Adhesion molecule-mediated hippo pathway modulates hemangioendothelioma cell behavior

Molecular and Cellular Biology

Volumn 34, Issue 24, 2014, Pages 4485-4499

  Tsuneki, Masayuki ^a   Madri, Joseph A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CELL ADHESION MOLECULE; EFFECTOR CASPASE; SEPANTRONIUM BROMIDE; SMALL INTERFERING RNA; SURVIVIN; VASCULAR ENDOTHELIAL CADHERIN; BIRC5 PROTEIN, MOUSE; CADHERIN; CD31 ANTIGEN; HIPPO PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; INHIBITOR OF APOPTOSIS PROTEIN; JUB PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; LIM PROTEIN; NAPHTHOQUINONE; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ADHESION; CELL DENSITY; CELL FUNCTION; CELL GROWTH; CELL JUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; HEMANGIOENDOTHELIOMA; HIPPOCAMPUS; IMMUNOFLUORESCENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR CELL; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; DRUG EFFECTS; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

MURINAE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD31; APOPTOSIS; BRAIN; CADHERINS; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; HEMANGIOENDOTHELIOMA; IMIDAZOLES; INHIBITOR OF APOPTOSIS PROTEINS; LIM DOMAIN PROTEINS; MICE; MICE, INBRED C57BL; NAPHTHOQUINONES; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84918825133     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00671-14     Document Type: Article

References (61)

1. Mitchell RN, Schoen FJ. 2010. Blood vessels-tumors, p 520. In Kumar V, Abbas AK, Fausto N, Aster JC (ed), Robbins&Cotran pathologic basis of disease, 8th ed. Saunders, Philadelphia, PA.
2. Fletcher CDM, Unni KK, Mertens F (ed). 2002. World Health Organization classification of tumours: pathology and genetics of tumours of soft tissue and bone, 3rd ed, p 155-177. IARC Press, Lyon, France.
3. Weiss SW, Enzinger FM. 1986. Spindle cell hemangioendothelioma. A low-grade angiosarcoma resembling a cavernous hemangioma and Kaposi's sarcoma. Am. J. Surg. Pathol. 10:521-530.
4. Hoak JC, Warner ED, Cheng HF, Fry GL, Hankenson RR. 1971. Hemangioma with thrombocytopenia and microangiopathic anemia (Kasabach-Merritt syndrome): an animal model. J. Lab. Clin. Med. 77:941-950.
5. Fry GL, Czervionke RL, Hoak JC, Smith JB, Haycraft DL. 1980. Platelet adherence to cultured vascular cells: influence of prostacyclin (PGI2). Blood 55:271-275.
6. Obeso J, Weber J, Auerbach R. 1990. A hemangioendothelioma-derived cell line: its use as a model for the study of endothelial cell biology. Lab. Invest. 63:259-269.
7. Flynn KM, Michaud M, Canosa S, Madri JA. 2013. CD44 regulates vascular endothelial barrier integrity via a PECAM-1 dependent mechanism. Angiogenesis 16:689-705. http://dx.doi.org/10.1007/s10456-013-9346-9.
8. Tsuneki M, Madri JA. 2014. CD44 regulation of endothelial cell proliferation and apoptosis via modulation of CD31 and VE-cadherin expression. J. Biol. Chem. 289:5357-5370. http://dx.doi.org/10.1074/jbc.M113.529313.
9. Ilan N, Tucker A, Madri JA. 2003. Vascular endothelial growth factor expression, beta-catenin tyrosine phosphorylation, and endothelial proliferative behavior: a pathway for transformation? Lab. Invest. 83:1105-1115. http://dx.doi.org/10.1097/01.LAB.0000083531.84403.8B.
10. Graesser D, Solowiej A, Bruckner M, Osterweil E, Juedes A, Davis S, Ruddle NH, Engelhardt B, Madri JA. 2002. Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109:383-392. http://dx.doi.org/10.1172/JCI13595.
