CCR6 Functions as a New Coreceptor for Limited Primary Human and Simian Immunodeficiency Viruses

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Islam, Salequl ^a,d   Shimizu, Nobuaki ^a   Hoque, Sheikh Ariful ^a,b   Jinno Oue, Atsushi ^a   Tanaka, Atsushi ^c   Hoshino, Hiroo ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF DHAKA   (Bangladesh)

^c OSAKA UNIVERSITY   (Japan)

^d JAHANGIRNAGAR UNIVERSITY   (Bangladesh)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR6; RNA DIRECTED DNA POLYMERASE; VIRUS ANTIGEN; VIRUS DNA;

AMINO ACID SUBSTITUTION; ARTICLE; CD4+ T LYMPHOCYTE; CLONAL SPECIES; CONTROLLED STUDY; DENDRITIC CELL; DISEASE PREDISPOSITION; DNA DETERMINATION; DNA SEQUENCE; ENZYME ASSAY; GIEMSA STAIN; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS CELL INTERACTION; VIRUS CULTURE; VIRUS ENVELOPE; VIRUS LATENCY; VIRUS PATHOGENESIS; VIRUS RELEASE; VIRUS RESISTANCE; VIRUS TRANSMISSION;

AMINO ACID SEQUENCE; ANTIGENS, CD4; CELL LINE; CYTOPATHOGENIC EFFECT, VIRAL; GENE EXPRESSION; GIANT CELLS; HIV; HUMANS; MOLECULAR SEQUENCE DATA; PROVIRUSES; RECEPTORS, CCR5; RECEPTORS, CCR6; RECEPTORS, CXCR4; RECEPTORS, HIV; RNA, MESSENGER; SEQUENCE ALIGNMENT; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 84883213124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073116     Document Type: Article

References (58)

1. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, et al. (1984) The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312: 763-767. doi:10.1038/312763a0. PubMed: 6096719.
2. Feng Y, Broder CC, Kennedy PE, Berger EA, (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272: 872-877. doi:10.1126/science.272.5263.872. PubMed: 8629022.
3. Smith AE, Helenius A, (2004) How viruses enter animal cells. Science 304: 237-242. doi:10.1126/science.1094823. PubMed: 15073366.
4. Rucker J, Edinger AL, Sharron M, Samson M, Lee B, et al. (1997) Utilization of chemokine receptors, orphan receptors, and herpesvirus-encoded receptors by diverse human and simian immunodeficiency viruses. J Virol 71: 8999-9007. PubMed: 9371556.
5. Gorry PR, Ancuta P, (2011) Coreceptors and HIV-1 pathogenesis. Curr HIV/AIDS Rep 8: 45-53. doi:10.1007/s11904-010-0069-x. PubMed: 21188555.
6. Shimizu N, Tanaka A, Oue A, Mori T, Ohtsuki T, et al. (2009) Broad usage spectrum of G protein-coupled receptors as coreceptors by primary isolates of HIV. AIDS 23: 761-769. PubMed: 19307942.
7. Isaacman-Beck J, Hermann EA, Yi Y, Ratcliffe SJ, Mulenga J, et al. (2009) Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization. J Virol 83: 8208-8220. doi:10.1128/JVI.00296-09. PubMed: 19515785.
8. Riddick NE, Hermann EA, Loftin LM, Elliott ST, Wey WC, et al. (2010) A novel CCR5 mutation common in sooty mangabeys reveals SIVsmm infection of CCR5-null natural hosts and efficient alternative coreceptor use in vivo. PLOS Pathog 6: e1001064.
9. Nedellec R, Coetzer M, Shimizu N, Hoshino H, Polonis VR, et al. (2009) Virus entry via the alternative coreceptors CCR3 and FPRL1 differs by human immunodeficiency virus type 1 subtype. J Virol 83: 8353-8363. doi:10.1128/JVI.00780-09. PubMed: 19553323.
10. Liao F, Lee HH, Farber JM, (1997) Cloning of STRL22, a new human gene encoding a G-protein-coupled receptor related to chemokine receptors and located on chromosome 6q27. Genomics 40: 175-180. doi:10.1006/geno.1996.4544. PubMed: 9070937.
11. Steinfelder S, Floess S, Engelbert D, Haeringer B, Baron U, et al. (2011) Epigenetic modification of the human CCR6 gene is associated with stable CCR6 expression in T cells. Blood 117: 2839-2846. doi:10.1182/blood-2010-06-293027. PubMed: 21228329.
12. Kleinewietfeld M, Puentes F, Borsellino G, Battistini L, Rötzschke O, et al. (2005) CCR6 expression defines regulatory effector/memory-like cells within the CD25(+)CD4+ T-cell subset. Blood 105: 2877-2886. doi:10.1182/blood-2004-07-2505. PubMed: 15613550.
13. Liao F, Rabin RL, Smith CS, Sharma G, Nutman TB, et al. (1999) CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J Immunol 162: 186-194. PubMed: 9886385.
14. Gosselin A, Monteiro P, Chomont N, Diaz-Griffero F, Said EA, et al. (2010) Peripheral blood CCR4+CCR6+ and CXCR3+CCR6+CD4+ T cells are highly permissive to HIV-1 infection. J Immunol 184: 1604-1616. doi:10.4049/jimmunol.0903058. PubMed: 20042588.
15. Soda Y, Shimizu N, Jinno A, Liu HY, Kanbe K, et al. (1999) Establishment of a new system for determination of coreceptor usages of HIV based on the human glioma NP-2 cell line. Biochem Biophys Res Commun 258: 313-321. doi:10.1006/bbrc.1999.0633. PubMed: 10329384.
16. Hoshino H, Esumi H, Miwa M, Shimoyama M, Minato K, et al. (1983) Establishment and characterization of 10 cell lines derived from patients with adult T-cell leukemia. Proc Natl Acad Sci U S A 80: 6061-6065. doi:10.1073/pnas.80.19.6061. PubMed: 6193528.
17. Schneider U, van Lessen A, Huhn D, Serke S, (1997) Two subsets of peripheral blood plasma cells defined by differential expression of CD45 antigen. Br J Haematol 97: 56-64. doi:10.1046/j.1365-2141.1997.d01-2115.x. PubMed: 9136942.
18. Klein E, Klein G, Nadkarni JS, Nadkarni JJ, Wigzell H, et al. (1968) Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res 28: 1300-1310. PubMed: 4174339.
19. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J, (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-3863. PubMed: 6286115.
20. Knowles BB, Howe CC, Aden DP, (1980) Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209: 497-499. doi:10.1126/science.6248960. PubMed: 6248960.
21. Nolan GP, Shatzman AR, (1998) Expression vectors and delivery systems. Curr Opin Biotechnol 9: 447-450. doi:10.1016/S0958-1669(98)80027-X. PubMed: 9821270.
