Neuropilin-2 expression is inhibited by secreted Wnt antagonists and its down-regulation is associated with reduced tumor growth and metastasis in osteosarcoma

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Ji, Tao ^a,b   Guo, Yi ^a   Kim, Kapjun ^a   McQueen, Peter ^a   Ghaffar, Samia ^a   Christ, Alexander ^a   Lin, Carol ^c   Eskander, Ramez ^d   Zi, Xiaolin ^e   Hoang, Bang H ^a,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

^c CHILDREN S HOSPITAL OF ORANGE COUNTY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Angiogenesis; Lung metastasis; Neuropilin; Osteosarcoma; Wnt pathway

Indexed keywords

NEUROPILIN 2; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; WNT PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER SURVIVAL; CAPILLARY DENSITY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MALE; MOUSE; NONHUMAN; OSTEOSARCOMA CELL LINE; PROTEIN EXPRESSION; TUMOR GROWTH; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE TUMOR; CELL ADHESION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; LUNG TUMOR; METABOLISM; METASTASIS; MORTALITY; NEOVASCULARIZATION (PATHOLOGY); OSTEOSARCOMA; PATHOLOGY; PROGNOSIS; SECONDARY; TUMOR INVASION; XENOGRAFT;

ANIMALS; BONE NEOPLASMS; CELL ADHESION; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MALE; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; NEUROPILIN-2; OSTEOSARCOMA; PROGNOSIS; RNA, SMALL INTERFERING; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84928571267     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0359-4     Document Type: Article

References (37)

