CXCR4 stimulates macropinocytosis: Implications for cellular uptake of arginine-rich cell-penetrating peptides and HIV

Chemistry and Biology

Volumn 19, Issue 11, 2012, Pages 1437-1446

  Tanaka, Gen ^a   Nakase, Ikuhiko ^a   Fukuda, Yasunori ^a   Masuda, Ryo ^a   Oishi, Shinya ^a   Shimura, Kazuya ^a   Kawaguchi, Yoshimasa ^a   Takatani Nakase, Tomoka ^c   Langel, Ülo ^d   Gräslund, Astrid ^e   Okawa, Katsuya ^b,g   Matsuoka, Masao ^a   Fujii, Nobutaka ^a   Hatanaka, Yasumaru ^f   Futaki, Shiroh ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY FACULTY OF MEDICINE   (Japan)

^c MUKOGAWA WOMEN'S UNIVERSITY   (Japan)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e STOCKHOLM UNIVERSITY   (Sweden)

^f UNIVERSITY OF TOYAMA   (Japan)

^g KYOWA HAKKO KOGYO CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

5 (N,N DIMETHYL)AMILORIDE; ACTIN; ARGININE 12 MER PEPTIDE; CELL PENETRATING PEPTIDE; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL VIABILITY; CONTROLLED STUDY; CROSS LINKING; CYTOPLASM; ENDOCYTOSIS; HUMAN; HUMAN CELL; INFECTION PREVENTION; INTERNALIZATION; LIGAND BINDING; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS INFECTION;

ARGININE; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; CHEMOKINE CXCL12; CROSS-LINKING REAGENTS; HELA CELLS; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; PINOCYTOSIS; RECEPTORS, CXCR4;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84870008010     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.09.011     Document Type: Article

References (48)

