Urokinase plasminogen activator inhibits HIV virion release from macrophage-differentiated chronically infected cells via activation of RhoA and PKCε

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Graziano, Francesca ^a   Elia, Chiara ^a   Laudanna, Carlo ^c   Poli, Guido ^a,b   Alfano, Massimo ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c Department of Pathology and Diagnostic   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHALASIN D; F ACTIN; G ACTIN; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UROKINASE; UROKINASE RECEPTOR; NUCLEIC ACID SYNTHESIS INHIBITOR; PHORBOL 13 ACETATE 12 MYRISTATE;

ACTIN POLYMERIZATION; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INTRACELLULAR SIGNALING; MACROPHAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRION; VIRUS RELEASE; CELL POLARITY; CELL STRAIN U937; CONFOCAL MICROSCOPY; CYTOPLASM VESICLE; DRUG EFFECT; ELECTRON MICROSCOPY; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; VIROLOGY;

CELL ADHESION; CELL DIFFERENTIATION; CELL POLARITY; CYTOCHALASIN D; CYTOPLASMIC VESICLES; ENZYME ACTIVATION; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN KINASE C-DELTA; PROTEIN KINASE C-EPSILON; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RHOA GTP-BINDING PROTEIN; TETRADECANOYLPHORBOL ACETATE; U937 CELLS; UROKINASE-TYPE PLASMINOGEN ACTIVATOR; VIRION; VIRUS RELEASE;

EID: 80051747048     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023674     Document Type: Article

References (78)

1. Dano K, Andreasen PA, Grondahl-Hansen J, Kristensen P, Nielsen LS, et al. (1985) Plasminogen activators, tissue degradation, and cancer. Adv Cancer Res 44: 139-266.
2. Blasi F, Vassalli JD, Dano K, (1987) Urokinase-type plasminogen activator: proenzyme, receptor, and inhibitors. J Cell Biol 104: 801-804.
3. Blasi F, Carmeliet P, (2002) uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 3: 932-943.
4. Ossowski L, Aguirre-Ghiso JA, (2000) Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth. Curr Opin Cell Biol 12: 613-620.
5. Blasi F, (1997) uPA, uPAR, PAI-1: key intersection of proteolytic, adhesive and chemotactic highways? Immunol Today 18: 415-417.
6. Alfano M, Sidenius N, Blasi F, Poli G, (2003) The role of urokinase-type plasminogen activator (uPA)/uPA receptor in HIV-1 infection. J Leukoc Biol 74: 750-756.
7. Sier CF, Nicoletti I, Santovito ML, Frandsen T, Aletti G, et al. (2004) Metabolism of tumour-derived urokinase receptor and receptor fragments in cancer patients and xenografted mice. Thromb Haemost 91: 403-411.
8. Sidenius N, Sier CF, Ullum H, Pedersen BK, Lepri AC, et al. (2000) Serum level of soluble urokinase-type plasminogen activator receptor is a strong and independent predictor of survival in human immunodeficiency virus infection [In Process Citation]. Blood 96: 4091-4095.
9. Andersen O, Eugen-Olsen J, Kofoed K, Iversen J, Haugaard SB, (2008) Soluble urokinase plasminogen activator receptor is a marker of dysmetabolism in HIV-infected patients receiving highly active antiretroviral therapy. J Med Virol 80: 209-216.
10. Sidenius N, Sier CF, Ullum H, Pedersen BK, Lepri AC, et al. (2000) Serum level of soluble urokinase-type plasminogen activator receptor is a strong and independent predictor of survival in human immunodeficiency virus infection. Blood 96: 4091-4095.
11. Ostrowski SR, Katzenstein TL, Pedersen M, Hoyer-Hansen G, Gerstoft J, et al. (2006) Plasma levels of intact and cleaved urokinase receptor decrease in HIV-1-infected patients initiating highly active antiretroviral therapy. Scand J Immunol 63: 478-486.
12. Sporer B, Koedel U, Popp B, Paul R, Pfister HW, (2005) Evaluation of cerebrospinal fluid uPA, PAI-1, and soluble uPAR levels in HIV-infected patients. J Neuroimmunol 163: 190-194.
13. Cinque P, Nebuloni M, Santovito ML, Price RW, Gisslen M, et al. (2004) The urokinase receptor is overexpressed in the AIDS dementia complex and other neurological manifestations. Ann Neurol 55: 687-694.
14. Alfano M, Sidenius N, Panzeri B, Blasi F, Poli G, (2002) Urokinase-urokinase receptor interaction mediates an inhibitory signal for HIV-1 replication. Proc Natl Acad Sci U S A 99: 8862-8867.
