Incorporation of podoplanin into HIV released from HEK-293T cells, but not PBMC, is required for efficient binding to the attachment factor CLEC-2

Retrovirology

Volumn 7, Issue , 2010, Pages

  Chaipan, Chawaree ^a   Steffen, Imke ^b   Tsegaye, Theodros S ^b   Bertram, Stephanie ^b   Glowacka, Ilona ^b   Kato, Yukinari ^c   Schmökel, Jan ^d   Münch, Jan ^d   Simmons, Graham ^e   Gerardy Schahn, Rita ^b   Pöhlmann, Stefan ^a,b  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c YAMAGATA UNIVERSITY   (Japan)

^d UNIVERSITY HOSPITAL ULM   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C TYPE LECTIN LIKE RECEPTOR 2; CD209 ANTIGEN; LECTIN; PODOPLANIN; UNCLASSIFIED DRUG; CLEC2B PROTEIN, HUMAN; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CELL STRAIN HEK293; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BINDING; PROTEIN EXPRESSION; T LYMPHOCYTE; VIRION; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS CULTURE; VIRUS TRANSMISSION; CELL CULTURE; CHEMISTRY; EPITHELIUM CELL; METABOLISM; MONONUCLEAR CELL; PHYSIOLOGY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CELLS, CULTURED; EPITHELIAL CELLS; HIV-1; HUMANS; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; MEMBRANE GLYCOPROTEINS; VIRION; VIRUS ATTACHMENT;

EID: 77952299532     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-7-47     Document Type: Article

References (82)

1. Pöhlmann S, Reeves JD. Cellular entry of HIV: Evaluation of therapeutic targets. Curr Pharm Des 2006, 12:1963-1973. 10.2174/138161206777442155, 16787241.
2. Alkhatib G, Berger EA. HIV coreceptors: from discovery and designation to new paradigms and promise. Eur J Med Res 2007, 12:375-384.
3. Moore JP, Klasse PJ. HIV-1 pathogenesis: the complexities of the CCR5-CCL3L1 complex. Cell Host Microbe 2007, 2:281-283. 10.1016/j.chom.2007.10.005, 18005746.
4. Fatkenheuer G, Nelson M, Lazzarin A, Konourina I, Hoepelman AI, Lampiris H, Hirschel B, Tebas P, Raffi F, Trottier B, Bellos N, Saag M, Cooper DA, Westby M, Tawadrous M, Sullivan JF, Ridgway C, Dunne MW, Felstead S, Mayer H, van der Ryst E. Subgroup analyses of maraviroc in previously treated R5 HIV-1 infection. N Engl J Med 2008, 359:1442-1455. 10.1056/NEJMoa0803154, 18832245.
5. Gulick RM, Lalezari J, Goodrich J, Clumeck N, DeJesus E, Horban A, Nadler J, Clotet B, Karlsson A, Wohlfeiler M, Montana JB, McHale M, Sullivan J, Ridgway C, Felstead S, Dunne MW, van der Ryst E, Mayer H. Maraviroc for previously treated patients with R5 HIV-1 infection. N Engl J Med 2008, 359:1429-1441. 10.1056/NEJMoa0803152, 18832244.
6. Bannert N, Schenten D, Craig S, Sodroski J. The level of CD4 expression limits infection of primary rhesus monkey macrophages by a T-tropic simian immunodeficiency virus and macrophagetropic human immunodeficiency viruses. J Virol 2000, 74:10984-10993. 10.1128/JVI.74.23.10984-10993.2000, 113178, 11069993.
7. Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc Natl Acad Sci USA 1999, 96:5215-5220. 10.1073/pnas.96.9.5215, 21844, 10220446.
8. O'Doherty U, Swiggard WJ, Malim MH. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 2000, 74:10074-10080. 10.1128/JVI.74.21.10074-10080.2000, 102046, 11024136.
9. Ugolini S, Mondor I, Sattentau QJ. HIV-1 attachment: another look. Trends Microbiol 1999, 7:144-149. 10.1016/S0966-842X(99)01474-2, 10217828.
10. Cantin R, Methot S, Tremblay MJ. Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. J Virol 2005, 79:6577-6587. 10.1128/JVI.79.11.6577-6587.2005, 1112128, 15890896.
