Transcriptional network analysis reveals that AT1 and AT2 Angiotensin II receptors are both involved in the regulation of genes essential for glioma progression

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Azevedo, Hátylas ^a   Fujita, André ^a   Bando, Silvia Yumi ^a   Iamashita, Priscila ^a   Moreira Filho, Carlos Alberto ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GLIOMA; GLIOMA CELL; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; TUMOR GROWTH; ANIMAL; BIOLOGY; DISEASE COURSE; ESSENTIAL GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; PATHOLOGY; REPRODUCIBILITY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; COMPUTATIONAL BIOLOGY; DISEASE PROGRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; GENES, ESSENTIAL; GLIOMA; RATS; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; REPRODUCIBILITY OF RESULTS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84909580207     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110934     Document Type: Article

References (138)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996.
2. Ehtesham M, Stevenson CB, Thompson RC (2005) Stem cell therapies for malignant glioma. Neurosurg Focus 19:5.
3. Arrieta O, Pineda-Olvera B, Guevara-Salazar P, Hernández-Pedro N, Morales-Espinosa D, et al. (2008) Expression of AT1 and AT2 angiotensin receptors in astrocytomas is associated with poor prognosis. Br J Cancer 99:160-166.
4. Kaschina E, Unger T (2003) Angiotensin AT1/AT2 receptors: regulation, signaling and function. Blood Press 12:70-88.
5. Vinson GP, Barker S, Puddefoot JR (2012) The renin-angiotensin system in the breast and breast cancer. Endocr Relat Cancer 19:1-19.
6. Ino K, Shibata K, Yamamoto E, Kajiyama H, Nawa A, et al. (2011) Role of the renin-angiotensin system in gynecologic cancers. Curr Cancer Drug Targets 11:405-411.
7. Ager EI, Neo J, Christophi C (2008) The renin-angiotensin system and malignancy. Carcinogenesis 29:1675-1684.
8. Kosaka T, Miyajima A, Takayama E, Kikuchi E, Nakashima J (2007) Angiotensin II type 1 receptor antagonist as an angiogenic inhibitor in prostate cancer. Prostate 67:41-49.
9. Funao K, Matsuyama M, Kawahito Y, Sano H, Chargui J, et al. (2008) Telmisartan is a potent target for prevention and treatment in human prostate cancer. Oncology reports 20:295-300.
10. Fujita M, Hayashi I, Yamashina S, Itoman M, Majima M (2002) Blockade of angiotensin AT1a receptor signaling reduces tumour growth, angiogenesis, and metastasis. Biochem Biophys Res Commun 294:441-447.
11. Nakai Y, Isayama H, Ijichi H, Sasaki T, Sasahira N, et al. (2010) Inhibition of renin-angiotensin system affects prognosis of advanced pancreatic cancer receiving gemcitabine. Br J Cancer 103:1644-1648.
12. Smith GR, Missailidis S (2004) Cancer, inflammation and the AT1 and AT2 receptors. J Inflamm 1:3.
13. Rhodes DR, Ateeq B, Cao Q, Tomlins SA, Mehra R, et al. (2009) AGTR1 overexpression defines a subset of breast cancer and confers sensitivity to losartan, an AGTR1 antagonist. PNAS 106:10284-10289.
14. Clere N, Corre I, Faure S, Guihot AL, Vessières E, et al. (2010) Deficiency or blockade of angiotensin II type 2 receptor delays tumorigenesis by inhibiting malignant cell proliferation and angiogenesis. Int J Cancer 127:2279-2291.
15. Ager EI, Chong WW, Wen SW, Christophi C (2010) Targeting the angiotensin II type 2 receptor (AT2R) in colorectal liver metastases. Cancer Cell Int 10:19.
16. Gallagher PE, Cook K, Soto-Pantoja D, Menon J, Tallant EA (2011). Angiotensin peptides and lung cancer. Curr Cancer Drug Targets 11:394-404.
17. Fogarty DJ, Sánchez-Gómez MV, Matute C (2002) Multiple angiotensin receptor subtypes in normal and tumor astrocytes in vitro. Glia 39:304-313.
