Expression of angiogenic factors vascular endothelial growth factor and interleukin-8/CXCL8 is highly responsive to ambient glutamine availability: Role of nuclear factor-κB and activating protein-1

Cancer Research

Volumn 64, Issue 14, 2004, Pages 4858-4869

  Bobrovnikova Marjon, Ekaterina V ^a   Marjon, Philip L ^a   Barbash, Olena ^a   Vander Jagt, David L ^a,b   Abcouwer, Steve F ^a,b  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A FOS PROTEIN; ADENOVIRUS VECTOR; ANGIOGENIC FACTOR; CURCUMIN; GENE PRODUCT; GLUTAMINE; I KAPPA BM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DNA BINDING; GENE TARGETING; GENETIC STABILITY; HUMAN; HUMAN CELL; METASTASIS; NORTHERN BLOTTING; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; UPREGULATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CHEMOKINES, CXC; CURCUMIN; DNA, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMINE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-8; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 3142708680     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-0682     Document Type: Article

References (69)

1. McCarty MF, Liu W, Fan F, et al. Promises and pitfalls of anti-angiogenic therapy in clinical trials. Trends Mol Med 2003;9:53-8.
2. Shima DT, Deutsch U, D'Amore PA. Hypoxic induction of vascular endothelial growth factor (VEGF) in human epithelial cells is mediated by increases in mRNA stability FEBS Lett 1995;370:203-8.
3. Ikeda E, Achen MG, Breier G, Risau W. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 1995;270:19761-6.
4. Levy AP, Levy NS, Wegner S, Goldberg MA. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 1995;270:13333-40.
5. Xie K. Interleukin-8 and human cancer biology. Cytokine Growth Factor Rev 2001;12:375-91.
6. De Larco JE, Wuertz BR, Rosner KA, et al. A potential role for interleukin-8 in the metastatic phenotype of breast carcinoma cells. Am J Pathol 2001;158:639-46.
7. Miller LJ, Kurtzman SH, Wang Y, Anderson KH, Lindquist RR, Kreutzer DL. Expression of interleukin-8 receptors on tumor cells and vascular endothelial cells in human breast cancer tissue. Anticancer Res 1998;18:77-81.
8. Salcedo R, Martins-Green M, Gertz B, Oppenheim JJ, Murphy WJ. Combined administration of antibodies to human interleukin 8 and epidermal growth factor receptor results in increased antimetastatic effects on human breast carcinoma xenografts. Clin Cancer Res 2002;8:2655-65.
9. Li A, Dubey S, Varney ML, Dave BJ, Singh RK. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol 2003;170:3369-76.
10. Heidemann J, Ogawa H, Dwinell MB, et al. Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J Biol Chem 2003;278:8508-15.
11. Benelli R, Morini M, Carrozzino F, et al. Neutrophils as a key cellular target for angiostatin: implications for regulation of angiogenesis and inflammation. FASEB J 2002;16:267-9.
12. Koch AE, Polverini PI, Kunkel SL, et al. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 1992;258:1798-801.
13. Reiland J, Furcht LT, McCarthy JB. CXC-chemokines stimulate invasion and chemotaxis in prostate carcinoma cells through the CXCR2 receptor. Prostate 1999;41:78-88.
14. Xie K. Interleukin-8 and human cancer biology. Cytokine Growth Factor Rev 2001;12:375-91.
15. Roslin M, Henriksson R, Bergstrom P, Ungerstedt U, Bergenheim AT. Baseline levels of glucose metabolites, glutamate and glycerol in malignant glioma assessed by stereotactic microdialysis. J Neurooncol 2003;61:151-60.
16. Kallinowskil F, Davel S, Vaupell P, Baessler KH, Wagner K. Glucose, lactate, and ketone body utilization by human mammary carcinomas in vivo. Adv Exp Med Biol 1985;191:763-73.
