Hypoxia negatively regulates antimetastatic PEDF in melanoma cells by a hypoxia inducible factor-independent, autophagy dependent mechanism

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Fernández Barral, Asunción ^a,b   Orgaz, José Luis ^a,b,c   Gomez, Valentí ^a,b,d   del Peso, Luis ^a,b   Calzada, María José ^a,b   Jiménez, Benilde ^a,b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; METALLOPROTEINASE; OXOGLUTARATE DEHYDROGENASE; PIGMENT EPITHELIUM DERIVED FACTOR; PROTEASOME; VASCULOTROPIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; EYE PROTEIN; NERVE GROWTH FACTOR; PIGMENT EPITHELIUM-DERIVED FACTOR; SERINE PROTEINASE INHIBITOR;

ANTIANGIOGENIC ACTIVITY; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME DEGRADATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPOXIA; MELANOCYTE; MELANOMA CELL; METASTASIS INHIBITION; METASTASIS POTENTIAL; PIGMENT EPITHELIUM; PROTEIN PROCESSING; UNTRANSLATED REGION; CELL HYPOXIA; MELANOMA; METABOLISM; METASTASIS; PATHOLOGY; PHYSIOLOGY; TUMOR CELL CULTURE;

AUTOPHAGY; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; DOWN-REGULATION; EYE PROTEINS; HUMANS; MELANOMA; NEOPLASM METASTASIS; NERVE GROWTH FACTORS; SERPINS; TUMOR CELLS, CULTURED; UNTRANSLATED REGIONS;

EID: 84858780407     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032989     Document Type: Article

References (64)

