Actin dynamics regulate multiple endosomal steps during Kaposi's sarcoma-associated herpesvirus entry and trafficking in endothelial cells

PLoS Pathogens

Volumn 5, Issue 7, 2009, Pages

  Greene, Whitney ^a   Gao, Shou Jiang ^a,b,c,d  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c University of Texas Health Science Center at San Antonio   (United States)

^d WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; CLATHRIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSFERRIN; VIRUS ENVELOPE PROTEIN; CHLORPROMAZINE; ENZYME INHIBITOR; ORF65 PROTEIN, HUMAN HERPESVIRUS 8; VIRUS PROTEIN;

ACIDIFICATION; ACTIN FILAMENT; ARTICLE; CAVEOLA; CELL MEMBRANE; CELL MIGRATION; CELL NUCLEUS MEMBRANE; CELL SELECTION; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; ENDOTHELIUM CELL; HERPES VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNOFLUORESCENCE; LIPID RAFT; MEMBRANE FUSION; MOLECULAR DYNAMICS; REPORTER GENE; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS INHIBITION; ACTIVE TRANSPORT; CELL LINE; CELL NUCLEUS; COATED VESICLE; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENCE MICROSCOPY; METABOLISM; PH; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VIROLOGY; VIRUS ENTRY;

HUMAN HERPESVIRUS 8; MAMMALIA; MIRIDAE;

ACTINS; ACTIVE TRANSPORT, CELL NUCLEUS; CAVEOLAE; CELL LINE; CELL NUCLEUS; CHLORPROMAZINE; CLATHRIN-COATED VESICLES; CYTOSKELETON; ENDOCYTOSIS; ENDOSOMES; ENDOTHELIAL CELLS; ENZYME INHIBITORS; HERPESVIRUS 8, HUMAN; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE MICRODOMAINS; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSFERRIN; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 70049116403     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000512     Document Type: Article

References (82)

