckhove L, Voet A, et al. (2007) Virus Evolution Reveals an Exclusive Role for LEDGF/p75 in Chromosomal Tethering of HIV. PLoS Pathog 3: e47. doi:10.1371/journal.ppat.0030047. (Pubitemid 46535814)
12. Shun MC, Raghavendra NK, Vandegraaff N, Daigle JE, Hughes S, et al. (2007) LEDGF/p75 functions downstream from preintegration complex formation to effect gene-specific HIV-1 integration. Genes Dev 21: 1767-1778. (Pubitemid 47076476)
13. Marshall HM, Ronen K, Berry C, Llano M, Sutherland H, et al. (2007) Role of PSIP1/LEDGF/p75 in Lentiviral Infectivity and Integration Targeting. PLoS ONE 2: e1340. doi:10.1371/journal.pone.0001340. (Pubitemid 351736604)
14. Engelman A, Cherepanov P (2008) The lentiviral integrase binding protein LEDGF/p75 and HIV-1 replication. PLoS Pathog 4: e1000046. 10.1371/journal.ppat. 1000046.
15. Poeschla EM (2008) Integrase, LEDGF/p75 and HIV replication. Cell Mol Life Sci 65: 1403-1424.
16. Ge H, Si Y, Roeder RG (1998) Isolation of cDNAs encoding novel transcription coactivators p52 and p75 reveals an alternate regulatory mechanism of transcriptional activation. Embo J 17: 6723-6729. (Pubitemid 28521805)
17. Maertens G, Cherepanov P, Pluymers W, Busschots K, De Clercq E, et al. (2003) LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J Biol Chem 278: 33528-33539. (Pubitemid 37055807)
18. Llano M, Vanegas M, Fregoso O, Saenz DT, Chung S, et al. (2004) LEDGF/p75 determines cellular trafficking of diverse lentiviral but not murine oncoretroviral integrase proteins and is a component of functional lentiviral pre-integration complexes. J Virol 78: 9524-9537. (Pubitemid 39096559)
19. Vanegas M, Llano M, Delgado S, Thompson D, Peretz M, et al. (2005) Identification of the LEDGF/p75 HIV-1 integrase-interaction domain and NLS reveals NLS-independent chromatin tethering. J Cell Sci 118: 1733-1743. (Pubitemid 40691901)
20. Llano M, Delgado S, Vanegas M, Poeschla EM (2004) LEDGF/p75 prevents proteasomal degradation of HIV-1 integrase. J Biol Chem 279: 55570-55577.
21. Cherepanov P, Devroe E, Silver PA, Engelman A (2004) Identification of an evolutionarily conserved domain in human lens epithelium-derived growth factor/transcriptional co-activator p75 (LEDGF/p75) that binds HIV-1 integrase. J Biol Chem 279: 48883-48892. (Pubitemid 39625769)
22. Cherepanov P, Sun ZY, Rahman S, Maertens G, Wagner G, et al. (2005) Solution structure of the HIV-1 integrase-binding domain in LEDGF/p75. Nat Struct Mol Biol 12: 526-532. (Pubitemid 43085883)
23. Cherepanov P, Ambrosio AL, Rahman S, Ellenberger T, Engelman A (2005) Structural basis for the recognition between HIV-1 integrase and transcriptional coactivator p75. Proc Natl Acad Sci U S A 102: 17308-17313. (Pubitemid 41740862)
24. Hare S, Shun MC, Gupta SS, Valkov E, Engelman A, et al. (2009) A novel co-crystal structure affords the design of gain-of-function lentiviral integrase mutants in the presence of modified PSIP1/LEDGF/p75. PLoS Pathog 5: e1000259. 10.1371/journal.ppat.1000259.
25. Llano M, Vanegas M, Hutchins N, Thompson D, Delgado S, et al. (2006) Identification and Characterization of the Chromatin Binding Domains of the HIV-1 Integrase Interactor LEDGF/p75. J Mol Biol 360: 760-773. (Pubitemid 43993915)
26. Turlure F, Maertens G, Rahman S, Cherepanov P, Engelman A (2006) A tripartite DNA-binding element, comprised of the nuclear localization signal and two AT-hook motifs, mediates the association of LEDGF/p75 with chromatin in vivo. Nucleic Acids Res 34: 1663-1675.
