HIV-1 capsids bind and exploit the kinesin-1 adaptor FEZ1 for inward movement to the nucleus

Nature Communications

Volumn 6, Issue , 2015, Pages

  Malikov, Viacheslav ^a,b   Da Silva, Eveline Santos ^a   Jovasevic, Vladimir ^a   Bennett, Geoffrey ^b,d   De Souza Aranha Vieira, Daniel A ^c   Schulte, Bianca ^c   Diaz Griffero, Felipe ^c   Walsh, Derek ^a   Naghavi, Mojgan H ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Columbia University ^*  (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; ELONGATION FACTOR; ELONGATION FACTOR ZETA 1 PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; KINESIN 1; MOLECULAR MOTOR; UNCLASSIFIED DRUG; VIRUS DNA; FEZ1 PROTEIN, HUMAN; KIF5B PROTEIN, HUMAN; KINESIN; NERVE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN; RNA;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FASCICULATION; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; INTRACELLULAR TRANSPORT; NEUROBLASTOMA CELL; NONHUMAN; PHASE 4 CLINICAL TRIAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; TRANS GOLGI NETWORK; VIRUS CAPSID; VIRUS ENTRY; VIRUS PARTICLE; CELL LINE; CELL NUCLEUS; FIBROBLAST; HEK293 CELL LINE; METABOLISM; MICROGLIA; MICROTUBULE; MONOCYTE; RNA INTERFERENCE; T LYMPHOCYTE; TRANSPORT AT THE CELLULAR LEVEL;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BIOLOGICAL TRANSPORT; CAPSID; CELL LINE; CELL NUCLEUS; DYNEINS; FIBROBLASTS; HEK293 CELLS; HIV-1; HUMANS; KINESIN; MICROGLIA; MICROTUBULES; MONOCYTES; NERVE TISSUE PROTEINS; RNA INTERFERENCE; T-LYMPHOCYTES;

EID: 84926393829     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7660     Document Type: Article

References (70)

