A novel synthetic bivalent ligand to probe chemokine receptor CXCR4 dimerization and inhibit HIV-1 entry

Biochemistry

Volumn 51, Issue 36, 2012, Pages 7078-7086

  Choi, Won Tak ^a,b   Kumar, Santhosh ^a   Madani, Navid ^c   Han, Xiaofeng ^d   Tian, Shaomin ^a   Dong, Chang Zhi ^a   Liu, Dongxiang ^a   Duggineni, Srinivas ^d   Yuan, Jian ^a   Sodroski, Joseph G ^c   Huang, Ziwei ^d   An, Jing ^d  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINUS; ANTIVIRAL ACTIVITIES; BINDING AFFINITIES; BINDING POCKETS; BIVALENT LIGANDS; CHEMOKINE RECEPTOR CXCR4; CORECEPTORS; CYSTEINE RESIDUES; DIMERIC MOLECULES; DIMERIC STRUCTURE; DISULFIDE BONDS; EXTRACELLULAR; HETERODIMERIZATION; HOMODIMERS; LIGAND-BINDING SITES; PEPTIDE SEQUENCES; TARGET CELLS; TRANSMEMBRANES;

AMINO ACIDS; BINDING ENERGY; BINDING SITES; COVALENT BONDS; CRYSTAL STRUCTURE; DIMERIZATION; LIGANDS; MONOMERS; PEPTIDES;

DIMERS;

CHEMOKINE RECEPTOR CXCR4; CYSTEINE; DV1 PEPTIDE; PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DISULFIDE BOND; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; VIRUS ENTRY;

DRUG DESIGN; HIV ENVELOPE PROTEIN GP120; HIV-1; LIGANDS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84866065396     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2016712     Document Type: Article

References (58)