11. Münch J, Rucker E, Ständker L, Adermann K, Goffinet C, Schindler M, Wildum S, Chinnadurai R, Rajan D, Specht A, Gimenez-Gallego G, Sanchez PC, Fowler DM, Koulov A, Kelly JW, Mothes W, Grivel JC, Margolis L, Keppler OT, Forssmann WG, Kirchhoff F. Semen-derived amyloid fibrils drastically enhance HIV infection. Cell 2007, 131:1059-1071. 10.1016/j.cell.2007.10.014, 18083097.
12. Fortin JF, Cantin R, Lamontagne G, Tremblay M. Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. J Virol 1997, 71:3588-3596. 191506, 9094631.
13. Pöhlmann S, Tremblay M. Attachment of human immunodeficiency virus to cells and its inhibition. Entry Inhibitors in HIV Therapy 2007, 31-47. Basel: Birkhäuser Verlag, Reeves JD, Derdeyn CA.
14. Cameron PU, Freudenthal PS, Barker JM, Gezelter S, Inaba K, Steinman RM. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 1992, 257:383-387. 10.1126/science.1352913, 1352913.
15. Wu L, KewalRamani VN. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 2006, 6:859-868. 10.1038/nri1960, 1796806, 17063186.
16. Geijtenbeek TB, Kwon DS, Torensma R, Van V, van SJ, Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000, 100:587-597. 10.1016/S0092-8674(00)80694-7, 10721995.
17. Appelmelk BJ, Van D I, Van Vliet SJ, Vandenbroucke-Grauls CM, Geijtenbeek TB, van Kooyk Y. Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells. J Immunol 2003, 170:1635-1639.
18. Feinberg H, Mitchell DA, Drickamer K, Weis WI. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 2001, 294:2163-2166. 10.1126/science.1066371, 11739956.
19. Lin G, Simmons G, Pöhlmann S, Baribaud F, Ni H, Leslie GJ, Haggarty BS, Bates P, Weissman D, Hoxie JA, Doms RW. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR. J Virol 2003, 77:1337-1346. 10.1128/JVI.77.2.1337-1346.2003, 140807, 12502850.
20. Lee B, Leslie G, Soilleux E, O'Doherty U, Baik S, Levroney E, Flummerfelt K, Swiggard W, Coleman N, Malim M, Doms RW. cis Expression of DC-SIGN allows for more efficient entry of human and simian immunodeficiency viruses via CD4 and a coreceptor. J Virol 2001, 75:12028-12038. 10.1128/JVI.75.24.12028-12038.2001, 116098, 11711593.
21. Boggiano C, Manel N, Littman DR. Dendritic cell-mediated trans-enhancement of human immunodeficiency virus type 1 infectivity is independent of DC-SIGN. J Virol 2007, 81:2519-2523. 10.1128/JVI.01661-06, 1865951, 17182696.
22. Gummuluru S, Rogel M, Stamatatos L, Emerman M. Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 2003, 77:12865-12874. 10.1128/JVI.77.23.12865-12874.2003, 262553, 14610207.
23. Martin MP, Lederman MM, Hutcheson HB, Goedert JJ, Nelson GW, van Kooyk Y, Detels R, Buchbinder S, Hoots K, Vlahov D, O'Brien SJ, Carrington M. Association of DC-SIGN promoter polymorphism with increased risk for parenteral, but not mucosal, acquisition of human immunodeficiency virus type 1 infection. J Virol 2004, 78:14053-14056. 10.1128/JVI.78.24.14053-14056.2004, 533922, 15564514.
24. Moris A, Pajot A, Blanchet F, Guivel-Benhassine F, Salcedo M, Schwartz O. Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T-cell activation, and viral transfer. Blood 2006, 108:1643-1651. 10.1182/blood-2006-02-006361, 16675708.
25. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, Miranda-Saksena M, Dable J, Stossel H, Romani N, Piatak M, Lifson JD, Pope M, Cunningham AL. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 2004, 103:2170-2179. 10.1182/blood-2003-09-3129, 14630806.