11. Pinter E, Barreuther M, Lu T, Imhof BA, Madri JA. 1997. Plateletendothelial cell adhesion molecule-1 (PECAM-1/CD31) tyrosine phosphorylation state changes during vasculogenesis in the murine conceptus. Am. J. Pathol. 150:1523-1530.
12. Minematsu T, Iwai M, Umehara K, Usui T, Kamimura H. 2010. Characterization of human organic cation transporter 1 (OCT1/SLC22A1)- and OCT2 (SLC22A2)-mediated transport of 1-(2-methoxyethyl)-2-methyl-4,9-dioxo-3-(pyrazin-2-ylmethyl)-4,9-dihydro-1H-naphtho[2,3-d]imidazolium bromide (YM155 monobromide), a novel small molecule survivin suppressant. Drug Metab. Dispos. 38:1-4. http://dx.doi.org/10.1124/dmd.109.028142.
13. Ilan N, Mahooti S, Rimm DL, Madri JA. 1999. PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated beta-catenin. J. Cell Sci. 112(Part 18):3005-3014.
14. Flynn KM, Michaud M, Madri JA. 2013. CD44 deficiency contributes to enhanced experimental autoimmune encephalomyelitis: a role in immune cells and vascular cells of the blood-brain barrier. Am. J. Pathol. 182:1322-1336. http://dx.doi.org/10.1016/j.ajpath.2013.01.003.
15. Biswas P, Canosa S, Schoenfeld D, Schoenfeld J, Li P, Cheas LC, Zhang J, Cordova A, Sumpio B, Madri JA. 2006. PECAM-1 affects GSK-3betamediated beta-catenin phosphorylation and degradation. Am. J. Pathol. 169:314-324. http://dx.doi.org/10.2353/ajpath.2006.051112.
16. Requena L, Kutzner H. 2013. Hemangioendothelioma. Semin. Diagn. Pathol. 30:29-44. http://dx.doi.org/10.1053/j.semdp.2012.01.003.
17. Aboutalebi A, Jessup CJ, North PE, Mihm MC, Jr. 2012. Histopathology of vascular anomalies. Facial Plast. Surg. 28:545-553. http://dx.doi.org/10.1055/s-0032-1329929.
18. Liu L, Kakiuchi-Kiyota S, Arnold LL, Johansson SL, Wert D, Cohen SM. 2013. Pathogenesis of human hemangiosarcomas and hemangiomas. Hum. Pathol. 44:2302-2311. http://dx.doi.org/10.1016/j.humpath.2013.05.012.
19. Antonescu C. 2014. Malignant vascular tumors-an update. Modern Pathol. 27(Suppl 1):S30-S38. http://dx.doi.org/10.1038/modpathol.2013.176.
20. Martin-Padura I, De Castellarnau C, Uccini S, Pilozzi E, Natali PG, Nicotra MR, Ughi F, Azzolini C, Dejana E, Ruco L. 1995. Expression of VE (vascular endothelial)-cadherin and other endothelial-specific markers in haemangiomas. J. Pathol. 175:51-57. http://dx.doi.org/10.1002/path.1711750109.
21. Rothermel TA, Engelhardt B, Sheibani N. 2005. Polyoma virus middle-T-transformed PECAM-1 deficient mouse brain endothelial cells proliferate rapidly in culture and form hemangiomas in mice. J. Cell. Physiol. 202:230-239. http://dx.doi.org/10.1002/jcp.20114.
22. Murakami M, Sakai H, Kodama A, Mori T, Maruo K, Yanai T, Masegi T. 2008. Expression of the anti-apoptotic factors Bcl-2 and survivin in canine vascular tumours. J. Comp. Pathol. 139:1-7. http://dx.doi.org/10.1016/j.jcpa.2008.02.001.
23. Mabeta P, Pepper MS. 2012. Inhibition of hemangioma development in a syngeneic mouse model correlates with bcl-2 suppression and the inhibition of Akt kinase activity. Angiogenesis 15:131-139. http://dx.doi.org/10.1007/s10456-011-9248-7.