15. Elia C, Cassol E, Sidenius N, Blasi F, Castagna A, et al. (2007) Inhibition of HIV replication by the plasminogen activator is dependent on vitronectin-mediated cell adhesion. J Leukoc Biol 82: 1212-1220.
16. Alfano MC, Poli LG, (2006) Glycosyl phosphatidylinositol-anchored proteins and HIV infection. Letters in Drug Design and Discovery 3: 598-604.
17. Shushakova N, Tkachuk N, Dangers M, Tkachuk S, Park JK, et al. (2005) Urokinase-induced activation of the gp130/Tyk2/Stat3 pathway mediates a pro-inflammatory effect in human mesangial cells via expression of the anaphylatoxin C5a receptor. J Cell Sci 118: 2743-2753.
18. Simon DI, Rao NK, Xu H, Wei Y, Majdic O, et al. (1996) Mac-1 (CD11b/CD18) and the urokinase receptor (CD87) form a functional unit on monocytic cells. Blood 88: 3185-3194.
19. Alfano M, Mariani SA, Elia C, Pardi R, Blasi F, et al. (2009) Ligand-engaged urokinase-type plasminogen activator receptor and activation of the CD11b/CD18 integrin inhibit late events of HIV expression in monocytic cells. Blood 113: 1699-1709.
20. Wada M, Wada NA, Shirono H, Taniguchi K, Tsuchie H, et al. (2001) Amino-terminal fragment of urokinase-type plasminogen activator inhibits HIV-1 replication. Biochem Biophys Res Commun 284: 346-351.
21. Stevenson M, (2003) HIV-1 pathogenesis. Nat Med 9: 853-860.
22. Gendelman HE, Lipton SA, Tardieu M, Bukrinsky MI, Nottet HS, (1994) The neuropathogenesis of HIV-1 infection. J Leukoc Biol 56: 389-398.
23. Biswas P, Poli G, Kinter AL, Justement JS, Stanley SK, et al. (1992) Interferon gamma induces the expression of human immunodeficiency virus in persistently infected promonocytic cells (U1) and redirects the production of virions to intracytoplasmic vacuoles in phorbol myristate acetate-differentiated U1 cells. J Exp Med 176: 739-750.
24. Fantuzzi L, Spadaro F, Vallanti G, Canini I, Ramoni C, et al. (2003) Endogenous CCL2 (monocyte chemotactic protein-1) modulates human immunodeficiency virus type-1 replication and affects cytoskeleton organization in human monocyte-derived macrophages. Blood.
25. Mulloy JC, Cancelas JA, Filippi MD, Kalfa TA, Guo F, et al. Rho GTPases in hematopoiesis and hemopathies. Blood 115: 936-947.
26. Alfano M, Rizzi C, Poli G, Biswas P, (2007) HIV-1 Infection of promonocytic U937 and U1 cell lines. Clonal distribution of innate restriction factors. In: Herbein G, editors. HIV and the Macrophage Kerala, India Transworld Research Network pp. 89-113.
27. Ploug M, Ellis V, (1994) Structure-function relationships in the receptor for urokinase-type plasminogen activator. Comparison to other members of the Ly-6 family and snake venom alpha-neurotoxins. FEBS Lett 349: 163-168.
28. Konecny G, Untch M, Pihan A, Kimmig R, Gropp M, et al. (2001) Association of urokinase-type plasminogen activator and its inhibitor with disease progression and prognosis in ovarian cancer. Clin Cancer Res 7: 1743-1749.
29. Sidenius N, Nebuloni M, Sala S, Zerbi P, Price RW, et al. (2004) Expression of the urokinase plasminogen activator and its receptor in HIV-1-associated central nervous system disease. J Neuroimmunol 157: 133-139.
30. Giagulli C, Scarpini E, Ottoboni L, Narumiya S, Butcher EC, et al. (2004) RhoA and zeta PKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity 20: 25-35.
31. Fernie BF, Poli G, Fauci AS, (1991) Alpha interferon suppresses virion but not soluble human immunodeficiency virus antigen production in chronically infected T-lymphocytic cells. J Virol 65: 3968-3971.
32. Bhadriraju K, Yang M, Alom Ruiz S, Pirone D, Tan J, et al. (2007) Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Exp Cell Res 313: 3616-3623.
33. Slater SJ, Seiz JL, Stagliano BA, Stubbs CD, (2001) Interaction of protein kinase C isozymes with Rho GTPases. Biochemistry 40: 4437-4445.