26. Moris A, Nobile C, Buseyne F, Porrot F, Abastado JP, Schwartz O. DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 2004, 103:2648-2654. 10.1182/blood-2003-07-2532, 14576049.
27. Sakuntabhai A, Turbpaiboon C, Casademont I, Chuansumrit A, Lowhnoo T, Kajaste-Rudnitski A, Kalayanarooj SM, Tangnararatchakit K, Tangthawornchaikul N, Vasanawathana S, Chaiyaratana W, Yenchitsomanus PT, Suriyaphol P, Avirutnan P, Chokephaibulkit K, Matsuda F, Yoksan S, Jacob Y, Lathrop GM, Malasit P, Despres P, Julier C. A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet 2005, 37:507-513. 10.1038/ng1550, 15838506.
28. Boukour S, Masse JM, Benit L, Dubart-Kupperschmitt A, Cramer EM. Lentivirus degradation and DC-SIGN expression by human platelets and megakaryocytes. J Thromb Haemost 2006, 4:426-435. 10.1111/j.1538-7836.2006.01749.x, 16420576.
29. Chaipan C, Soilleux EJ, Simpson P, Hofmann H, Gramberg T, Marzi A, Geier M, Stewart EA, Eisemann J, Steinkasserer A, Suzuki-Inoue K, Fuller GL, Pearce AC, Watson SP, Hoxie JA, Baribaud F, Pöhlmann S. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol 2006, 80:8951-8960. 10.1128/JVI.00136-06, 1563896, 16940507.
30. Colonna M, Samaridis J, Angman L. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol 2000, 30:697-704. 10.1002/1521-4141(200002)30:2<697::AID-IMMU697>3.0.CO;2-M, 10671229.
31. Suzuki-Inoue K, Fuller GL, Garcia A, Eble JA, Pöhlmann S, Inoue O, Gartner TK, Hughan SC, Pearce AC, Laing GD, Theakston RD, Schweighoffer E, Zitzmann N, Morita T, Tybulewicz VL, Ozaki Y, Watson SP. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood 2006, 107:542-549. 10.1182/blood-2005-05-1994, 16174766.
32. Fuller GL, Williams JA, Tomlinson MG, Eble JA, Hanna SL, Pöhlmann S, Suzuki-Inoue K, Ozaki Y, Watson SP, Pearce AC. The C-type lectin receptors CLEC-2 and Dectin-1, but not DC-SIGN, signal via a novel YXXL-dependent signaling cascade. J Biol Chem 2007, 282:12397-12409. 10.1074/jbc.M609558200, 1997429, 17339324.
33. Watson AA, O'Callaghan CA. Crystallization and X-ray diffraction analysis of human CLEC-2. Acta Crystallogr Sect F Struct Biol Cryst Commun 2005, 61:1094-1096. 10.1107/S1744309105037991, 1978148, 16511244.
34. Watson AA, Brown J, Harlos K, Eble JA, Walter TS, O'Callaghan CA. The crystal structure and mutational binding analysis of the extracellular domain of the platelet-activating receptor CLEC-2. J Biol Chem 2007, 282:3165-3172. 10.1074/jbc.M610383200, 17132623.
35. Lu TC, He JC, Klotman PE. Podocytes in HIV-associated nephropathy. Nephron Clin Pract 2007, 106:c67-c71. 10.1159/000101800, 17570932.
36. Zimmer G, Oeffner F, Von MV, Tschernig T, Groness HJ, Klenk HD, Herrler G. Cloning and characterization of gp36, a human mucin-type glycoprotein preferentially expressed in vascular endothelium. Biochem J 1999, 341(Pt 2):277-284. 10.1042/0264-6021:3410277, 1220357, 10393083.
37. Breiteneder-Geleff S, Matsui K, Soleiman A, Meraner P, Poczewski H, Kalt R, Schaffner G, Kerjaschki D. Podoplanin, novel 43-kd membrane protein of glomerular epithelial cells, is down-regulated in puromycin nephrosis. Am J Pathol 1997, 151:1141-1152. 1858024, 9327748.
38. Kato Y, Fujita N, Kunita A, Sato S, Kaneko M, Osawa M, Tsuruo T. Molecular identification of Aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors. J Biol Chem 2003, 278:51599-51605. 10.1074/jbc.M309935200, 14522983.