1. J. Arii, H. Goto, T. Suenaga, M. Oyama, H. Kozuka-Hata, T. Imai, A. Minowa, H. Akashi, H. Arase, Y. Kawaoka, and Y. Kawaguchi Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1 Nature 467 2010 859 862
2. S.D. Conner, and S.L. Schmid Regulated portals of entry into the cell Nature 422 2003 37 44
3. B.J. Doranz, K. Grovit-Ferbas, M.P. Sharron, S.-H. Mao, M.B. Goetz, E.S. Daar, R.W. Doms, and W.A. O'Brien A small-molecule inhibitor directed against the chemokine receptor CXCR4 prevents its use as an HIV-1 coreceptor J. Exp. Med. 186 1997 1395 1400
4. B.J. Doranz, L.G. Filion, F. Diaz-Mitoma, D.S. Sitar, J. Sahai, F. Baribaud, M.J. Orsini, J.L. Benovic, W. Cameron, and R.W. Doms Safe use of the CXCR4 inhibitor ALX40-4C in humans AIDS Res. Hum. Retroviruses 17 2001 475 486
5. K. Ezzat, H. Helmfors, O. Tudoran, C. Juks, S. Lindberg, K. Padari, S. El-Andaloussi, M. Pooga, and U. Langel Scavenger receptor-mediated uptake of cell-penetrating peptide nanocomplexes with oligonucleotides FASEB J. 26 2012 1172 1180
6. S. Falcone, E. Cocucci, P. Podini, T. Kirchhausen, E. Clementi, and J. Meldolesi Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events J. Cell Sci. 119 2006 4758 4769
7. N. Fujii, S. Oishi, K. Hiramatsu, T. Araki, S. Ueda, H. Tamamura, A. Otaka, S. Kusano, S. Terakubo, and H. Nakashima Molecular-size reduction of a potent CXCR4-chemokine antagonist using orthogonal combination of conformation- and sequence-based libraries Angew. Chem. Int. Ed. Engl. 42 2003 3251 3253
8. S. Futaki Oligoarginine vectors for intracellular delivery: design and cellular-uptake mechanisms Biopolymers 84 2006 241 249
9. S. Futaki, T. Suzuki, W. Ohashi, T. Yagami, S. Tanaka, K. Ueda, and Y. Sugiura Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery J. Biol. Chem. 276 2001 5836 5840
10. S. Gerbal-Chaloin, C. Gondeau, G. Aldrian-Herrada, F. Heitz, C. Gauthier-Rouvière, and G. Divita First step of the cell-penetrating peptide mechanism involves Rac1 GTPase-dependent actin-network remodelling Biol. Cell 99 2007 223 238
11. M. Hamon, E. Mbemba, N. Charnaux, H. Slimani, S. Brule, L. Saffar, R. Vassy, C. Prost, N. Lievre, A. Starzec, and L. Gattegno A syndecan-4/CXCR4 complex expressed on human primary lymphocytes and macrophages and HeLa cell line binds the CXC chemokine stromal cell-derived factor-1 (SDF-1) Glycobiology 14 2004 311 323
12. M. Ishihara Biosynthesis, structure, and biological activity of basic FGF binding domains of heparan sulfate Trends Glycosci. Glycotechnol. 5 1993 343 354
13. J. Kimpton, and M. Emerman Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated β-galactosidase gene J. Virol. 66 1992 2232 2239
14. E.I. Kodama, S. Kohgo, K. Kitano, H. Machida, H. Gatanaga, S. Shigeta, M. Matsuoka, H. Ohrui, and H. Mitsuya 4′-ethynyl nucleoside analogs: potent inhibitors of multidrug-resistant human immunodeficiency virus variants in vitro Antimicrob. Agents Chemother. 45 2001 1539 1546
15. M. Kosuge, T. Takeuchi, I. Nakase, A.T. Jones, and S. Futaki Cellular internalization and distribution of arginine-rich peptides as a function of extracellular peptide concentration, serum, and plasma membrane associated proteoglycans Bioconjug. Chem. 19 2008 656 664
16. Y. Koyanagi, S. Harada, M. Takahashi, F. Uchino, and N. Yamamoto Selective cytotoxicity of AIDS virus infection towards HTLV-I-transformed cell lines Int. J. Cancer 36 1985 445 451
17. T. Letoha, A. Keller-Pintér, E. Kusz, C. Kolozsi, Z. Bozsó, G. Tóth, C. Vizler, Z. Oláh, and L. Szilák Cell-penetrating peptide exploited syndecans Biochim. Biophys. Acta 1798 2010 2258 2265
18. V. Maréchal, M.-C. Prevost, C. Petit, E. Perret, J.-M. Heard, and O. Schwartz Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis J. Virol. 75 2001 11166 11177
19. O. Meier, K. Boucke, S.V. Hammer, S. Keller, R.P. Stidwill, S. Hemmi, and U.F. Greber Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake J. Cell Biol. 158 2002 1119 1131
20. J. Mercer, and A. Helenius Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells Science 320 2008 531 535
21. J. Mercer, and A. Helenius Virus entry by macropinocytosis Nat. Cell Biol. 11 2009 510 520
22. S. Mitola, S. Sozzani, W. Luini, L. Primo, A. Borsatti, H. Weich, and F. Bussolino Tat-human immunodeficiency virus-1 induces human monocyte chemotaxis by activation of vascular endothelial growth factor receptor-1 Blood 90 1997 1365 1372
23. R. Möhle, F. Bautz, C. Denzlinger, and L. Kanz Transendothelial migration of hematopoietic progenitor cells. Role of chemotactic factors Ann. N Y Acad. Sci. 938 2001 26 34 discussion 34-35
24. I. Nakase, M. Niwa, T. Takeuchi, K. Sonomura, N. Kawabata, Y. Koike, M. Takehashi, S. Tanaka, K. Ueda, and J.C. Simpson Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement Mol. Ther. 10 2004 1011 1022
25. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, and S. Futaki Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 2007 492 501
26. I. Nakase, H. Hirose, G. Tanaka, A. Tadokoro, S. Kobayashi, T. Takeuchi, and S. Futaki Cell-surface accumulation of flock house virus-derived peptide leads to efficient internalization via macropinocytosis Mol. Ther. 17 2009 1868 1876
27. H. Nakashima, M. Hashimoto, Y. Sadakane, T. Tomohiro, and Y. Hatanaka Simple and versatile method for tagging phenyldiazirine photophores J. Am. Chem. Soc. 128 2006 15092 15093
28. M.J. Orsini, J.L. Parent, S.J. Mundell, A. Marchese, and J.L. Benovic Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the C-terminal tail that mediate receptor internalization J. Biol. Chem. 274 1999 31076 31086
29. R. Phillips, and A. Ager Activation of pertussis toxin-sensitive CXCL12 (SDF-1) receptors mediates transendothelial migration of T lymphocytes across lymph node high endothelial cells Eur. J. Immunol. 32 2002 837 847
30. M. Rey, A. Valenzuela-Fernández, A. Urzainqui, M. Yáñez-Mó, M. Pérez-Martínez, P. Penela, F. Mayor Jr., and F. Sánchez-Madrid Myosin IIA is involved in the endocytosis of CXCR4 induced by SDF-1α J. Cell Sci. 120 2007 1126 1133
31. A. Rubio Demirovic, J. Canadi, W. Weiglhofer, P. Scheidegger, R. Jaussi, and B.-H. Kurt HIV TAT basic peptide is not a high-affinity ligand for VEGF receptor 2 Biol. Chem. 384 2003 1435 1441
32. E. Schaeffer, R. Geleziunas, and W.C. Greene Human immunodeficiency virus type 1 Nef functions at the level of virus entry by enhancing cytoplasmic delivery of virions J. Virol. 75 2001 2993 3000
33. B. Schramm, M.L. Penn, R.F. Speck, S.Y. Chan, E. De Clercq, D. Schols, R.I. Connor, and M.A. Goldsmith Viral entry through CXCR4 is a pathogenic factor and therapeutic target in human immunodeficiency virus type 1 disease J. Virol. 74 2000 184 192
34. N. Signoret, J. Oldridge, A. Pelchen-Matthews, P.J. Klasse, T. Tran, L.F. Brass, M.M. Rosenkilde, T.W. Schwartz, W. Holmes, and W. Dallas Phorbol esters and SDF-1 induce rapid endocytosis and down modulation of the chemokine receptor CXCR4 J. Cell Biol. 139 1997 651 664
35. J.A. Swanson, and C. Watts Macropinocytosis Trends Cell Biol. 5 1995 424 428
36. H. Tamamura, A. Otaka, and N. Fujii Development of anti-HIV agents targeting dynamic supramolecular mechanism: entry and fusion inhibitors based on CXCR4/CCR5 antagonists and gp41-C34-remodeling peptides Curr. HIV Res. 3 2005 289 301
37. E. Tkachenko, E. Lutgens, R.-V. Stan, and M. Simons Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4-dependent activation of Rac1 and a Cdc42-dependent macropinocytic pathway J. Cell Sci. 117 2004 3189 3199
38. T. Tomohiro, M. Hashimoto, and Y. Hatanaka Cross-linking chemistry and biology: development of multifunctional photoaffinity probes Chem. Rec. 5 2005 385 395
39. S. Venkatesan, J.J. Rose, R. Lodge, P.M. Murphy, and J.F. Foley Distinct mechanisms of agonist-induced endocytosis for human chemokine receptors CCR5 and CXCR4 Mol. Biol. Cell 14 2003 3305 3324
40. C. Voermans, E.C. Anthony, E. Mul, E. van der Schoot, and P. Hordijk SDF-1-induced actin polymerization and migration in human hematopoietic progenitor cells Exp. Hematol. 29 2001 1456 1464
41. J.S. Wadia, R.V. Stan, and S.F. Dowdy Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nat. Med. 10 2004 310 315
42. + T cells Virology 381 2008 143 154
43. P.A. Wender, W.C. Galliher, E.A. Goun, L.R. Jones, and T.H. Pillow The design of guanidinium-rich transporters and their internalization mechanisms Adv. Drug Deliv. Rev. 60 2008 452 472
44. Y. Wu, and A. Yoder Chemokine coreceptor signaling in HIV-1 infection and pathogenesis PLoS Pathog. 5 2009 e1000520
45. H. Xiao, C. Neuveut, H.L. Tiffany, M. Benkirane, E.A. Rich, P.M. Murphy, and K.T. Jeang Selective CXCR4 antagonism by Tat: implications for in vivo expansion of coreceptor use by HIV-1 Proc. Natl. Acad. Sci. USA 97 2000 11466 11471
46. Y. Yano, A. Yano, S. Oishi, Y. Sugimoto, G. Tsujimoto, N. Fujii, and K. Matsuzaki Coiled-coil tag-probe system for quick labeling of membrane receptors in living cells ACS Chem. Biol. 3 2008 341 345
47. A. Yoder, D. Yu, L. Dong, S.R. Iyer, X. Xu, J. Kelly, J. Liu, W. Wang, P.J. Vorster, and L. Agulto HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells Cell 134 2008 782 792
48. W.-B. Zhang, J.-M. Navenot, B. Haribabu, H. Tamamura, K. Hiramatu, A. Omagari, G. Pei, J.P. Manfredi, N. Fujii, J.R. Broach, and S.C. Peiper A point mutation that confers constitutive activity to CXCR4 reveals that T140 is an inverse agonist and that AMD3100 and ALX40-4C are weak partial agonists J. Biol. Chem. 277 2002 24515 24521