Preclinical Development of a Novel Class of CXCR4 Antagonist Impairing Solid Tumors Growth and Metastases

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Portella, Luigi ^a   Vitale, Rosamaria ^b   De Luca, Stefania ^b   D'Alterio, Crescenzo ^a   Ieranò, Caterina ^a   Napolitano, Maria ^a   Riccio, Anna ^a   Polimeno, Maria Neve ^a   Monfregola, Luca ^b   Barbieri, Antonio ^a   Luciano, Antonio ^a   Ciarmiello, Andrea ^d   Arra, Claudio ^a   Castello, Giuseppe ^c   Amodeo, Pietro ^b   Scala, Stefania ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b CNR   (Italy)

^c IBB CNR CNR ^*  (Italy)

^d Ospedale Azienda Sanitaria Locale 5   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

[CYSTEINYLTRYPTOPHANYLHISTIDYLARGINYLCYSTEINE]; ARGINYLALANINE [CYSTEINYLARGINYLTYROSYLTRYPTOPHANYLCYSTEINE]; ARGINYLALANINE[CYSTEINYLARGINYLHISTIDYLTRYPTOPHANYLCYSTEINE]; ARGINYLALANINE[CYSTEINYLARGINYLPHENYLALANYLPHENYLALANYLCYSTEINE]; CHEMOKINE RECEPTOR CXCR4; CYCLOPEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PEPTIDE; PLERIXAFOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CANCER CELL; CANCER INHIBITION; CELL MIGRATION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG DESIGN; ENZYME INDUCTION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CANCER; LUNG METASTASIS; MELANOMA B16; MELANOMA CELL; METASTASIS INHIBITION; MOUSE; NONHUMAN; OSTEOSARCOMA CELL; RECEPTOR BINDING; TUMOR XENOGRAFT; WOUND HEALING;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINE CXCL12; DRUG DESIGN; DRUG SCREENING ASSAYS, ANTITUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; OSTEOSARCOMA; PEPTIDES, CYCLIC; PHOSPHORYLATION; PROTEIN BINDING; RECEPTORS, CXCR4; WOUND HEALING;

EID: 84884132303     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074548     Document Type: Article

References (48)