39. Eckhardt M, Muhlenhoff M, Bethe A, Koopman J, Frosch M, Gerardy-Schahn R. Molecular characterization of eukaryotic polysialyltransferase-1. Nature 1995, 373:715-718. 10.1038/373715a0, 7854457.
40. Eckhardt M, Muhlenhoff M, Bethe A, Gerardy-Schahn R. Expression cloning of the Golgi CMP-sialic acid transporter. Proc Natl Acad Sci USA 1996, 93:7572-7576. 10.1073/pnas.93.15.7572, 38787, 8755516.
41. Puthalakath H, Burke J, Gleeson PA. Glycosylation defect in Lec1 Chinese hamster ovary mutant is due to a point mutation in N-acetylglucosaminyltransferase I gene. J Biol Chem 1996, 271:27818-27822. 10.1074/jbc.271.44.27818, 8910379.
42. Wu L, Martin TD, Carrington M, KewalRamani VN. Raji B cells, misidentified as THP-1 cells, stimulate DC-SIGN-mediated HIV transmission. Virology 2004, 318:17-23. 10.1016/j.virol.2003.09.028, 14972530.
43. Means RE, Greenough T, Desrosiers RC. Neutralization sensitivity of cell culture-passaged simian immunodeficiency virus. J Virol 1997, 71:7895-7902. 192146, 9311879.
44. Hsu M, Harouse JM, Gettie A, Buckner C, Blanchard J, Cheng-Mayer C. Increased mucosal transmission but not enhanced pathogenicity of the CCR5-tropic, simian AIDS-inducing simian/human immunodeficiency virus SHIV(SF162P3) maps to envelope gp120. J Virol 2003, 77:989-998. 10.1128/JVI.77.2.989-998.2003, 140803, 12502815.
45. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 1986, 59:284-291. 253077, 3016298.
46. Munch J, Rajan D, Rucker E, Wildum S, Adam N, Kirchhoff F. The role of upstream U3 sequences in HIV-1 replication and CD4+ T cell depletion in human lymphoid tissue ex vivo. Virology 2005, 341:313-320. 10.1016/j.virol.2005.07.023, 16102792.
47. Gramberg T, Zhu T, Chaipan C, Marzi A, Liu H, Wegele A, Andrus T, Hofmann H, Pöhlmann S. Impact of polymorphisms in the DC-SIGNR neck domain on the interaction with pathogens. Virology 2006, 347:354-363. 10.1016/j.virol.2005.11.033, 16413044.
48. Andre S, Seed B, Eberle J, Schraut W, Bultmann A, Haas J. Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J Virol 1998, 72:1497-1503. 124631, 9445053.
49. Birkmann A, Mahr K, Ensser A, Yaguboglu S, Titgemeyer F, Fleckenstein B, Neipel F. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J Virol 2001, 75:11583-11593. 10.1128/JVI.75.23.11583-11593.2001, 114745, 11689640.
50. Pöhlmann S, Baribaud F, Lee B, Leslie GJ, Sanchez MD, Hiebenthal-Millow K, Munch J, Kirchhoff F, Doms RW. DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J Virol 2001, 75:4664-4672. 10.1128/JVI.75.10.4664-4672.2001, 114220, 11312337.
51. Marzi A, Akhavan A, Simmons G, Gramberg T, Hofmann H, Bates P, Lingappa VR, Pöhlmann S. The signal peptide of the ebolavirus glycoprotein influences interaction with the cellular lectins DC-SIGN and DC-SIGNR. J Virol 2006, 80:6305-6317. 10.1128/JVI.02545-05, 1488929, 16775318.
52. Wies E, Mori Y, Hahn A, Kremmer E, Sturzl M, Fleckenstein B, Neipel F. The viral interferon-regulatory factor-3 is required for the survival of KSHV-infected primary effusion lymphoma cells. Blood 2008, 111:320-327. 10.1182/blood-2007-05-092288, 17890449.
53. Suzuki-Inoue K, Kato Y, Inoue O, Kaneko MK, Mishima K, Yatomi Y, Yamazaki Y, Narimatsu H, Ozaki Y. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem 2007, 282:25993-26001. 10.1074/jbc.M702327200, 17616532.