18. Arrieta O, Guevara P, Escobar E, García-Navarrete R, Pineda B, et al. (2005) Blockage of angiotensin II type I receptor decreases the synthesis of growth factors and induces apoptosis in C6 cultured cells and C6 rat glioma. Br J Cancer 92:1247-1252.
19. Rivera E, Arrieta O, Guevara P, Duarte-Rojo A, Sotelo J (2001) AT1 receptor is present in glioma cells; its blockage reduces the growth of rat glioma. Br J Cancer 85:1396-1399.
20. Naville D, Bordet E, Berthelon MC, Durand P, Bégeot M (2001). Activator protein-1 is necessary for angiotensin-II stimulation of human adrenocorticotropin receptor gene transcription. Eur J Biochem 268:1802-1810.
21. Li J, Feltzer RE, Dawson KL, Hudson EA, Clark BJ (2003) Janus kinase 2 and calcium are required for angiotensin II-dependent activation of steroidogenic acute regulatory protein transcription in H295R human adrenocortical cells. J Biol Chem 278:52355-52362.
22. Bassett MH, White PC, Rainey WE (2004) The regulation of aldosterone synthase expression. Mol Cell Endocrinol 217:67-74.
23. Romero DG, Rilli S, Plonczynski MW, Yanes LL, Zhou MY, et al. (2007) Adrenal transcription regulatory genes modulated by angiotensin II and their role in steroidogenesis. Physiol Genomics 30:26-34.
24. Kurella M, Hsiao LL, Yoshida T, Randall JD, Chow G, et al. (2001) DNA microarray analysis of complex biologic processes. J Am Soc Nephrol 12:1072-1078.
25. Keiser JA, Bjork FA, Hodges JC, Taylor DG Jr (1992) Renal hemodynamic and excretory responses to PD123319 and losartan, nonpeptide AT1 and AT2 subtype-specific angiotensin II ligands. J Pharmacol Exp Ther 262:1154-1160.
26. Romero DG, Plonczynski M, Vergara GR, Gomez-Sanchez EP, Gomez-Sanchez CE (2004) Angiotensin II early regulated genes in H295R human adrenocortical cells. Physiol Genomics 19:106-116.
27. Roos WP, Tsaalbi-Shtylik A, Tsaryk R, Güvercin F, de Wind N, et al. (2009) The translesion polymerase Rev3L in the tolerance of alkylating anticancer drugs. Mol Pharmacol 76:927-34.
28. Yamamura M, Noguchi K, Nakano Y, Segawa E, Zushi Y, et al. (2013) Functional analysis of Zyxin in cell migration and invasive potential of oral squamous cell carcinoma cells. Int J Oncol 42:873-80.
29. Zhou W, Yang Y, Xia J, Wang H, Salama ME, et al. (2013) NEK2 induces drug resistance mainly through activation of efflux drug pumps and is associated with poor prognosis in myeloma and other cancers. Cancer Cell 23:48-62.
30. Brantley EC, Nabors LB, Gillespie GY, Choi YH, Palmer CA, et al. (2008) Loss of protein inhibitors of activated STAT-3 expression in glioblastoma multiforme tumors: implications for STAT-3 activation and gene expression. Clin Cancer Res 14:4694-4704.
31. Li L, Fan D, Wang C, Wang JY, Cui XB, et al. (2011) Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF-b1 pathways in cardiac fibroblasts. Cardiovasc Res 91:80-89.
32. Kim YC, Day RM (2012) Angiotensin II regulates activation of Bim via Rb/E2F1 during apoptosis: involvement of interaction between AMPKb1/2 and Cdk4. Am J Physiol Lung Cell Mol Physiol, 303:L228-38.
33. Thiel G, Rössler OG (2011) Immediate-early transcriptional response to angiotensin II in human adrenocortical cells. Endocrinology 2011, 152:4211-4223.
34. Li L, Zhang ZG, Lei H, Wang C, Wu LP, et al (2013) Angiotensin II reduces cardiac AdipoR1 expression through AT1 receptor/ROS/ERK1/2/c-Myc pathway. PLoS One 8:e49915.
35. Zhan Y, Brown C, Maynard E, Anshelevich A, Ni W, et al. (2005) Ets-1 is a critical regulator of Ang II-mediated vascular inflammation and remodeling. J Clin Invest 115:2508-2516.