27. Stec I, Nagl SB, van Ommen GJ, den Dunnen JT (2000) The PWWP domain: a potential protein-protein interaction domain in nuclear proteins influencing differentiation? FEBS Lett 473: 1-5.
28. Qiu C, Sawada K, Zhang X, Cheng X (2002) The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat Struct Biol 9: 217-224. (Pubitemid 34171315)
29. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, et al. (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311: 856-861. (Pubitemid 43228851)
30. Brown DT, Izard T, Misteli T (2006) Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo. Nat Struct Mol Biol 13: 250-255. (Pubitemid 43348511)
31. Harvey AC, Downs JA (2004) What functions do linker histones provide? Mol Microbiol 53: 771-775.
32. Bednar J, Horowitz RA, Grigoryev SA, Carruthers LM, Hansen JC, et al. (1998) Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc Natl Acad Sci U S A 95: 14173-14178. (Pubitemid 28549340)
33. Th'ng JP, Sung R, Ye M, Hendzel MJ (2005) H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J Biol Chem 280: 27809-27814.
34. Routh A, Sandin S, Rhodes D (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci U S A 105: 8872-8877.
35. Bates DL, Thomas JO (1981) Histones H1 and H5: one or two molecules per nucleosome? Nucleic Acids Res 9: 5883-5894.
36. Bustin M, Catez F, Lim JH (2005) The dynamics of histone H1 function in chromatin. Mol Cell 17: 617-620.
37. Woodcock CL, Skoultchi AI, Fan Y (2006) Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14: 17-25.
38. Misteli T, Gunjan A, Hock R, Bustin M, Brown DT (2000) Dynamic binding of histone H1 to chromatin in living cells. Nature 408: 877-881. (Pubitemid 32016100)
39. Lever MA, Th'ng JP, Sun X, Hendzel MJ (2000) Rapid exchange of histone H1.1 on chromatin in living human cells. Nature 408: 873-876. (Pubitemid 32016099)
40. Hendzel MJ, Lever MA, Crawford E, Th'ng JP (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279: 20028-20034.
41. Catez F, Ueda T, Bustin M (2006) Determinants of histone H1 mobility and chromatin binding in living cells. Nat Struct Mol Biol 13: 305-310. (Pubitemid 43873500)
42. Izzo A, Kamieniarz K, Schneider R (2008) The histone H1 family: specific members, specific functions? Biol Chem 389: 333-343.
43. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869.
44. Ballestas ME, Chatis PA, Kaye KM (1999) Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284: 641-644.
45. Sutherland HG, Newton K, Brownstein DG, Holmes MC, Kress C, et al. (2006) Disruption of Ledgf/Psip1 results in perinatal mortality and homeotic skeletal transformations. Mol Cell Biol 26: 7201-7210. (Pubitemid 44477696)
46. Sutherland HG, Mumford GK, Newton K, Ford LV, Farrall R, et al. (2001) Large-scale identification of mammalian proteins localized to nuclear subcompartments. Hum Mol Genet 10: 1995-2011. (Pubitemid 32910544)
47. Roe T, Reynolds TC, Yu G, Brown PO (1993) Integration of murine leukemia virus DNA depends on mitosis. Embo J 12: 2099-2108. (Pubitemid 23157725)
48. Lewis PF, Emerman M (1994) Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. Journal of Virology 68: 510-516. (Pubitemid 24974657)
49. Soutoglou E, Misteli T (2007) Mobility and immobility of chromatin in transcription and genome stability. Curr Opin Genet Dev 17: 435-442. (Pubitemid 350016896)
50. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921. (Pubitemid 32165345)
51. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Luger K, Kaye KM (2006) Kaposi's sarcoma-associated herpesvirus LANA hitches a ride on the chromosome. Cell Cycle 5: 1048-1052. (Pubitemid 43765297)
52. Kanda T, Otter M, Wahl GM (2001) Coupling of mitotic chromosome tethering and replication competence in epstein-barr virus-based plasmids. Mol Cell Biol 21: 3576-3588. (Pubitemid 32381793)
53. Sears J, Kolman J, Wahl GM, Aiyar A (2003) Metaphase chromosome tethering is necessary for the DNA synthesis and maintenance of oriP plasmids but is insufficient for transcription activation by Epstein-Barr nuclear antigen 1. J Virol 77: 11767-11780. (Pubitemid 37271674)
54. You J, Croyle JL, Nishimura A, Ozato K, Howley PM (2004) Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell 117: 349-360. (Pubitemid 38534541)
55. Oliveira JG, Colf LA, McBride AA (2006) Variations in the association of papillomavirus E2 proteins with mitotic chromosomes. Proc Natl Acad Sci U S A 103: 1047-1052. (Pubitemid 43212219)
56. Hung SC, Kang MS, Kieff E (2001) Maintenance of Epstein-Barr virus (EBV) oriP-based episomes requires EBV-encoded nuclear antigen-1 chromosome-binding domains, which can be replaced by high-mobility group-I or histone H1. Proc Natl Acad Sci U S A 98: 1865-1870.
