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BMC Cancer

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Open Access 01-12-2011 | Research article

Targeting surface nucleolin with multivalent HB-19 and related Nucant pseudopeptides results in distinct inhibitory mechanisms depending on the malignant tumor cell type

Authors: Bernard Krust, Diala El Khoury, Isabelle Nondier, Calaiselvy Soundaramourty, Ara G Hovanessian

Published in: BMC Cancer | Issue 1/2011

Abstract

Background

Nucleolin expressed at the cell surface is a binding protein for a variety of ligands implicated in tumorigenesis and angiogenesis. By using a specific antagonist that binds the C-terminal RGG domain of nucleolin, the HB-19 pseudopeptide, we recently reported that targeting surface nucleolin with HB-19 suppresses progression of established human breast tumor cells in the athymic nude mice, and delays development of spontaneous melanoma in the RET transgenic mice.

Methods

By the capacity of HB-19 to bind stably surface nucleolin, we purified and identified nucleolin partners at the cell surface. HB-19 and related multivalent Nucant pseudopeptides, that present pentavalently or hexavalently the tripeptide Lysψ(CH₂N)-Pro-Arg, were then used to show that targeting surface nucleolin results in distinct inhibitory mechanisms on breast, prostate, colon carcinoma and leukemia cells.

Results

Surface nucleolin exists in a 500-kDa protein complex including several other proteins, which we identified by microsequencing as two Wnt related proteins, Ku86 autoantigen, signal recognition particle subunits SRP68/72, the receptor for complement component gC1q-R, and ribosomal proteins S4/S6. Interestingly, some of the surface-nucleolin associated proteins are implicated in cell signaling, tumor cell adhesion, migration, invasion, cell death, autoimmunity, and bacterial infections. Surface nucleolin in the 500-kDa complex is highly stable. Surface nucleolin antagonists, HB-19 and related multivalent Nucant pseudopeptides, exert distinct inhibitory mechanisms depending on the malignant tumor cell type. For example, in epithelial tumor cells they inhibit cell adhesion or spreading and induce reversion of the malignant phenotype (BMC cancer 2010, 10:325) while in leukemia cells they trigger a rapid cell death associated with DNA fragmentation. The fact that these pseudopeptides do not cause cell death in epithelial tumor cells indicates that cell death in leukemia cells is triggered by a specific signaling mechanism, rather than nonspecific cellular injury.

Conclusions

Our results suggest that targeting surface nucleolin could change the organization of the 500-kDa complex to interfere with the proper functioning of surface nucleolin and the associated proteins, and thus lead to distinct inhibitory mechanisms. Consequently, HB-19 and related Nucant pseudopeptides provide novel therapeutic opportunities in treatment of a wide variety of cancers and related malignancies.

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Srivastava M, Pollard HB: Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J. 1999, 13: 1911-1922.PubMed

Ginisty H, Sicard H, Roger B, Bouvet P: Structure and functions of nucleolin. J Cell Science. 1999, 112: 761-772.PubMed

Storck S, Shukla M, Dimitrov S, Bouvet P: Functions of the histone chaperone nucleolin in diseases. Subcell Biochem. 2007, 41: 125-144. 10.1007/1-4020-5466-1_7.PubMed

Fahling M, Steege A, Perlewitz A, Nafz B, Mrowka R, Persson PB, Thiele BJ: Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim Biophys Acta. 2005, 1731: 32-40.PubMed

Otake Y, Soundararajan S, Sengupta TK, Kio EA, Smith JC, Pineda-Roman M, Stuart RK, Spicer EK, Fernandes DJ: Overexpression of nucleolin in chronic lymphocytic leukemia cells induces stabilization of bcl2 mRNA. Blood. 2007, 109: 3069-3075.PubMedPubMedCentral

Hovanessian AG, Puvion-Dutilleul F, Nisole S, Svab J, Perret E, Deng JS, Krust B: The cell-surface-expressed nucleolin is associated with the actin cytoskeleton. Exp Cell Res. 2000, 261: 312-328. 10.1006/excr.2000.5071.PubMed

