Targeting Syndecan-1, a molecule implicated in the process of vasculogenic mimicry, enhances the therapeutic efficacy of the L19-IL2 immunocytokine in human melanoma xenografts

Oncotarget

Volumn 6, Issue 35, 2015, Pages 37426-37442

  Orecchia, Paola ^a,b   Conte, Romana ^a   Balza, Enrica ^a   Pietra, Gabriella ^a,b   Mingari, Maria Cristina ^a,b   Carnemolla, Barbara ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Angiogenesis; Immunocytokine L19 IL2; Melanoma combined therapy; scFv OC 46F2 anti Syndecan 1; vasculogenic vascular mimicry

Indexed keywords

DARLEUKIN; OC 46F2 ANTIBODY; RECOMBINANT ANTIBODY; SYNDECAN 1; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; CADHERIN; HYBRID PROTEIN; KDR PROTEIN, HUMAN; L19-IL2 IMMUNOCYTOKINE; LEUKOCYTE ANTIGEN; MONOCLONAL ANTIBODY; SDC1 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER TISSUE; CONTROLLED STUDY; DRUG EFFICACY; DRUG TARGETING; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MELANOMA; MELANOMA CELL LINE; MONOTHERAPY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CANCER STEM CELL; COCULTURE; DRUG EFFECTS; DRUG SCREENING; IMMUNOLOGY; LUNG NEOPLASMS; METABOLISM; MOLECULAR MIMICRY; MOLECULARLY TARGETED THERAPY; NEOVASCULARIZATION (PATHOLOGY); NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SECONDARY; SKIN NEOPLASMS; TIME FACTOR; TUMOR CELL LINE; TUMOR VOLUME; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CADHERINS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; FEMALE; HUMANS; LUNG NEOPLASMS; MALE; MELANOMA; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MOLECULAR MIMICRY; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; RECOMBINANT FUSION PROTEINS; SKIN NEOPLASMS; SYNDECAN-1; TIME FACTORS; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84947714390     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6055     Document Type: Article

References (49)