1. Welte, M. A. Bidirectional transport along microtubules. Curr. Biol. 14, R525-R537 (2004).
2. Dodding, M. P. & Way, M. Coupling viruses to dynein and kinesin-1. EMBO J. 30, 3527-3539 (2011).
3. Fassati, A. Multiple roles of the capsid protein in the early steps of HIV-1 infection. Virus Res. 170, 15-24 (2012).
4. McDonald, D. et al. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159, 441-452 (2002).
5. Arhel, N. et al. Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat. Methods 3, 817-824 (2006).
6. Arhel, N. J. et al. HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J. 26, 3025-3037 (2007).
7. Desfarges, S. et al. HIV-1 integrase trafficking in S. cerevisiae: a useful model to dissect the microtubule network involvement of viral protein nuclear import. Yeast 26, 39-54 (2009).
8. Naghavi, M. H., Hatziioannou, T., Gao, G. & Goff, S. P. Overexpression of fasciculation and elongation protein zeta-1 (FEZ1) induces a post-entry block to retroviruses in cultured cells. Genes Dev. 19, 1105-1115 (2005).
9. Haedicke, J., Brown, C. & Naghavi, M. H. The brain-specific factor FEZ1 is a determinant of neuronal susceptibility to HIV-1 infection. Proc. Natl Acad. Sci. USA 106, 14040-14045 (2009).
10. Miyauchi, K., Kim, Y., Latinovic, O., Morozov, V. & Melikyan, G. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137, 433-444 (2009).
11. Herold, N. et al. HIV-1 entry in SupT1-R5, CEM-ss and primary CD4+ T-cells occurs at the plasma membrane and does not require endocytosis. J. Virol. 88, 13956-13970 (2014).
12. McClure, M. O., Sommerfelt, M. A., Marsh, M. & Weiss, R. A. The pH independence of mammalian retrovirus infection. J. Gen. Virol. 71(Pt 4): 767-773 (1990).
13. O'Reilly, L. & Roth, M. J. G541R within the 4070A TM protein regulates fusion in murine leukemia viruses. J. Virol. 77, 12011-12021 (2003).
14. Ganser, B. K., Li, S., Klishko, V. Y., Finch, J. T. & Sundquist, W. I. Assembly and analysis of conical models for the HIV-1 core. Science 283, 80-83 (1999).
15. Fricke, T. et al. The ability of TNPO3-depleted cells to inhibit HIV-1 infection requires CPSF6. Retrovirology 10, 46 (2013).
16. Lee, K. et al. Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 7, 221-233 (2010).
17. Brandariz-Nunez, A. et al. Role of SAMHD1 nuclear localization in restriction of HIV-1 and SIVmac. Retrovirology 9, 49 (2012).
18. Goff, S. P. HIV: Slipping under the radar. Nature 503, 352-353 (2013).
19. Schaller, T. et al. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 7, e1002439 (2011).
20. Blasius, T. L., Cai, D., Jih, G. T., Toret, C. P. & Verhey, K. J. Two binding partners cooperate to activate the molecular motor Kinesin-1. J. Cell Biol. 176, 11-17 (2007).
21. Campbell, E. M., Perez, O., Melar, M. & Hope, T. J. Labeling HIV-1 virions with two fluorescent proteins allows identification of virions that have productively entered the target cell. Virology 360, 286-293 (2007).
22. Bowman, E. J., Siebers, A. & Altendorf, K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl Acad. Sci. USA 85, 7972-7976 (1988).
23. Cavrois, M., De Noronha, C. & Greene, W. C. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nature Biotechnol. 20, 1151-1154 (2002).
24. Jaulin, F., Xue, X., Rodriguez-Boulan, E. & Kreitzer, G. Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev. Cell 13, 511-522 (2007).
25. Zhang, J., Li, S., Fischer, R. & Xiang, X. Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol. Biol. Cell 14, 1479-1488 (2003).
26. rd J. A. Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 22, 479-487 (2010).
27. Firestone, A. J. et al. Small-molecule inhibitors of the AAA + ATPase motor cytoplasmic dynein. Nature 484, 125-129 (2012).
28. Chua, J. J. et al. Phosphorylation-regulated axonal dependent transport of syntaxin 1 is mediated by a Kinesin-1 adapter. Proc. Natl Acad. Sci. USA 109, 5862-5867 (2012).
29. Rothbauer, U. et al. A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol. Cell. Proteomics. 7, 282-289 (2008).
30. Suzuki, T. et al. Identification of FEZ1 as a protein that interacts with JC virus agnoprotein and microtubules: role of agnoprotein-induced dissociation of FEZ1 from microtubules in viral propagation. J. Biol. Chem. 280, 24948-24956 (2005).
31. Furtak, V. et al. Perturbation of the P-body component Mov10 inhibits HIV-1 infectivity. PLoS ONE 5, e9081 (2010).
32. Gonzalez-Scarano, F. & Martin-Garcia, J. The neuropathogenesis of AIDS. Nat. Rev. Immunol. 5, 69-81 (2005).
33. Lanza, D. C., Trindade, D. M., Assmann, E. M. & Kobarg, J. Over-expression of GFP-FEZ1 causes generation of multi-lobulated nuclei mediated by microtubules in HEK293 cells. Exp. Cell Res. 314, 2028-2039 (2008).
34. Lanza, D. C. et al. FEZ1 interacts with CLASP2 and NEK1 through coiled-coil regions and their cellular colocalization suggests centrosomal functions and regulation by PKC. Mol. Cell. Biochem. 338, 35-45 (2010).
35. Surpili, M. J., Delben, T. M. & Kobarg, J. Identification of proteins that interact with the central coiled-coil region of the human protein kinase NEK1. Biochemistry 42, 15369-15376 (2003).
36. O'Connell, M. J., Krien, M. J. & Hunter, T. Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol. 13, 221-228 (2003).