1. Murphy, P. M. (1994) The molecular biology of leukocyte chemoattractant receptors Annu. Rev. Immunol. 12, 593-633 (Pubitemid 24140426)
2. Kobilka, B. (1992) Adrenergic receptors as models for G protein-coupled receptors Annu. Rev. Neurosci. 15, 87-114
3. Strader, C. D., Fong, T. M., Tota, M. R., and Underwood, D. (1994) Structure and function of G protein-coupled receptors Annu. Rev. Biochem. 63, 101-132 (Pubitemid 24218630)
4. Choi, W. T., Duggineni, S., Xu, Y., Huang, Z., and An, J. (2012) Drug discovery research targeting the CXC chemokine receptor 4 (CXCR4) J. Med. Chem. 55, 977-994
5. Baggiolini, M., Dewald, B., and Moser, B. (1997) Human chemokines: An update Annu. Rev. Immunol. 15, 675-705 (Pubitemid 27169296)
6. Berger, E. A., Murphy, P. M., and Farber, J. M. (1999) Chemokine receptors as HIV-1 coreceptors: Roles in viral entry, tropism, and disease Annu. Rev. Immunol. 17, 657-700 (Pubitemid 29241137)
7. Proudfoot, A. (2002) Chemokine receptors: Multifaceted therapeutic targets Nat. Rev. Immunol. 2, 106-115 (Pubitemid 37323234)
8. Feng, Y., Broder, C. C., Kennedy, P. E., and Berger, E. A. (1996) HIV-1 entry cofactor: Functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor Science 272, 872-877 (Pubitemid 26154590)
9. Hill, C. M. and Littman, D. R. (1996) Natural resistance to HIV? Nature 382, 668-669 (Pubitemid 26282153)
10. Trkola, A., Dragic, T., Arthos, J., Binley, J. M., Olson, W. C., Allaway, G. P., Cheng-Mayer, C., Robinson, J., Maddon, P. J., and Moore, J. P. (1996) CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR5 Nature 384, 184-187 (Pubitemid 26386476)
11. Wu, L., Gerard, N. P., Wyatt, R., Choe, H., Parolin, C., Ruffing, N., Borsetti, A., Cardoso, A. A., Desjardin, E., Newman, W., Gerard, C., and Sodroski, J. (1996) CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR5 Nature 384, 179-183 (Pubitemid 26386475)
12. Alkhatib, G., Combadiere, C., Broder, C. C., Feng, Y., Kennedy, P. E., and Murphy, P. M. (1996) CC CKR5: A RANTES, MIP-1α, MIP-1β receptor as a fusion cofactor for macrophage-tropic HIV-1 Science 272, 1955-1958 (Pubitemid 26234510)
13. Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M., Marzio, P. D., Marmon, S., Sutton, R. E., Hill, C. M., Davis, C. B., Peiper, S. C., Schall, T. J., Littman, D. R., and Landau, N. R. (1996) Identification of a major co-receptor for primary isolates of HIV-1 Nature 381, 661-666 (Pubitemid 26197679)
14. Dragic, T., Litwin, V., Allaway, G. P., Martin, S. R., Huang, Y., Nagashima, K. A., Cayanan, C., Maddon, P. J., Koup, R. A., Moore, J. P., and Paxton, W. A. (1996) HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5 Nature 381, 667-673 (Pubitemid 26197680)
15. Cheng-Mayer, C., Seto, D., Tateno, M., and Levy, J. A. (1988) Biologic features of HIV-1 that correlate with virulence in the host Science 240, 80-82
16. Tersmette, M., Lange, J. M., de Goede, R. E., de Wolf, F., Eeftink-Schattenkerk, J. K., Schellekens, P. T., Coutinho, R. A., Huisman, J. G., Goudsmit, J., and Miedema, F. (1989) Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality Lancet 1, 983-985 (Pubitemid 19123574)
17. Schellekens, P. T., Tersmette, M., Roos, M. T., Keet, R. P., de Wolf, F., Coutinho, R. A., and Miedema, F. (1992) Biphasic rate of CD4+ cell count decline during progression to AIDS correlates with HIV-1 phenotype AIDS 6, 665-669
18. Bleul, C. C., Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., and Sodroski, J. (1996) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry Nature 382, 829-833 (Pubitemid 26299570)
19. Oberlin, E., Amara, A., Bachelerie, F., Bessia, C., Virelizier, J. L., Arenzana-Seisdedos, F., Schwartz, O., Heard, J. M., Clark-Lewis, I., Legler, D. F., Loetscher, M., Baggiolini, M., and Moser, B. (1996) The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1 Nature 382, 833-835 (Pubitemid 26299571)
20. Oravecz, T., Pall, M., and Norcross, M. A. (1996) β-Chemokine inhibition of monocytotropic HIV-1 infection. Interference with a postbinding fusion step J. Immunol. 157, 1329-1332 (Pubitemid 126449067)
21. Arenzana-Seisdedos, F., Virelizier, J. L., Rousset, D., Clark-Lewis, I., Loetscher, P., Moser, B., and Baggiolini, M. (1996) HIV blocked by chemokine antagonist Nature 383, 400 (Pubitemid 26330820)
22. Amara, A., Gall, S. L., Schwartz, O., Salamero, J., Montes, M., Loetscher, P., Baggiolini, M., Virelizier, J.-L., and Arenzana-Seisdedos, F. (1997) HIV coreceptor downregulation as antiviral principle: SDF-1α-dependent internalization of the chemokine receptor CXCR4 contributes to inhibition of HIV replication J. Exp. Med. 186, 139-146 (Pubitemid 27304856)