24. Amin RM, Hiroshima K, Miyagi Y, Kokubo T, Hoshi K, Fujisawa T, Nakatani Y. 2008. Role of the PI3K/Akt, mTOR, and STK11/LKB1 pathways in the tumorigenesis of sclerosing hemangioma of the lung. Pathol. Int. 58:38-44. http://dx.doi.org/10.1111/j.1440-1827.2007.02186.x.
25. Iurlaro M, Demontis F, Corada M, Zanetta L, Drake C, Gariboldi M, Peiro S, Cano A, Navarro P, Cattelino A, Tognin S, Marchisio PC, Dejana E. 2004. VE-cadherin expression and clustering maintain low levels of survivin in endothelial cells. Am. J. Pathol. 165:181-189. http://dx.doi.org/10.1016/S0002-9440(10)63287-7.
26. Nabilsi NH, Broaddus RR, Loose DS. 2009. DNA methylation inhibits p53-mediated survivin repression. Oncogene 28:2046-2050. http://dx.doi.org/10.1038/onc.2009.62.
27. Boidot R, Vegran F, Lizard-Nacol S. 2014. Transcriptional regulation of the survivin gene. Mol. Biol. Rep. 41:233-240. http://dx.doi.org/10.1007/s11033-013-2856-0.
28. Blanc-Brude OP, Yu J, Simosa H, Conte MS, Sessa WC, Altieri DC. 2002. Inhibitor of apoptosis protein survivin regulates vascular injury. Nat. Med. 8:987-994. http://dx.doi.org/10.1038/nm750.
29. Ryan BM, O'Donovan N, Duffy MJ. 2009. Survivin: a new target for anti-cancer therapy. Cancer Treat. Rev. 35:553-562. http://dx.doi.org/10.1016/j.ctrv.2009.05.003.
30. Mesri M, Morales-Ruiz M, Ackermann EJ, Bennett CF, Pober JS, Sessa WC, Altieri DC. 2001. Suppression of vascular endothelial growth factormediated endothelial cell protection by survivin targeting. Am. J. Pathol. 158:1757-1765. http://dx.doi.org/10.1016/S0002-9440(10)64131-4.
31. Xu R, Zhang P, Huang J, Ge S, Lu J, Qian G. 2007. Sp1 and Sp3 regulate basal transcription of the survivin gene. Biochem. Biophys. Res. Commun. 356:286-292. http://dx.doi.org/10.1016/j.bbrc.2007.02.140.
32. Cheng Q, Ling X, Haller A, Nakahara T, Yamanaka K, Kita A, Koutoku H, Takeuchi M, Brattain MG, Li F. 2012. Suppression of survivin promoter activity by YM155 involves disruption of Sp1-DNA interaction in the survivin core promoter. Int. J. Biochem. Mol. Biol. 3:179-197.
33. Cheung CH, Huang CC, Tsai FY, Lee JY, Cheng SM, Chang YC, Huang YC, Chen SH, Chang JY. 2013. Survivin-biology and potential as a therapeutic target in oncology. Onco Targets Ther. 6:1453-1462. http://dx.doi.org/10.2147/OTT.S33374.
34. Coumar MS, Tsai FY, Kanwar JR, Sarvagalla S, Cheung CH. 2013. Treat cancers by targeting survivin: just a dream or future reality? Cancer Treat. Rev. 39:802-811. http://dx.doi.org/10.1016/j.ctrv.2013.02.002.
35. Satoh T, Okamoto I, Miyazaki M, Morinaga R, Tsuya A, Hasegawa Y, Terashima M, Ueda S, Fukuoka M, Ariyoshi Y, Saito T, Masuda N, Watanabe H, Taguchi T, Kakihara T, Aoyama Y, Hashimoto Y, Nakagawa K. 2009. Phase I study of YM155, a novel survivin suppressant, in patients with advanced solid tumors. Clin. Cancer Res. 15:3872-3880. http://dx.doi.org/10.1158/1078-0432.CCR-08-1946.
