An interdomain binding site on HIV-1 Nef interacts with PACS-1 and PACS-2 on endosomes to down-regulate MHC-I

Molecular Biology of the Cell

Volumn 23, Issue 11, 2012, Pages 2184-2197

  Dikeakos, Jimmy D ^a,b   Thomas, Laurel ^a,c   Kwon, Grace ^a   Elferich, Johannes ^a   Shinde, Ujwal ^a   Thomas, Gary ^a,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b WESTERN UNIVERSITY   (Canada)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; PROTEIN PACS 1; PROTEIN PACS 2; RAB PROTEIN; RAB7 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; ENDOSOME; FLUORESCENCE; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; AMINO ACIDS; BINDING SITES; DOWN-REGULATION; ENDOSOMES; FURIN; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP; VESICULAR TRANSPORT PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84861708657     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-11-0928     Document Type: Article

References (60)

1. Ali SA, Huang MB, Campbell PE, Roth WW, Campbell T, Khan M, Newman G, Villinger F, Powell MD, Bond VC (2010). Genetic characterization of HIV type 1 Nef-induced vesicle secretion. AIDS Res Hum Retroviruses 26, 173-192.
2. Arold S, Franken P, Strub MP, Hoh F, Benichou S, Benarous R, Dumas C (1997). The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure 5, 1361-1372. (Pubitemid 27484477)
3. Aslan JE et al. (2009). Akt and 14-3-3 control a PACS-2 homeostatic switch that integrates membrane traffic with TRAIL-induced apoptosis. Mol Cell 34, 497-509.
4. Atkins KM, Thomas L, Youker RT, Harriff MJ, Pissani F, You H, Thomas G (2008). HIV-1 Nef binds PACS-2 to assemble a multikinase cascade that triggers major histocompatibility complex class I (MHC-I) down-regulation: analysis using short interfering RNA and knock-out mice. J Biol Chem 283, 11772-11784.
5. Blagoveshchenskaya AD, Thomas L, Feliciangeli SF, Hung CH, Thomas G (2002). HIV-1 Nef down-regulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 111, 853-866. (Pubitemid 36106406)
6. Bouard D, Sandrin V, Boson B, Negre D, Thomas G, Granier C, Cosset FL (2007). An acidic cluster of the cytoplasmic tail of the RD114 virus glyco-protein controls assembly of retroviral envelopes. Traffic 8, 835-847. (Pubitemid 46971631)
7. Casartelli N, Giolo G, Neri F, Haller C, Potesta M, Rossi P, Fackler OT, Doria M (2006). The Pro78 residue regulates the capacity of the human immunodeficiency virus type 1 Nef protein to inhibit recycling of major histocompatibility complex class I molecules in an SH3-independent manner. J Gen Virol 87, 2291-2296. (Pubitemid 44178105)
8. Chen J, Wang J, Meyers KR, Enns CA (2009). Transferrin-directed internalization and cycling of transferrin receptor 2. Traffic 10, 1488-1501.
9. Comeau SR, Gatchell DW, Vajda S, Camacho CJ (2004). ClusPro: a fully automated algorithm for protein-protein docking. Nucleic Acids Res 32, W96-W99. (Pubitemid 38997307)
10. Crump CM, Hung CH, Thomas L, Wan L, Thomas G (2003). Role of PACS-1 in trafficking of human cytomegalovirus glycoprotein B and virus production. J Virol 77, 11105-11113. (Pubitemid 37204300)
11. Crump CM, Xiang Y, Thomas L, Gu F, Austin C, Tooze SA, Thomas G (2001). PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J 20, 2191-2201.
12. Dascher C, VanSlyke JK, Thomas L, Balch WE, Thomas G (1995). Preparation of recombinant vaccinia virus for expression of small GTPases. Methods Enzymol 257, 174-188.
13. Dikeakos JD et al. (2010). Small molecule inhibition of HIV-1-induced MHC-I down-regulation identifies a temporally regulated switch in Nef action. Mol Biol Cell 21, 3279-3292.
14. Fackler OT, Baur AS (2002). Live and let die: Nef functions beyond HIV replication. Immunity 16, 493-497. (Pubitemid 34442574)
15. Faure J, Stalder R, Borel C, Sobo K, Piguet V, Demaurex N, Gruenberg J, Trono D (2004). ARF1 regulates Nef-induced CD4 degradation. Curr Biol 14, 1056-1064. (Pubitemid 38791567)