57. Anderson DJ, Hetzer MW (2008) The life cycle of the metazoan nuclear envelope. Curr Opin Cell Biol 20: 386-392.
58. Swanson JA, McNeil PL (1987) Nuclear reassembly excludes large macromolecules. Science 238: 548-550.
59. Benavente R, Scheer U, Chaly N (1989) Nucleocytoplasmic sorting of macromolecules following mitosis: fate of nuclear constituents after inhibition of pore complex function. Eur J Cell Biol 50: 209-219. (Pubitemid 19261750)
60. Tobaly-Tapiero J, Bittoun P, Lehmann-Che J, Delelis O, Giron ML, et al. (2008) Chromatin tethering of incoming foamy virus by the structural Gag protein. Traffic 9: 1717-1727.
61. Bartholomeeusen K, De Rijck J, Busschots K, Desender L, Gijsbers R, et al. (2007) Differential Interaction of HIV-1 Integrase and JPO2 with the C Terminus of LEDGF/p75. J Mol Biol 372: 407-421. (Pubitemid 47267963)
62. Maertens GN, Cherepanov P, Engelman A (2006) Transcriptional co-activator p75 binds and tethers the Myc-interacting protein JPO2 to chromatin. J Cell Sci 119: 2563-2571. (Pubitemid 44070437)
63. Yokoyama A, Cleary ML (2008) Menin critically links MLL proteins with LEDGF on cancer-associated target genes. Cancer Cell 14: 36-46. (Pubitemid 351885493)
64. Bartholomeeusen K, Gijsbers R, Christ F, Hendrix J, Rain JC, et al. (2009) Lens Epithelium Derived Growth Factor/p75 interacts with the transposase derived DDE domain of pogZ. J Biol Chem 284: 11467-11477.
65. Roudaia L, Speck NA (2008) A MENage a Trois in leukemia. Cancer Cell 14: 3-5.
66. Wang GP, Ciuffi A, Leipzig J, Berry CC, Bushman FD (2007) HIV integration site selection: Analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res 17: 1186-1194. (Pubitemid 47204862)
67. Ciuffi A, Diamond TL, Hwang Y, Marshall HM, Bushman FD (2006) Modulating target site selection during human immunodeficiency virus DNA integration in vitro with an engineered tethering factor. Hum Gene Ther 17: 960-967. (Pubitemid 46076756)
68. Poeschla E, Looney D (1998) CXCR4 is required by a non-primate lentivirus: heterologous expression of feline immunodeficiency virus in human, rodent and feline cells. J Virol 72: 6858-6866. (Pubitemid 28324006)
69. Harrer M, Luhrs H, Bustin M, Scheer U, Hock R (2004) Dynamic interaction of HMGA1a proteins with chromatin. J Cell Sci 117: 3459-3471. (Pubitemid 39206386)
70. Llano M, Gaznick N, Poeschla EM (2008) Rapid, controlled and intensive lentiviral vector-based RNAi. In: Kalpana G, Prasad V, eds. HIV Protocols, second edition. Totowa, NJ: Humana Press.
71. Saenz DT, Loewen N, Peretz M, Whitwam T, Barraza R, et al. (2004) Unintegrated lentiviral DNA persistence and accessibility to expression in nondividing cells: analysis with class I integrase mutants. Journal of Virology 78: 2906-2920. (Pubitemid 38314348)