Elevated expression of the C-Type Lectin CD93 in the glioblastoma vasculature regulates cytoskeletal rearrangements that enhance vessel function and reduce host survival

Cancer Research

Volumn 75, Issue 21, 2015, Pages 4504-4516

  Langenkamp, Elise ^a   Zhang, Lei ^a   Lugano, Roberta ^a   Huang, Hua ^a   Elhassan, Tamador Elsir Abu ^b   Georganaki, Maria ^a   Bazzar, Wesam ^a   Lööf, Johan ^a   Trendelenburg, George ^c   Essand, Magnus ^a   Pontén, Fredrik ^a   Smits, Anja ^b,d,e   Dimberg, Anna ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d DANISH EPILEPSY CENTRE   (Denmark)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; PROTEIN CD93; UNCLASSIFIED DRUG; CADHERIN; COMPLEMENT 1Q RECEPTOR; COMPLEMENT RECEPTOR; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN; SMALL INTERFERING RNA; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOMA; CANCER GRADING; CANCER GROWTH; CANCER SURVIVAL; CELL ADHESION; CELL CONTACT; CELL MIGRATION; CELL PROLIFERATION; CELL SPREADING; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FIBROSARCOMA; GLIOBLASTOMA; GROWTH INHIBITION; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE MICROARRAY; ACTIN FILAMENT; ANIMAL; BRAIN TUMOR; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL MOTION; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MORTALITY; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; RNA INTERFERENCE; STRESS FIBER; TUMOR CELL LINE; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ACTIN CYTOSKELETON; ANIMALS; ANTIGENS, CD; BRAIN NEOPLASMS; CADHERINS; CAPILLARY PERMEABILITY; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GLIOBLASTOMA; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, COMPLEMENT; RNA INTERFERENCE; RNA, SMALL INTERFERING; STRESS FIBERS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84946600655     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3636     Document Type: Article

