Kaposi's Sarcoma-Associated Herpesvirus K3 and K5 Proteins Down Regulate Both DC-SIGN and DC-SIGNR

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Lang, Sabine M ^a   Bynoe, Meisha O F ^a   Karki, Roshan ^a,b   Tartell, Michael A ^a,c   Means, Robert E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Biomedical Research Institute   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD209 ANTIGEN; LECTIN; PROTEIN DC SIGNR; PROTEIN K3; PROTEIN K5; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOCYTOSIS; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; VIRUS INFECTIVITY;

AMINO ACID MOTIFS; CELL ADHESION MOLECULES; CELL MEMBRANE; DOWN-REGULATION; ENDOCYTOSIS; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HUMANS; IMMUNOPRECIPITATION; LECTINS, C-TYPE; LYSOSOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RECEPTORS, CELL SURFACE; STRUCTURE-ACTIVITY RELATIONSHIP; TYROSINE; UBIQUITINATION; VIRAL PROTEINS;

EID: 84874526441     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058056     Document Type: Article

References (60)

1. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM, (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 332: 1186-1191.
2. 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.
3. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280.
4. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, et al. (1996) Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci U S A 93: 14862-14867.
5. Rimessi P, Bonaccorsi A, Stürzl M, Fabris M, Brocca-Cofano E, et al. (2001) Transcription pattern of human herpesvirus 8 open reading frame K3 in primary effusion lymphoma and Kaposi's sarcoma. J Virol 75: 7161-7174.
6. Sun R, Lin SF, Staskus K, Gradoville L, Grogan E, et al. (1999) Kinetics of Kaposi's sarcoma-associated herpesvirus gene expression. J Virol 73: 2232-2242.
7. Chang H, Dittmer DP, Shin YC, Chul S-Y, Hong Y, et al. (2005) Role of Notch signal transduction in Kaposi's sarcoma-associated herpesvirus gene expression. J Virol 79: 14371-14382.
8. Coscoy L, Ganem D, (2001) A viral protein that selectively downregulates ICAM-1 and B7-2 and modulates T cell costimulation. J Clin Invest 107: 1599-1606.
9. Dodd RB, Allen MD, Brown SE, Sanderson CM, Duncan LM, et al. (2004) Solution structure of the Kaposi's sarcoma-associated herpesvirus K3 N-terminal domain reveals a Novel E2-binding C4HC3-type RING domain. J Biol Chem 279: 53840-53847.
10. Coscoy L, Sanchez DJ, Ganem D, (2001) A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J Cell Biol 155: 1265-1273.
11. Means RE, Lang SM, Jung JU, (2007) The Kaposi's sarcoma-associated herpesvirus K5 E3 ubiquitin ligase modulates targets by multiple molecular mechanisms. J Virol 81: 6573-6583.
12. Navarro-Sanchez E, Altmeyer R, Amara A, Schwartz O, Fieschi F, et al. (2003) Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep 4: 723-728.
13. Ohmura-Hoshino M, Goto E, Matsuki Y, Aoki M, Mito M, et al. (2006) A novel family of membrane-bound E3 ubiquitin ligases. J Biochem 140: 147-154.
14. Ishido S, Choi JK, Lee BS, Wang C, DeMaria M, et al. (2000) Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein. Immunity 13: 365-374.
15. Ishido S, Wang C, Lee BS, Cohen GB, Jung JU, (2000) Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 74: 5300-5309.
16. Mansouri M, Douglas J, Rose PP, Gouveia K, Thomas G, et al. (2006) Kaposi sarcoma herpesvirus K5 removes CD31/PECAM from endothelial cells. Blood 108: 1932-1940.
17. Mansouri M, Rose PP, Moses AV, Früh K, (2008) Remodeling of endothelial adherens junctions by Kaposi's sarcoma-associated herpesvirus. J Virol 82: 9615-9628.
18. Mansouri M, Viswanathan K, Douglas JL, Hines J, Gustin J, et al. (2009) Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol 83: 9672-9681.
19. Sanchez DJ, Gumperz JE, Ganem D, (2005) Regulation of CD1d expression and function by a herpesvirus infection. J Clin Invest 115: 1369-1378.
20. Li Q, Means R, Lang S, Jung JU, (2007) Downregulation of gamma interferon receptor 1 by Kaposi's sarcoma-associated herpesvirus K3 and K5. J Virol 81: 2117-2127.
21. Karki R, Lang SM, Means RE, (2011) The MARCH family E3 ubiquitin ligase K5 alters monocyte metabolism and proliferation through receptor tyrosine kinase modulation. PLoS Pathog 7: e1001331.
22. Means RE, Ishido S, Alvarez X, Jung JU, (2002) Multiple endocytic trafficking pathways of MHC class I molecules induced by a Herpesvirus protein. EMBO J 21: 1638-1649.
23. Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, et al. (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575-585.
24. Granelli-Piperno A, Pritsker A, Pack M, Shimeliovich I, Arrighi J-F, et al. (2005) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J Immunol 175: 4265-4273.
25. Puig-Kröger A, Serrano-Gómez D, Caparrós E, Domínguez-Soto A, Relloso M, et al. (2004) Regulated expression of the pathogen receptor dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin in THP-1 human leukemic cells, monocytes, and macrophages. J Biol Chem 279: 25680-25688.
26. Rappocciolo G, Hensler HR, Jais M, Reinhart TA, Pegu A, et al. (2008) Human herpesvirus 8 infects and replicates in primary cultures of activated B lymphocytes through DC-SIGN. J Virol 82: 4793-4806.
27. Rappocciolo G, Jenkins FJ, Hensler HR, Piazza P, Jais M, et al. (2006) DC-SIGN is a receptor for human herpesvirus 8 on dendritic cells and macrophages. J Immunol 176: 1741-1749.
