Novel paracrine modulation of Notch-DLL4 signaling by Fibulin-3 promotes angiogenesis in high-grade gliomas

Cancer Research

Volumn 74, Issue 19, 2014, Pages 5435-5448

  Nandhu, Mohan S ^a   Hu, Bin ^b   Cole, Susan E ^b   Erdreich Epstein, Anat ^c,d   Rodriguez Gil, Diego J ^e   Viapiano, Mariano S ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DLL4 PROTEIN, HUMAN; EFEMP1 PROTEIN, HUMAN; NOTCH RECEPTOR; SCLEROPROTEIN; SIGNAL PEPTIDE;

ANIMAL; BRAIN TUMOR; DISEASE MODEL; GLIOMA; HUMAN; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); RAT; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX PROTEINS; GLIOMA; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; RATS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84907482234     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0685     Document Type: Article

References (49)

1. Zong H, Verhaak RG, Canoll P. The cellular origin for malignant glioma and prospects for clinical advancements. Expert Rev Mol Diagn 2012;12:383-94.
2. Omuro A, DeAngelis LM. Glioblastoma and other malignant gliomas: a clinical review. JAMA 2013;310:1842-50.
3. 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.
4. Robles Irizarry L, Hambardzumyan D, Nakano I, Gladson CL, Ahluwalia MS. Therapeutic targeting of VEGF in the treatment of glioblastoma. Expert Opin Ther Targets 2012;16:973-84.
5. Hardee ME, Zagzag D. Mechanisms of glioma-associated neovascularization. Am J Pathol 2012;181:1126-41.
6. Norden AD, Drappatz J, Muzikansky A, David K, Gerard M, McNamara MB, et al. An exploratory survival analysis of anti-angiogenic therapy for recurrent malignant glioma. J Neurooncol 2009;92:149-55.
7. Weller M, Yung WK. Angiogenesis inhibition for glioblastoma at the edge: beyond AVAGlio and RTOG 0825. Neuro Oncol 2013;15:971.
8. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci U S A 2011;108:3749-54.
9. Hu B, Nandhu MS, Sim H, Agudelo-Garcia PA, Saldivar JC, Dolan CE, et al. Fibulin-3 promotes glioma growth and resistance through a novel paracrine regulation of Notch signaling. Cancer Res 2012;72:3873-85.
10. Hu B, Thirtamara-Rajamani KK, Sim H, Viapiano MS. Fibulin-3 is uniquely upregulated in malignant gliomas and promotes tumor cell motility and invasion. Mol Cancer Res 2009;7:1756-70.
11. Giltay R, Timpl R, Kostka G. Sequence, recombinant expression and tissue localization of two novel extracellular matrix proteins, fibulin-3 and fibulin-4. Matrix Biol 1999;18:469-80.
12. Hwang CF, Chien CY, Huang SC, Yin YF, Huang CC, Fang FM, et al. Fibulin-3 is associated with tumour progression and a poor prognosis in nasopharyngeal carcinomas and inhibits cell migration and invasion via suppressed AKT activity. J Pathol 2010;222:367-79.
13. En-lin S, Sheng-guo C, Hua-qiao W. The expression of EFEMP1 in cervical carcinoma and its relationship with prognosis. Gynecol Oncol 2010;117:417-22.
14. Lathia JD, Mattson MP, Cheng A. Notch: from neural development to neurological disorders. J Neurochem 2008;107:1471-81.
15. Pierfelice TJ, Schreck KC, Eberhart CG, Gaiano N. Notch, neural stem cells, and brain tumors. Cold Spring Harb Symp Quant Biol 2008;73:367-75.