1. Mosesson Y, Mills GB, Yarden Y (2008) Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8: 835-850.
2. Gruenberg J, van der Goot FG (2006) Mechanisms of pathogen entry through the endosomal compartments. Nat Rev Mol Cell Biol 7: 495-504. (Pubitemid 44036455)
3. Rappoport JZ (2008) Focusing on clathrin-mediated endocytosis. Biochem J 412: 415-423.
4. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422: 37-44.
5. Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404-414. (Pubitemid 44050094)
6. Smythe E, Ayscough KR (2006) Actin regulation in endocytosis. J Cell Sci 119: 4589-4598.
7. Ascough KR (2004) Endocytosis: Actin in the driving seat. Curr Biol 14: R124-126.
8. Engqvist-Goldstein AE, Drubin DG (2003) Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19: 287-332.
9. Kaksonen M, Toret CP, Drubin DG (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123: 305-320. (Pubitemid 41457219)
10. Fujimoto LM, Roth R, Heuser JE, Schmid SL (2000) Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1: 161-171.
11. Lamaze C, Fujimoto LM, Yin HL, Schmid SL (1997) The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J Biol Chem 272: 20332-20335. (Pubitemid 27355580)
12. Salisbury JL, Condeelis JS, Satir P (1980) Role of coated vesicles, microfilaments, and calmodulin in receptor-mediated endocytosis by cultured B lymphoblastoid cells. J Cell Biol 87: 132-141.
13. Roth MG (2007) Integrating actin assembly and endocytosis. Dev Cell 13: 3-4.
14. Merrifield CJ, Qualmann B, Kessels MM, Almers W (2004) Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts. Eur J Cell Biol 83: 13-18. (Pubitemid 38455602)
15. Gottlieb TA, Ivanov IE, Adesnik M, Sabatini DD (1993) Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 120: 695-710. (Pubitemid 23035139)
16. Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16: 964-975. (Pubitemid 40165585)
17. Dai J, Sheetz MP (1995) Regulation of endocytosis, exocytosis, and shape by membrane tension. Cold Spring Harb Symp Quant Biol 60: 567-571. (Pubitemid 26202066)
18. Dai J, Sheetz MP (1999) Membrane tether formation from blebbing cells. Biophys J 77: 3363-3370.
19. Karl I, Bereiter-Hahn J (1999) Tension modulates cell surface motility: A scanning acoustic microscopy study. Cell Motil Cytoskeleton 43: 349-359. (Pubitemid 29368207)
20. Sun X, Whittaker GR (2007) Role of the actin cytoskeleton during influenza virus internalization into polarized epithelial cells. Cell Microbiol 9: 1672-1682. (Pubitemid 46958794)
21. Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4: 691-698. (Pubitemid 34993705)
22. Merrifield CJ, Perrais D, Zenisek D (2005) Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121: 593-606. (Pubitemid 40720012)
23. Bretscher A, Edwards K, Fehon RG (2002) ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3: 586-599. (Pubitemid 34886970)
24. Weed SA, Parsons JT (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20: 6418-6434.
25. Kiuchi T, Ohashi K, Kurita S, Mizuno K (2007) Cofilin promotes stimulus-induced lamellipodium formation by generating an abundant supply of actin monomers. J Cell Biol 177: 465-476. (Pubitemid 46718275)
26. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, et al. (1998) Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393: 809-812. (Pubitemid 28299495)
27. Goley ED, Welch MD (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7: 713-726.
28. Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9: 1110-1121.
29. Qualmann B, Kessels MM (2008) Actin nucleation: putting the brakes on Arp2/3. Curr Biol 18: R420-423. (Pubitemid 351672038)
30. Hao M, Maxfield FR (2000) Characterization of rapid membrane internalization and recycling. J Biol Chem 275: 15279-15286. (Pubitemid 30337254)
31. Mayor S, Presley JF, Maxfield FR (1993) Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J Cell Biol 121: 1257-1269. (Pubitemid 23174544)
32. Presley JF, Mayor S, Dunn KW, Johnson LS, McGraw TE, et al. (1993) The End2 mutation in CHO cells slows the exit of transferrin receptors from the recycling compartment but bulk membrane recycling is unaffected. J Cell Biol 122: 1231-1241. (Pubitemid 23277292)
33. Presley JF, Mayor S, McGraw TE, Dunn KW, Maxfield FR (1997) Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J Biol Chem 272: 13929-13936. (Pubitemid 27224837)