34. Laurence J, Sikder SK, Jhaveri S, Salmon JE, (1990) Phorbol ester-mediated induction of HIV-1 from a chronically infected promonocyte clone: blockade by protein kinase inhibitors and relationship to tat-directed trans-activation. Biochem Biophys Res Commun 166: 349-357.
35. Thodeti CK, Albrechtsen R, Grauslund M, Asmar M, Larsson C, et al. (2003) ADAM12/syndecan-4 signaling promotes beta 1 integrin-dependent cell spreading through protein kinase Calpha and RhoA. J Biol Chem 278: 9576-9584.
36. Mackay HJ, Twelves CJ, (2007) Targeting the protein kinase C family: are we there yet? Nat Rev Cancer 7: 554-562.
37. Busso N, Masur SK, Lazega D, Waxman S, Ossowski L, (1994) Induction of cell migration by pro-urokinase binding to its receptor: possible mechanism for signal transduction in human epithelial cells. J Cell Biol 126: 259-270.
38. Kamiya K, Ryer E, Sakakibara K, Zohlman A, Kent KC, et al. (2007) Protein kinase C delta activated adhesion regulates vascular smooth muscle cell migration. J Surg Res 141: 91-96.
39. Kindzelskii AL, Laska ZO, Todd RF 3rd, Petty HR, (1996) Urokinase-type plasminogen activator receptor reversibly dissociates from complement receptor type 3 (alpha M beta 2′ CD11b/CD18) during neutrophil polarization. J Immunol 156: 297-309.
40. Estreicher A, Muhlhauser J, Carpentier JL, Orci L, Vassalli JD, (1990) The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J Cell Biol 111: 783-792.
41. Soede RD, Zeelenberg IS, Wijnands YM, Kamp M, Roos E, (2001) Stromal cell-derived factor-1-induced LFA-1 activation during in vivo migration of T cell hybridoma cells requires Gq/11, RhoA, and myosin, as well as Gi and Cdc42. J Immunol 166: 4293-4301.
42. Larsson C, (2006) Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal 18: 276-284.
43. Picone R, Kajtaniak EL, Nielsen LS, Behrendt N, Mastronicola MR, et al. (1989) Regulation of urokinase receptors in monocytelike U937 cells by phorbol ester phorbol myristate acetate. J Cell Biol 108: 693-702.
44. Audoly G, Popoff MR, Gluschankof P, (2005) Involvement of a small GTP binding protein in HIV-1 release. Retrovirology 2: 48.
45. Sasaki H, Nakamura M, Ohno T, Matsuda Y, Yuda Y, et al. (1995) Myosin-actin interaction plays an important role in human immunodeficiency virus type 1 release from host cells. Proc Natl Acad Sci U S A 92: 2026-2030.
46. Ren XD, Kiosses WB, Schwartz MA, (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. Embo J 18: 578-585.
47. Luckenbill-Edds L, (1990) Effect of cytochalasin D on the adhesion of a neuroblastoma x glioma cell line (NG108-15) to laminin and plastic substrates. Cell Tissue Res 260: 485-493.
48. Casella JF, Flanagan MD, Lin S, (1981) Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293: 302-305.
49. Wakatsuki T, Schwab B, Thompson NC, Elson EL, (2001) Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J Cell Sci 114: 1025-1036.
50. Kiian I, Tkachuk N, Haller H, Dumler I, (2003) Urokinase-induced migration of human vascular smooth muscle cells requires coupling of the small GTPases RhoA and Rac1 to the Tyk2/PI3-K signalling pathway. Thromb Haemost 89: 904-914.
51. Laudanna C, Campbell JJ, Butcher EC, (1996) Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271: 981-983.
52. Bolomini-Vittori M, Montresor A, Giagulli C, Staunton D, Rossi B, et al. (2009) Regulation of conformer-specific activation of the integrin LFA-1 by a chemokine-triggered Rho signaling module. Nat Immunol 10: 185-194.
53. Surin B, Rouillard D, Bauvois B, (2002) Interactions between human monocytes and fibronectin are suppressed by interferons beta and gamma, but not alpha: correlation with Rho-paxillin signaling. Int J Mol Med 10: 25-31.
54. Aepfelbacher M, Essler M, Huber E, Czech A, Weber PC, (1996) Rho is a negative regulator of human monocyte spreading. J Immunol 157: 5070-5075.
55. Cavnar PJ, Berthier E, Beebe DJ, Huttenlocher A, Hax1 regulates neutrophil adhesion and motility through RhoA. J Cell Biol 193: 465-473.
56. Wang L, Zhang H, Solski PA, Hart MJ, Der CJ, et al. (2000) Modulation of HIV-1 replication by a novel RhoA effector activity. J Immunol 164: 5369-5374.