Hovanessian AG: Midkine is a cytokine that inhibits HIV infection by binding to the cell surface expressed nucleolin. Cell Res. 2006, 16: 174-181. 10.1038/sj.cr.7310024.PubMed

Callebaut C, Blanco J, Benkirane N, Krust B, Jacotot E, Guichard G, Seddiki N, Svab J, Dam E, Muller S, Briand JP, Hovanessian AG: Identification of V3 loop-binding proteins as potential receptors implicated in the binding of HIV particles to CD4⁺ cells. J Biol Chem. 1998, 273: 21988-21997. 10.1074/jbc.273.34.21988.PubMed

Nisole S, Said EA, Mische C, Prevost MC, Krust B, Bouvet P, Bianco A, Briand JP, Hovanessian AG: The anti-HIV pentameric pseudopeptide HB-19 binds the C-terminal end of nucleolin and prevents anchorage of virus particles in the plasma membrane of target cells. J Biol Chem. 2002, 277: 20877-20886. 10.1074/jbc.M110024200.PubMed

10.

Nisole S, Krust B, Hovanessian AG: Anchorage of HIV on permissive cells leads to co-aggregation of viral particles with surface nucleolin at membrane raft microdomains. Exp Cell Res. 2002, 276: 155-173. 10.1006/excr.2002.5522.PubMed

11.

Sinclair JF, O'Brien AD: Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J Biol Chem. 2002, 277: 2876-2885. 10.1074/jbc.M110230200.PubMed

12.

Barel M, Hovanessian AG, Meibom K, Briand JP, Dupuis M, Charbit A: A novel receptor - ligand pathway for entry of Francisella tularensis in monocyte-like THP-1 cells: interaction between surface nucleolin and bacterial elongation factor Tu. BMC Microbiol. 2008, 8: 145-10.1186/1471-2180-8-145.PubMedPubMedCentral

13.

Losfeld ME, El Khoury D, Mariot P, Carpentier M, Krust B, Briand JP, Mazurier J, Hovanessian AG, Legrand D: The cell surface expressed nucleolin is a glycoprotein that triggers calcium entry into mammalian cells. Exp Cell Res. 2009, 315: 357-369. 10.1016/j.yexcr.2008.10.039.PubMed

14.

Aldi S, Della Giovampaola C, Focarelli R, Armini A, Ziche M, Finetti F, Rosati F: A fucose-containing O-glycoepitope on bovine and human nucleolin. Glycobiology. 2009, 19: 337-343.PubMed

15.

Hovanessian AG, Soundaramourty C, El Khoury D, Nondier I, Svab J, Krust B: Surface expressed nucleolin is constantly induced in tumor cells to mediate calcium-dependent ligand internalization. PLoS One. 2010, 5 (12): e15787-10.1371/journal.pone.0015787.PubMedPubMedCentral

16.

Nisole S, Krust B, Callebaut C, Guichard G, Muller S, Briand JP, Hovanessian AG: The anti-HIV pseudopeptide HB-19 forms a complex with the cell-surface expressed nucleolin independent of heparan sulfate proteoglycans. J Biol Chem. 1999, 274: 27875-27884. 10.1074/jbc.274.39.27875.PubMed

17.

Said AE, Krust B, Nisole S, Briand JP, Hovanessian AG: The anti-HIV cytokine midkine binds the cell-surface-expressed nucleolin as a low affinity receptor. J Biol Chem. 2002, 277: 37492-37502. 10.1074/jbc.M201194200.PubMed

18.

Legrand D, Vigie K, Said EA, Elass E, Masson M, Slomianny MC, Carpentier M, Briand JP, Mazurier J, Hovanessian AG: Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells. Eur J Biochem. 2004, 271: 303-317. 10.1046/j.1432-1033.2003.03929.x.PubMed

19.

Said EA, Courty J, Svab J, Delbé J, Krust B, Hovanessian AG: Pleiotrophin inhibits HIV infection by binding the cell surface expressed nucleolin. FEBS J. 2005, 272: 4646-4659. 10.1111/j.1742-4658.2005.04870.x.PubMed

20.