54. Kaneko M, Kato Y, Kunita A, Fujita N, Tsuruo T, Osawa M. Functional sialylated O-glycan to platelet aggregation on Aggrus (T1alpha/Podoplanin) molecules expressed in Chinese hamster ovary cells. J Biol Chem 2004, 279:38838-38843. 10.1074/jbc.M407210200, 15231832.
55. Rudensey LM, Papenhausen MD, Overbaugh J. Replication and persistence of simian immunodeficiency virus variants after passage in macaque lymphocytes and established human cell lines. J Virol 1993, 67:1727-1733. 237552, 8437241.
56. Sei Y, Inoue M, Yokoyama MM, Bekesi JG, Arora PK. Characterization of human B cell (DK) and promonocyte (U937) clones after HIV-1 exposure: accumulation of viral reverse transcriptase activity in cells and early syncytia induction against SupT1 cells. Cell Immunol 1990, 125:1-13. 10.1016/0008-8749(90)90058-Y, 1688402.
57. Franz S, Herrmann K, Furnrohr BG, Sheriff A, Frey B, Gaipl US, Voll RE, Kalden JR, Jack HM, Herrmann M. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ 2007, 14:733-742. 10.1038/sj.cdd.4402066, 17170754.
58. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, Bratton DL, Oldenborg PA, Michalak M, Henson PM. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005, 123:321-l334. 10.1016/j.cell.2005.08.032, 16239148.
59. Perfetto SP, Chattopadhyay PK, Roederer M. Seventeen-colour flow cytometry: unravelling the immune system. Nat Rev Immunol 2004, 4:648-655. 10.1038/nri1416, 15286731.
60. Kato Y, Kaneko MK, Kuno A, Uchiyama N, Amano K, Chiba Y, Hasegawa Y, Hirabayashi J, Narimatsu H, Mishima K, Osawa M. Inhibition of tumor cell-induced platelet aggregation using a novel anti-podoplanin antibody reacting with its platelet-aggregation-stimulating domain. Biochem Biophys Res Commun 2006, 349:1301-1307. 10.1016/j.bbrc.2006.08.171, 16979138.
61. Ogasawara S, Kaneko MK, Price JE, Kato Y. Characterization of anti-podoplanin monoclonal antibodies: critical epitopes for neutralizing the interaction between podoplanin and CLEC-2. Hybridoma (Larchmt) 2008, 27:259-267. 10.1089/hyb.2008.0017, 18707544.
62. Noble ME, Endicott JA, Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 2004, 303:1800-1805. 10.1126/science.1095920, 15031492.
63. Cossarizza A. Apoptosis and HIV infection: about molecules and genes. Curr Pharm Des 2008, 14:237-244. 10.2174/138161208783413293, 18220834.
64. Bolton DL, Hahn BI, Park EA, Lehnhoff LL, Hornung F, Lenardo MJ. Death of CD4(+) T-cell lines caused by human immunodeficiency virus type 1 does not depend on caspases or apoptosis. J Virol 2002, 76:5094-5107. 10.1128/JVI.76.10.5094-5107.2002, 136143, 11967325.
65. Bashirova AA, Wu L, Cheng J, Martin TD, Martin MP, Benveniste RE, Lifson JD, KewalRamani VN, Hughes A, Carrington M. Novel member of the CD209 (DC-SIGN) gene family in primates. J Virol 2003, 77:217-227. 10.1128/JVI.77.1.217-227.2003, 140574, 12477827.
66. Gramberg T, Soilleux E, Fisch T, Lalor PF, Hofmann H, Wheeldon S, Cotterill A, Wegele A, Winkler T, Adams DH, Pöhlmann S. Interactions of LSECtin and DC-SIGN/DC-SIGNR with viral ligands: Differential pH dependence, internalization and virion binding. Virology 2008, 373:189-201. 10.1016/j.virol.2007.11.001, 18083206.
67. Pöhlmann S, Soilleux EJ, Baribaud F, Leslie GJ, Morris LS, Trowsdale J, Lee B, Coleman N, Doms RW. DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci USA 2001, 98:2670-2675. 10.1073/pnas.051631398, 30196, 11226297.