28. Kerur N, Veettil MV, Sharma-Walia N, Sadagopan S, Bottero V, et al. (2010) Characterization of entry and infection of monocytic THP-1 cells by Kaposi's sarcoma associated herpesvirus (KSHV): role of heparan sulfate, DC-SIGN, integrins and signaling. Virology 406: 103-116.
29. Engering A, Geijtenbeek TBH, van Vliet SJ, Wijers M, van Liempt E, et al. (2002) The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 168: 2118-2126.
30. Geijtenbeek TB, Krooshoop DJ, Bleijs DA, van Vliet SJ, van Duijnhoven GC, et al. (2000) DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol 1: 353-357.
31. Gringhuis SI, den Dunnen J, Litjens M, van der Vlist M, Geijtenbeek TBH, (2009) Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat Immunol 10: 1081-1088.
32. Gringhuis SI, den Dunnen J, Litjens M, van Het Hof B, van Kooyk Y, et al. (2007) C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26: 605-616.
33. Geijtenbeek TBH, den Dunnen J, Gringhuis SI, (2009) Pathogen recognition by DC-SIGN shapes adaptive immunity. Future Microbiol 4: 879-890.
34. Gringhuis SI, van der Vlist M, van den Berg LM, den Dunnen J, Litjens M, et al. (2010) HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat Immunol 11: 419-426.
35. Schneider-Schaulies J, Schneider-Schaulies S, (2008) Receptor interactions, tropism, and mechanisms involved in morbillivirus-induced immunomodulation. Adv Virus Res 71: 173-205.
36. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, et al. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
37. Tailleux L, Schwartz O, Herrmann J-L, Pivert E, Jackson M, et al. (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197: 121-127.
38. Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, et al. (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197: 823-829.
39. Pöhlmann S, Baribaud F, Lee B, Leslie GJ, Sanchez MD, et al. (2001) DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J Virol 75: 4664-4672.
40. Alvarez CP, Lasala F, Carrillo J, Muñiz O, Corbí AL, et al. (2002) C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol 76: 6841-6844.
41. Davis CW, Nguyen H-Y, Hanna SL, Sánchez MD, Doms RW, et al. (2006) West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol 80: 1290-1301.
42. Bashirova AA, Geijtenbeek TB, van Duijnhoven GC, van Vliet SJ, Eilering JB, et al. (2001) A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J Exp Med 193: 671-678.
43. Pöhlmann S, Soilleux EJ, Baribaud F, Leslie GJ, Morris LS, et al. (2001) DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci U S A 98: 2670-2675.
44. Soilleux EJ, (2003) DC-SIGN (dendritic cell-specific ICAM-grabbing non-integrin) and DC-SIGN-related (DC-SIGNR): friend or foe? Clin Sci (Lond) 104: 437-446.
45. Soilleux EJ, Barten R, Trowsdale J, (2000) DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 165: 2937-2942.
46. Vieira J, O'Hearn PM, (2004) Use of the red fluorescent protein as a marker of Kaposi's sarcoma-associated herpesvirus lytic gene expression. Virology 325: 225-240.
47. Brulois KF, Chang H, Lee AS, Ensser A, Wong LY, et al. (2012) Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J Virol 86: 9708-9720.
48. Mansouri M, Douglas J, Rose PP, Gouveia K, Thomas G, et al. (2006) Kaposi sarcoma herpesvirus K5 removes CD31/PECAM from endothelial cells. Blood 108: 1932-1940.
49. Rhodes DA, Boyle LH, Boname JM, Lehner PJ, Trowsdale J, (2010) Ubiquitination of lysine-331 by Kaposi's sarcoma-associated herpesvirus protein K5 targets HFE for lysosomal degradation. Proc Natl Acad Sci U S A 107: 16240-16245.
50. Coscoy L, Ganem D, (2000) Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc Natl Acad Sci U S A 97: 8051-8056.
51. Geijtenbeek TBH, van Kooyk Y, (2003) Pathogens target DC-SIGN to influence their fate DC-SIGN functions as a pathogen receptor with broad specificity. APMIS 111: 698-714.
52. Geijtenbeek TBH, Van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CMJE, et al. (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197: 7-17.
53. Kong K-F, Delroux K, Wang X, Qian F, Arjona A, et al. (2008) Dysregulation of TLR3 impairs the innate immune response to West Nile virus in the elderly. J Virol 82: 7613-7623.
54. Aiken C, Konner J, Landau NR, Lenburg ME, Trono D, (1994) Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76: 853-864.
55. Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, et al. (2010) The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS Pathog 6: e1000843.
56. Boname JM, de Lima BD, Lehner PJ, Stevenson PG, (2004) Viral degradation of the MHC class I peptide loading complex. Immunity 20: 305-317.
57. Boname JM, May JS, Stevenson PG, (2005) The murine gamma-herpesvirus-68 MK3 protein causes TAP degradation independent of MHC class I heavy chain degradation. Eur J Immunol 35: 171-179.
58. Cadwell K, Coscoy L, (2005) Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309: 127-130.
59. Lybarger L, Wang X, Harris MR, Virgin HW, Hansen TH, (2003) Virus subversion of the MHC class I peptide-loading complex. Immunity 18: 121-130.
60. Cadwell K, Coscoy L, (2008) The specificities of Kaposi's sarcoma-associated herpesvirus-encoded E3 ubiquitin ligases are determined by the positions of lysine or cysteine residues within the intracytoplasmic domains of their targets. J Virol 82: 4184-4189.