17. Stein I, Neeman M, Shweiki D, Itin A, Keshet E. Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol Cell Biol 1995;15:5363-8.
18. Shweiki D, Neeman M, Itin A, Keshet E. Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc Natl Acad Sci USA 1995;92:768-72.
19. Collins CL, Wasa M, Souba WW, Abcouwer SF. Regulation of glutamine synthetase in human breast carcinoma cells and experimental tumors. Surgery 1997;122:451-63.
20. Marjon PL, Bobrovnikova-Marjon EV, Abcouwer SF. Expression of the proangiogenic factors vascular endothelial growth factor and interleukin-8/CXCL8 by human breast carcinomas is responsive to nutrient deprivation and endoplasmic reticulum stress. Mol Cancer 2004;3:4.
21. Abcouwer SF, Marjon PL, Loper RK, Vander Jagt DL. Response of VEGF expression to amino acid deprivation and inducers of endoplasmic reticulum stress. Investig Ophthalmol Vis Sci 2002;43:2791-8.
22. Roebuck KA. Regulation of interleukin-8 gene expression. J Interferon Cytokine Res 1999;19:429-38.
23. Mastronarde JG, Monick MM, Mukaida N, Matsushima K, Hunninghake GW. Activator protein-1 is the preferred transcription factor for cooperative interaction with nuclear factor-κB in respiratory syncytial virus-induced interleukin-8 gene expression in airway epithelium. J Infect Dis 1998;177:1275-81.
24. Huang S, DeGuzman A, Bucana CD, Fidler IJ. Level of interleukin-8 expression by metastatic human melanoma cells directly correlates with constitutive NF-κB activity. Cytokines Cell Mol Ther 2000;6:9-17.
25. Takaya H, Andoh A, Shimada M, Hata K, Fujiyama Y, Bamba T. The expression of chemokine genes correlates with nuclear factor-κB activation in human pancreatic cancer cell lines. Pancreas 2000;21:32-40.
26. Bancroft CC, Chen Z, Dong G, et al. Coexpression of proangiogenic factors IL-8 and VEGF by human head and neck squamous cell carcinoma involves coactivation by MEK-MAPK and IKK-NF-κB signal pathways. Clin Cancer Res 2001;7:435-42.
27. Chua CC, Hamdy RC, Chua BH. Mechanism of transforming growth factor-β1-induced expression of vascular endothelial growth factor in murine osteoblastic MC3T3-E1 cells. Biochim Biophys Acta 2000;1497:69-76.
28. Yoshida S, Ono M, Shono T, et al. Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor α-dependent angiogenesis. Mol Cell Biol 1997;17:4015-23.
29. Eisma RJ, Spiro JD, Kreutzer DL. Role of angiogenic factors: coexpression of interleukin-8 and vascular endothelial growth factor in patients with head and neck squamous carcinoma. Laryngoscope 1999;109:687-93.
30. Fasciani A, D'Ambrogio G, Bocci G, Monti M, Genazzani AR, Artini PG. High concentrations of the vascular endothelial growth factor and interleukin-8 in ovarian endometriomata. Mol Hum Reprod 2000;6:50-4.
31. Bancroft CC, Chen Z, Dong G, et al. Coexpression of proangiogenic factors IL-8 and VEGF by human head and neck squamous cell carcinoma involves coactivation by MEK-MAPK and IKK-NF-κB signal pathways. Clin Cancer Res 2001;7:435-42.
32. Yuan A, Yu CJ, Luh KT, Kuo SH, Lee YC, Yang PC. Aberrant p53 expression correlates with expression of vascular endothelial growth factor mRNA and interleukin-8 mRNA and neoangiogenesis in non-small-cell lung cancer. J Clin Oncol 2002;20:900-10.
33. Huang S, Pettaway CA, Uehara H, Bucana CD, Fidler IJ. Blockade of NF-κB activity in human prostate cancer cells is associated with suppression of angiogenesis, invasion, and metastasis. Oncogene 2001;20:4188-97.