34. Schwiegelshohn B, Presley JF, Gorecki M, Vogel T, Carpentier YA, et al. (1995) Effects of apoprotein E on intracellular metabolism of model triglyceride-rich particles are distinct from effects on cell particle uptake. J Biol Chem 270: 1761-1769.
35. Dabiri GA, Sanger JM, Portnoy DA, Southwick FS (1990) Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc Natl Acad Sci U S A 87: 6068-6072. (Pubitemid 20258957)
36. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, et al. (1992) L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-531.
37. Tilney LG, Portnoy DA (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109: 1597-1608.
38. Smith GA, Enquist LW (2002) Break ins and break outs: viral interactions with the cytoskeleton of Mammalian cells. Annu Rev Cell Dev Biol 18: 135-161.
39. Spear PG, Longnecker R (2003) Herpesvirus entry: an update. J Virol 77: 10179-10185.
40. Nicola AV, Hou J, Major EO, Straus SE (2005) Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J Virol 79: 7609-7616. (Pubitemid 40756794)
41. Nicola AV, Straus SE (2004) Cellular and viral requirements for rapid endocytic entry of herpes simplex virus. J Virol 78: 7508-7517.
42. Nicola AV, McEvoy AM, Straus SE (2003) Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol 77: 5324-5332.
43. Greene W, Kuhne K, Ye F, Chen J, Zhou F, et al. (2007) Molecular biology of KSHV in relation to AIDS-associated oncogenesis. Cancer Treat Res 133: 69-127.
44. Akula SM, Naranatt PP, Walia NS, Wang FZ, Fegley B, et al. (2003) Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) infection of human fibroblast cells occurs through endocytosis. J Virol 77: 7978-7990. (Pubitemid 36792794)
45. Naranatt PP, Krishnan HH, Smith MS, Chandran B (2005) Kaposi's sarcoma-associated herpesvirus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J Virol 79: 1191-1206.
46. Sharma-Walia N, Naranatt PP, Krishnan HH, Zeng L, Chandran B (2004) Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 envelope glycoprotein gB induces the integrin-dependent focal adhesion kinase-Src-phosphatidylinositol 3-kinase-rho GTPase signal pathways and cytoskeletal rearrangements. J Virol 78: 4207-4223. (Pubitemid 38437226)
47. Veettil MV, Sharma-Walia N, Sadagopan S, Raghu H, Sivakumar R, et al. (2006) RhoA-GTPase facilitates entry of Kaposi's sarcoma-associated herpesvirus into adherent target cells in a Src-dependent manner. J Virol 80: 11432-11446. (Pubitemid 44788859)
48. Raghu H, Sharma-Walia N, Veettil MV, Sadagopan S, Caballero A, et al. (2007) Lipid rafts of primary endothelial cells are essential for Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8-induced phosphatidylinositol 3-kinase and RhoA-GTPases critical for microtubule dynamics and nuclear delivery of viral DNA but dispensable for binding and entry. J Virol 81: 7941-7959. (Pubitemid 47101480)
49. Ferreira DF, Santo MP, Rebello MA, Rebello MC (2000) Weak bases affect late stages of Mayaro virus replication cycle in vertebrate cells. J Med Microbiol 49: 313-318.
50. Inabayashi M, Miyauchi S, Kamo N, Jin T (1995) Conductance change in phospholipid bilayer membrane by an electroneutral ionophore, monensin. Biochemistry 34: 3455-3460.
51. Bowman EJ, Siebers A, Altendorf K (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 85: 7972-7976. (Pubitemid 18272062)
52. Marsh M, McMahon HT (1999) The structural era of endocytosis. Science 285: 215-220.
53. Wang LH, Rothberg KG, Anderson RG (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117. (Pubitemid 23352421)
54. Merritt EA, Sixma TK, Kalk KH, van Zanten BA, Hol WG (1994) Galactose-binding site in Escherichia coli heat-labile enterotoxin (LT) and cholera toxin (CT). Mol Microbiol 13: 745-753. (Pubitemid 24266209)
55. Pang H, Le PU, Nabi IR (2004) Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus. J Cell Sci 117: 1421-1430. (Pubitemid 38559818)
56. Reed RA, Mattai J, Shipley GG (1987) Interaction of cholera toxin with ganglioside GM1 receptors in supported lipid monolayers. Biochemistry 26: 824-832. (Pubitemid 17021062)
57. Fielding CJ, Fielding PE (2003) Relationship between cholesterol trafficking and signaling in rafts and caveolae. Biochim Biophys Acta 1610: 219-228.