36. Droit A, Poirier GG, Hunter JM (2005) Experimental and bioinformatic approaches for interrogating protein-protein interactions to determine protein function. J Mol Endocrinol 34:263-80.
37. Alm E, Arkin AP (2003) Biological networks. Curr Opin Struct Biol 13:193-202.
38. Nogueira EF, Bollag WB, Rainey WE (2009) Angiotensin II regulation of adrenocortical gene transcription. Mol Cell Endocrinol 302:230-236.
39. Rodrigues-Ferreira S, Abdelkarim M, Dillenburg-Pilla P, Luissint AC, di-Tommaso A, et al. (2012) Angiotensin II facilitates breast cancer cell migration and metastasis. PLoS One 7:e35667.
40. Szekeres M, Turu G, Orient A, Szalai B, Süpeki K, et al. (2009) Mechanisms of angiotensin II-mediated regulation of aldosterone synthase expression in H295R human adrenocortical and rat adrenal glomerulosa cells. Mol Cell Endocrinol 302:244-253.
41. Nogueira EF, Bollag WB, Rainey WE (2009) Angiotensin II regulation of adrenocortical gene transcription. Mol Cell Endocrinol 302:230-236.
42. Hunyady L, Catt KJ (2006) Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol 20:953-970.
43. Godin CM, Ferguson SS (2012) Biased agonism of the angiotensin II type 1 receptor. Mini Rev Med Chem 12:812-816.
44. Kim KS, Abraham D, Williams B, Violin JD, Mao L, et al. (2012) β-Arrestinbiased AT1R stimulation promotes cell survival during acute cardiac injury. Am J Physiol Heart Circ Physiol 303:1001-1010.
45. de Godoy MA, Rattan S (2006) Translocation of AT1- and AT2-receptors by higher concentrations of angiotensin II in the smooth muscle cells of rat internal anal sphincter. J Pharmacol Exp Ther 319:1088-1095.
46. Spin JM, Hsu M, Azuma J, Tedesco MM, Deng A, et al. (2011) Transcriptional profiling and network analysis of the murine angiotensin II-induced abdominal aortic aneurysm. Physiol Genomics 43:993-1003.
47. Zhu X, Gerstein M, Snyder M (2007) Getting connected: analysis and principles of biological networks. Genes Dev 21:1010-1024.
48. Missiuro PV, Liu K, Zou L, Ross BC, Zhao G, et al. (2009) Information flow analysis of interactome networks. PLoS Comput Biol 5:e1000350.
49. Erten S, Koyutürk M (2010) Role of Centrality in Network-Based Prioritization of Disease Genes. Lecture Notes in Computer Science 6023:13-25.
50. Poirel CL, Owens CC 3rd, Murali TM (2011) Network-based functional enrichment. BMC Bioinformatics 12:S14.
51. Vidal M, Cusick ME, Barabási AL (2011) Interactome networks and human disease. Cell, 144:986-998.
52. Soni D, King JA, Kaye AH, Hovens CM (2005) Genetics of glioblastoma multiforme: mitogenic signaling and cell cycle pathways converge. J Clin Neurosci 12:1-5.
53. Lo HW (2010) Targeting Ras-RAF-ERK and its interactive pathways as a novel therapy for malignant gliomas. Curr Cancer Drug Targets 10:840-848.
54. Trojan J, Cloix JF, Ardourel MY, Chatel M, Anthony DD (2007) Insulin-like growth factor type I biology and targeting in malignant gliomas. Neuroscience 145:795-811.
55. Wong ML, Kaye AH, Hovens CM (2007) Targeting malignant glioma survival signaling to improve clinical outcomes. J Clin Neurosci 14:301-308.
56. Mani A, Gelmann EP (2005) The ubiquitin-proteasome pathway and its role in cancer. J Clin Oncol 23:4776-4789.
57. Spin JM, Hsu M, Azuma J, Tedesco MM, Deng A, et al. (2011) Transcriptional profiling and network analysis of the murine angiotensin II-induced abdominal aortic aneurysm. Physiol Genomics 43:993-1003.
58. Merlo A (2003) Genes and pathways driving glioblastomas in humans and murine disease models. Neurosurg Rev 26:145-158.