57. Hodges A, Sharrocks K, Edelmann M, Baban D, Moris A, et al. (2007) Activation of the lectin DC-SIGN induces an immature dendritic cell phenotype triggering Rho-GTPase activity required for HIV-1 replication. Nat Immunol 8: 569-577.
58. Fackler OT, Krausslich HG, (2006) Interactions of human retroviruses with the host cell cytoskeleton. Curr Opin Microbiol 9: 409-415.
59. Ott DE, Coren LV, Johnson DG, Kane BP, Sowder RC 2nd, et al. (2000) Actin-binding cellular proteins inside human immunodeficiency virus type 1. Virology 266: 42-51.
60. Kinter AL, Poli G, Maury W, Folks TM, Fauci AS, (1990) Direct and cytokine-mediated activation of protein kinase C induces human immunodeficiency virus expression in chronically infected promonocytic cells. J Virol 64: 4306-4312.
61. Rabbi MF, al-Harthi L, Saifuddin M, Roebuck KA, (1998) The cAMP-dependent protein kinase A and protein kinase C-beta pathways synergistically interact to activate HIV-1 transcription in latently infected cells of monocyte/macrophage lineage. Virology 245: 257-269.
62. Wolf D, Giese SI, Witte V, Krautkramer E, Trapp S, et al. (2008) Novel (n)PKC kinases phosphorylate Nef for increased HIV transcription, replication and perinuclear targeting. Virology 370: 45-54.
63. Ivaska J, Vuoriluoto K, Huovinen T, Izawa I, Inagaki M, et al. (2005) PKCepsilon-mediated phosphorylation of vimentin controls integrin recycling and motility. Embo J 24: 3834-3845.
64. Wichroski MJ, Ichiyama K, Rana TM, (2005) Analysis of HIV-1 viral infectivity factor-mediated proteasome-dependent depletion of APOBEC3G: correlating function and subcellular localization. J Biol Chem 280: 8387-8396.
65. Karczewski MK, Strebel K, (1996) Cytoskeleton association and virion incorporation of the human immunodeficiency virus type 1 Vif protein. J Virol 70: 494-507.
66. Shoeman RL, Huttermann C, Hartig R, Traub P, (2001) Amino-terminal polypeptides of vimentin are responsible for the changes in nuclear architecture associated with human immunodeficiency virus type 1 protease activity in tissue culture cells. Mol Biol Cell 12: 143-154.
67. Vieira OV, Botelho RJ, Grinstein S, (2002) Phagosome maturation: aging gracefully. Biochem J 366: 689-704.
68. Carter CA, Ehrlich LS, (2008) Cell biology of HIV-1 infection of macrophages. Annu Rev Microbiol 62: 425-443.
69. Banerjee J, Wedegaertner PB, (2004) Identification of a novel sequence in PDZ-RhoGEF that mediates interaction with the actin cytoskeleton. Mol Biol Cell 15: 1760-1775.
70. Niggli V, (2003) Microtubule-disruption-induced and chemotactic-peptide-induced migration of human neutrophils: implications for differential sets of signalling pathways. J Cell Sci 116: 813-822.
71. Laudanna C, Alon R, (2006) Right on the spot. Chemokine triggering of integrin-mediated arrest of rolling leukocytes. Thromb Haemost 95: 5-11.
72. Azab AK, Azab F, Blotta S, Pitsillides CM, Thompson B, et al. (2009) RhoA and Rac1 GTPases play major and differential roles in stromal cell-derived factor-1-induced cell adhesion and chemotaxis in multiple myeloma. Blood 114: 619-629.
73. Faix J, Breitsprecher D, Stradal TE, Rottner K, (2009) Filopodia: Complex models for simple rods. Int J Biochem Cell Biol 41: 1656-1664.
74. Madsen CD, Sarra Ferraris GM, Andolfo AP, Cunningham O, Sidenius N, (2007) uPAR-induced cell adhesion and migration: vitronectin provides the key. Journal of Cell Biology 177: 927-939.
75. Sidenius N, Andolfo A, Fesce R, Blasi F, (2002) Urokinase regulates vitronectin binding by controlling urokinase receptor oligomerization. J Biol Chem 277: 27982-27990.
76. Madsen CD, Sidenius N, (2008) The interaction between urokinase receptor and vitronectin in cell adhesion and signalling. Eur J Cell Biol 87: 617-629.
77. Petzinger J, Saltel F, Hersemeyer K, Daniel JM, Preissner KT, et al. (2007) Urokinase receptor (CD87) clustering in detergent-insoluble adhesion patches leads to cell adhesion independently of integrins. Cell Commun Adhes 14: 137-155.
78. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709.