16. Dufraine J, Funahashi Y, Kitajewski J. Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene 2008;27:5132-7.
17. Jakobsson L, Bentley K, Gerhardt H. VEGFRs and Notch: a dynamic collaboration in vascular patterning. Biochem Soc Trans 2009;37:1233-6.
18. El Hindy N, Keyvani K, Pagenstecher A, Dammann P, Sandalcioglu IE, Sure U, et al. Implications of Dll4-Notch signaling activation in primary glioblastoma multiforme. Neuro Oncol 2013;15:1366-78.
19. Li JL, Sainson RC, Oon CE, Turley H, Leek R, Sheldon H, et al. DLL4-Notch signaling mediates tumor resistance to anti-VEGF therapy in vivo. Cancer Res 2011;71:6073-83.
20. Xu J, Millard M, Ren X, Cox OT, Erdreich-Epstein A. c-Abl mediates endothelial apoptosis induced by inhibition of integrins alphavbeta3 and alphavbeta5 and by disruption of actin. Blood 2010;115:2709-18.
21. Kumar TP, Vasudevan A. Isolation and culture of endothelial cells from the embryonic forebrain. J Vis Exp 2014:e51021.
22. Agudelo-Garcia PA, De Jesus JK, Williams SP, Nowicki MO, Chiocca EA, Liyanarachchi S, et al. Glioma cell migration on three-dimensional nanofiber scaffolds is regulated by substrate topography and abolished by inhibition of STAT3 signaling. Neoplasia 2011;13:831-40.
23. Scehnet JS, Jiang W, Kumar SR, Krasnoperov V, Trindade A, Benedito R, et al. Inhibition of Dll4-mediated signaling induces proliferation of immature vessels and results in poor tissue perfusion. Blood 2007;109:4753-60.
24. Del Barrio MG, Taveira-Marques R, Muroyama Y, Yuk DI, Li S, Wines-Samuelson M, et al. A regulatory network involving Foxn4, Mash1 and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 2007;134:3427-36.
25. Hale AT, Tian H, Anih E, Recio FO III, Shatat MA, Johnson T, et al. Endothelial Kruppel-like factor 4 regulates angiogenesis and the Notch signaling pathway. J Biol Chem 2014;289:12016-28.
26. Klenotic PA, Munier FL, Marmorstein LY, nand-Apte B. Tissue inhibitor of metalloproteinases-3 (TIMP-3) is a binding partner of epithelial growth factor-containing fibulin-like extracellular matrix protein 1 (EFEMP1). Implications for macular degenerations. J Biol Chem 2004;279:30469-73.
27. Kwak HI, Mendoza EA, Bayless KJ. ADAM17 co-purifies with TIMP-3 and modulates endothelial invasion responses in three-dimensional collagen matrices. Matrix Biol 2009;28:470-9.
28. Obaya AJ, Rua S, Moncada-Pazos A, Cal S. The dual role of fibulins in tumorigenesis. Cancer Lett 2012;325:132-8.
29. Kanda M, Nomoto S, Okamura Y, Hayashi M, Hishida M, Fujii T, et al. Promoter hypermethylation of fibulin 1 gene is associated with tumor progression in hepatocellular carcinoma. Mol Carcinog 2011;50:571-9.
30. Xie L, Palmsten K, MacDonald B, Kieran MW, Potenta S, Vong S, et al. Basement membrane derived fibulin-1 and fibulin-5 function as angiogenesis inhibitors and suppress tumor growth. Exp Biol Med 2008;233:155-62.
31. Baird BN, Schliekelman MJ, Ahn YH, Chen Y, Roybal JD, Gill BJ, et al. Fibulin-2 is a driver of malignant progression in lung adenocarcinoma. PLoS ONE 2013;8:e67054.
32. Law EW, Cheung AK, Kashuba VI, Pavlova TV, Zabarovsky ER, Lung HL, et al. Anti-angiogenic and tumor-suppressive roles of candidate tumor-suppressor gene, Fibulin-2, in nasopharyngeal carcinoma. Oncogene 2012;31:728-38.
