MULTIMERIN2 binds VEGF-A primarily via the carbohydrate chains exerting an angiostatic function and impairing tumor growth

Oncotarget

Volumn 7, Issue 2, 2016, Pages 2022-2037

  Colladel, Roberta ^a   Pellicani, Rosanna ^a   Andreuzzi, Eva ^a   Paulitti, Alice ^a   Tarticchio, Giulia ^a   Todaro, Federico ^a   Colombatti, Alfonso ^a   Mongiat, Maurizio ^a  

^a CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

Author keywords

Angiogenesis; Endothelial cell sprouting; Extracellular matrix (ECM); Tumor microenvironment; Vascular endothelial growth factor (VEGF)

Indexed keywords

BINDING PROTEIN; CARBOHYDRATE; MITOGEN ACTIVATED PROTEIN KINASE P38; MULTIMERIN2 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 2; EMILIN3 PROTEIN, HUMAN; MEMBRANE ANTIGEN; MEMBRANE PROTEIN; MESSENGER RNA; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CELL MOTION; CHEMISTRY; DRUG SCREENING; ENZYME IMMUNOASSAY; FIBROSARCOMA; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GLYCOSYLATION; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURFACE PLASMON RESONANCE; TUMOR CELL CULTURE; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ANIMALS; ANTIGENS, SURFACE; APOPTOSIS; CARBOHYDRATES; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; FIBROSARCOMA; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSYLATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOENZYME TECHNIQUES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURFACE PLASMON RESONANCE; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84957629240     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6515     Document Type: Article

References (63)

