Four Jointed Box 1 Promotes Angiogenesis and Is Associated with Poor Patient Survival in Colorectal Carcinoma

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Al Greene, Nicole T ^a   Means, Anna L ^a,b   Lu, Pengcheng ^b   Jiang, Aixiang ^b,f   Schmidt, Carl R ^b,g   Chakravarthy, A Bapsi ^b   Merchant, Nipun B ^b,c   Washington, M Kay ^a,b   Zhang, Bing ^e   Shyr, Yu ^b   Deane, Natasha G ^b,c,d   Beauchamp, R Daniel ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^f MCGILL UNIVERSITY   (Canada)

^g OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; DEXTRAN SULFATE; FOUR JOINTED BOX 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; ONCOPROTEIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURVIVAL; CAPILLARY TUBE; CELL PROLIFERATION; COLON POLYP; COLORECTAL ADENOMA; COLORECTAL CARCINOMA; COLORECTAL EPITHELIUM; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOTHELIUM CELL; FEMALE; FJX1 GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; REGULATOR GENE; TUMOR XENOGRAFT; UPREGULATION; WILD TYPE;

ANIMALS; AZOXYMETHANE; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DEXTRAN SULFATE; FEMALE; HUMANS; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NERVE TISSUE PROTEINS;

EID: 84880845400     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069660     Document Type: Article

References (58)