16. Friedrich TC et al. (2004). Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 10, 275-281. (Pubitemid 38667618)
17. Friedrich TC et al. (2010). High viremia is associated with high levels of in vivo major histocompatibility complex class I down-regulation in rhesus macaques infected with simian immunodeficiency virus SIVmac239. J Virol 84, 5443-5447.
18. Furman C, Short SM, Subramanian RR, Zetter BR, Roberts TM (2002). DEF-1/ASAP1 is a GTPase-activating protein (GAP) for ARF1 that enhances cell motility through a GAP-dependent mechanism. J Biol Chem 277, 7962-7969. (Pubitemid 34968247)
19. Geijtenbeek TB, Gringhuis SI (2009). Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9, 465-479.
20. Gerlach H, Laumann V, Martens S, Becker CF, Goody RS, Geyer M (2009). HIV-1 Nef membrane association depends on charge, curvature, composition and sequence. Nat Chem Biol 6, 46-53.
21. Geyer M, Fackler OT, Peterlin BM (2001). Structure-function relationships in HIV-1 Nef. EMBO Rep 2, 580-585. (Pubitemid 32707703)
22. Greenberg ME, Iafrate AJ, Skowronski J (1998). The SH3 domain-binding surface and an acidic motif in HIV-1 Nef regulate trafficking of class I MHC complexes. EMBO J 17, 2777-2789. (Pubitemid 28227124)
23. Grzesiek S, Bax A, Hu JS, Kaufman J, Palmer I, Stahl SJ, Tjandra N, Wingfield PT (1997). Refined solution structure and backbone dynamics of HIV-1 Nef. Protein Sci 6, 1248-1263. (Pubitemid 27260159)
24. Guruprasad K, Reddy BV, Pandit MW (1990). Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng 4, 155-161.
25. Gustafsson MG (2000). Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198, 82-87.
26. Haberg K, Lundmark R, Carlsson SR (2008). SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking. J Cell Sci 121, 1495-1505. (Pubitemid 351936314)
27. Harbour ME, Breusegem SY, Antrobus R, Freeman C, Reid E, Seaman MN (2010). The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J Cell Sci 123, 3703-3717.
28. Horenkamp FA, Breuer S, Schulte A, Lulf S, Weyand M, Saksela K, Geyer M (2011). Conformation of the dileucine-based sorting motif in HIV-1 Nef revealed by intermolecular domain assembly. Traffic 12, 867-877.
29. Hung CH et al. (2007). HIV-1 Nef assembles a Src family kinase-ZAP-70/Syk-PI3K cascade to down-regulate cell-surface MHC-I. Cell Host Microbe 1, 121-133. (Pubitemid 46554916)
30. Huotari J, Helenius A (2011). Endosome maturation. EMBO J 30, 3481-3500.
31. Jenkins PM, Zhang L, Thomas G, Martens JR (2009). PACS-1 mediates phosphorylation-dependent ciliary trafficking of the cyclic-nucleotide-gated channel in olfactory sensory neurons. J Neurosci 29, 10541-10551.
32. Kerppola TK (2008). Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu Rev Biophys 37, 465-487.
33. Kirchhoff F (2010). Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8, 55-67.
34. Kirchhoff F, Easterbrook PJ, Douglas N, Troop M, Greenough TC, Weber J, Carl S, Sullivan JL, Daniels RS (1999). Sequence variations in human immunodeficiency virus type 1 Nef are associated with different stages of disease. J Virol 73, 5497-5508. (Pubitemid 29274833)
35. Kottgen M et al. (2005). Trafficking of TRPP2 by PACS proteins represents a novel mechanism of ion channel regulation. EMBO J 24, 705-716. (Pubitemid 40396101)
36. Kozakov D et al. (2010). Achieving reliability and high accuracy in automated protein docking: ClusPro, PIPER, SDU, and stability analysis in CAPRI rounds 13-19. Proteins 78, 3124-3130.
37. Lee CH, Saksela K, Mirza UA, Chait BT, Kuriyan J (1996). Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell 85, 931-942.
38. Lieberman J (2003). The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat Rev Immunol 3, 361-370.