1. Risau W. Mechanisms of angiogenesis. Nature. 1997; 386: 671-674.
2. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000; 6: 389-395.
3. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003; 9: 653-660.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646-674.
5. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971; 285: 1182-1186.
6. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, and Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009; 15: 232-239.
7. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011; 473: 298-307.
8. Cascone T, Heymach JV. Targeting the angiopoietin/Tie2 pathway: cutting tumor vessels with a double-edged sword? J Clin Oncol. 2012; 30: 441-444.
9. Chung AS, Lee J, and Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat Rev Cancer. 2010; 10: 505-514.
10. Ohtsu A, Shah MA, Van CE, Rha SY, Sawaki A, Park SR, Lim HY, Yamada Y, Wu J, Langer B, Starnawski M, and Kang YK. Bevacizumab in combination with chemotherapy as first-line therapy in advanced gastric cancer: a randomized, double-blind, placebo-controlled phase III study. J Clin Oncol. 2011; 29: 3968-3976.
11. Okines A, Cunningham D. Current perspective: bevacizumab in colorectal cancer-a time for reappraisal? Eur J Cancer. 2009; 45: 2452-2461.
12. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, Inoue M, Bergers G, Hanahan D, and Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009; 15: 220-231.
13. Ferrara N. VEGF as a therapeutic target in cancer. Oncology. 2005; 69 Suppl 3: 11-16.
14. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005; 307: 58-62.
15. Sorensen AG, Emblem KE, Polaskova P, Jennings D, Kim H, Ancukiewicz M, Wang M, Wen PY, Ivy P, Batchelor TT, and Jain RK. Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion. Cancer Res. 2012; 72: 402-407.
16. Emblem KE, Mouridsen K, Bjornerud A, Farrar CT, Jennings D, Borra RJ, Wen PY, Ivy P, Batchelor TT, Rosen BR, Jain RK, and Sorensen AG. Vessel architectural imaging identifies cancer patient responders to anti-angiogenic therapy. Nat Med. 2013; 19: 1178-1183.
17. Jain RK. Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell. 2014; 26: 605-622.
18. Maes H, Kuchnio A, Peric A, Moens S, Nys K, De-áBock K, Quaegebeur A, Schoors S, Georgiadou M, Wouters J, Vinckier S, Vankelecom H, Garmyn M, Vion ACm, Radtke F, Boulanger C, Gerhardt H, Dejana E, Dewerchin M, Ghesquiere B, Annaert W, Agostinis P, and Carmeliet P. Tumor Vessel Normalization by Chloroquine Independent of Autophagy. Cancer Cell. 2014; 26: 190-206.
19. Wong PP, Demircioglu F, Ghazaly E, Alrawashdeh W, Stratford MR, Scudamore CL, Cereser B, Crnogorac-Jurcevic T, McDonald S, Elia G, Hagemann T, Kocher HM, and Hodivala-Dilke KM. Dual-Action Combination Therapy Enhances Angiogenesis while Reducing Tumor Growth and Spread. Cancer Cell. 2015; 27: 123-137.
20. Naldini A, Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy. 2005; 4: 3-8.
21. Ronca R, Giacomini A, Di SE, Coltrini D, Pagano K, Ragona L, Matarazzo S, Rezzola S, Maiolo D, Torrella R, Moroni E, Mazzieri R, Escobar G, Mor M, Colombo G, and Presta M. Long-Pentraxin 3 Derivative as a Small-Molecule FGF Trap for Cancer Therapy. Cancer Cell. 2015; 28: 225-239.
22. Tarallo V, De Falco S. The vascular endothelial growth factors and receptors family: Up to now the only target for anti-angiogenesis therapy. Int J Biochem Cell Biol. 2015; 64: 185-189.
23. Ingber DE, Folkman J. How does extracellular matrix control capillary morphogenesis? Cell. 1989; 58: 803-805.
24. Slevin M, Krupinski J, Gaffney J, Matou S, West D, Delisser H, Savani RC, and Kumar S. Hyaluronan-mediated angiogenesis in vascular disease: Uncovering RHAMM and CD44 receptor signaling pathways. Matrix Biol. 2007; 26: 58-68.
25. Neve A, Cantatore FP, Maruotti N, Corrado A, and Ribatti D. Extracellular matrix modulates angiogenesis in physiological and pathological conditions. Biomed Res Int. 2014; 2014: 756078.
26. Senger DR, Davis GE. Angiogenesis. Cold Spring Harb Perspect Biol. 2011; 3: a005090.
27. Cheresh DA, Stupack DG. Regulation of angiogenesis: apoptotic cues from the ECM. Oncogene. 2008; 27: 6285-6298.
28. Nyberg P, Salo T, and Kalluri R. Tumor microenvironment and angiogenesis. Front Biosci. 2008; 13: 6537-6553.
29. Sweeney SM, DiLullo G, Slater SJ, Martinez J, Iozzo RV, Lauer-Fields JL, Fields GB, and Antonio JDS. Angiogenesis in Collagen I Requires alpha2beta1 Ligation of a GFP*GER Sequence and Possibly p38 MAPK Activation and Focal Adhesion Disassembly. J Biol Chem. 2003; 278: 30516-30524.
30. Mammoto T, Jiang A, Jiang E, Panigrahy D, Kieran MW, and Mammoto A. Role of Collagen Matrix in Tumor Angiogenesis and Glioblastoma Multiforme Progression. Am J Pathol. 2013; 183: 1293-1305.
31. Nicosia RF, Bonanno E, and Smith M. Fibronectin promotes the elongation of microvessels during angiogenesis in vitro. J Cell Physiol. 1993; 154: 654-661.
32. Yi M, Ruoslahti E. A fibronectin fragment inhibits tumor growth, angiogenesis, and metastasis. Proc Natl Acad Sci. 2001; 98: 620-624.
33. Li R, Luo M, Ren M, Chen N, Xia J, Deng X, Zeng M, Yan K, Luo T, and Wu J. Vitronectin Regulation of Vascular Endothelial Growth Factor-Mediated Angiogenesis. J Vasc Res. 2014; 51: 110-117.
34. Simon-Assmann P, Orend G, Mammadova-Bach E, Spenle C, and Lefebvre O. Role of laminins in physiological and pathological angiogenesis. Int J Dev Biol. 2011; 55: 455-465.
35. Lawler PR, Lawler J. Molecular Basis for the Regulation of Angiogenesis by Thrombospondin-1 and-2. Cold Spring Harb Perspect Med. 2012; 2.