59. Thomas CY, Chouinard M, Cox M, Parsons S, Stallings-Mann M, et al. (2003) Spontaneous activation and signaling by overexpressed epidermal growth factor receptors in glioblastoma cells. Int J Cancer 104:19-27.
60. Campos AH, Zhao Y, Pollman MJ, Gibbons GH (2003) DNA microarray profiling to identify angiotensin-responsive genes in vascular smooth muscle cells: potential mediators of vascular disease. Circ Res 92:111-118.
61. Nagano M, Hoshino D, Koshikawa N, Akizawa T, Seiki M (2012) Turnover of focal adhesions and cancer cell migration. Int J Cell Biol 2012:310616.
62. Zagzag D, Friedlander DR, Margolis B, Grumet M, Semenza GL, et al. (2000) Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg 33:49-55.
63. Günther W, Skaftnesmo KO, Arnold H, Terzis AJ (2003) Molecular approaches to brain tumor invasion. Acta Neurochir 145:1029-1036.
64. Kwiatkowska A, Symons M (2013). Signaling determinants of glioma cell invasion. Adv Exp Med Biol 986:121-141.
65. Miura SI, Imaizumi S, Saku K (2013) Recent progress in molecular mechanisms of angiotensin II type 1 and 2 receptors. Curr Pharm Des 19:2981-2987.
66. Inagami T, Eguchi S, Numaguchi K, Motley ED, Tang H, et al. (1999) Crosstalk between angiotensin II receptors and the tyrosine kinases and phosphatases. J Am Soc Nephrol 11:S57-61.
67. De Paolis P, Porcellini A, Savoia C, Lombardi A, Gigante B, et al. (2002) Functional cross-talk between angiotensin II and epidermal growth factor receptors in NIH3T3 fibroblasts. J Hypertens 20:693-9.
68. de Godoy MA, de Oliveira AM (2002) Cross-talk between AT (1) and AT (2) angiotensin receptors in rat anococcygeus smooth muscle. J Pharmacol Exp Ther 303:333-339.
69. Itabashi H, Maesawa C, Oikawa H, Kotani K, Sakurai E, et al. (2008) Angiotensin II and epidermal growth factor receptor cross-talk mediated by a disintegrin and metalloprotease accelerates tumor cell proliferation of hepatocellular carcinoma cell lines. Hepatol Res 38:601-613.
70. Carpentier AF, Ferrari D, Bailon O, Ursu R, Banissi C, et al. (2012) Steroidsparing effects of angiotensin-II inhibitors in glioblastoma patients. Eur - J Neurol 19:1337-1342.
71. Benda P, Lightbody J, Sato G, Levine L, Sweet W (1968) Differentiated rat glial cell strain in tissue culture. Science 161:370-371.
72. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, et al. (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Molecular Biology 7:3.
73. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, et al. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:15.
74. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25-29.
75. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:354-357.
76. Prifti E, Zucker JD, Clement K, Henegar C (2008) FunNet: an integrative tool for exploring transcriptional interactions. Bioinformatics 24:2636-2638.
77. Pirooznia M, Nagarajan V, Deng Y (2007) GeneVenn - A web application for comparing gene lists using Venn diagrams. Bioinformation 1:420-422.
78. Chen EY 1, Tan CM, Kou Y, Duan Q, Wang Z, et al (2013) Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14:128.
79. Montojo J, Zuberi K, Rodriguez H, Kazi F, Wright G, et al. (2010) GeneMANIA Cytoscape plugin: fast gene function predictions on the desktop. Bioinformatics 26:2927-2928.
80. Scardoni G, Petterlini M, Laudanna C (2009) Analyzing biological network parameters with Centiscape. Bioinformatics 25:2857-2859.
81. Killcoyne S, Carter GW, Smith J, Boyle J (2009) Cytoscape: a communitybased framework for network modeling. Methods Mol Biol 563:219-39.
82. Huang ZX, Tian HY, Hu ZF, Zhou YB, Zhao J, et al. (2008) GenCLiP: a software program for clustering gene lists by literature profiling and constructing gene co-occurrence networks related to custom keywords. BMC Bioinformatics 9:308.
83. Ono R, Matsuoka J, Yamatsuji T, Naomoto Y, Tanaka N, et al. (2008) M-RIP, a novel target of JNK signaling and a requirement for human cancer cell invasion. Int J Mol Med 22:199-203.