58. Katzman RB, Longnecker R (2003) Cholesterol-dependent infection of Burkitt's lymphoma cell lines by Epstein-Barr virus. J Gen Virol 84: 2987-2992. (Pubitemid 37336782)
59. Schnitzer JE, Oh P, Jacobson BS, Dvorak AM (1995) Caveolae from luminal plasmalemma of rat lung endothelium: microdomains enriched in caveolin, Ca(2+)-ATPase, and inositol trisphosphate receptor. Proc Natl Acad Sci U S A 92: 1759-1763.
60. Schubert W, Frank PG, Razani B, Park DS, Chow CW, et al. (2001) Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem 276: 48619-48622. (Pubitemid 37370554)
61. Coue M, Brenner SL, Spector I, Korn ED (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett 213: 316-318.
62. Spector I, Shochet NR, Kashman Y, Groweiss A (1983) Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219: 493-495. (Pubitemid 13189272)
63. Goddette DW, Frieden C (1986) Actin polymerization. The mechanism of action of cytochalasin D. J Biol Chem 261: 15974-15980. (Pubitemid 17202846)
64. Sampath P, Pollard TD (1991) Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30: 1973-1980.
65. Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED (1994) Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871.
66. Symons M, Rusk N (2003) Control of vesicular trafficking by Rho GTPases. Curr Biol 13: R409-418. (Pubitemid 36573246)
67. Tapon N, Hall A (1997) Rho, Rac and Cdc42 GTPases regulate the organization of the actin cytoskeleton. Curr Opin Cell Biol 9: 86-92.
68. Foerg C, Ziegler U, Fernandez-Carneado J, Giralt E, Merkle HP (2007) Differentiation restricted endocytosis of cell penetrating peptides in MDCK cells corresponds with activities of Rho-GTPases. Pharm Res 24: 628-642. (Pubitemid 46411971)
69. Just I, Fritz G, Aktories K, Giry M, Popoff MR, et al. (1994) Clostridium difficile toxin B acts on the GTP-binding protein Rho. J Biol Chem 269: 10706-10712. (Pubitemid 24982164)
70. Benesch S, Polo S, Lai FP, Anderson KI, Stradal TE, et al. (2005) N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits. J Cell Sci 118: 3103-3115. (Pubitemid 41149914)
71. Peterson JR, Bickford LC, Morgan D, Kim AS, Ouerfelli O, et al. (2004) Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation. Nat Struct Mol Biol 11: 747-755. (Pubitemid 39014500)
72. Lakadamyali M, Rust MJ, Zhuang X (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124: 997-1009. (Pubitemid 43344239)
73. Trischler M, Stoorvogel W, Ullrich O (1999) Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway. J Cell Sci 112(Pt 24): 4773-4783. (Pubitemid 30034824)
74. Johnson MB, Chen J, Murchison N, Green FA, Enns CA (2007) Transferrin receptor 2: evidence for ligand-induced stabilization and redirection to a recycling pathway. Mol Biol Cell 18: 743-754. (Pubitemid 46399482)
75. Pan H, Xie J, Ye F, Gao SJ (2006) Modulation of Kaposi's sarcoma-associated herpesvirus infection and replication by MEK/ERK, JNK, and p38 multiple mitogen-activated protein kinase pathways during primary infection. J Virol 80: 5371-5382. (Pubitemid 43752782)
76. Damke H, Baba T, van der Bliek AM, Schmid SL (1995) Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol 131: 69-80.
77. Sheetz MP, Dai J (1996) Modulation of membrane dynamics and cell motility by membrane tension. Trends Cell Biol 6: 85-89. (Pubitemid 26059740)
78. Eisenmann KM, Harris ES, Kitchen SM, Holman HA, Higgs HN, et al. (2007) Dia-interacting protein modulates formin-mediated actin assembly at the cell cortex. Curr Biol 17: 579-591.
79. Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, et al. (2008) The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 181: 523-536. (Pubitemid 351645041)
80. Wallar BJ, Deward AD, Resau JH, Alberts AS (2007) RhoB and the mammalian Diaphanous-related formin mDia2 in endosome trafficking. Exp Cell Res 313: 560-571.
81. Gao SJ, Kingsley L, Li M, Zheng W, Parravicini C, et al. (1996) KSHV antibodies among Americans, Italians and Ugandans with and without Kaposi's sarcoma. Nat Med 2: 925-928.
82. Gao SJ, Deng JH, Zhou FC (2003) Productive lytic replication of a recombinant Kaposi's sarcoma-associated herpesvirus in efficient primary infection of primary human endothelial cells. J Virol 77: 9738-9749. (Pubitemid 37122054)