1. Baggiolini M, (2001) Chemokines in pathology and medicine. J Intern Med 250: 91-104.
2. Allen SJ, Crown SE, Handel TM, (2007) Chemokine: receptor structure, interactions, and antagonism. Annu Rev Immunol 25: 787-820.
3. Wu X, Lee VC, Chevalier E, Hwang ST, (2009) Chemokine receptors as targets for cancer therapy. Curr Pharm Des 2009 15: 742-57.
4. Teicher BA, Fricker SP, (2010) CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 16: 2927-31.
5. Muller A, Homey B, Soto H, Ge N, Catron D, et al. (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410: 50-6.
6. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, et al. (2005) The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 280: 35760-6.
7. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B, (2009) CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 113: 6085-93.
8. Duda DG, Kozin SV, Kirkpatrick ND, Xu L, Fukumura D, et al. (2011) CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies? Clin Cancer Res 17: 2074-80.
9. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, et al. (2008) Control of chemokine-guided cell migration by ligand sequestration. Cell 132: 463-73.
10. Zabel BA, Wang Y, Lewen S, Berahovich RD, Penfold ME, et al. (2009) Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol 183: 3204-11.
11. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, et al. (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382: 635-8.
12. Sierro F, Biben C, Martinez-Munoz L, Mellado M, Ransohoff RM, et al. (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A 104: 14759-64.
13. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, et al. (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393: 591-4.
14. Scala S, Ottaiano A, Ascierto PA, Cavalli M, Simeone E, et al. (2005) Expression of CXCR4 predicts poor prognosis in patients with malignant melanoma. Clin Cancer Res 2005 11: 1835-41.
15. Scotton CJ, Wilson JL, Scott K, Stamp G, Wilbanks GD, et al. (2002) Multiple actions of the chemokine CXCL12 on epithelial tumor cells in human ovarian cancer. Cancer Res 62: 5930-8.
16. Ottaiano A, Franco R, Aiello Talamanca A, Liguori G, Tatangelo F, et al. (2006) Overexpression of both CXC chemokine receptor 4 and vascular endothelial growth factor proteins predicts early distant relapse in stage II-III colorectal cancer patients. Clin Cancer Res 12: 2795-803.
17. Tavor S, Petit I, (2010) Can inhibition of the SDF-1/CXCR4 axis eradicate acute leukemia? Semin Cancer Biol 20: 178-85.
18. Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, et al. (2010) Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest 120: 694-705.
19. Kozin SV, Kamoun WS, Huang Y, Dawson MR, Jain RK, et al. (2010) Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res 70: 5679-85.
20. D'Alterio C, Barbieri A, Portella L, Palma G, Polimeno M, et al. (2012) Inhibition of stromal CXCR4 impairs development of lung metastases. Cancer Immunol Immunother 61(10): 1713-20.
21. Hiratsuka S, Duda DG, Huang Y, Goel S, Sugiyama T, et al. (2011) C-X-C receptor type 4 promotes metastasis by activating p38 mitogen-activated protein kinase in myeloid differentiation antigen (Gr-1)-positive cells. Proc Natl Acad Sci U S A. 108: 302-7.
22. Vose JM, Ho AD, Coiffier B, Corradini P, Khouri I, et al. (2009) Advances in mobilization for the optimization of autologous stem cell transplantation. Leuk Lymphoma 50: 1412-21.
23. De Clercq E, (2009) The AMD3100 story: the path to the discovery of a stem cell mobilizer (Mozobil). Biochem Pharmacol 77: 1655-64.
24. Hendrix CW, Collier AC, Lederman MM, Schols D, Pollard RB, et al. (2004) Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. J Acquir Immune Defic Syndr 37: 1253-62.
25. Clark-Lewis I, Kim KS, Rajarathnam K, Gong JH, Dewald B, et al. (1995) Structure-activity relationships of chemokines. J Leukoc Biol 57: 703-11.
26. Baggiolini M, Dewald B, Moser B, (1997) Human chemokines: an update. Annu Rev Immunol 15: 675-705.
27. Crump MP, Gong JH, Loetscher P, Rajarathnam K, Amara A, et al. (1997) Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J 16: 6996-7007.
28. Kledal TN, Rosenkilde MM, Coulin F, Simmons G, Johnsen AH, et al. (1997) A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma-associated herpesvirus. Science 277: 1656-9.
29. Shan L, Qiao X, Oldham E, Catron D, Kaminski H, et al. (2000) Identification of viral macrophage inflammatory protein (vMIP)-II as a ligand for GPR5/XCR1. Biochem Biophys Res Commun 268: 938-41.
30. Crump MP, Elisseeva E, Gong J, Clark-Lewis I, Sykes BD, (2001) Structure/function of human herpesvirus-8 MIP-II (1-71) and the antagonist N-terminal segment (1-10). FEBS Lett 489: 171-5.
31. Booth V, Slupsky CM, Clark-Lewis I, Sykes BD, (2003) Unmasking ligand binding motifs: identification of a chemokine receptor motif by NMR studies of antagonist peptides. J Mol Biol 327: 329-34.
32. Amodeo P, Vitale RM, De Luca S, Scala S, Castello G et al. (2010) Cyclic peptides binding CXCR4 receptor and relative medical and diagnostic uses. Italian patent: no. MI2010A 000093; international patent n° WO2011/092575 A.
33. Fricker SP, Anastassov V, Cox J, Darkes MC, Grujic O, et al. (2006) Characterization of the molecular pharmacology of AMD3100: a specific antagonist of the G-protein coupled chemokine receptor, CXCR4. Biochem Pharmacol 2006 72: 588-96.
34. Scala S, Giuliano P, Ascierto PA, Ieranò C, Franco R, et al. (2006) Human melanoma metastases express functional CXCR4. Clin Cancer Res 12: 2427-33.
35. Murakami T, Maki W, Cardones AR, Fang H, Tun Kyi A, et al. (2002) Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16 melanoma cells. Cancer Res 62: 7328-34.
36. Richert MM, Vaidya KS, Mills CN, Wong D, Korz W, et al. (2009) Inhibition of CXCR4 by CTCE-9908 inhibits breast cancer metastasis to lung and bone. Oncol Rep 21: 761-7.
37. Smith MC, Luker KE, Garbow JR, Prior JL, Jackson E, et al. (2004) CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res 64: 8604-12.
38. Gravel S, Malouf C, Boulais PE, Berchiche YA, Oishi S, et al. (2010) The peptidomimetic CXCR4 antagonist TC14012 recruits beta-arrestin to CXCR7: roles of receptor domains. J Biol Chem 285: 37939-43.
39. Rettig MP, Ansstas G, DiPersio JF, (2012) Mobilization of hematopoietic stem and progenitor cells using inhibitors of CXCR4 and VLA-4. Leukemia 26: 34-53.
40. Masuda M, Nakashima H, Ueda T, Naba H, Ikoma R, et al. (1992) A novel anti-HIV synthetic peptide, T-22 ([Tyr5,12,Lys7]-polyphemusin II). Biochem Biophys Res Commun 189: 845-50.
41. Beider K, Begin M, Abraham M, Wald H, Weiss ID, et al. (2011) CXCR4 antagonist 4F-benzoyl-TN14003 inhibits leukemia and multiple myeloma tumor growth. Exp Hematol 39: 282-92.
42. Tamamura H, Hori A, Kanzaki N, Hiramatsu K, Mizumoto M, et al. (2003) T140 analogs as CXCR4 antagonists identified as anti-metastatic agents in the treatment of breast cancer. FEBS Lett 550: 79-83.
43. Mori T, Doi R, Koizumi M, Toyoda E, Ito D, et al. (2004) CXCR4 antagonist inhibits stromal cell-derived factor 1-induced migration and invasion of human pancreatic cancer. Mol Cancer Ther 3: 29-37.
44. Abraham M, Biyder K, Begin M, Wald H, Weiss ID, et al. (2007) Enhanced unique pattern of hematopoietic cell mobilization induced by the CXCR4 antagonist 4F-benzoyl-TN14003. Stem Cells 25: 2158-66.
45. Porvasnik S, Sakamoto N, Kusmartsev S, Eruslanov E, Kim WJ, et al. (2009) Effects of CXCR4 antagonist CTCE-9908 on prostate tumor growth. Prostate 69: 1460-9.
46. Kwong J, Kulbe H, Wong D, Chakravarty P, Balkwill F, (2009) An antagonist of the chemokine receptor CXCR4 induces mitotic catastrophe in ovarian cancer cells. Mol Cancer Ther 8: 1893-905.
47. Xu L, Duda DG, di Tomaso E, Ancukiewicz M, Chung DC, et al. (2009) Direct evidence that bevacizumab, an anti-VEGF antibody, up-regulates SDF1alpha, CXCR4, CXCL6, and neuropilin 1 in tumors from patients with rectal cancer. Cancer Res 69: 7905-10.
48. Rao S, Sengupta R, Choe EJ, Woerner BM, Jackson E, et al. (2012) CXCL12 mediates trophic interactions between endothelial and tumor cells PLoS One.; 7 (3).: e 3305.