84. L'Espérance S, Popa I, Bachvarova M, Plante M, Patten N, et al. (2006) Gene expression profiling of paired ovarian tumors obtained prior to and following adjuvant chemotherapy: molecular signatures of chemoresistant tumors. Int J Oncol 29:5-24.
85. Fowler A, Thomson D, Giles K, Maleki S, Mreich E, et al. (2011) miR-124a is frequently down-regulated in glioblastoma and is involved in migration and invasion. Eur J Cancer 47:953-63.
86. Ohira K, Homma KJ, Hirai H, Nakamura S, Hayashi M (2006) TrkB-T1 regulates the RhoA signaling and actin cytoskeleton in glioma cells. Biochem Biophys Res Commun 342:867-74.
87. Yokota T, Kouno J, Adachi K, Takahashi H, Teramoto A, et al. (2006) Identification of histological markers for malignant glioma by genome-wide expression analysis: dynein, alpha-PIX and sorcin. Acta Neuropathol 111:29-38.
88. Tatenhorst L, Senner V, Püttmann S, Paulus W (2004) Regulators of G-protein signaling 3 and 4 (RGS3, RGS4) are associated with glioma cell motility. J Neuropathol Exp Neurol 63:210-22.
89. Ni L, Yang CS, Gioeli D, Frierson H, Toft DO, et al. (2010) FKBP51 promotes assembly of the Hsp90 chaperone complex and regulates androgen receptor signaling in prostate cancer cells. Mol Cell Biol 30:1243-53.
90. Jones DT, Gronych J, Lichter P, Witt O, Pfister SM (2012) MAPK pathway activation in pilocytic astrocytoma. Cell Mol Life Sci 69:1799-1811.
91. Yamazaki K, Takamura M, Masugi Y, Mori T, Du W, et al. (2009) Adenylate cyclase-associated protein 1 overexpressed in pancreatic cancers is involved in cancer cell motility. Lab Invest 89:425-432.
92. Vomastek T, Iwanicki MP, Schaeffer HJ, Tarcsafalvi A, Parsons JT, et al. (2007) RACK1 targets the extracellular signal-regulated kinase/mitogenactivated protein kinase pathway to link integrin engagement with focal adhesion disassembly and cell motility. Mol Cell Biol 27:8296-305.
93. Crea F, Hurt EM, Farrar WL (2010) Clinical significance of Polycomb gene expression in brain tumors. Mol Cancer 9:265.
94. Honjho Y, Fujiwara T, Nagao S, Tuchida T (1996) Analysis of proliferating cell nuclear antigen (PCNA) expression in brain tumors. No Shinkei Geka 24:143-8.
95. Breuss M, Heng JI, Poirier K, Tian G, Jaglin XH, et al. (2012) Mutations in the β-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell Rep 2:1554-62.
96. Yang X, Cao W, Zhou J, Zhang W, Zhang X, et al. (2011) 14-3-3f positive expression is associated with a poor prognosis in patients with glioblastoma. Neurosurgery 68:932-938.
97. Hu B, Shi B, Jarzynka MJ, Yiin JJ, D'Souza-Schorey C, et al. (2009) ADP-ribosylation factor 6 regulates glioma cell invasion through the IQ-domain GTPase-activating protein 1-Rac1-mediated pathway. Cancer Res 69:794-801.
98. Efeyan A, Zoncu R, Chang S, Gumper I, Snitkin H, et al. (2013) Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 493:679-683.
99. Rekers NH, Sminia P, Peters GJ (2011) Towards tailored therapy of glioblastoma multiforme. J Chemother 23:187-99.
100. Yang W, Wang L, Roehn G, Pearlstein RD, Ali-Osman F, et al. (2013) Small ubiquitin-like modifier 1-3 conjugation [corrected] is activated in human astrocytic brain tumors and is required for glioblastoma cell survival. Cancer Sci 104:70-7.
101. Hodgson JG, Yeh RF, Ray A, Wang NJ, Smirnov I, et al. (2009) Comparative analyses of gene copy number and mRNA expression in glioblastoma multiforme tumors and xenografts. Neuro Oncol 11:477-87.