Stepanova V, Lebedeva T, Kuo A, Yarovoi S, Tkachuk S, Zaitsev S, Bdeir K, Dumler I, Marks MS, Parfyonova Y, Tkachuk VA, Higazi AA, Cines DB: Nuclear translocation of urokinase-type plasminogen activator. Blood. 2008, 112: 100-110. 10.1182/blood-2007-07-104455.PubMedPubMedCentral

21.

Shibata Y, Muramatsu T, Hirai M, Inui M, Kimura T, Saito H, McCormack LM, Bu G, Kadomatsu K: Nuclear targeting by the growth factor midkine. Mol Cell Biol. 2002, 22: 6788-6796. 10.1128/MCB.22.19.6788-6796.2002.PubMedPubMedCentral

22.

Alete DE, Weeks ME, Hovanessian AG, Hawadle M, Stoker AW: Cell surface nucleolin on developing muscle is a potential ligand for the axonal receptor protein tyrosine phosphatase-sigma. FEBS J. 2006, 273 (20): 4668-4681. 10.1111/j.1742-4658.2006.05471.x.PubMedPubMedCentral

23.

Grinstein E, Wernet P: Cellular signaling in normal and cancerous stem cells. Cell Signal. 2007, 19: 2428-2433. 10.1016/j.cellsig.2007.06.021.PubMed

24.

Di Segni A, Farin K, Pinkas-Kramarski R: Identification of nucleolin as new ErbB receptors-interacting protein. PLoS ONE. 2008, 3 (6): e2310-10.1371/journal.pone.0002310.PubMedPubMedCentral

25.

Inder KL, Lau C, Loo D, Chaudhary N, Goodall A, Martin S, Jones A, van der Hoeven D, Parton RG, Hill MM, Hancock JF: Nucleophosmin and nucleolin regulate K-Ras plasma membrane interactions and MAPK signal transduction. J Biol Chem. 2009, 284: 28410-28419. 10.1074/jbc.M109.001537.PubMedPubMedCentral

26.

Reyes-Reyes EM, Akiyama SK: Cell-surface nucleolin is a signal transducing P-selectin binding protein for human colon carcinoma cells. Exp Cell Res. 2008, 314: 2212-2223. 10.1016/j.yexcr.2008.03.016.PubMedPubMedCentral

27.

Kleinman HK, Weeks BS, Cannon FB, Sweeney TM, Sephel GC, Clement B, Zain M, Olson MOJ, Jucker M, Burrous BA: Identification of a 110-kDa nonintegrin cell surface laminin-binding protein which recognizes an A chain neurite-promoting peptide. Arch Biochem Biophys. 1991, 290: 320-325. 10.1016/0003-9861(91)90547-V.PubMed

28.

Larrucea S, Gonzalez-Rubio C, Cambronero R, Ballou B, Bonay P, Lopez-Granados E, Bouver P, Fontan M, Fresno M, Lopez-Trascasa M: Cellular adhesion mediated by factor J, a complement inhibitor. Evidence for nucleolin involvement. J Biol Chem. 1998, 273: 31718-31725. 10.1074/jbc.273.48.31718.PubMed

29.

Harms G, Kraft R, Grelle G, Volz B, Dernedde J, Tauber R: Identification of nucleolin as a new L-selectin ligand. Biochem J. 2001, 360: 531-538. 10.1042/0264-6021:3600531.PubMedPubMedCentral

30.

Christian S, Pilch J, Akerman ME, Porkka K, Laakkonen P, Ruoslahti E: Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J Cell Biol. 2003, 163: 871-878. 10.1083/jcb.200304132.PubMedPubMedCentral

31.

Kadomatsu K, Muramatsu T: Midkine and pleiotrophin in neural development and cancer. Cancer Lett. 2004, 204: 127-143. 10.1016/S0304-3835(03)00450-6.PubMed

32.

Tate A, Isotani S, Bradley MJ, Sikes RA, Davis R, Chung LW, Edlund M: Met-independent hepatocyte growth factor-mediated regulation of cell adhesion in human prostate cancer cells. BMC Cancer. 2006, 6: 197-212. 10.1186/1471-2407-6-197.PubMedPubMedCentral

33.