1. Folkman J, Watson K, Ingber D, Hanahan D, (1989) Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 339: 58-61.
2. Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, et al. (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93: 705-716.
3. Eberhart CE, Coffey RJ, Radhika A, Giardiello FM, Ferrenbach S, et al. (1994) Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 107: 1183-1188.
4. Fujita T, Matsui M, Takaku K, Uetake H, Ichikawa W, et al. (1998) Size- and invasion-dependent increase in cyclooxygenase 2 levels in human colorectal carcinomas. Cancer Res 58: 4823-4826.
5. Sheehan KM, Sheahan K, O'Donoghue DP, MacSweeney F, Conroy RM, et al. (1999) The relationship between cyclooxygenase-2 expression and colorectal cancer. JAMA 282: 1254-1257.
6. Kober L, Swedberg K, McMurray JJ, Pfeffer MA, Velazquez EJ, et al. (2006) Previously known and newly diagnosed atrial fibrillation: a major risk indicator after a myocardial infarction complicated by heart failure or left ventricular dysfunction. Eur J Heart Fail 8: 591-598.
7. Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Solomon SD, et al. (2006) Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med 355: 873-884.
8. Snijders AM, Schmidt BL, Fridlyand J, Dekker N, Pinkel D, et al. (2005) Rare amplicons implicate frequent deregulation of cell fate specification pathways in oral squamous cell carcinoma. Oncogene 24: 4232-4242.
9. Jarvinen AK, Autio R, Kilpinen S, Saarela M, Leivo I, et al. (2008) High-resolution copy number and gene expression microarray analyses of head and neck squamous cell carcinoma cell lines of tongue and larynx. Genes Chromosomes Cancer 47: 500-509.
10. Buckanovich RJ, Sasaroli D, O'Brien-Jenkins A, Botbyl J, Hammond R, et al. (2007) Tumor vascular proteins as biomarkers in ovarian cancer. J Clin Oncol 25: 852-861.
11. Lu C, Bonome T, Li Y, Kamat AA, Han LY, et al. (2007) Gene alterations identified by expression profiling in tumor-associated endothelial cells from invasive ovarian carcinoma. Cancer Res 67: 1757-1768.
12. Aird WC, (2009) Molecular heterogeneity of tumor endothelium. Cell Tissue Res 335: 271-281.
13. Smith JJ, Deane NG, Wu F, Merchant NB, Zhang B, et al. (2010) Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 138: 958-968.
14. Johnson JC, Schmidt CR, Shrubsole MJ, Billheimer DD, Joshi PR, et al. (2006) Urine PGE-M: A metabolite of prostaglandin E2 as a potential biomarker of advanced colorectal neoplasia. Clin Gastroenterol Hepatol 4: 1358-1365.
15. Zhang B, Kirov S, Snoddy J, (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Research 33: W741-W748.
16. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
17. Morikawa K, Walker SM, Nakajima M, Pathak S, Jessup JM, et al. (1988) Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res 48: 6863-6871.
18. Nam KT, Varro A, Coffey RJ, Goldenring JR, (2007) Potentiation of oxyntic atrophy-induced gastric metaplasia in amphiregulin-deficient mice. Gastroenterology 132: 1804-1819.
19. Blaine SA, Ray KC, Anunobi R, Gannon MA, Washington MK, et al. (2010) Adult pancreatic acinar cells give rise to ducts but not endocrine cells in response to growth factor signaling. Development 137: 2289-2296.
20. Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, et al. (2008) Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 40: 1010-1015.
21. Okayasu I, Ohkusa T, Kajiura K, Kanno J, Sakamoto S, (1996) Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut 39: 87-92.
22. Neufert C, Becker C, Neurath MF, (2007) An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc 2: 1998-2004.
23. Dieleman LA, Palmen MJ, Akol H, Bloemena E, Pena AS, et al. (1998) Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol 114: 385-391.
24. Buckles GR, Rauskolb C, Villano JL, Katz FN, (2001) Four-jointed interacts with dachs, abelson and enabled and feeds back onto the Notch pathway to affect growth and segmentation in the Drosophila leg. Development 128: 3533-3542.
25. Rock R, Heinrich AC, Schumacher N, Gessler M, (2005) Fjx1: a notch-inducible secreted ligand with specific binding sites in developing mouse embryos and adult brain. Dev Dyn 234: 602-612.
26. Strutt H, Mundy J, Hofstra K, Strutt D, (2004) Cleavage and secretion is not required for Four-jointed function in Drosophila patterning. Development 131: 881-890.
27. Kubota Y, Kleinman HK, Martin GR, Lawley TJ, (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107: 1589-1598.
28. Arnaoutova I, George J, Kleinman HK, Benton G, (2009) The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis 12: 267-274.
29. Simon MP, Tournaire R, Pouyssegur J, (2008) The angiopoietin-2 gene of endothelial cells is up-regulated in hypoxia by a HIF binding site located in its first intron and by the central factors GATA-2 and Ets-1. J Cell Physiol 217: 809-818.
30. Wolf N, Yang W, Dunk CE, Gashaw I, Lye SJ, et al. (2010) Regulation of the matricellular proteins CYR61 (CCN1) and NOV (CCN3) by hypoxia-inducible factor-1{alpha} and transforming-growth factor-{beta}3 in the human trophoblast. Endocrinology 151: 2835-2845.
31. Wan J, Chai H, Yu Z, Ge W, Kang N, et al. (2011) HIF-1alpha effects on angiogenic potential in human small cell lung carcinoma. J Exp Clin Cancer Res 30: 77.
32. Sanchez-Elsner T, Botella LM, Velasco B, Langa C, Bernabeu C, (2002) Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J Biol Chem 277: 43799-43808.
33. Okuyama H, Krishnamachary B, Zhou YF, Nagasawa H, Bosch-Marce M, et al. (2006) Expression of vascular endothelial growth factor receptor 1 in bone marrow-derived mesenchymal cells is dependent on hypoxia-inducible factor 1. J Biol Chem 281: 15554-15563.
34. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, et al. (2006) Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 281: 15215-15226.
35. Anelli V, Gault CR, Cheng AB, Obeid LM, (2008) Sphingosine kinase 1 is up-regulated during hypoxia in U87MG glioma cells. Role of hypoxia-inducible factors 1 and 2. J Biol Chem 283: 3365-3375.
36. Lai VK, Afzal MR, Ashraf M, Jiang S, Haider H, (2012) Non-hypoxic stabilization of HIF-Ialpha during coordinated interaction between Akt and angiopoietin-1 enhances endothelial commitment of bone marrow stem cells. J Mol Med (Berl) 90: 719-730.
37. Osada-Oka M, Ikeda T, Akiba S, Sato T, (2008) Hypoxia stimulates the autocrine regulation of migration of vascular smooth muscle cells via HIF-1alpha-dependent expression of thrombospondin-1. J Cell Biochem 104: 1918-1926.
38. Spinella F, Garrafa E, Di Castro V, Rosano L, Nicotra MR, et al. (2009) Endothelin-1 stimulates lymphatic endothelial cells and lymphatic vessels to grow and invade. Cancer Res 69: 2669-2676.
39. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613.
40. Arber N, Eagle CJ, Spicak J, Racz I, Dite P, et al. (2006) Celecoxib for the prevention of colorectal adenomatous polyps. N Engl J Med 355: 885-895.
41. Buchanan FG, Holla V, Katkuri S, Matta P, DuBois RN, (2007) Targeting cyclooxygenase-2 and the epidermal growth factor receptor for the prevention and treatment of intestinal cancer. Cancer Res 67: 9380-9388.
42. Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Wu K, et al. (2008) Aspirin dose and duration of use and risk of colorectal cancer in men. Gastroenterology 134: 21-28.
43. Naumov GN, Akslen LA, Folkman J, (2006) Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle 5: 1779-1787.
44. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, et al. (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60.
45. Lobov IB, Brooks PC, Lang RA, (2002) Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci U S A 99: 11205-11210.
46. Ferrara N, (2010) Binding to the extracellular matrix and proteolytic processing: two key mechanisms regulating vascular endothelial growth factor action. Mol Biol Cell 21: 687-690.
47. Seppinen L, Pihlajaniemi T, (2011) The multiple functions of collagen XVIII in development and disease. Matrix Biol 30: 83-92.
48. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, et al. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54.
49. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, et al. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275.
50. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, et al. (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275: 25130-25138.
51. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, et al. (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1: 401-408.
52. Hagen T, Taylor CT, Lam F, Moncada S, (2003) Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science 302: 1975-1978.
53. Chua YL, Dufour E, Dassa EP, Rustin P, Jacobs HT, et al. (2010) Stabilization of hypoxia-inducible factor-1alpha protein in hypoxia occurs independently of mitochondrial reactive oxygen species production. J Biol Chem 285: 31277-31284.
54. Melani M, Weinstein BM, (2010) Common factors regulating patterning of the nervous and vascular systems. Annu Rev Cell Dev Biol 26: 639-665.
55. Nasarre P, Potiron V, Drabkin H, Roche J, (2010) Guidance molecules in lung cancer. Cell Adh Migr 4: 130-145.
56. Legg JA, Herbert JM, Clissold P, Bicknell R, (2008) Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 11: 13-21.
57. Ashery-Padan R, Alvarez-Bolado G, Klamt B, Gessler M, Gruss P, (1999) Fjx1, the murine homologue of the Drosophila four-jointed gene, codes for a putative secreted protein expressed in restricted domains of the developing and adult brain. Mech Dev 80: 213-217.
58. Probst B, Rock R, Gessler M, Vortkamp A, Puschel AW, (2007) The rodent Four-jointed ortholog Fjx1 regulates dendrite extension. Dev Biol 312: 461-470.