102. Glass TL, Liu TJ, Yung WK (2000) Inhibition of cell growth in human glioblastoma cell lines by farnesyltransferase inhibitor SCH66336. Neuro Oncol 2:151-8.
103. Deng X, Ma L, Wu M, Zhang G, Jin C, et al. (2013) miR-124 radiosensitizes human glioma cells by targeting CDK4. J Neurooncol 114:263-274.
104. Chen H, Huang Q, Zhai DZ, Dong J, Wang AD, et al (2007) CDK1 expression and effects of CDK1 silencing on the malignant phenotype of glioma cells. Zhonghua Zhong Liu Za Zhi 29:484-8.
105. Facoetti A, Ranza E, Grecchi I, Benericetti E, Ceroni M, et al. (2006) Immunohistochemical evaluation of minichromosome maintenance protein 7 in astrocytoma grading. Anticancer Res 26:3513-3516.
106. Zhao Z, Liu Y, He H, Chen X, Chen J, et al. (2011) Candidate genes influencing sensitivity and resistance of human glioblastoma to Semustine. Brain Res Bull 86:189-94.
107. De S, Cipriano R, Jackson MW, Stark GR (2009) Overexpression of kinesins mediates docetaxel resistance in breast cancer cells. Cancer Res 69:8035-8042.
108. Wiese AH, Auer J, Lassmann S, Nährig J, Rosenberg R, et al. (2007) Identification of gene signatures for invasive colorectal tumor cells. Cancer Detect Prev 31:282-95.
109. Ke HL, Ke RH, Li ST, Li B, Lu HT, et al (2013) Expression of RACGAP1 in high grade meningiomas: a potential role in cancer progression. J Neurooncol 113:327-332.
110. Ma Z, Lin M, Li K, Fu Y, Liu X, et al. (2013) Knocking down SMC1A inhibits growth and leads to G2/M arrest in human glioma cells. Int J Clin Exp Pathol 6:862-869.
111. Momota H, Narita Y, Matsushita Y, Miyakita Y, Shibui S (2010) p53 abnormality and tumor invasion in patients with malignant astrocytoma. Brain Tumor Pathol 27:95-101.
112. Yamaguchi K, Richardson MD, Bigner DD, Kwatra MM (2005) Signal transduction through substance P receptor in human glioblastoma cells: roles for Src and PKCdelta. Cancer Chemother Pharmacol 56:585-93.
113. Tatenhorst L, Rescher U, Gerke V, Paulus W (2006) Knockdown of annexin 2 decreases migration of human glioma cells in vitro. Neuropathol Appl Neurobiol 32:271-277.
114. Jones DT, Mulholland SA, Pearson DM, Malley DS, Openshaw SW, et al. (2011) Adult grade II diffuse astrocytomas are genetically distinct from and more aggressive than their paediatric counterparts. Acta Neuropathol 121:753-61.
115. Kozlowski L, Wojtukiewicz MZ, Ostrowska H (2000) Cathepsin A activity in primary and metastatic human melanocytic tumors. Arch Dermatol Res 292:68-71.
116. Chen W, Palanisamy N, Schmidt H, Teruya-Feldstein J, Jhanwar SC, et al. (2001) Deregulation of FCGR2B expression by 1q21 rearrangements in follicular lymphomas. Oncogene 20:7686-7693.
117. Quick Q, Skalli O (2010) Alpha-actinin 1 and alpha-actinin 4: contrasting roles in the survival, motility, and RhoA signaling of astrocytoma cells. Exp Cell Res 316:1137-47.
118. Hui W, Yuntao L, Lun L, WenSheng L, ChaoFeng L, et al. (2013) MicroRNA-195 inhibits the proliferation of human glioma cells by directly targeting cyclin D1 and cyclin E1. PLoS One 8:e54932.
119. Kurisu J, Honma A, Miyajima H, Kondo S, Okumura M, et al. (2003) MDG1/ERdj4, an ER-resident DnaJ family member, suppresses cell death induced by ER stress. Genes Cells 8:189-202.
120. Bredel M, Pollack IF, Freund JM, Hamilton AD, Sebti SM (1998) Inhibition of Ras and related G-proteins as a therapeutic strategy for blocking malignant glioma growth. Neurosurgery 43:124-31.