Turck N, Lefebvre O, Gross I, Gendry P, Kedinger M, Simon-Assmann P, Launay JF: Effect of laminin-1 on intestinal cell differentiation involves inhibition of nuclear nucleolin. J Cell Physiol. 2006, 2006: 545-555.

34.

Huang Y, Shi H, HZ, Song X, Yuan S, Luo Y: The angiogenesis function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin. Blood. 2006, 107: 3564-3571. 10.1182/blood-2005-07-2961.PubMed

35.

Shi H, Huang Y, Zhou H, Song X, Yuan S, Fu Y, Luo Y: Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood. 2007, 110: 2899-2906. 10.1182/blood-2007-01-064428.PubMed

36.

Perez-Pinera P, Berenson JR, Deuel TF: Pleiotrophin, a multifunctional angiogenic factor: mechanisms and pathways in normal and pathological angiogenesis. Curr Opin Hematol. 2008, 15: 210-214. 10.1097/MOH.0b013e3282fdc69e.PubMed

37.

Destouches D, El Khoury D, Hamma-Kourbali Y, Krust B, Albanese P, Katsoris P, Guichard G, Briand JP, Courty J, Hovanessian AG: Suppression of tumor growth and angiogenesis by a specific antagonist of the cell-surface expressed nucleolin. PLoS ONE. 2008, 3 (6): e2518-10.1371/journal.pone.0002518.PubMedPubMedCentral

38.

El Khoury D, Destouches D, Lengagne R, Krust B, Hamma-Kourbali Y, Garcette M, Niro S, Kato M, Briand JP, Courty J, Hovanessian AG: Targeting Surface Nucleolin with a Multivalent Pseudopeptide Delays Development of Spontaneous Melanoma in RET Transgenic Mice. BMC Cancer. 2010, 10: 325-10.1186/1471-2407-10-325.PubMedPubMedCentral

39.

Xu X, Hamhouyia F, Thomas SD, Burke TJ, Girvan AC, McGregor WG, Trent JO, Miller DM, Bates PJ: Inhibition of DNA replication and induction of S phase cell cycle arrest by G-rich oligonucleotides. J Biol Chem. 2001, 276: 43221-43230. 10.1074/jbc.M104446200.PubMed

40.

Bates PJ, Laber DA, Miller DM, Thomas SD, Trent JO: Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp Mol Pathol. 2009, 86: 151-164. 10.1016/j.yexmp.2009.01.004.PubMedPubMedCentral

41.

Soundararajan S, Wang L, Sridharan V, Chen W, Courtenay-Luck N, Jones D, Spicer EK, Fernandes DJ: Plasma membrane nucleolin is a receptor for the anticancer aptamer AS1411 in MV4-11 leukemia cells. Mol Pharmacol. 2009, 76: 984-991. 10.1124/mol.109.055947.PubMedPubMedCentral

42.

Krust B, El Khoury D, Soundaramourty C, Nondier I, Hovanessian AG: Suppression of tumorigenicity of rhabdoid tumor derived G401 cells by the multivalent HB-19 pseudopeptide that targets surface nucleolin. Biochimie. 2011, 93: 426-433. 10.1016/j.biochi.2010.10.015.PubMed

43.

Courty J, Hovanessian AG, Briand JP, Guichard G, Hamma-Kourbali Y: Use of multivalent synthetic ligands of surface nucleolin for treating cancer or inflammation. WO 2007/125210 A2. 2007

44.

Briand JP, Guichard G, Zimmer R: New optically pure compounds for improved therapeutic efficiency. WO 2009/141687 A1. 2009

45.

Nisole S, Krust B, Dam E, Blanco A, Seddiki N, Loaec S, Callebaut C, Guichard G, Muller S, Briand JP, Hovanessian AG: The HB-19 pseudopeptide 5[Kψ(CH₂N)PR]-TASP inhibits attachment of T-lymphocyte- and macrophage-tropic HIV to permissive cells. AIDS Res Hum Retroviruses. 2000, 16: 237-249. 10.1089/088922200309331.PubMed

46.