22. Shimizu NS, Shimizu NG, Takeuchi Y, Hoshino H, (1994) Isolation and characterization of human immunodeficiency virus type 1 variants infectious to brain-derived cells: detection of common point mutations in the V3 region of the env gene of the variants. J Virol 68: 6130-6135. PubMed: 7980782.
23. Ratner L, Fisher A, Jagodzinski LL, Liou RS, Mitsuya H, et al. (1987) Complete nucleotide sequences of functional clones of the virus associated with the acquired immunodeficiency syndrome, HTLV-III/LAV. Haematol Blood Transfus 31: 404-406. PubMed: 3443402.
24. Yamaguchi K, Byrn RA, (1995) Clinical isolates of HIV-1 contain few pre-existing proteinase inhibitor resistance-conferring mutations. Biochim Biophys Acta 1253: 136-140. doi:10.1016/0167-4838(95)00167-1. PubMed: 8519793.
25. Shimizu N, Tanaka A, Oue A, Mori T, Apichartpiyakul C, et al. (2008) A short amino acid sequence containing tyrosine in the N-terminal region of G protein-coupled receptors is critical for their potential use as co-receptors for human and simian immunodeficiency viruses. J Gen Virol 89: 3126-3136. doi:10.1099/vir.0.2008/002188-0. PubMed: 19008402.
26. Islam S, Hoque SA, Adnan N, Tanaka A, Jinno-Oue A, et al. (2013) X4-Tropic Human Immunodeficiency Virus (HIV), IIIB Utilizes CXCR4 As Coreceptor Distinctly From R5 x 4-Tropic Viruses. Microbiol Immunol. doi:10.1111/j.1348-0421.12051.
27. Shimizu N, Gojobori T, (2000) How can human and simian immunodeficiency viruses utilize chemokine receptors as their coreceptors? Gene 259: 199-205. doi:10.1016/S0378-1119(00)00432-7. PubMed: 11163977.
28. Jinno A, Shimizu N, Soda Y, Haraguchi Y, Kitamura T, et al. (1998) Identification of the chemokine receptor TER1/CCR8 expressed in brain-derived cells and T cells as a new coreceptor for HIV-1 infection. Biochem Biophys Res Commun 243: 497-502. doi:10.1006/bbrc.1998.8130. PubMed: 9480837.
29. Johnson PR, Hirsch VM, (1992) Genetic variation of simian immunodeficiency viruses in nonhuman primates. AIDS Res Hum Retrovir 8: 367-372. doi:10.1089/aid.1992.8.367. PubMed: 1571196.
30. Dehghani H, Puffer BA, Doms RW, Hirsch VM, (2003) Unique pattern of convergent envelope evolution in simian immunodeficiency virus-infected rapid progressor macaques: association with CD4-independent usage of CCR5. J Virol 77: 6405-6418. doi:10.1128/JVI.77.11.6405-6418.2003. PubMed: 12743298.
31. Ai LS, Lee SF, Chen SS, Liao F, (2004) Molecular characterization of CCR6: involvement of multiple domains in ligand binding and receptor signaling. J Biomed Sci 11: 818-828. doi:10.1007/BF02254367. PubMed: 15591779.
32. Hoque SA, Ohtsuki T, Tatsumi M, Shimizu N, Islam S, et al. (2012) Lack of the trans-receptor mechanism of HIV-1 infection: CD4- and coreceptor-independent incorporation of HIV-1-resistant cells into syncytia induced by HIV-1. Microbes Infect 14: 357-368. doi:10.1016/j.micinf.2011.11.005. PubMed: 22178016.
33. Popovic M, Sarngadharan MG, Read E, Gallo RC, (1984) Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 224: 497-500. doi:10.1126/science.6200935. PubMed: 6200935.
34. Sylwester A, Wessels D, Anderson SA, Warren RQ, Shutt DC, et al. (1993) HIV-induced syncytia of a T cell line form single giant pseudopods and are motile. J Cell Sci 106(3):: 941-953.
35. Shimizu N, Tanaka A, Mori T, Ohtsuki T, Hoque A, et al. (2008) A formylpeptide receptor, FPRL1, acts as an efficient coreceptor for primary isolates of human immunodeficiency virus. Retrovirology 5: 52. doi:10.1186/1742-4690-5-52. PubMed: 18577234.
36. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, et al. (1996) A dual-tropic primary HIV-1 isolate that uses fusion and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85: 1149-1158. doi:10.1016/S0092-8674(00)81314-8. PubMed: 8674120.
37. Deng HK, Unutmaz D, KewalRamani VN, Littman DR, (1997) Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388: 296-300. doi:10.1038/40894. PubMed: 9230441.
38. Kanbe K, Shimizu N, Soda Y, Takagishi K, Hoshino H, (1999) A CXC chemokine receptor, CXCR5/BLR1, is a novel and specific coreceptor for human immunodeficiency virus type 2. Virology 265: 264-273. doi:10.1006/viro.1999.0036. PubMed: 10600598.
39. Liao F, Alkhatib G, Peden KW, Sharma G, Berger EA, et al. (1997) STRL33, A novel chemokine receptor-like protein, functions as a fusion cofactor for both macrophage-tropic and T cell line-tropic HIV-1. J Exp Med 185: 2015-2023. doi:10.1084/jem.185.11.2015. PubMed: 9166430.