1. Tombran-Tink J, (2005) The neuroprotective and angiogenesis inhibitory serpin, PEDF: new insights into phylogeny, function, and signaling. Front Biosci 10: 2131-2149.
2. Tombran-Tink J, Barnstable CJ, (2003) PEDF: a multifaceted neurotrophic factor. Nat Rev Neurosci 4: 628-636.
3. Becerra SP, (2006) Focus on Molecules: Pigment epithelium-derived factor (PEDF). Exp Eye Res 82: 739-740.
4. Ek ET, Dass CR, Choong PF, (2006) Pigment epithelium-derived factor: a multimodal tumor inhibitor. Mol Cancer Ther 5: 1641-1646.
5. Filleur S, Nelius T, de Riese W, Kennedy RC, (2009) Characterization of PEDF: a multi-functional serpin family protein. J Cell Biochem 106: 769-775.
6. Bouck N, (2002) PEDF: anti-angiogenic guardian of ocular function. Trends Mol Med 8: 330-334.
7. Tombran-Tink J, (2010) PEDF in angiogenic eye diseases. Curr Mol Med 10: 267-278.
8. Fernandez-Garcia NI, Volpert OV, Jimenez B, (2007) Pigment epithelium-derived factor as a multifunctional antitumor factor. J Mol Med 85: 15-22.
9. Broadhead ML, Dass CR, Choong PF, (2009) In vitro and in vivo biological activity of PEDF against a range of tumors. Expert Opin Ther Targets 13: 1429-1438.
10. Hoshina D, Abe R, Yamagishi SI, Shimizu H, (2010) The role of PEDF in tumor growth and metastasis. Curr Mol Med 10: 292-295.
11. Matsumoto K, Ishikawa H, Nishimura D, Hamasaki K, Nakao K, et al. (2004) Antiangiogenic property of pigment epithelium-derived factor in hepatocellular carcinoma. Hepatology 40: 252-259.
12. Halin S, Wikstrom P, Rudolfsson SH, Stattin P, Doll JA, et al. (2004) Decreased pigment epithelium-derived factor is associated with metastatic phenotype in human and rat prostate tumors. Cancer Res 64: 5664-5671.
13. Qingyi Z, Lin Y, Junhong W, Jian S, Weizhou H, et al. (2009) Unfavorable prognostic value of human PEDF decreased in high-grade prostatic intraepithelial neoplasia: a differential proteomics approach. Cancer Invest 27: 794-801.
14. Cai J, Parr C, Watkins G, Jiang WG, Boulton M, (2006) Decreased pigment epithelium-derived factor expression in human breast cancer progression. Clin Cancer Res 12: 3510-3517.
15. Guan M, Yam HF, Su B, Chan KP, Pang CP, et al. (2003) Loss of pigment epithelium derived factor expression in glioma progression. J Clin Pathol 56: 277-282.
16. Abramson LP, Stellmach V, Doll JA, Cornwell M, Arensman RM, et al. (2003) Wilms' tumor growth is suppressed by antiangiogenic pigment epithelium-derived factor in a xenograft model. J Pediatr Surg 38: 336-342; discussion 336-342.
17. Orgaz JL, Ladhani O, Hoek KS, Fernandez-Barral A, Mihic D, et al. (2009) 'Loss of pigment epithelium-derived factor enables migration, invasion and metastatic spread of human melanoma'. Oncogene 28: 4147-4161.
18. Garcia M, Fernandez-Garcia NI, Rivas V, Carretero M, Escamez MJ, et al. (2004) Inhibition of xenografted human melanoma growth and prevention of metastasis development by dual antiangiogenic/antitumor activities of pigment epithelium-derived factor. Cancer Res 64: 5632-5642.
19. Ladhani O, Sanchez-Martinez C, Orgaz JL, Jimenez B, Volpert OV, (2011) Pigment epithelium-derived factor blocks tumor extravasation by suppressing amoeboid morphology and mesenchymal proteolysis. Neoplasia 13: 633-642.
20. Doll JA, Stellmach VM, Bouck NP, Bergh AR, Lee C, et al. (2003) Pigment epithelium-derived factor regulates the vasculature and mass of the prostate and pancreas. Nat Med 9: 774-780.
21. Abe R, Shimizu T, Yamagishi S, Shibaki A, Amano S, et al. (2004) Overexpression of pigment epithelium-derived factor decreases angiogenesis and inhibits the growth of human malignant melanoma cells in vivo. Am J Pathol 164: 1225-1232.
22. Bedogni B, Powell MB, (2009) Hypoxia, melanocytes and melanoma- survival and tumor development in the permissive microenvironment of the skin. Pigment Cell Melanoma Res 22: 166-174.
23. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, et al. (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 10: 295-305.
24. Rey S, Semenza GL, (2010) Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 86: 236-242.
25. Wang GL, Jiang BH, Rue EA, Semenza GL, (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 92: 5510-5514.
26. Gu YZ, Moran SM, Hogenesch JB, Wartman L, Bradfield CA, (1998) Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3alpha. Gene Expr 7: 205-213.
27. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, et al. (1998) Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 92: 2260-2268.
28. Bruick RK, McKnight SL, (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337-1340.
29. 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.
30. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468.
31. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
32. Wouters BG, van den Beucken T, Magagnin MG, Koritzinsky M, Fels D, et al. (2005) Control of the hypoxic response through regulation of mRNA translation. Semin Cell Dev Biol 16: 487-501.