Dumortier A, Jeannet R, Kirstetter P, Kleinmann E, Sellars M, dos Santos NR, Thibault C, Barths J, Ghysdael J, Punt JA, Kastner P, Chan S: Notch activation is an early and critical event during T-Cell leukemogenesis in Ikaros-deficient mice. Mol Cell Biol. 2006, 26: 209-220. 10.1128/MCB.26.1.209-220.2006.PubMedPubMedCentral

47.

FitzGerald DJ, Fryling CM, Zdanovsky A, Saelinger CB, Kounnas M, Winkles JA, Strickland D, Leppla S: Pseudomonas exotoxin-mediated selection yields cells with altered expression of low-density lipoprotein receptor-related protein. J Cell Biol. 1995, 129: 1533-1541. 10.1083/jcb.129.6.1533.PubMed

48.

Callebaut C, Jacotot E, Guichard G, Krust B, Rey-Cuille MA, Cointe D, Benkirane N, Blanco J, Muller S, Briand JP, Hovanessian AG: Inhibition of HIV infection by pseudopeptides blocking viral envelope glycoprotein-mediated membrane fusion and cell death. Virology. 1996, 218: 181-192. 10.1006/viro.1996.0178.PubMed

49.

Destouches D, Page N, Hamma-Kourbali Y, Machi V, Chaloin O, Frechault S, Birmpas C, Katsoris P, Beyrath J, Albanese P, Maurer M, Carpentier G, Strub JM, Van Dorsselaer A, Muller S, Bagnard D, Briand JP, Courty J: A Simple Approach to Cancer Therapy Afforded by Multivalent Pseudopeptides That Target Cell-Surface Nucleoproteins. Cancer Res. 2011, 71 (3296-3305):

50.

Jacotot E, Callebaut C, Blanco J, Krust B, Neubert K, Barth A, Hovanessian AG: Dipeptidyl-peptidase IV-Beta, a novel form of cell-surface-expressed protein with dipeptidyl-peptidase IV activity. Eur J Biochem. 1996, 239: 248-258. 10.1111/j.1432-1033.1996.0248u.x.PubMed

51.

Laurent-Crawford AG, Krust B, Rivière Y, Desgranges C, Muller S, Kieny MP, Dauguet C, Hovanessian AG: Membrane expression of HIV envelope glycoproteins triggers apoptosis in CD4 cells. AIDS Res Hum Retroviruses. 1993, 9: 761-773. 10.1089/aid.1993.9.761.PubMed

52.

Callebaut C, Jacotot E, Krust B, Guichar G, Blanco J, Svab J, Muller S, Briand JP, Hovanessian AG: Pseudopeptides TASP inhibitors of HIV infection block viral entry by binding to a 95 kDa cell surface protein. J Biol Chem. 1997, 272: 7159-7166. 10.1074/jbc.272.11.7159.PubMed

53.

Ghebrehiwet B, Lim BL, Peerschke EY, Willis AC, Reid KB: Isolation, cDNA cloning, and overexpression of a 33-kD cell surface glycoprotein that binds to the globular "heads" of C1q. J Exp Med. 1994, 179: 1809-1821. 10.1084/jem.179.6.1809.PubMed

54.

Fogal V, Richardson AD, Karmali PP, Scheffler IE, Smith JW, Ruoslahti E: Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol Cell Biol. 2010, 30: 1303-1318. 10.1128/MCB.01101-09.PubMedPubMedCentral

55.

Peerschke EI, Ghebrehiwet B: The contribution of gC1qR/p33 in infection and inflammation. Immunobiology. 2007, 212: 333-342. 10.1016/j.imbio.2006.11.011.PubMedPubMedCentral

56.

Dumler I, Stepanova V, Jerke U, Mayboroda OA, Vogel F, Bouvet P, Thachuk V, Haller H, Gulba DC: Urokinase-induced mitogenesis is mediated by casein kinase 2 and nucleolin. Current Biology. 1999, 9: 1468-1476. 10.1016/S0960-9822(00)80116-5.PubMed

57.

Jarjour WN, Minota S, Roubey RA, Mimura T, Winfield JB: Autoantibodies to nucleolin cross-react with histone H1 in systemic lupus erythematosus. Mol Biol Rep. 1992, 16: 263-266. 10.1007/BF00419666.PubMed

58.