1. Carmeliet P and Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473:298-307.
2. Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov. 2007; 6:273-286.
3. Weis SM and Cheresh DA. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med. 2011; 17:1359-1370.
4. Chung AS, Lee J and Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat Rev Cancer. 2010; 10:505-514.
5. Corrie PG, Basu B and Zaki KA. Targeting angiogenesis in melanoma: prospects for the future. Ther Adv Med Oncol. 2010; 2:367-380.
6. Emmett MS, Dewing D and Pritchard-Jones RO. Angiogenesis and melanoma-from basic science to clinical trials. Am J Cancer Res. 2011; 1:852-868.
7. Abdollahi A and Folkman J. Evading tumor evasion: current concepts and perspectives of anti-angiogenic cancer therapy. Drug Resist Updat. 2010; 13:16-28.
8. Moserle L, Jimenez-Valerio G and Casanovas O. Antiangiogenic therapies: going beyond their limits. Cancer Discov. 2014; 4:31-41.
9. Helfrich I and Schadendorf D. Blood vessel maturation, vascular phenotype and angiogenic potential in malignant melanoma: one step forward for overcoming antiangiogenic drug resistance? Mol Oncol. 2011; 5:137-149.
10. Pretto F and Neri D. Pharmacotherapy of metastatic melanoma: emerging trends and opportunities for a cure. Pharmacol Ther. 2013; 139:405-411.
11. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, Davidson N, Richards J, Maio M, Hauschild A, Miller WH, Jr., Gascon P, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med. 2011; 364:2517-2526.
12. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011; 364:2507-2516.
13. Ferrucci PF, Minchella I, Mosconi M, Gandini S, Verrecchia F, Cocorocchio E, Passoni C, Pari C, Testori A, Coco P and Munzone E. Dacarbazine in combination with bevacizumab for the treatment of unresectable/metastatic melanoma: a phase II study. Melanoma research. 2015; 25:239-245.
14. Danielli R, Patuzzo R, Ruffini PA, Maurichi A, Giovannoni L, Elia G, Neri D and Santinami M. Armed antibodies for cancer treatment: a promising tool in a changing era. Cancer immunology, immunotherapy. 2015; 64:113-121.
15. Borsi L, Balza E, Bestagno M, Castellani P, Carnemolla B, Biro A, Leprini A, Sepulveda J, Burrone O, Neri D and Zardi L. Selective targeting of tumoral vasculature: comparison of different formats of an antibody (L19) to the ED-B domain of fibronectin. International journal of cancer. 2002; 102:75-85.
16. Eigentler TK, Weide B, de Braud F, Spitaleri G, Romanini A, Pflugfelder A, Gonzalez-Iglesias R, Tasciotti A, Giovannoni L, Schwager K, Lovato V, Kaspar M, Trachsel E, Menssen HD, Neri D and Garbe C. A dose-escalation and signal-generating study of the immunocytokine L19-IL2 in combination with dacarbazine for the therapy of patients with metastatic melanoma. Clin Cancer Res. 2011; 17:7732-7742.
17. Weide B, Eigentler TK, Pflugfelder A, Zelba H, Martens A, Pawelec G, Giovannoni L, Ruffini PA, Elia G, Neri D, Gutzmer R, Becker JC and Garbe C. Intralesional treatment of stage III metastatic melanoma patients with L19-IL2 results in sustained clinical and systemic immunologic responses. Cancer Immunol Res. 2014; 2:668-678.
18. Danielli R, Patuzzo R, Di Giacomo AM, Gallino G, Maurichi A, Di Florio A, Cutaia O, Lazzeri A, Fazio C, Miracco C, Giovannoni L, Elia G, Neri D, Maio M and Santinami M. Intralesional administration of L19-IL2/L19-TNF in stage III or stage IVM1a melanoma patients: results of a phase II study. Cancer immunology, immunotherapy. 2015; 64:999-1009.
19. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS and Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol. 1999; 155:739-752.
20. Qiao L, Liang N, Zhang J, Xie J, Liu F, Xu D, Yu X and Tian Y. Advanced research on vasculogenic mimicry in cancer. J Cell Mol Med. 2015; 19:315-326.
21. Yao X, Ping Y, Liu Y, Chen K, Yoshimura T, Liu M, Gong W, Chen C, Niu Q, Guo D, Zhang X, Wang JM and Bian X. Vascular endothelial growth factor receptor 2 (VEGFR-2) plays a key role in vasculogenic mimicry formation, neovascularization and tumor initiation by Glioma stem-like cells. Plos One. 2013; 8:e57188.
22. Orecchia P, Conte R, Balza E, Petretto A, Mauri P, Mingari MC and Carnemolla B. A novel human anti-Syndecan-1 antibody inhibits vascular maturation and tumour growth in melanoma. Eur J Cancer. 2013; 49:2022-2033.
23. Francescone R, Scully S, Bentley B, Yan W, Taylor SL, Oh D, Moral L and Shao R. Glioblastoma-derived tumor cells induce vasculogenic mimicry through Flk-1 protein activation. The Journal of biological chemistry. 2012; 287:24821-24831.
24. Frank NY, Schatton T, Kim S, Zhan Q, Wilson BJ, Ma J, Saab KR, Osherov V, Widlund HR, Gasser M, Waaga-Gasser AM, Kupper TS, Murphy GF and Frank MH. VEGFR-1 expressed by malignant melanoma-initiating cells is required for tumor growth. Cancer research. 2011; 71:1474-1485.
25. Hendrix MJ, Seftor EA, Meltzer PS, Gardner LM, Hess AR, Kirschmann DA, Schatteman GC and Seftor RE. Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry. Proc Natl Acad Sci U S A. 2001; 98:8018-8023.