34. Huang S, Robinson JB, Deguzman A, Bucana CD, Fidler IJ. Blockade of nuclear factor-κB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8. Cancer Res 2000;60:5334-9.
35. Shi Q, Le X, Abbruzzese JL, et al. Cooperation between transcription factor AP-1 and NF-κB in the induction of interleukin-8 in human pancreatic adenocarcinoma cells by hypoxia. J Interferon Cytokine Res 1999;19:1363-71.
36. Collins TS, Lee LF, Ting JP, Paclitaxel up-regulates interleukin-8 synthesis in human lung carcinoma through an NF-κB- and AP-1-dependent mechanism. Cancer Immunol Immunother 2000;49:78-84.
37. Desbaillets I, Diserens AC, de Tribolet N, Hamou MF, Van Meir EG. Regulation of interleukin-8 expression by reduced oxygen pressure in human glioblastoma. Oncogene 1999;18:1447-56.
38. Damert A, Ikeda E, Risau W. Activator-protein-1 binding potentiates the hypoxiainduciblefactor-1-mediated hypoxia-induced transcriptional activation of vascularendothelial growth factor expression in C6 glioma cells. Biochem J 1997;327:419-23.
39. Xu L, Fukumura D, Jain RK. Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF. J Biol Chem 2002;277:11368-74.
40. Shih SC, Claffey KP. Role of AP-1 and HIF-1 transcription factors in TGF-β activation of VEGF expression. Growth Factors 2001;19:19-34.
41. Michiels C, Minet E, Michel G, Mottet D, Piret JP, Raes M. HIF-1 and AP-1 cooperate to increase gene expression in hypoxia: role of MAP kinases. IUBMB Life 2001;52:49-53.
42. Jiang HY, Wek SA, McGrath BC, et al. Phosphorylation of the α subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses. Mol Cell Biol 2003;23:5651-63.
43. Olive M, Krylov D, Echlin DR, Gardner K, Taparowsky E, Vinson C. A dominant negative to activation protein-1 (AP1) that abolishes DNA binding and inhibits oncogenesis. J Biol Chem 1997;272:18586-94.
44. Chomcynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162:156-9.
45. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998;95:2509-14.
46. Abcouwer SF, Schwarz C, Meguid RA. Glutamine deprivation induces the expression of GADD45 and GADD153 primarily by mRNA stabilization. J Biol Chem 1999;274:28645-51.
47. Levy AP, Levy NS, Goldberg MA. Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J Biol Chem 1996;271:2746-53.
48. Park S, Lee DK, Yang CH. Inhibition of fos-jun-DNA complex formation by dihydroguaiaretic acid and in vitro cytotoxic effects on cancer cells. Cancer Lett 1998;127:23-8.
49. Jobin C, Bradham CA, Russo MP, et al. Curcumin blocks cytokine-mediated NF-κB activation and proinflammatory gene expression by inhibiting inhibitory factor I-κB kinase activity. J Immunol 1999;163:3474-83.
50. Xu YX, Pindolia KR, Janakiraman N, Chapman RA, Gautam SC. Curcumin inhibits IL1 α and TNF-α induction of AP-1 and NF-κB DNA binding activity in bone marrow stromal cells. Hematopathol Mol Hematol 1997;11:49-62.
51. Bierhaus A, Zhang Y, Quehenberger P, et al. The dietary pigment curcumin reduces endothelial tissue factor gene expression by inhibiting binding of AP-1 to the DNA and activation of NF-κB. Thromb Haemostasis 1997;77:772-82.
52. Feig BW, Lu X, Hunt KK, et al. Inhibition of the transcription factor nuclear factor-κ B by adenoviral-mediated expression of I κ B α M results in tumor cell death. Surgery 1999;126:399-405.