Tai YT, Podar K, Kraeft SK, Wang F, Young G, Lin B, Gupta D, Chen LB, Anderson KC: Translocation of Ku86/Ku70 to the multiple myeloma cell membrane: functional implications. Exp Hematol. 2002, 30: 212-220. 10.1016/S0301-472X(01)00786-X.PubMed

59.

Paupert J, Dauvillier S, Salles B, Muller C: Transport of the leaderless protein Ku on the cell surface of activated monocytes regulates their migratory abilities. EMBO Rep. 2007, 8: 583-588. 10.1038/sj.embor.7400976.PubMedPubMedCentral

60.

Keenan RJ, Freymann DM, Stroud RM, Walter P: The signal recognition particle. Annu Rev Biochem. 2001, 70: 7555-7775.

61.

Cross BC, Sinning I, Luirink J, High S: Delivering proteins for export from the cytosol. Nat Rev Mol cell Biol. 2009, 10: 255-264. 10.1038/nrm2657.PubMed

62.

Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK: LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev. 2008, 88: 887-918. 10.1152/physrev.00033.2007.PubMedPubMedCentral

63.

Dedieu S, Langlois B: LRP-1: a new modulator of cytoskeleton dynamics and adhesive complex turnover in cancer cells. Cell Adh Migr. 2008, 2: 77-80. 10.4161/cam.2.2.6374.PubMedPubMedCentral

64.

Semenkovich CF, Ostlund REJ, Olson MO, Yang JW: A protein partially expressed on the surface of HepG2 cells that binds lipoproteins specifically is nucleolin. Biochemistry. 1990, 29: 9708-9713. 10.1021/bi00493a028.PubMed

65.

Grey A, Banovic T, Zhu Q, Watson M, Callon K, Palmano K, Ross J, Naot D, Reid IR, Cornish J: The low-density lipoprotein receptor-related protein 1 is a mitogenic receptor for lactoferrin in osteoblastic cells. Mol Endocrinol. 2004, 18: 2268-2278. 10.1210/me.2003-0456.PubMed

66.

Lin WW, Karin M: A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest. 2007, 117: 1175-1183. 10.1172/JCI31537.PubMedPubMedCentral

67.

Sinclair JF, O'Brien AD: Intimin types alpha, beta, and gamma bind to nucleolin with equivalent affinity but lower avidity than to the translocated intimin receptor. J Biol Chem. 2004, 279: 33751-33758. 10.1074/jbc.M401616200.PubMed

68.

Messi E, Florian MC, Caccia C, Zanisi M, Maggi R: Retinoic acid reduces human neuroblastoma cell migration and invasiveness: effects on DCX, LISI, neurofilaments-68 and vimentin expression. BMC Cancer. 2008, 8: 30-10.1186/1471-2407-8-30.PubMedPubMedCentral

69.

Cavallaro U, Christofori G: Cell adhesion in tumor invasion and metastasis: loss of the glue is not enough. Biochim Biophys Acta. 2001, 1552: 39-45.PubMed

70.

Kobayashi H, Boelte KC, Lin PC: Endothelial cell adhesion molecules and cancer progression. Curr Med Chem. 2007, 14: 377-386. 10.2174/092986707779941032.PubMed

71.

Kessenbrock K, Plaks V, Werb Z: Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010, 141: 52-67. 10.1016/j.cell.2010.03.015.PubMedPubMedCentral

72.

Cruz-Munoz W, Khokha R: The role of tissue inhibitors of metalloproteinases in tumorigenesis and metastasis. Crit Rev Clin Lab Sci. 2008, 45: 291-338. 10.1080/10408360801973244.PubMed

73.

Bachmeier BE, Albini A, Vené R, Benelli R, Noonan D, Weigert C, Weiler C, Lichtinghagen R, Jochum M, Nerlich AG: Cell density-dependent regulation of matrix metalloproteinase and TIMP expression in differently tumorigenic breast cancer cell lines. Exp Cell Res. 2005, 305: 83-98. 10.1016/j.yexcr.2004.12.019.PubMed

74.