40. Shimizu N, Sekine T, Itoh K, Nakamura T, Iwamoto A, et al. (2000) Large-scale ex vivo expansion of primary T lymphocytes in late-stage AIDS patients. AIDS Res Hum Retrovir 16: 611-612. doi:10.1089/088922200309034. PubMed: 10777152.
41. Combadiere C, Salzwedel K, Smith ED, Tiffany HL, Berger EA, et al. (1998) Identification of CX3CR1. A chemotactic receptor for the human CX3C chemokine fractalkine and a fusion coreceptor for HIV-1. J Biol Chem 273: 23799-23804. doi:10.1074/jbc.273.37.23799. PubMed: 9726990.
42. Neil SJ, Aasa-Chapman MM, Clapham PR, Nibbs RJ, McKnight A, et al. (2005) The promiscuous CC chemokine receptor D6 is a functional coreceptor for primary isolates of human immunodeficiency virus type 1 (HIV-1) and HIV-2 on astrocytes. J Virol 79: 9618-9624. doi:10.1128/JVI.79.15.9618-9624.2005. PubMed: 16014924.
43. Choe H, Farzan M, Konkel M, Martin K, Sun Y, et al. (1998) The orphan seven-transmembrane receptor apj supports the entry of primary T-cell-line-tropic and dualtropic human immunodeficiency virus type 1. J Virol 72: 6113-6118. PubMed: 9621075.
44. Shimizu N, Soda Y, Kanbe K, Liu HY, Jinno A, et al. (1999) An orphan G protein-coupled receptor, GPR1, acts as a coreceptor to allow replication of human immunodeficiency virus types 1 and 2 in brain-derived cells. J Virol 73: 5231-5239. PubMed: 10233994.
45. Zaballos A, Varona R, Gutiérrez J, Lind P, Márquez G, (1996) Molecular cloning and RNA expression of two new human chemokine receptor-like genes. Biochem Biophys Res Commun 227: 846-853. doi:10.1006/bbrc.1996.1595. PubMed: 8886020.
46. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, et al. (2008) Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112: 2826-2835. doi:10.1182/blood-2008-05-159301. PubMed: 18664624.
47. Lafferty MK, Sun L, DeMasi L, Lu W, Garzino-Demo A, (2010) CCR6 ligands inhibit HIV by inducing APOBEC3G. Blood 115: 1564-1571. doi:10.1182/blood-2009-06-226423. PubMed: 20023216.
48. Elliott ST, Riddick NE, Francella N, Paiardini M, Vanderford TH, et al. (2012) Cloning and analysis of sooty mangabey alternative coreceptors that support simian immunodeficiency virus SIVsmm entry independently of CCR5. J Virol 86: 898-908. doi:10.1128/JVI.06415-11. PubMed: 22090107.
49. Farzan M, Choe H, Vaca L, Martin K, Sun Y, et al. (1998) A tyrosine-rich region in the N terminus of CCR5 is important for human immunodeficiency virus type 1 entry and mediates an association between gp120 and CCR5. J Virol 72: 1160-1164. PubMed: 9445013.
50. Doranz BJ, Lu ZH, Rucker J, Zhang TY, Sharron M, et al. (1997) Two distinct CCR5 domains can mediate coreceptor usage by human immunodeficiency virus type 1. J Virol 71: 6305-6314. PubMed: 9261347.
51. Reeves JD, Heveker N, Brelot A, Alizon M, Clapham PR, et al. (1998) The second extracellular loop of CXCR4 is involved in CD4-independent entry of human immunodeficiency virus type 2. J Gen Virol 79(Pt 7):: 1793-1799. PubMed: 9680144.
52. Huang CC, Tang M, Zhang MY, Majeed S, Montabana E, et al. (2005) Structure of a V3-containing HIV-1 gp120 core. Science 310: 1025-1028. doi:10.1126/science.1118398. PubMed: 16284180.
53. Hwang SS, Boyle TJ, Lyerly HK, Cullen BR, (1991) Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253: 71-74. doi:10.1126/science.1905842. PubMed: 1905842.
54. Burns DP, Desrosiers RC, (1991) Selection of genetic variants of simian immunodeficiency virus in persistently infected rhesus monkeys. J Virol 65: 1843-1854. PubMed: 2002545.
55. Javaherian K, Langlois AJ, Schmidt S, Kaufmann M, Cates N, et al. (1992) The principal neutralization determinant of simian immunodeficiency virus differs from that of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 89: 1418-1422. doi:10.1073/pnas.89.4.1418. PubMed: 1371358.
56. Fortgang IS, Rege T, Baskin GB, Murphey-Corb M, Levy LS, (2001) Variation in simian immunodeficiency virus env V1 region in simian AIDS-associated lymphoma. AIDS Res Hum Retrovir 17: 459-465. doi:10.1089/088922201750102580. PubMed: 11282015.
57. Almond N, Jenkins A, Heath AB, Kitchin P, (1993) Sequence variation in the env gene of simian immunodeficiency virus recovered from immunized macaques is predominantly in the V1 region. J Gen Virol 74(5):: 865-871. doi:10.1099/0022-1317-74-5-865. PubMed: 8492090.
58. Ancuta P, Monteiro P, Sekaly RP, (2010) Th17 lineage commitment and HIV-1 pathogenesis. Curr Opin HIV Aids 5: 158-165. doi:10.1097/COH.0b013e3283364733. PubMed: 20543594.