39. Liu G, Thomas L, Warren RA, Enns CA, Cunningham CC, Hartwig JH, Thomas G (1997). Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J Cell Biol 139, 1719-1733. (Pubitemid 28079237)
40. Luo P, Baldwin RL (1997). Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water. Biochemistry 36, 8413-8421. (Pubitemid 27297553)
41. Mangino G et al. (2011). HIV-1 Nef induces proinflammatory state in macrophages through its acidic cluster domain: involvement of TNF alpha receptor associated factor 2. PLoS One 6, e22982.
42. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF (2010). The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 10, 11-23.
43. Molloy SS, Thomas L, Kamibayashi C, Mumby MC, Thomas G (1998). Regulation of endosome sorting by a specific PP2A isoform. J Cell Biol 142, 1399-1411. (Pubitemid 28452592)
44. Myhill N, Lynes EM, Nanji JA, Blagoveshchenskaya AD, Fei H, Simmen KC, Cooper TJ, Thomas G, Simmen T (2008). The subcellular distribution of calnexin is mediated by PACS-2. Mol Biol Cell 19, 2777-2788.
45. Noviello CM, Benichou S, Guatelli JC (2008). Cooperative binding of the class I major histocompatibility complex cytoplasmic domain and human immunodeficiency virus type 1 Nef to the endosomal AP-1 complex via its mu subunit. J Virol 82, 1249-1258.
46. Peterlin BM, Trono D (2003). Hide, shield and strike back: how HIV-infected cells avoid immune eradication. Nat Rev Immunol 3, 97-107. (Pubitemid 37328688)
47. Piguet V, Wan L, Borel C, Mangasarian A, Demaurex N, Thomas G, Trono D (2000). HIV-1 Nef protein binds to the cellular protein PACS-1 to down-regulate class I major histocompatibility complexes. Nat Cell Biol 2, 163-167.
48. Poe JA, Smithgall TE (2009). HIV-1 Nef dimerization is required for Nef-mediated receptor down-regulation and viral replication. J Mol Biol 394, 329-342.
49. Roeth JF, Williams M, Kasper MR, Filzen TM, Collins KL (2004). HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. J Cell Biol 167, 903-913. (Pubitemid 39628112)
50. Sarmady M, Dampier W, Tozeren A (2011). HIV protein sequence hotspots for crosstalk with host hub proteins. PLoS One 6, e23293.
51. Schaefer MR, Wonderlich ER, Roeth JF, Leonard JA, Collins KL (2008). HIV-1 Nef targets MHC-I and CD4 for degradation via a final common beta-COP-dependent pathway in T cells. PLoS Pathog 4, e1000131.
52. Schermer B et al. (2005). Phosphorylation by casein kinase 2 induces PACS-1 binding of nephrocystin and targeting to cilia. EMBO J 24, 4415-4424. (Pubitemid 41828915)
53. Scott GK, Fei H, Thomas L, Medigeshi GR, Thomas G (2006). A PACS-1, GGA3 and CK2 complex regulates CI-MPR trafficking. EMBO J 25, 4423-4435. (Pubitemid 44498117)
54. Sieburth D et al. (2005). Systematic analysis of genes required for synapse structure and function. Nature 436, 510-517.
55. Simmen T, Aslan JE, Blagoveshchenskaya AD, Thomas L, Wan L, Xiang Y, Feliciangeli SF, Hung CH, Crump CM, Thomas G (2005). PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J 24, 717-729. (Pubitemid 40396102)
56. Singh RK, Lau D, Noviello CM, Ghosh P, Guatelli JC (2009). An MHC-I cytoplasmic domain/HIV-1 Nef fusion protein binds directly to the mu subunit of the AP-1 endosomal coat complex. PLoS One 4, e8364.
57. Wan L, Molloy SS, Thomas L, Liu G, Xiang Y, Rybak SL, Thomas G (1998). PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 94, 205-216. (Pubitemid 28348008)
58. Xu W et al. (2009). HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Immunol 10, 1008-1017.
59. Yamada T, Kaji N, Odawara T, Chiba J, Iwamoto A, Kitamura Y (2003). Proline 78 is crucial for human immunodeficiency virus type 1 Nef to down-regulate class I human leukocyte antigen. J Virol 77, 1589-1594. (Pubitemid 36055579)
60. Youker RT, Shinde U, Day R, Thomas G (2009). At the crossroads of homoeostasis and disease: roles of the PACS proteins in membrane traffic and apoptosis. Biochem J 421, 1-15.