26. Xian X, Gopal S and Couchman JR. Syndecans as receptors and organizers of the extracellular matrix. Cell Tissue Res. 2010; 339:31-46.
27. Sanderson RD, Lalor P and Bernfield M. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul. 1989; 1:27-35.
28. O'Connell MP, Fiori JL, Kershner EK, Frank BP, Indig FE, Taub DD, Hoek KS and Weeraratna AT. Heparan sulfate proteoglycan modulation of Wnt5A signal transduction in metastatic melanoma cells. The Journal of biological chemistry. 2009; 284:28704-28712.
29. Teng YH, Aquino RS and Park PW. Molecular functions of Syndecan-1 in disease. Matrix Biol. 2012; 31:3-16.
30. Gharbaran R. Advances in the molecular functions of Syndecan-1 (SDC1/CD138) in the pathogenesis of malignancies. Crit Rev Oncol Hematol. 2015; 94:1-17.
31. Purushothaman A, Uyama T, Kobayashi F, Yamada S, Sugahara K, Rapraeger AC and Sanderson RD. Heparanaseenhanced shedding of Syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis. Blood. 2010; 115:2449-2457.
32. Wang X, Katayama A, Wang Y, Yu L, Favoino E, Sakakura K, Favole A, Tsuchikawa T, Silver S, Watkins SC, Kageshita T and Ferrone S. Functional characterization of an scFv-Fc antibody that immunotherapeutically targets the common cancer cell surface proteoglycan CSPG4. Cancer research. 2011; 71:7410-7422.
33. Huang S, Luca M, Gutman M, McConkey DJ, Langley KE, Lyman SD and Bar-Eli M. Enforced c-KIT expression renders highly metastatic human melanoma cells susceptible to stem cell factor-induced apoptosis and inhibits their tumorigenic and metastatic potential. Oncogene. 1996; 13:2339-2347.
34. Carnemolla B, Borsi L, Balza E, Castellani P, Meazza R, Berndt A, Ferrini S, Kosmehl H, Neri D and Zardi L. Enhancement of the antitumor properties of interleukin-2 by its targeted delivery to the tumor blood vessel extracellular matrix. Blood. 2002; 99:1659-1665.
35. Kaspar M, Zardi L and Neri D. Fibronectin as target for tumor therapy. International journal of cancer. 2006; 118:1331-1339.
36. Cao Z, Bao M, Miele L, Sarkar FH, Wang Z and Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013; 49:3914-3923.
37. Zhang S, Li M, Gu Y, Liu Z, Xu S, Cui Y and Sun B. Thalidomide influences growth and vasculogenic mimicry channel formation in melanoma. J Exp Clin Cancer Res. 2008; 27:60.
38. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C and Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010; 468:829-833.
39. Seftor RE, Hess AR, Seftor EA, Kirschmann DA, Hardy KM, Margaryan NV and Hendrix MJ. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol. 2012; 181:1115-1125.
40. Zhang D, Sun B, Zhao X, Ma Y, Ji R, Gu Q, Dong X, Li J, Liu F, Jia X, Leng X, Zhang C, Sun R and Chi J. Twist1 expression induced by sunitinib accelerates tumor cell vasculogenic mimicry by increasing the population of CD133+ cells in triple-negative breast cancer. Mol Cancer. 2014; 13:207.
41. Rapraeger AC, Ell BJ, Roy M, Li X, Morrison OR, Thomas GM and Beauvais DM. Vascular endothelial-cadherin stimulates Syndecan-1-coupled insulin-like growth factor-1 receptor and cross-talk between alphaVbeta3 integrin and vascular endothelial growth factor receptor 2 at the onset of endothelial cell dissemination during angiogenesis. The FEBS journal. 2013; 280:2194-2206.
42. Lamorte S, Ferrero S, Aschero S, Monitillo L, Bussolati B, Omede P, Ladetto M and Camussi G. Syndecan-1 promotes the angiogenic phenotype of multiple myeloma endothelial cells. Leukemia. 2012; 26:1081-1090.
43. Civenni G, Walter A, Kobert N, Mihic-Probst D, Zipser M, Belloni B, Seifert B, Moch H, Dummer R, van den Broek M and Sommer L. Human CD271-Positive Melanoma Stem Cells Associated with Metastasis Establish Tumor Heterogeneity and Long-term Growth. Cancer research. 2011; 71:3098-3109.
44. Dunleavey JM, Xiao L, Thompson J, Kim MM, Shields JM, Shelton SE, Irvin DM, Brings VE, Ollila DW, Brekken RA, Dayton PA, Melero-Martin JM and Dudley AC. Vascular channels formed by subpopulations of PECAM1+ melanoma cells. Nat Commun. 2014; 5:5200.
45. Pietra G, Manzini C, Vitale M, Balsamo M, Ognio E, Boitano M, Queirolo P, Moretta L and Mingari MC. Natural killer cells kill human melanoma cells with characteristics of cancer stem cells. Int Immunol. 2009; 21:793-801.
46. Delcommenne M and Klingemann HG. Detection and characterization of Syndecan-1-associated heparan sulfate 6-O-sulfated motifs overexpressed in multiple myeloma cells using single chain antibody variable fragments. Hum Antibodies. 2012; 21:29-40.
47. Carnemolla B, Neri D, Castellani P, Leprini A, Neri G, Pini A, Winter G and Zardi L. Phage antibodies with panspecies recognition of the oncofoetal angiogenesis marker fibronectin ED-B domain. International journal of cancer. 1996; 68:397-405.
48. Passaniti A, Taylor RM, Pili R, Guo Y, Long PV, Haney JA, Pauly RR, Grant DS and Martin GR. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest. 1992; 67:519-528.
49. Prewett M, Huber J, Li Y, Santiago A, O'Connor W, King K, Overholser J, Hooper A, Pytowski B, Witte L, Bohlen P and Hicklin DJ. Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer research. 1999; 59:5209-5218.