23. Förster, R., Kremmer, E., Schubel, A., Breitfeld, D., Kleinschmidt, A., Nerl, C., Bernhardt, G., and Lipp, M. (1998) Intracellular and surface expression of the HIV-1 coreceptor CXCR4/fusin on various leukocyte subsets: Rapid internalization and recycling upon activation J. Immunol. 160, 1522-1531 (Pubitemid 28093457)
24. Prinster, S. C., Hague, C., and Hall, R. A. (2005) Heterodimerization of G-protein-coupled receptors: Specificity and functional significance Pharmacol. Rev. 57, 289-298 (Pubitemid 41196951)
25. Bouvier, M. (2001) Oligomerization of G-protein-coupled transmitter receptors Nat. Rev. Neurosci. 2, 274-286 (Pubitemid 33673068)
26. White, J. H., Wise, A., Main, M. J., Green, A., Fraser, N. J., Disney, G. H., Barnes, A. A., Emson, P., Foord, S. M., and Marshall, F. H. (1998) Heterodimerization is required for the formation of a functional GABA(B) receptor Nature 396, 679-682 (Pubitemid 29003946)
27. Kaupmann, K., Malitschek, B., Schuler, V., Heid, J., Froestl, W., Beck, P., Mosbacher, J., Bischoff, S., Kulik, A., Shigemoto, R., Karschin, A., and Bettler, B. (1998) GABA(B)-receptor subtypes assemble into functional heteromeric complexes Nature 396, 683-687 (Pubitemid 29003947)
28. Jones, K. A., Borowsky, B., Tamm, J. A., Craig, D. A., Durkin, M. M., Dai, M., Yao, W. J., Johnson, M., Gunwaldsen, C., Huang, L. Y., Tang, C., Shen, Q., Salon, J. A., Morse, K., Laz, T., Smith, K. E., Nagarathnam, D., Noble, S. A., Branchek, T. A., and Gerald, C. (1998) GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2 Nature 396, 674-679 (Pubitemid 29003945)
29. Benkirane, M., Jin, D. Y., Chun, R. F., Koup, R. A., and Jeang, K. T. (1997) Mechanism of transdominant inhibition of CCR5-mediated HIV-1 infection by ccr5delta32 J. Biol. Chem. 272, 30603-30606 (Pubitemid 27527488)
30. Vila-Coro, A. J., Mellado, M., Martín de Ana, A., Lucas, P., del Real, G., Martínez-A, C., and Rodríguez-Frade, J. M. (2000) HIV-1 infection through the CCR5 receptor is blocked by receptor dimerization Proc. Natl. Acad. Sci. U.S.A. 97, 3388-3393 (Pubitemid 30183312)
31. Babcock, G. J., Farzan, M., and Sodroski, J. (2003) Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor J. Biol. Chem. 278, 3378-3385 (Pubitemid 36801253)
32. Percherancier, Y., Berchiche, Y. A., Slight, I., Volkmer-Engert, R., Tamamura, H., Fujii, N., Bouvier, M., and Heveker, N. (2005) Bioluminescence resonance energy transfer reveals ligand-induced conformational changes in CXCR4 homo- and heterodimers J. Biol. Chem. 280, 9895-9903 (Pubitemid 40395837)
33. Veldkamp, C. T., Seibert, C., Peterson, F. C., De la Cruz, N. B., Haugner, J. C., III, Basnet, H., Sakmar, T. P., and Volkman, B. F. (2008) Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12 Sci. Signaling 16, 37
34. Hernandez, P. A., Gorlin, R. J., Lukens, J. N., Taniuchi, S., Bohinjec, J., Francois, F., Klotman, M. E., and Diaz, G. A. (2003) Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease Nat. Genet. 34, 70-74 (Pubitemid 36548793)
35. Lagane, B., Chow, K. Y., Balabanian, K., Levoye, A., Harriague, J., Planchenault, T., Baleux, F., Gunera-Saad, N., Arenzana-Seisdedos, F., and Bachelerie, F. (2008) CXCR4 dimerization and β-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome Blood 112, 34-44
36. Luo, Z., Fan, X., Zhou, N., Hiraoka, M., Luo, J., Kaji, H., and Huang, Z. (2000) Structure-function study and anti-HIV activity of synthetic peptide analogues derived from viral chemokine vMIP-II Biochemistry 39, 13545-13550
37. Zhou, N., Luo, Z., Luo, J., Fan, X., Cayabyab, M., Hiraoka, M., Liu, D., Han, X., Pesavento, J., Dong, C. Z., Wang, Y., An, J., Kaji, H., Sodroski, J. G., and Huang, Z. (2002) Exploring the stereochemistry of CXCR4-peptide recognition and inhibiting HIV-1 entry with d -peptides derived from chemokines J. Biol. Chem. 277, 17476-17485 (Pubitemid 34967547)
38. Daniels, D. J., Lenard, N. R., Etienne, C. L., Law, P. Y., Roerig, S. C., and Portoghese, P. S. (2005) Opioid-induced tolerance and dependence in mice is modulated by the distance between pharmacophores in a bivalent ligand series Proc. Natl. Acad. Sci. U.S.A. 102, 19208-19213 (Pubitemid 43049591)
39. George, S. R., O'Dowd, B. F., and Lee, S. P. (2002) G-protein-coupled receptor oligomerization and its potential for drug discovery Nat. Rev. Drug Discovery 1, 808-820 (Pubitemid 37361564)
40. Messer, W. S. J. (2004) Bivalent ligands for G protein-coupled receptors Curr. Pharm. Des. 10, 2015-2020
41. Kiessling, L. L., Gestwicki, J. E., and Strong, L. E. (2006) Synthetic multivalent ligands as probes of signal transduction Angew. Chem., Int. Ed. 45, 2348-2368 (Pubitemid 44105109)