36. Jendraschak E, Helene Sage E. Regulation of angiogenesis by SPARC and angiostatin: implications for tumor cell biology. Semin Cancer Biol. 1996; 7: 139-146.
37. Aviezer D, Hecht D, Safran M, Eisinger M, David G, and Yayon A. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell. 1994; 79: 1005-1013.
38. Jarvelainen H, Sainio A, and Wight TN. Pivotal role for decorin in angiogenesis. Matrix Biol. 2015; 43: 15-26.
39. Marneros AG, Olsen BR. Physiological role of collagen XVIII and endostatin. FASEB J. 2005; 19: 716-728.
40. Kamphaus GD, Colorado PC, Panka DJ, Hopfer H, Ramchandran R, Torre A, Maeshima Y, Mier JW, Sukhatme VP, and Kalluri R. Canstatin, a Novel Matrixderived Inhibitor of Angiogenesis and Tumor Growth. J Biol Chem. 2000; 275: 1209-1215.
41. Maeshima Y, Sudhakar A, Lively JC, Ueki K, Kharbanda S, Kahn CR, Sonenberg N, Hynes RO, and Kalluri R. Tumstatin, an Endothelial Cell-Specific Inhibitor of Protein Synthesis. Science. 2002; 295: 140-143.
42. Mongiat M, Sweeney SM, San Antonio JD, Fu J, and Iozzo RV. Endorepellin, a novel inhibitor of angiogenesis derived from the C terminus of perlecan. J Biol Chem. 2003; 278: 4238-4249.
43. Willis CD, Poluzzi C, Mongiat M, and Iozzo RV. Endorepellin laminin-like globular 1/2 domains bind Ig3-5 of vascular endothelial growth factor (VEGF) receptor 2 and block pro-angiogenic signaling by VEGFA in endothelial cells. FEBS J. 2013; 280: 2271-2284.
44. Braghetta P, Ferrari A, De GP, Zanetti M, Volpin D, Bonaldo P, and Bressan GM. Overlapping, complementary and site-specific expression pattern of genes of the EMILIN/Multimerin family. Matrix Biol. 2004; 22: 549-556.
45. Christian S, Ahorn H, Novatchkova M, Garin-Chesa P, Park JE, Weber G, Eisenhaber F, Rettig WJ, and Lenter MC. Molecular cloning and characterization of EndoGlyx-1, an EMILIN-like multisubunit glycoprotein of vascular endothelium. J Biol Chem. 2001; 276: 48588-48595.
46. Sanz-Moncasi MP, Garin-Chesa P, Stockert E, Jaffe EA, Old LJ, and Rettig WJ. Identification of a high molecular weight endothelial cell surface glycoprotein, endoGlyx-1, in normal and tumor blood vessels. Lab Invest. 1994; 71: 366-373.
47. Huber MA, Kraut N, Schweifer N, Dolznig H, Peter RU, Schubert RD, Scharffetter-Kochanek K, Pehamberger H, and Garin-Chesa P. Expression of stromal cell markers in distinct compartments of human skin cancers. J Cutan Pathol. 2006; 33: 145-155.
48. Koperek O, Scheuba C, Puri C, Birner P, Haslinger C, Rettig W, Niederle B, Kaserer K, and Garin CP. Molecular characterization of the desmoplastic tumor stroma in medullary thyroid carcinoma. Int J Oncol. 2007; 31: 59-67.
49. Lorenzon E, Colladel R, Andreuzzi E, Marastoni S, Todaro F, Schiappacassi M, Ligresti G, Colombatti A, and Mongiat M. MULTIMERIN2 impairs tumor angiogenesis and growth by interfering with VEGF-A/VEGFR2 pathway. Oncogene. 2012; 31: 3136-3147.
50. Mongiat M, Ligresti G, Marastoni S, Lorenzon E, Doliana R, and Colombatti A. Regulation of the extrinsic apoptotic pathway by the extracellular matrix glycoprotein EMILIN2. Mol Cell Biol. 2007; 27: 7176-7187.
51. Marastoni S, Andreuzzi E, Paulitti A, Colladel R, Pellicani R, Todaro F, Schiavinato A, Bonaldo P, Colombatti A, and Mongiat M. EMILIN2 down-modulates the Wnt signalling pathway and suppresses breast cancer cell growth and migration. J Pathol. 2014; 232: 391-404.
52. Mongiat M, Marastoni S, Ligresti G, Lorenzon E, Schiappacassi M, Perris R, Frustaci S, and Colombatti A. The extracellular matrix glycoprotein elastin microfibril interface located protein 2: a dual role in the tumor microenvironment. Neoplasia. 2010; 12: 294-304.
53. Vempati P, Popel AS, and Mac GF. Extracellular regulation of VEGF: isoforms, proteolysis, and vascular patterning. Cytokine Growth Factor Rev. 2014; 25: 1-19.
54. Chiodelli P, Bugatti A, Urbinati C, and Rusnati M. Heparin/Heparan sulfate proteoglycans glycomic interactome in angiogenesis: biological implications and therapeutical use. Molecules. 2015; 20: 6342-6388.
55. Lamalice L, Houle F, and Huot J. Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. J Biol Chem. 2006; 281: 34009-34020.
56. Manickam V, Tiwari A, Jung JJ, Bhattacharya R, Goel A, Mukhopadhyay D, and Choudhury A. Regulation of vascular endothelial growth factor receptor 2 trafficking and angiogenesis by Golgi localized t-SNARE syntaxin 6. Blood. 2011; 117: 1425-1435.
57. Noy PJ, Lodhia P, Khan K, Zhuang X, Ward DG, Verissimo AR, Bacon A, and Bicknell R. Blocking CLEC14AMMRN2 binding inhibits sprouting angiogenesis and tumour growth. Oncogene. 2015.
58. Soltermann A, Ossola R, Kilgus-Hawelski S, von EA, Suter T, Aebersold R, and Moch H. N-glycoprotein profiling of lung adenocarcinoma pleural effusions by shotgun proteomics. Cancer. 2008; 114: 124-133.
59. Shield-Artin KL, Bailey MJ, Oliva K, Liovic AK, Barker G, Dellios NL, Reisman S, Ayhan M, and Rice GE. Identification of ovarian cancer-associated proteins in symptomatic women: a novel method for semi-quantitative plasma proteomics. Proteomics Clin Appl. 2012n/a.
60. Zanivan S, Maione F, Hein MY, Hernandez-Fernaud JR, Ostasiewicz P, Giraudo E, and Mann M. SILACBased Proteomics of Human Primary Endothelial Cell Morphogenesis Unveils Tumor Angiogenic Markers. Mol Cell Proteomics. 2013; 12: 3599-3611.
61. Jaffe EA, Nachman RL, Becker CG, and Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest. 1973; 52: 2745-2756.
62. Nakatsu MN, Davis J, and Hughes CC. Optimized fibrin gel bead assay for the study of angiogenesis. J Vis Exp. 2007186.
63. Kang K, Lim JS. Induction of functional changes of dendritic cells by silica nanoparticles. Immune Netw. 2012; 12: 104-112.