36. Tao YF, Lu J, Du XJ, Sun LC, Zhao X, Peng L, Cao L, Xiao PF, Pang L, Wu D, Wang N, Feng X, Li YH, Ni J, Wang J, Pan J. 2012. Survivin selective inhibitor YM155 induce apoptosis in SK-NEP-1 Wilms tumor cells. BMC Cancer 12:619. http://dx.doi.org/10.1186/1471-2407-12-619.
37. Ji Y, Li K, Xiao X, Zheng S, Xu T, Chen S. 2012. Effects of propranolol on the proliferation and apoptosis of hemangioma-derived endothelial cells. J. Pediatr. Surg. 47:2216-2223. http://dx.doi.org/10.1016/j.jpedsurg.2012.09.008.
38. Tu JB, Ma RZ, Dong Q, Jiang F, Hu XY, Li QY, Pattar P, Zhang H. 2013. Induction of apoptosis in infantile hemangioma endothelial cells by propranolol. Exp. Ther. Med. 6:574-578. http://dx.doi.org/10.3892/etm.2013.1159.
39. Kum JJ, Khan ZA. 2014. Propranolol inhibits growth of hemangiomainitiating cells but does not induce apoptosis. Pediatr. Res. 75:381-388. http://dx.doi.org/10.1038/pr.2013.231.
40. Antonescu CR, Le Loarer F, Mosquera JM, Sboner A, Zhang L, Chen CL, Chen HW, Pathan N, Krausz T, Dickson BC, Weinreb I, Rubin MA, Hameed M, Fletcher CD. 2013. Novel YAP1-TFE3 fusion defines a distinct subset of epithelioid hemangioendothelioma. Genes Chromosomes Cancer 52:775-784. http://dx.doi.org/10.1002/gcc.22073.
41. Goyal RK, Lin P, Kanungo J, Payne AS, Muslin AJ, Longmore GD. 1999. Ajuba, a novel LIM protein, interacts with Grb2, augments mitogenactivated protein kinase activity in fibroblasts, and promotes meiotic maturation of Xenopus oocytes in a Grb2- and Ras-dependent manner. Mol. Cell. Biol. 19:4379-4389.
42. Kanungo J, Pratt SJ, Marie H, Longmore GD. 2000. Ajuba, a cytosolic LIM protein, shuttles into the nucleus and affects embryonal cell proliferation and fate decisions. Mol. Biol. Cell 11:3299-3313. http://dx.doi.org/10.1091/mbc.11.10.3299.
43. Das Thakur M, Feng Y, Jagannathan R, Seppa MJ, Skeath JB, Longmore GD. 2010. Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr. Biol. 20:657-662. http://dx.doi.org/10.1016/j.cub.2010.02.035.
44. Reddy BV, Irvine KD. 2013. Regulation of Hippo signaling by EGFRMAPK signaling through Ajuba family proteins. Dev. Cell 24:459-471. http://dx.doi.org/10.1016/j.devcel.2013.01.020.
45. Sun G, Irvine KD. 2013. Ajuba family proteins link JNK to Hippo signaling. Sci. Signal. 6:ra81. http://dx.doi.org/10.1126/scisignal.2004324.
46. Marie H, Pratt SJ, Betson M, Epple H, Kittler JT, Meek L, Moss SJ, Troyanovsky S, Attwell D, Longmore GD, Braga VM. 2003. The LIM protein Ajuba is recruited to cadherin-dependent cell junctions through an association with alpha-catenin. J. Biol. Chem. 278:1220-1228. http://dx.doi.org/10.1074/jbc.M205391200.
47. Haraguchi K, Ohsugi M, Abe Y, Semba K, Akiyama T, Yamamoto T. 2008. Ajuba negatively regulates the Wnt signaling pathway by promoting GSK-3beta-mediated phosphorylation of beta-catenin. Oncogene 27:274-284. http://dx.doi.org/10.1038/sj.onc.1210644.