68. Piguet V, Steinman RM. The interaction of HIV with dendritic cells: outcomes and pathways. Trends Immunol 2007, 28:503-510. 10.1016/j.it.2007.07.010, 17950666.
69. Christou CM, Pearce AC, Watson AA, Mistry AR, Pollitt AY, Fenton-May AE, Johnson LA, Jackson DG, Watson SP, O'Callaghan CA. enal cells activate the platelet receptor CLEC-2 through podoplanin. Biochem J 2008, 411:133-140. 10.1042/BJ20071216, 2749330, 18215137.
70. Suzuki H, Kato Y, Kaneko MK, Okita Y, Narimatsu H, Kato M. Induction of podoplanin by transforming growth factor-beta in human fibrosarcoma. FEBS Lett 2008, 582:341-345. 10.1016/j.febslet.2007.12.028, 18158922.
71. Kato Y, Kaneko MK, Kunita A, Ito H, Kameyama A, Ogasawara S, Matsuura N, Hasegawa Y, Suzuki-Inoue K, Inoue O, Ozaki Y, Narimatsu H. Molecular analysis of the pathophysiological binding of the platelet aggregation-inducing factor podoplanin to the C-type lectin-like receptor CLEC-2. Cancer Sci 2008, 99:54-61.
72. Kalof AN, Cooper K. D2-40 immunohistochemistry--so far!. Adv Anat Pathol 2009, 16:62-64. 10.1097/PAP.0b013e3181915e94, 19098468.
73. Gessain A, Duprez R. Spindle cells and their role in Kaposi's sarcoma. Int J Biochem Cell Biol 2005, 37:2457-2465. 10.1016/j.biocel.2005.01.018, 16188485.
74. Kunita A, Kashima TG, Morishita Y, Fukayama M, Kato Y, Tsuruo T, Fujita N. The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am J Pathol 2007, 170:1337-1347. 10.2353/ajpath.2007.060790, 1829466, 17392172.
75. Ozaki Y, Suzuki-Inoue K, Inoue O. Novel interactions in platelet biology: CLEC-2/podoplanin and laminin/GPVI. J Thromb Haemost 2009, (7 Suppl 1):191-194. 10.1111/j.1538-7836.2009.03372.x, 19630798.
76. Batisse C, Marquet J, Greffard A, Fleury-Feith J, Jaurand MC, Pilatte Y. Lectin-based three-color flow cytometric approach for studying cell surface glycosylation changes that occur during apoptosis. Cytometry A 2004, 62:81-88. 10.1002/cyto.a.20094, 15536639.
77. Scaradavou A. HIV-related thrombocytopenia. Blood Rev 2002, 16:73-76. 10.1054/blre.2001.0188, 11914001.
78. Shen YM, Frenkel EP. Thrombosis and a hypercoagulable state in HIV-infected patients. Clin Appl Thromb Hemost 2004, 10:277-280. 10.1177/107602960401000311, 15247986.
79. Steffan AM, Lafon ME, Gendrault JL, Schweitzer C, Royer C, Jaeck D, Arnaud JP, Schmitt MP, Aubertin AM, Kirn A. Primary cultures of endothelial cells from the human liver sinusoid are permissive for human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1992, 89:1582-1586. 10.1073/pnas.89.5.1582, 48496, 1371878.
80. Zucker-Franklin D, Cao YZ. Megakaryocytes of human immunodeficiency virus-infected individuals express viral RNA. Proc Natl Acad Sci USA 1989, 86:5595-5599. 10.1073/pnas.86.14.5595, 297669, 2748605.
81. Zucker-Franklin D, Seremetis S, Zheng ZY. Internalization of human immunodeficiency virus type I and other retroviruses by megakaryocytes and platelets. Blood 1990, 75:1920-1923.
82. Bailey D, Baumal R, Law J, Sheldon K, Kannampuzha P, Stratis M, Kahn H, Marks A. Production of a monoclonal antibody specific for seminomas and dysgerminomas. Proc Natl Acad Sci USA 1986, 83:5291-5295. 10.1073/pnas.83.14.5291, 323937, 3523489.