121. Liu Q, Li G, Li R, Shen J, He Q, et al. (2010) IL-6 promotion of glioblastoma cell invasion and angiogenesis in U251 and T98G cell lines. J Neurooncol 100:165-176.
122. Zheng PP, Sieuwerts AM, Luider TM, van der Weiden M, Sillevis-Smitt PA, et al. (2004) Differential expression of splicing variants of the human caldesmon gene (CALD1) in glioma neovascularization versus normal brain microvasculature. Am J Pathol 164:2217-28.
123. de Tayrac M, Aubry M, Säikali S, Etcheverry A, Surbled C, et al. (2011) A 4-gene signature associated with clinical outcome in high-grade gliomas. Clin Cancer Res 17:317-27.
124. Du L, Zhao Z, Ma X, Hsiao TH, Chen Y, et al. (2013) miR-93-directed downregulation of DAB2 defines a novel oncogenic pathway in lung cancer. Oncogene Epub ahead of print.
125. Weiser DC, Row RH, Kimelman D (2009) Rho-regulated myosin phosphatase establishes the level of protrusive activity required for cell movements during zebrafish gastrulation. Development 136:2375-2384.
126. Yang XY, Guan M, Vigil D, der CJ, Lowy DR, et al. (2009) p120Ras-GAP binds the DLC1 Rho-GAP tumor suppressor protein and inhibits its RhoA GTPase and growth-suppressing activities. Oncogene 28:1401-1409.
127. Yamaki T, Suenaga Y, Iuchi T, Alagu J, Takatori A, et al. (2013) Temozolomide suppresses MYC via activation of TAp63 to inhibit progression of human glioblastoma. Sci Rep 3:1160.
128. Xiong G, Wang C, Evers BM, Zhou BP, Xu R (2012) RORa suppresses breast tumor invasion by inducing SEMA3F expression. Cancer Res 72:1728-1739.
129. Messina S, Frati L, Leonetti C, Zuchegna C, Di Zazzo E, et al (2011) Dualspecificity phosphatase DUSP6 has tumor-promoting properties in human glioblastomas. Oncogene 30:3813-20.
130. Johnson H, Del Rosario AM, Bryson BD, Schroeder MA, Sarkaria JN, et al. (2012) Molecular characterization of EGFR and EGFRvIII signaling networks in human glioblastoma tumor xenografts. Mol Cell Proteomics 11:1724-40.
131. Fan Y, Eswarappa SM, Hitomi M, Fox PL (2012) Myo1c facilitates G-actin transport to the leading edge of migrating endothelial cells. J Cell Biol 198:47-55.
132. Banakh I, Sali A, Dubljevic V, Grobben B, Slegers H, et al. (2002) Structural basis of allotypes of ecto-nucleotide pyrophosphatase/phosphodiesterase (plasma cell membrane glycoprotein PC-1) in the mouse and rat, and analysis of allele-specific xenogeneic antibodies. Eur J Immunogenet 29:307-313.
133. Rostila A, Puustinen A, Toljamo T, Vuopala K, Lindström I, et al. (2012) Peroxiredoxins and tropomyosins as plasma biomarkers for lung cancer and asbestos exposure. Lung Cancer 77:450-9.
134. Nawashiro H, Otani N, Uozumi Y, Ooigawa H, Toyooka T, et al. (2005) High expression of L-type amino acid transporter 1 in infiltrating glioma cells. Brain Tumor Pathol 22:89-91.
135. Sanderson RJ, Mosbaugh DW (1998) Fidelity and mutational specificity of uracil-initiated base excision DNA repair synthesis in human glioblastoma cell extracts. J Biol Chem 273:24822-24831.
136. Mishima K, Kato Y, Kaneko MK, Nishikawa R, Hirose T, et al. (2006) Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression. Acta Neuropathol 111:483-488.
137. Orr BA, Bai H, Odia Y, Jain D, Anders RA, et al. (2011) Yes-associated protein 1 is widely expressed in human brain tumors and promotes glioblastoma growth. J Neuropathol Exp Neurol 70:568-577.
138. Kusano S, Eizuru Y (2010) Human I-mfa domain proteins specifically interact with KSHV LANA and affect its regulation of Wnt signaling-dependent transcription. Biochem Biophys Res Commun 396:608-613.