1. Luetke A, Meyers PA, Lewis I, Juergens H. Osteosarcoma treatment - Where do we stand? A state of the art review. Cancer Treat Rev. 2014;40:523-32.
2. Plein A, Fantin A, Ruhrberg C. Neuropilin regulation of angiogenesis, arteriogenesis and vascular permeability. Microcirculation. 2014;21:315-23.
3. Prud'homme GJ, Glinka Y. Neuropilins are multifunctional coreceptors involved in tumor initiation, growth, metastasis and immunity. Oncotarget. 2012;3:921-39.
4. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, et al. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 1997;19:995-1005.
5. Yuan L, Moyon D, Pardanaud L, Breant C, Karkkainen MJ, Alitalo K, et al. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development. 2002;129:4797-806.
6. Staton CA, Kumar I, Reed MW, Brown NJ. Neuropilins in physiological and pathological angiogenesis. J Pathol. 2007;212:237-48.
7. Karpanen T, Heckman CA, Keskitalo S, Jeltsch M, Ollila H, Neufeld G, et al. Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J. 2006;20:1462-72.
8. Xu Y, Yuan L, Mak J, Pardanaud L, Caunt M, Kasman I, et al. Neuropilin-2 mediates VEGF-C-induced lymphatic sprouting together with VEGFR3. J Cell Biol. 2010;188:115-30.
9. Bagri A, Tessier-Lavigne M, Watts RJ. Neuropilins in tumor biology. Clin Cancer Res. 2009;15:1860-4.
10. Grandclement C, Pallandre JR, Valmary Degano S, Viel E, Bouard A, Balland J, et al. Neuropilin-2 expression promotes TGF-beta1-mediated epithelial to mesenchymal transition in colorectal cancer cells. PLoS One. 2011;6:e20444.
11. Jubb AM, Sa SM, Ratti N, Strickland LA, Schmidt M, Callahan CA, et al. Neuropilin-2 expression in cancer. Histopathology. 2012;61:340-9.
12. Nasarre P, Gemmill RM, Potiron VA, Roche J, Lu X, Baron AE, et al. Neuropilin-2 is upregulated in lung cancer cells during TGFbeta1-induced epithelialmesenchymal transition. Cancer Res. 2013;73:7111-21.
13. Ruffini F, D'Atri S, Lacal PM. Neuropilin-1 expression promotes invasiveness of melanoma cells through vascular endothelial growth factor receptor-2-dependent and -independent mechanisms. Int J Oncol. 2013;43:297-306.
14. Yasuoka H, Kodama R, Tsujimoto M, Yoshidome K, Akamatsu H, Nakahara M, et al. Neuropilin-2 expression in breast cancer: correlation with lymph node metastasis, poor prognosis, and regulation of CXCR4 expression. BMC Cancer. 2009;9:220.
15. Pellet-Many C, Frankel P, Jia H, Zachary I. Neuropilins: structure, function and role in disease. Biochem J. 2008;411:211-26.
16. Handa A, Tokunaga T, Tsuchida T, Lee YH, Kijima H, Yamazaki H, et al. Neuropilin-2 expression affects the increased vascularization and is a prognostic factor in osteosarcoma. Int J Oncol. 2000;17:291-5.
17. Caunt M, Mak J, Liang WC, Stawicki S, Pan Q, Tong RK, et al. Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell. 2008;13:331-42.
18. Gray MJ, Van Buren G, Dallas NA, Xia L, Wang X, Yang AD, et al. Therapeutic targeting of neuropilin-2 on colorectal carcinoma cells implanted in the murine liver. J Natl Cancer Inst. 2008;100:109-20.
19. Dallas NA, Gray MJ, Xia L, Fan F, van Buren G, Gaur P, et al. Neuropilin-2-mediated tumor growth and angiogenesis in pancreatic adenocarcinoma. Clin Cancer Res. 2008;14:8052-60.
20. Guo Y, Rubin EM, Xie J, Zi X, Hoang BH. Dominant negative LRP5 decreases tumorigenicity and metastasis of osteosarcoma in an animal model. Clin Orthop Relat Res. 2008;466:2039-45.
21. Guo Y, Xie J, Rubin E, Tang YX, Lin F, Zi X, et al. Frzb, a secreted Wnt antagonist, decreases growth and invasiveness of fibrosarcoma cells associated with inhibition of Met signaling. Cancer Res. 2008;68:3350-60.
22. Hoang BH, Kubo T, Healey JH, Yang R, Nathan SS, Kolb EA, et al. Dickkopf 3 inhibits invasion and motility of Saos-2 osteosarcoma cells by modulating the Wnt-beta-catenin pathway. Cancer Res. 2004;64:2734-9.
23. Lin CH, Guo Y, Ghaffar S, McQueen P, Pourmorady J, Christ A, et al. Dkk-3, a secreted wnt antagonist, suppresses tumorigenic potential and pulmonary metastasis in osteosarcoma. Sarcoma. 2013;2013:147541.
24. Rubin EM, Guo Y, Tu K, Xie J, Zi X, Hoang BH. Wnt inhibitory factor 1 decreases tumorigenesis and metastasis in osteosarcoma. Mol Cancer Ther. 2010;9:731-41.
25. Zhang X, Gaspard JP, Chung DC. Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res. 2001;61:6050-4.
26. Cao Y, Hoeppner L, Bach S, Guangqi E, Guo Y, Wang E, et al. Neuropilin-2 promotes extravasation and metastasis by interacting with endothelial alpha5 integrin. Cancer Res. 2013;73:4579-90.
27. Aplin AC, Ligresti G, Fogel E, Zorzi P, Smith K, Nicosia RF. Regulation of angiogenesis, mural cell recruitment and adventitial macrophage behavior by Toll-like receptors. Angiogenesis. 2014;17:147-61.
28. Shaked Y, Ciarrocchi A, Franco M, Lee CR, Man S, Cheung AM, et al. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science. 2006;313:1785-7.
29. Urbich C, Aicher A, Heeschen C, Dernbach E, Hofmann WK, Zeiher AM, et al. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol. 2005;39:733-42.
30. Strieter RM, Burdick MD, Mestas J, Gomperts B, Keane MP, Belperio JA. Cancer CXC chemokine networks and tumour angiogenesis. Eur J Cancer. 2006;42:768-78.
31. Ferrara N. Pathways mediating VEGF-independent tumor angiogenesis. Cytokine Growth Factor Rev. 2010;21:21-6.
32. Guo Y, Zi X, Koontz Z, Kim A, Xie J, Gorlick R, et al. Blocking Wnt/LRP5 signaling by a soluble receptor modulates the epithelial to mesenchymal transition and suppresses met and metalloproteinases in osteosarcoma Saos-2 cells. J Orthop Res. 2007;25:964-71.
33. Takagi S, Kasuya Y, Shimizu M, Matsuura T, Tsuboi M, Kawakami A, et al. Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system. Dev Biol. 1995;170:207-22.
34. Goel HL, Chang C, Pursell B, Leav I, Lyle S, Xi HS, et al. VEGF/neuropilin-2 regulation of Bmi-1 and consequent repression of IGF-IR define a novel mechanism of aggressive prostate cancer. Cancer Discov. 2012;2:906-21.
35. Abarzua F, Sakaguchi M, Takaishi M, Nasu Y, Kurose K, Ebara S, et al. Adenovirus-mediated overexpression of REIC/Dkk-3 selectively induces apoptosis in human prostate cancer cells through activation of c-Jun-NH2-kinase. Cancer Res. 2005;65:9617-22.
36. Oh W, Lee EW, Lee D, Yang MR, Ko A, Yoon CH, et al. Hdm2 negatively regulates telomerase activity by functioning as an E3 ligase of hTERT. Oncogene. 2010;29:4101-12.
37. Andree HA, Reutelingsperger CP, Hauptmann R, Hemker HC, Hermens WT, Willems GM. Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J Biol Chem. 1990;265:4923-8.