33. Kim IG, Kim SY, Choi SI, Lee JH, Kim KC, Cho EW. Fibulin-3-mediated inhibition of epithelial-to-mesenchymal transition and self-renewal of ALDHH+ lung cancer stem cells through IGF1R signaling. Oncogene 2014;33:3908-91.
34. Xiao W, Zhou S, Xu H, Li H, He G, Liu Y, et al. Nogo-B promotes the epithelial-mesenchymal transition in HeLa cervical cancer cells via Fibulin-5. Oncol Rep 2013;29:109-16.
35. Gallagher WM, Currid CA, Whelan LC. Fibulins and cancer: friend or foe? Trends Mol Med 2005;11:336-40.
36. Song EL, Hou YP, Yu SP, Chen SG, Huang JT, Luo T, et al. EFEMP1 expression promotes angiogenesis and accelerates the growth of cervical cancer in vivo. Gynecol Oncol 2011;121:174-80.
37. Chen J, Wei D, Zhao Y, Liu X, Zhang J. Overexpression of EFEMP1 correlates with tumor progression and poor prognosis in human ovarian carcinoma. PLoS ONE 2013;8:e78783.
38. Seeliger H, Camaj P, Ischenko I, Kleespies A, De Toni EN, Thieme SE, et al. EFEMP1 expression promotes in vivo tumor growth in human pancreatic adenocarcinoma. Mol Cancer Res 2009;7:189-98.
39. Tong JD, Jiao NL, Wang YX, Zhang YW, Han F. Downregulation of fibulin-3 gene by promoter methylation in colorectal cancer predicts adverse prognosis. Neoplasma 2011;58:441-8.
40. Nomoto S, Kanda M, Okamura Y, Nishikawa Y, Qiyong L, Fujii T, et al. Epidermal growth factor-containing fibulin-like extracellular matrix protein 1, EFEMP1, a novel tumor-suppressor gene detected in hepatocellular carcinoma using double combination array analysis. Ann Surg Oncol 2010;17:923-32.
41. Albig AR, Neil JR, Schiemann WP. Fibulins 3 and 5 antagonize tumor angiogenesis in vivo. Cancer Res 2006;66:2621-9.
42. Kundzewicz A, Munier F, Matter JM. Expression and cell compartmentalization of EFEMP1, a protein associated with Malattia Leventinese. Adv Exp Med Biol 2008;613:277-81.
43. Hu Y, Pioli PD, Siegel E, Zhang Q, Nelson J, Chaturbedi A, et al. EFEMP1 suppresses malignant glioma growth and exerts its action within the tumor extracellular compartment. Mol Cancer 2011;10:123.
44. Marmorstein L. Association of EFEMP1 with malattia leventinese and age-related macular degeneration: a mini-review. Ophthalmic Genet 2004;25:219-26.
45. Caolo V, van den Akker NM, Verbruggen S, Donners MM, Swennen G, Schulten H, et al. Feed-forward signaling by membrane-bound ligand receptor circuit: the case of NOTCH DELTA-like 4 ligand in endothelial cells. J Biol Chem 2010;285:40681-9.
46. Bozkulak EC, Weinmaster G. Selectiveuse of ADAM10and ADAM17in activation of Notch1 signaling. Mol Cell Biol 2009;29:5679-95.
47. Sainson RC, Harris AL. Anti-Dll4 therapy: can we block tumour growth by increasing angiogenesis? Trends Mol Med 2007;13:389-95.
48. Kobayashi N, Kostka G, Garbe JH, Keene DR, Bäachinger HP, Hanisch FG, et al. A comparative analysis of the fibulin protein family. Biochemical characterization, binding interactions, and tissue localization. J Biol Chem 2007;282:11805-16.
49. El-Hallous E, Sasaki T, Hubmacher D, Getie M, Tiedemann K, Brinckmann J, et al. Fibrillin-1 interactions with fibulins depend on the first hybrid domain and provide an adaptor function to tropoelastin. J Biol Chem 2007;282:8935-46.