Horita H, Frankel AE, Thorburn A: Acute myeloid leukemia-targeted toxin activates both apoptotic and necroptotic mechanisms. PLoS ONE. 2008, 3 (12): e3909-10.1371/journal.pone.0003909.PubMedPubMedCentral

75.

Golstein P, Kroemer G: Cell death by necrosis: towards a molecular definition. Trends Biochem Sci. 2007, 32: 37-43. 10.1016/j.tibs.2006.11.001.PubMed

76.

Dong Z, Saikumar P, Weinberg JM, Venkatachalam MA: Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am J pathol. 1997, 151: 1205-1213.PubMedPubMedCentral

77.

Grisendi S, Mecucci C, Falini B, Pandolfi PP: Nucleophosmin and cancer. Nature Rev Cancer. 2006, 6: 493-505. 10.1038/nrc1885.

78.

Matilla A, Radrizzani M: The Anp32 family of proteins containing leucine-rich repeats. Cerebellum. 2005, 4: 7-18. 10.1080/14734220410019020.PubMed

79.

Liu Z, Jang SW, Liu X, Cheng D, Peng J, Yepes M, Li XJ, Matthews S, Watts C, Asano M, Hara-Nishimura I, Luo HR, Ye K: Neuroprotective actions of PIKE-L by inhibition of SET proteolytic degradation by asparagine endopeptidase. Molecular Cell. 2008, 29: 665-678. 10.1016/j.molcel.2008.02.017.PubMedPubMedCentral

80.

Gamble MJ, Fisher RP: SET and PARP1 remove DEK from chromatin to permit access by the transcription machinery. Nat Struct Mol Biol. 2007, 14: 548-555. 10.1038/nsmb1248.PubMed

81.

Jiang X, Kim HE, Shu H, Zhao Y, Zhang H, Kofron J, Donnelly J, Burns D, Ng SC, Rosenberg SA, Wang X: Distinctive roles of PHAP proteins and prothymosin-alpha in a death regulatory pathway. Science. 2003, 299: 223-226. 10.1126/science.1076807.PubMed

82.

Bains SK, Mone A, Tso JY, Lucas D, Byrd JC, Weiner GJ, Green JM: Mitochondria control of cell death induced by anti-HLA-DR antibodies. Leukemia. 2003, 17: 1357-1365. 10.1038/sj.leu.2402976.PubMed

83.

Mehindate K, Thibodeau J, Dohlsten M, Kalland T, Sékaly RP, Walid Mourad W: Cross-linking of major histocompatibility complex class II molecules by Staphylococcal enterotoxin A superantigen Is a requirement for Inflammatory cytokine gene expression. J Exp Med. 1995, 182: 1573-1577. 10.1084/jem.182.5.1573.PubMed

84.

Bertho N, Laupèze B, Mooney N, Le Berre C, Charron D, Dre'nou B, Fauchet E: HLA-DR mediated cell death is associated with, but not induced by TNF-alpha secretion in APC. Human Immunology. 2001, 62: 106-112. 10.1016/S0198-8859(00)00240-8.PubMed

85.

Folkman J: Endostatin finds a new partner: nucleolin. Blood. 2007, 110: 2786-2787. 10.1182/blood-2007-08-102178.

86.

Fogal V, Sugahara KN, Ruoslahti E, Christian S: Cell surface nucleolin antagonist causes endothelial cell apoptosis and normalization of tumor vasculature. Angiogenesis. 2009, 12: 91-100. 10.1007/s10456-009-9137-5.PubMed

87.

Smolich BD, McMahon JA, McMahon AP, Papkoff J: Wnt family proteins are secreted and associated with the cell surface. Mol Biol Cell. 1993, 4: 1267-1275.PubMedPubMedCentral

88.

Busse U, Guay J, Seguin C: Nucleotide sequence of a cDNA encoding Wnt-1 of the Mexican axolotl Ambystoma mexicanum. Nucleic Acids Res. 1991, 19: 981-10.1093/nar/19.4.981.PubMedPubMedCentral

89.

Downs JA, Jackson SP: A means to a DNA end: the many roles of Ku. Nat Rev Mol cell Biol. 2004, 5: 367-378. 10.1038/nrm1367.PubMed

90.