42. Tian, S., Choi, W. T., Liu, D., Pesavento, J., Wang, Y., An, J., Sodroski, J. G., and Huang, Z. (2005) Distinct functional sites for human immunodeficiency virus type 1 and stromal cell-derived factor 1a on CXCR4 transmembrane helical domains J. Virol. 79, 12667-12673 (Pubitemid 41433186)
43. Choi, W. T., Tian, S., Dong, C. Z., Kumar, S., Liu, D., Madani, N., An, J., Sodroski, J. G., and Huang, Z. (2005) Unique ligand binding sites on CXCR4 probed by a chemical biology approach: Implications for the design of selective human immunodeficiency virus type 1 inhibitors J. Virol. 79, 15398-15404 (Pubitemid 43032322)
44. Kumar, S., Choi, W. T., Dong, C. Z., Madani, N., Tian, S., Liu, D., Wang, Y., Pesavento, J., Wang, J., Fan, X., Yuan, J., Fritzsche, W. R., An, J., Sodroski, J. G., Richman, D. D., and Huang, Z. (2006) SMM-Chemokines: A class of unnatural synthetic molecules as chemical probes of chemical receptor biology and leads for therapeutic development Chem. Biol. 13, 69-79 (Pubitemid 43102581)
45. Zhou, N. L., Luo, Z., Fan, J., Cayabyab, X., Hiraoka, M., Liu, D., Han, X., Pesavento, J., Dong, C. Z., Wang, Y., An, J., Kaji, H., Sodroski, J. G., and Huang, Z. (2002) Exploring the stereochemistry of CXCR4-peptide recognition and inhibiting HIV-1 entry with d -peptides derived from chemokines J. Biol. Chem. 277, 17476-17485 (Pubitemid 34967547)
46. Dong, C. Z., Kumar, S., Choi, W. T., Madani, N., Tian, S., An, J., Sodroski, J. G., and Huang, Z. (2005) Different stereochemical requirements for CXCR4 binding and signaling functions as revealed by an anti-HIV, d -amino acid-containing SMM-chemokine ligand J. Med. Chem. 48, 7923-7924 (Pubitemid 41798424)
47. Chen, S. S., Lee, S. F., Hao, H. J., and Chuang, C. K. (1998) Mutations in the leucine zipper-like heptad repeat sequence of human immunodeficiency virus type 1 gp41 dominantly interfere with wild-type virus infectivity J. Virol. 72, 4765-4774 (Pubitemid 28215652)
48. Platt, E. J., Wehrly, K., Kuhmann, S. E., Chesebro, B., and Kabat, D. (1998) Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1 J. Virol. 72, 2855-2864 (Pubitemid 28175522)
49. LiWang, A. C., Cao, J. J., Zheng, H., Lu, Z., Peiper, S. C., and LiWang, P. J. (1999) Dynamics study on the anti-human immunodeficiency virus chemokine viral macrophage-inflammatory protein-II (VMIP-II) reveals a fully monomeric protein Biochemistry 38, 442-453 (Pubitemid 29035715)
50. Demmer, O., Dijkgraaf, I., Schumacher, U., Marinelli, L., Cosconati, S., Wester, H. J., and Kessler, H. (2011) Design, synthesis and functionalization of dimeric peptides targetting chemokine receptor CXCR4 J. Med. Chem. 54, 7648-7662
51. Wu, B., Chien, E. Y., Mol, C. D., Fenalti, G., Liu, W., Katritch, V., Abagyan, R., Brooun, A., Wells, P., Bi, F. C., Hamel, D. J., Kuhn, P., Handel, T. M., Cherezov, V., and Stevens, R. C. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 330, 1066-1071
52. Turner, S., Tizard, R., DeMarinis, J., Pepinsky, R. B., Zullo, J., Schooley, R., and Fisher, R. (1992) Resistance of primary isolates of human immunodeficiency virus type 1 to neutralization by soluble CD4 is not due to lower affinity with the viral envelope glycoprotein gp120 Proc. Natl. Acad. Sci. U.S.A. 89, 1335-1339
53. Peden, K., Emerman, M., and Montagnier, L. (1991) Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI Virology 185, 661-672
54. Brelot, A., Heveker, N., Pleskoff, O., Sol, N., and Alizon, M. (1997) Role of the first and third extracellular domains of CXCR-4 in human immunodeficiency virus coreceptor activity J. Virol. 71, 4744-4751 (Pubitemid 27204167)
55. Doranz, B., Orsini, M., Turner, J., Hoffman, T., Berson, J., Hoxie, J., Peiper, S., Brass, L., and Doms, R. (1999) Identification of CXCR4 domains that support coreceptor and chemokine receptor functions J. Virol. 73, 2752-2761 (Pubitemid 29135661)
56. Chabot, D. J., Zhang, P. F., Quinnan, G. V., and Broder, C. C. (1999) Mutagenesis of CXCR4 identifies important domains for human immunodeficiency virus type 1 X4 isolate envelope-mediated membrane fusion and virus entry and reveals cryptic coreceptor activity for R5 isolates J. Virol. 73, 6598-6609 (Pubitemid 29327842)
57. Zhou, N., Luo, Z., Luo, J., Liu, D., Hall, J. W., Pomerantz, R. J., and Huang, Z. (2001) Structural and functional characterization of human CXCR4 as a chemokine receptor and HIV-1 co-receptor by mutagenesis and molecular modeling studies J. Biol. Chem. 276, 42826-42833
58. Tanaka, T., Nomura, W., Narumi, T., Masuda, A., and Tamamura, H. (2010) Bivalent ligands of CXCR4 with rigid linkers for elucidation of the dimerization state in cells J. Am. Chem. Soc. 132, 15899-15901