References (39)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359:492-507.
2. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97-109.
3. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. Angiogenesis in brain tumours. Nat Rev Neurosci 2007;8:610-22.
4. Jansen M, De Witt Hamer PC, Witmer AN, Troost D, van Noorden CJ. Current perspectives on antiangiogenesis strategies in the treatment of malignant gliomas. Brain Res Brain Res Rev 2004;45:143-63.
5. Wong ML, Prawira A, Kaye AH, Hovens CM. Tumour angiogenesis: its mechanism and therapeutic implications in malignant gliomas. J Clin Neurosci 2009;16:1119-30.
6. Langenkamp E, Molema G. Microvascular endothelial cell heterogeneity: general concepts and pharmacological consequences for anti-angiogenic therapy of cancer. Cell Tissue Res 2009;335:205-22.
7. Dieterich LC, Mellberg S, Langenkamp E, Zhang L, Zieba A, Salomaki H, et al. Transcriptional profiling of human glioblastoma vessels indicates a key role of VEGF-A and TGF-beta2 in vascular abnormalization. J Pathol 2012;228:378-90.
8. St. Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, et al. Genes expressed in human tumor endothelium. Science 2000;289: 1197-202.
9. Langenkamp E, Vom Hagen FM, Zwiers PJ, Moorlag HE, Schouten JP, Hammes HP, et al. Tumor vascular morphology undergoes dramatic changes during outgrowth of B16 melanoma while proangiogenic gene expression remains unchanged. ISRN Oncol 2011;2011:409308.
10. Nepomuceno RR, Henschen-Edman AH, Burgess WH, Tenner AJ. cDNA cloning and primary structure analysis of C1qR(P), the human C1q/MBL/SPA receptor that mediates enhanced phagocytosis in vitro. Immunity 1997;6:119-29.
11. Bohlson SS, Silva R, Fonseca MI, Tenner AJ. CD93 is rapidly shed from the surface of humanmyeloid cells and the soluble form is detected in human plasma. J Immunol 2005;175:1239-47.
12. Greenlee MC, Sullivan SA, Bohlson SS. Detection and characterization of soluble CD93 released during inflammation. Inflamm Res 2009;58: 909-19.
13. Norsworthy PJ, Fossati-Jimack L, Cortes-Hernandez J, Taylor PR, Bygrave AE, Thompson RD, et al. Murine CD93 (C1qRp) contributes to the removal of apoptotic cells in vivo but is not required for C1q-mediated enhancement of phagocytosis. J Immunol 2004;172:3406-14.
14. Chevrier S, Genton C, Kallies A, Karnowski A, Otten LA, Malissen B, et al. CD93 is required formaintenance of antibody secretion and persistence of plasma cells in the bone marrow niche. Proc Natl Acad Sci U S A 2009;106:3895-900.
15. Masiero M, Simoes FC, Han HD, Snell C, Peterkin T, Bridges E, et al. A core human primary tumor angiogenesis signature identifies the endothelial orphan receptor ELTD1 as a key regulator of angiogenesis. Cancer Cell 2013;24:229-41.
16. Kao YC, Jiang SJ, Pan WA, Wang KC, Chen PK, Wei HJ, et al. The epidermal growth factor-like domain of CD93 is a potent angiogenic factor. PloS One 2012;7:e51647.
17. Orlandini M, Galvagni F, BardelliM, Rocchigiani M, Lentucci C, Anselmi F, et al. The characterization of a novel monoclonal antibody against CD93 unveils a new antiangiogenic target. Oncotarget 2014;5:2750-60.
18. Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, et al. Towards a knowledge-based Human Protein Atlas. Nat Biotechnol 2010;28:1248-50.
19. Mellberg S, Dimberg A, Bahram F, Hayashi M, Rennel E, Ameur A, et al. Transcriptional profiling reveals a critical role for tyrosine phosphatase VEPTP in regulation of VEGFR2 activity and endothelial cell morphogenesis. FASEB J 2009;23:1490-502.
20. Koh W, Stratman AN, Sacharidou A, Davis GE. In vitro three dimensional collagen matrix models of endothelial lumen formation during vasculogenesis and angiogenesis. Methods Enzymol 2008;443: 83-101.
21. Bisel B, Calamai M, Vanzi F, Pavone FS. Decoupling polarization of the Golgi apparatus and GM1 in the plasma membrane. PLoS One 2013;8: e80446.
22. Zhang M, Bohlson SS, Dy M, Tenner AJ. Modulated interaction of the ERM protein, moesin, with CD93. Immunology. 2005;115:63-73.
23. Elsir T, Edqvist PH, Carlson J, Ribom D, Bergqvist M, Ekman S, et al. A study of embryonic stem cell-related proteins in human astrocytomas: identification of Nanog as a predictor of survival. Int J Cancer 2014; 134:1123-31.
24. Petrenko O, Beavis A, Klaine M, Kittappa R, Godin I, Lemischka IR. The molecular characterization of the fetal stem cell marker AA4. Immunity 1999;10:691-700.
25. Maruno M, Yoshimine T, Isaka T, Kuroda R, Ishii H, Hayakawa T. Expression of thrombomodulin in astrocytomas of various malignancy and in gliotic and normal brains. J Neurooncol 1994;19:155-60.
26. Carson-Walter EB, Winans BN, Whiteman MC, Liu Y, Jarvela S, Haapasalo H, et al. Characterization of TEM1/endosialin in human and murine brain tumors. BMC Cancer 2009;9:417.
27. Maia M, DeVriese A, Janssens T, Moons M, Lories RJ, Tavernier J, et al. CD248 facilitates tumor growth via its cytoplasmic domain. BMC Cancer 2011;11:162.
28. McGreal EP, Ikewaki N, Akatsu H, Morgan BP, Gasque P. Human C1qRp is identical with CD93 and the mNI-11 antigen but does not bind C1q. J Immunol 2002;168:5222-32.
29. Greenlee-Wacker MC, Galvan MD, Bohlson SS. CD93: recent advances and implications in disease. Curr Drug Targets 2012;13:411-20.
30. Tsukita S, Yonemura S. Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J Biol Chem 1999;274:34507-10.
31. Hsu YY, Shi GY, Kuo CH, Liu SL, Wu CM, Ma CY, et al. Thrombomodulin is an ezrin-interacting protein that controls epithelial morphology and promotes collective cell migration. Faseb J 2012;26:3440-52.
32. Greenlee MC, Sullivan SA, Bohlson SS. CD93 and related family members: Their role in innate immunity. Curr Drug Targets 2008;9:130-8.
33. Harhausen D, Prinz V, Ziegler G, Gertz K, Endres M, Lehrach H, et al. CD93/AA4.1: A novel regulator of inflammation in murine focal cerebral ischemia. J Immunol 2010;184:6407-17.
34. Greenlee-Wacker MC, Briseno C, Galvan M, Moriel G, Velazquez P, Bohlson SS. Membrane-associated CD93 regulates leukocyte migration and C1q-hemolytic activity during murine peritonitis. J Immunol 2011; 187:3353-61.
35. Sieveking DP, Lim P, Chow RW, Dunn LL, Bao S, McGrath KC, et al. A sex-specific role for androgens in angiogenesis. J Exp Med 2010;207: 345-52.
36. Sader MA, Celermajer DS. Endothelial function, vascular reactivity and gender differences in the cardiovascular system. Cardiovasc Res 2002;53: 597-604.
37. Pepine CJ, Nichols WW, Pauly DF. Estrogen and different aspects of vascular disease in women and men. Circ Res 2006;99:459-61.
38. Dorak MT, Karpuzoglu E. Gender differences in cancer susceptibility: An inadequately addressed issue. Front Genet 2012;3:268.
39. Ricard D, Idbaih A, Ducray F, Lahutte M, Hoang-Xuan K, Delattre JY. Primary brain tumours in adults. Lancet 2012;379:1984-96.