Fogal V, Zhang L, Krajewski S, Ruoslahti E: Mitochondrial/cell-surface protein p32/gC1qR as a molecular target in tumor cells and tumor stroma. Cancer Res. 2008, 68: 7210-7218. 10.1158/0008-5472.CAN-07-6752.PubMedPubMedCentral

91.

Bouvet P, Diaz J-J, Kindbeiter K, Madjar J-J, Amalric F: Nucleolin interacts with several ribosomal proteins through its RGG domain. J Biol Chem. 1998, 273: 19025-19029. 10.1074/jbc.273.30.19025.PubMed

92.

Kirikoshi H, Katoh M: Expression of WNT7A in human normal tissues and cancer, and regulation of WNT7A and WNT7B in human cancer. Int J Oncol. 2002, 21: 895-900.PubMed

93.

Bui TD, O'Brien T, Crew J, Cranston D, Harris AL: High expression of Wnt7b in human superficial bladder cancer vs invasive bladder cancer. Br J Cancer. 1998, 77: 319-324. 10.1038/bjc.1998.49.PubMedPubMedCentral

94.

Memarian A, Hojjat-Farsangi M, Asgarian-Omran H, Younesi V, Jeddi-Tehrani M, Sharifian RA, Khoshnoodi J, Razavi SM, Rabbani H, Shokri F: Variation in WNT genes expression in different subtypes of chronic lymphocytic leukemia. Leuk Lymphoma. 2009, 12: 2061-2070.

95.

Lynch EM, Moreland RB, Ginis I, Perrine SP, Faller DV: Hypoxia-activated ligand HAL-1/13 is lupus autoantigen Ku80 and mediates lymphoid cell adhesion in vitro. Am J Physiol Cell Physiol. 2001, 280: C897-C911.PubMed

96.

Iakhiaeva E, Bhuiyan SH, Yin J, Zwieb C: Protein SRP68 of human signal recognition particle: identification of the RNA and SRP72 binding domains. Protein Sci. 2006, 15: 1290-1302. 10.1110/ps.051861406.PubMedPubMedCentral

97.

Ghebrehiwet B, Peerschke EI: cC1q-R (calreticulin) and gC1q-R/p33: ubiquitously expressed multi ligand binding cellular proteins involved in inflammation and infection. Mol Immunol. 2004, 41: 173-183. 10.1016/j.molimm.2004.03.014.PubMed

98.

Bourguignon LYW: Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin Cancer Biol. 2008, 18: 251-259. 10.1016/j.semcancer.2008.03.007.PubMedPubMedCentral

99.

Rubinstein DB, Stortchevoi A, Boosalis M, Ashfaq R, Ghebrehiwet B, Peerschke EI, Calvo F, Guillaume T: Receptor for the globular heads of C1q (gC1q-R, p33, hyaluronan binding protein) is preferentially expressed by adenocarcinoma cells. Int J Cancer. 2004, 110: 741-750. 10.1002/ijc.20105.PubMed

100.

Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, Lees JA, Hopkins N: Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biology. 2004

101.

Rau R, Brown P: Nucleophosmin (NPM1) mutations in adult and childhood acute myeloid leukemia: towards definition of a new leukemia entity. Hematol Oncol. 2009, 27: 171-181. 10.1002/hon.904.PubMedPubMedCentral

102.

Falini B, Boli N, Liso A, Martelli MP, Mannucci R, Pileri S, Nicoletti I: Altered nucleophosmin transport in acute myeloid leukemia with mutated NPM1: molecular basis and clinical implications. Leukemia. 2009, 23: 1731-1743. 10.1038/leu.2009.124.PubMed

The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2407/11/333/prepub

Title: Targeting surface nucleolin with multivalent HB-19 and related Nucant pseudopeptides results in distinct inhibitory mechanisms depending on the malignant tumor cell type
Authors: Bernard Krust
Diala El Khoury
Isabelle Nondier
Calaiselvy Soundaramourty
Ara G Hovanessian
Publication date: 01-12-2011
Publisher: BioMed Central
Published in: BMC Cancer / Issue 1/2011
Electronic ISSN: 1471-2407
DOI: https://doi.org/10.1186/1471-2407-11-333

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