48. Nola S, Daigaku R, Smolarczyk K, Carstens M, Martin-Martin B, Longmore G, Bailly M, Braga VM. 2011. Ajuba is required for Rac activation and maintenance of E-cadherin adhesion. J. Cell Biol. 195:855-871. http://dx.doi.org/10.1083/jcb.201107162.
49. Liang XH, Zhang GX, Zeng YB, Yang HF, Li WH, Liu QL, Tang YL, He WG, Huang YN, Zhang L, Yu LN, Zeng XC. 2014. The LIM protein JUB promotes epithelial-mesenchymal transition in colorectal cancer. Cancer Sci. 105:660-666. http://dx.doi.org/10.1111/cas.12404.
50. Tanaka I, Osada H, Fujii M, Fukatsu A, Hida T, Horio Y, Kondo Y, Sato A, Hasegawa Y, Tsujimura T, Sekido Y. 16 December 2013. LIM-domain protein AJUBA suppresses malignant mesothelioma cell proliferation via Hippo signaling cascade. Oncogene. http://dx.doi.org/10.1038/onc.2013.528.
51. Da CL, Xin Y, Zhao J, Luo XD. 2009. Significance and relationship between Yes-associated protein and survivin expression in gastric carcinoma and precancerous lesions. World J. Gastroenterol. 15:4055-4061. http://dx.doi.org/10.3748/wjg.15.4055.
52. Li H, Wolfe A, Septer S, Edwards G, Zhong X, Abdulkarim AB, Ranganathan S, Apte U. 2012. Deregulation of Hippo kinase signalling in human hepatic malignancies. Liver Int. 32:38-47. http://dx.doi.org/10.1111/j.1478-3231.2011.02646.x.
53. Badouel C, McNeill H. 2011. SnapShot: the hippo signaling pathway. Cell 145:484-484.e1. http://dx.doi.org/10.1016/j.cell.2011.04.009.
54. Low BC, Pan CQ, Shivashankar GV, Bershadsky A, Sudol M, Sheetz M. 2014. YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett. 588:2663-2670. http://dx.doi.org/10.1016/j.febslet.2014.04.012.
55. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, Elvassore N, Piccolo S. 2011. Role of YAP/TAZ in mechanotransduction. Nature 474:179-183. http://dx.doi.org/10.1038/nature10137.
56. Hau JC, Erdmann D, Mesrouze Y, Furet P, Fontana P, Zimmermann C, Schmelzle T, Hofmann F, Chene P. 2013. The TEAD4-YAP/TAZ protein-protein interaction: expected similarities and unexpected differences. Chembiochem 14:1218-1225. http://dx.doi.org/10.1002/cbic.201300163.
57. Yan L, Cai Q, Xu Y. 29 July 2014. Hypoxic conditions differentially regulate TAZ and YAP in cancer cells. Arch. Biochem. Biophys. http://dx.doi.org/10.1016/j.abb.2014.07.024.
58. Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL. 2012. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 26:54-68. http://dx.doi.org/10.1101/gad.173435.111.
59. Chen Y, Huang Y, Huang Y, Xia X, Zhang J, Zhou Y, Tan Y, He S, Qiang F, Li A, Re OD, Li G, Zhou J. 2014. JWA suppresses tumor angiogenesis via Sp1-activated matrix metalloproteinase-2 and its prognostic significance in human gastric cancer. Carcinogenesis 35:442-451. http://dx.doi.org/10.1093/carcin/bgt311.
60. Haas TL, Stitelman D, Davis SJ, Apte SS, Madri JA. 1999. Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J. Biol. Chem. 274:22679-22685. http://dx.doi.org/10.1074/jbc.274.32.22679.
61. Oka T, Remue E, Meerschaert K, Vanloo B, Boucherie C, Gfeller D, Bader GD, Sidhu SS, Vandekerckhove J, Gettemans J, Sudol M. 2010. Functional complexes between YAP2 and ZO-2 are PDZ domaindependent, and regulate YAP2 nuclear localization and signalling. Biochem. J. 432:461-472. http://dx.doi.org/10.1042/BJ20100870.