53. Salnikow K, Kluz T, Costa M, et al. The regulation of hypoxic genes by calcium involves c-Jun/AP-1, which cooperates with hypoxia-inducible factor 1 in response to hypoxia. Mol Cell Biol 2002;22:1734-41.
54. de Beaux AC, O'Riordain MG, Ross JA, Jodozi L, Carter DC, Fearon KC. Glutamine-supplemented total parenteral nutrition reduces blood mononuclear cell interleukin-8 release in severe acute pancreatitis. Nutrition 1998;14:261-5.
55. Lin MT, Saito H, Furukawa S, et al. Alanyl-glutamine enriched total parenteral nutrition improves local, systemic, and remote organ responses to intraperitoneal bacterial challenge. J Parenter Enteral Nutr 2001;25:346-51.
56. Huang Y, Li N, Liboni K, Neu J. Glutamine decreases lipopolysaccharide- induced IL-8 production in Caco-2 cells through a non-NF-κB p50 mechanism. Cytokine 2003;22:77-83.
57. Coeffier M, Marion R, Ducrotte P, Dechelotte P. Modulating effect of glutamine on 1L-1β-induced cytokine production by human gut. Clin Nutr 2003;22:407-13.
58. Williams BR. PKR: a sentinel kinase for cellular stress. Oncogene 1999;18:6112-20.
59. Rhoads JM, Argenzio RA, Chen W, et al. L-Glutamine stimulates intestinal cell proliferation and activates mitogen-activated protein kinases. Am J Physiol 1997;272: G943-53.
60. Roybal CN, Yang S, Sun CW, et al. Homocysteine increases the expression of VEGF by a mechanism involving endoplasmic reticulum stress and transcription factor ATF4. J Biol Chem 2004;279:14844-52.
61. Huang S, DeGuzman A, Bucana CD, Fidler IJ. Nuclear factor-κB activity correlates with growth, angiogenesis, and metastasis of human melanoma cells in nude mice. Clin Cancer Res 2000;6:2573-81.
62. Bancroft CC, Chen Z, Yeh J, et al. Effects of pharmacologic antagonists of epidermal growth factor receptor, P13K and MEK signal kinases on NF-κB and AP-1 activation and IL-8 and VEGF expression in human head and neck squamous cell carcinoma lines. Int J Cancer 2002;99:538-48.
63. Lee TH, Avraham H, Lee SH, Avraham S. Vascular endothelial growth factor modulates neutrophil transendothelial migration via up-regulation of interleukin-8 in human brain microvascular endothelial cells. J Biol Chem 2002;277:10445-51.
64. Loukinova E, Chen Z, Van Waes C, Dong G. Expression of proangiogenic chemokine Gro 1 in low and high metastatic variants of Pam murine squamous cell carcinoma is differentially regulated by IL-1α, EGF and TGF-β1 through NF-κB dependent and independent mechanisms. Int J Cancer 2001;94:637-44.
65. Lane BR, Liu J, Bock PJ, et al. Interleukin-8 and growth-regulated oncogene α mediate angiogenesis in Kaposi's sarcoma. J Virol 2002;76:11570-83.
66. Loukinova E, Dong G, Enamorado-Ayalya I, et al. Growth regulated oncogene-α expression by murine squamous cell carcinoma promotes tumor growth, metastasis, leukocyte infiltration and angiogenesis by a host CXC receptor-2 dependent mechanism. Oncogene 2000;19:3477-86.
67. Moore BB, Arenberg DA, Stoy K, et al. Distinct CXC chemokines mediate tumorigenicity of prostate cancer cells. Am J Pathol 1999;154:1503-12.
68. Youngs SJ, Ali SA, Taub DD, Rees RC. Chemokines induce migrational responses in human breast carcinoma cell lines. Int J Cancer 1997;71:257-66.
69. Fuchs IB, Lichtenegger W, Buehler H, et al. The prognostic significance of epithelial-mesenchymal transition in breast cancer. Anticancer Res 2002;22:3415-9.