33. Wouters BG, Koritzinsky M, (2008) Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 8: 851-864.
34. Rocha S, (2007) Gene regulation under low oxygen: holding your breath for transcription. Trends Biochem Sci 32: 389-397.
35. McCormick R, Buffa FM, Ragoussis J, Harris AL, (2010) The role of hypoxia regulated microRNAs in cancer. Curr Top Microbiol Immunol 345: 47-70.
36. Masuda K, Abdelmohsen K, Gorospe M, (2009) RNA-binding proteins implicated in the hypoxic response. J Cell Mol Med 13: 2759-2769.
37. Notari L, Miller A, Martinez A, Amaral J, Ju M, et al. (2005) Pigment epithelium-derived factor is a substrate for matrix metalloproteinase type 2 and type 9: implications for downregulation in hypoxia. Invest Ophthalmol Vis Sci 46: 2736-2747.
38. Gross C, Buchwalter G, Dubois-Pot H, Cler E, Zheng H, et al. (2007) The ternary complex factor net is downregulated by hypoxia and regulates hypoxia-responsive genes. Mol Cell Biol 27: 4133-4141.
39. Galban S, Kuwano Y, Pullmann R Jr, Martindale JL, Kim HH, et al. (2008) RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol Cell Biol 28: 93-107.
40. Chang C, Werb Z, (2001) The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 11: S37-43.
41. Kessenbrock K, Plaks V, Werb Z, (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141: 52-67.
42. Chen JL, Lin HH, Kim KJ, Lin A, Forman HJ, et al. (2008) Novel roles for protein kinase Cdelta-dependent signaling pathways in acute hypoxic stress-induced autophagy. J Biol Chem 283: 34432-34444.
43. Chen JL, Lin HH, Kim KJ, Lin A, Ou JH, et al. (2009) PKC delta signaling: a dual role in regulating hypoxic stress-induced autophagy and apoptosis. Autophagy 5: 244-246.
44. Pursiheimo JP, Rantanen K, Heikkinen PT, Johansen T, Jaakkola PM, (2009) Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62. Oncogene 28: 334-344.
45. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
46. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, et al. (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117: 2805-2812.
47. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, et al. (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23: 33-42.
48. Dawson DW, Volpert OV, Gillis P, Crawford SE, Xu H, et al. (1999) Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285: 245-248.
49. Pouyssegur J, Dayan F, Mazure NM, (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443.
50. Hoek KS, Schlegel NC, Brafford P, Sucker A, Ugurel S, et al. (2006) Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res 19: 290-302.
51. Ortiz-Barahona A, Villar D, Pescador N, Amigo J, del Peso L, (2010) Genome-wide identification of hypoxia-inducible factor binding sites and target genes by a probabilistic model integrating transcription-profiling data and in silico binding site prediction. Nucleic Acids Res 38: 2332-2345.
52. Gorospe M, Tominaga K, Wu X, Fahling M, Ivan M, (2011) Post-Transcriptional Control of the Hypoxic Response by RNA-Binding Proteins and MicroRNAs. Front Mol Neurosci 4: 7.
53. van den Beucken T, Koritzinsky M, Wouters BG, (2006) Translational control of gene expression during hypoxia. Cancer Biol Ther 5: 749-755.
54. Kraggerud SM, Sandvik JA, Pettersen EO, (1995) Regulation of protein synthesis in human cells exposed to extreme hypoxia. Anticancer Res 15: 683-686.
55. Braunstein S, Karpisheva K, Pola C, Goldberg J, Hochman T, et al. (2007) A hypoxia-controlled cap-dependent to cap-independent translation switch in breast cancer. Mol Cell 28: 501-512.
56. Lopez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M, (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci U S A 101: 2987-2992.
57. Lopez de Silanes I, Galban S, Martindale JL, Yang X, Mazan-Mamczarz K, et al. (2005) Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol Cell Biol 25: 9520-9531.
58. Bedogni B, Welford SM, Cassarino DS, Nickoloff BJ, Giaccia AJ, et al. (2005) The hypoxic microenvironment of the skin contributes to Akt-mediated melanocyte transformation. Cancer Cell 8: 443-454.
59. Adams AE, Chudnovsky Y, Khavari PA, (2006) Oxygen deprivation provokes melanoma. Nat Med 12: 168-169.
60. Michaylira CZ, Nakagawa H, (2006) Hypoxic microenvironment as a cradle for melanoma development and progression. Cancer Biol Ther 5: 476-479.
61. Li G, Schaider H, Satyamoorthy K, Hanakawa Y, Hashimoto K, et al. (2001) Downregulation of E-cadherin and Desmoglein 1 by autocrine hepatocyte growth factor during melanoma development. Oncogene 20: 8125-8135.
62. Hoek KS, Eichhoff OM, Schlegel NC, Dobbeling U, Kobert N, et al. (2008) In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res 68: 650-656.
63. Garcia-Lopez MA, Barreiro O, Garcia-Diez A, Sanchez-Madrid F, Penas PF, (2005) Role of tetraspanins CD9 and CD151 in primary melanocyte motility. J Invest Dermatol 125: 1001-1009.
64. Punzon I, Criado LM, Serrano A, Serrano F, Bernad A, (2004) Highly efficient lentiviral-mediated human cytokine transgenesis on the NOD/scid background. Blood 103: 580-582.