37. Polci, R., Peng, A., Chen, P. L., Riley, D. J. & Chen, Y. NIMA-related protein kinase 1 is involved early in the ionizing radiation-induced DNA damage response. Cancer Res. 64, 8800-8803 (2004).
38. Mahjoub, M. R., Trapp, M. L. & Quarmby, L. M. NIMA-related kinases defective in murine models of polycystic kidney diseases localize to primary cilia and centrosomes. J. Am. Soc. Nephrol. 16, 3485-3489 (2005).
39. Shalom, O., Shalva, N., Altschuler, Y. & Motro, B. The mammalian Nek1 kinase is involved in primary cilium formation. FEBS Lett. 582, 1465-1470 (2008).
40. Lanza, D. C. et al. Human FEZ1 has characteristics of a natively unfolded protein and dimerizes in solution. Proteins 74, 104-121 (2009).
41. Maturana, A. D., Fujita, T. & Kuroda, S. Functions of fasciculation and elongation protein zeta-1 (FEZ1) in the brain. Scientific World Journal 10, 1646-1654 (2010).
42. Alborghetti, M. R. et al. Human FEZ1 protein forms a disulfide bond mediated dimer: implications for cargo transport. J. Proteome Res. 9, 4595-4603 (2010).
43. Kuroda, S., Nakagawa, N., Tokunaga, C., Tatematsu, K. & Tanizawa, K. Mammalian homologue of the Caenorhabditis elegans UNC-76 protein involved in axonal outgrowth is a protein kinase C zeta-interacting protein. J. Cell Biol. 144, 403-411 (1999).
44. Gindhart, J. G. et al. The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol. Biol. Cell 14, 3356-3365 (2003).
45. Okumura, F., Hatakeyama, S., Matsumoto, M., Kamura, T. & Nakayama, K. I. Functional regulation of FEZ1 by the U-box-type ubiquitin ligase E4B contributes to neuritogenesis. J. Biol. Chem. 279, 53533-53543 (2004).
46. Ikuta, J. et al. Fasciculation and elongation protein zeta-1 (FEZ1) participates in the polarization of hippocampal neuron by controlling the mitochondrial motility. Biochem. Biophys. Res. Commun. 353, 127-132 (2007).
47. Fujita, T. et al. Axonal guidance protein FEZ1 associates with tubulin and kinesin motor protein to transport mitochondria in neurites of NGF-stimulated PC12 cells. Biochem. Biophys. Res. Commun. 361, 605-610 (2007).
48. Sodeik, B. Unchain my heart, baby let me go - the entry and intracellular transport of HIV. J. Cell Biol. 159, 393-395 (2002).
49. Suomalainen, M. et al. Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144, 657-672 (1999).
50. Smith, G. A., Gross, S. P. & Enquist, L. W. Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl Acad. Sci. USA 98, 3466-3470 (2001).
51. Dohner, K. et al. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13, 2795-2809 (2002).
52. Smith, G. A., Pomeranz, L., Gross, S. P. & Enquist, L. W. Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc. Natl Acad. Sci. USA 101, 16034-16039 (2004).
53. Radtke, K. et al. Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog. 6, e1000991 (2010).
54. Gazzola, M. et al. A stochastic model for microtubule motors describes the in vivo cytoplasmic transport of human adenovirus. PLoS Comput. Biol. 5, e1000623 (2009).
55. Bremner, K. H. et al. Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe 6, 523-535 (2009).
56. Scherer, J. & Vallee, R. B. Adenovirus recruits dynein by an evolutionary novel mechanism involving direct binding to pH-primed hexon. Viruses 3, 1417-1431 (2011).
57. Strunze, S. et al. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10, 210-223 (2011).
58. Lukic, Z., Dharan, A., Fricke, T., Diaz-Griffero, F. & Campbell, E. M. HIV-1 uncoating is facilitated by dynein and kinesin 1. J. Virol. 88, 13613-13625 (2014).
59. Ally, S., Larson, A. G., Barlan, K., Rice, S. E. & Gelfand, V. I. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J. Cell Biol. 187, 1071-1082 (2009).
60. Petit, C. et al. Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8. J. Cell Sci. 116, 3433-3442 (2003).
61. Su, Y. et al. Microtubule-dependent retrograde transport of bovine immunodeficiency virus. Cell Microbiol. 12, 1098-1107 (2010).
62. Suzuki, Y. & Craigie, R. The road to chromatin - nuclear entry of retroviruses. Nat. Rev. Microbiol. 5, 187-196 (2007).
63. Tang, Y. et al. Cellular motor protein KIF-4 associates with retroviral Gag. J. Virol. 73, 10508-10513 (1999).
64. Martinez, N. W., Xue, X., Berro, R. G., Kreitzer, G. & Resh, M. D. Kinesin KIF4 regulates intracellular trafficking and stability of the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 82, 9937-9950 (2008).
65. Sabo, Y. et al. HIV-1 induces the formation of stable microtubules to enhance early infection. Cell Host Microbe 14, 535-546 (2013).
66. Azevedo, C., Burton, A., Ruiz-Mateos, E., Marsh, M. & Saiardi, A. Inositol pyrophosphate mediated pyrophosphorylation of AP3B1 regulates HIV-1 Gag release. Proc. Natl Acad. Sci. USA 106, 21161-21166 (2009).
67. Gaudin, R. et al. Critical role for the kinesin KIF3A in the HIV life cycle in primary human macrophages. J. Cell Biol. 199, 467-479 (2012).
68. Connor, R. I., Chen, B. K., Choe, S. & Landau, N. R. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206, 935-944 (1995).
69. Naldini, L. et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (1996).
70. rd A. B. & Diaz-Griffero, F. Human cytosolic extracts stabilize the HIV-1 core. J. Virol. 87, 10587-10597 (2013).