Hypoxia enhances cancer cell invasion through relocalization of the proprotein convertase furin from the trans-golgi network to the cell surface

Journal of Cellular Physiology

Volumn 227, Issue 2, 2012, Pages 789-800

  Arsenault, Dominique ^a   Lucien, Fabrice ^a   Dubois, Claire M ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMIN A; FURIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; ENZYME LOCALIZATION; FEMALE; FIBROSARCOMA; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TRANS GOLGI NETWORK; TUMOR MICROENVIRONMENT;

ANOXIA; CELL LINE; CELL MEMBRANE; CONTRACTILE PROTEINS; FIBROSARCOMA; FURIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICROFILAMENT PROTEINS; NEOPLASM INVASIVENESS; PROPROTEIN CONVERTASES; PROTEIN TRANSPORT; RAB4 GTP-BINDING PROTEINS; TRANS-GOLGI NETWORK;

EID: 82155192278     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22792     Document Type: Article

References (60)

1. Anderson ED, VanSlyke JK, Thulin CD, Jean F, Thomas G. 1997. Activation of the furin endoprotease is a multiple-step process: Requirements for acidification and internal propeptide cleavage. EMBO J 16: 1508-1518.
2. Annabi B, Lachambre M, Bousquet-Gagnon N, Page M, Gingras D, Beliveau R. 2001. Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains. Biochem J 353: 547-553.
3. Arabi M, Piert M. 2010. Hypoxia PET/CT imaging: Implications for radiation oncology. Q J Nucl Med Mol Imaging 54: 500-509.
4. Basak A, Khatib AM, Mohottalage D, Basak S, Kolajova M, Bag SS. 2009. A novel enediynyl peptide inhibitor of furin that blocks processing of proPDGF-A, B and proVEGF-C. PLoS One 4: e7700.
5. Bassi DE, Fu J, Lopez de Cicco R, Klein-Szanto AJ. 2005. Proprotein convertases: "Master switches" in the regulation of tumor growth and progression. Mol Carcinog 44: 151-161.
6. Belien AT, Paganetti PA, Schwab ME. 1999. Membrane-type 1 matrix metalloprotease (MT1-MMP) enables invasive migration of glioma cells in central nervous system white matter. J Cell Biol 144: 373-384.
7. Bergeron E, Basak A, Decroly E, Seidah NG. 2003. Processing of alpha4 integrin by the proprotein convertases: Histidine at position P6 regulates cleavage. Biochem J 373: 475-484.
8. Blanchet MH, Le Good JA, Mesnard D, Oorschot V, Baflast S, Minchiotti G, Klumperman J, Constam DB. 2008. Cripto recruits Furin and PACE4 and controls Nodal trafficking during proteolytic maturation. EMBO J 27: 2580-2591.
9. Blanchette F, Rivard N, Rudd P, Grondin F, Attisano L, Dubois CM. 2001. Cross-talk between the p42/p44 MAP kinase and Smad pathways in transforming growth factor beta 1-induced furin gene transactivation. J Biol Chem 276: 33986-33994.
10. Bontemps Y, Scamuffa N, Calvo F, Khatib AM. 2007. Potential opportunity in the development of new therapeutic agents based on endogenous and exogenous inhibitors of the proprotein convertases. Med Res Rev 27: 631-648.
11. Bosshart H, Humphrey J, Deignan E, Davidson J, Drazba J, Yuan L, Oorschot V, Peters PJ, Bonifacino JS. 1994. The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J Cell Biol 126: 1157-1172.
12. Chapman RE, Munro S. 1994. Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J 13: 2305-2312.
13. Cormont M, Bortoluzzi MN, Gautier N, Mari M, van Obberghen E, Le Marchand-Brustel Y. 1996. Potential role of Rab4 in the regulation of subcellular localization of Glut4 in adipocytes. Mol Cell Biol 16: 6879-6886.
14. Cowden Dahl KD, Robertson SE, Weaver VM, Simon MC. 2005. Hypoxia-inducible factor regulates alphavbeta3 integrin cell surface expression. Mol Biol Cell 16: 1901-1912.
15. Crump CM, Xiang Y, Thomas L, Gu F, Austin C, Tooze SA, Thomas G. 2001. PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J 20: 2191-2201.
16. Denny WA. 2010. Hypoxia-activated prodrugs in cancer therapy: Progress to the clinic. Future Oncol 6: 419-428.
17. di Blasio L, Droetto S, Norman J, Bussolino F, Primo L. 2010. Protein kinase D1 regulates VEGF-a-induced alphavbeta3 integrin trafficking and endothelial cell migration. Traffic 11: 1107-1118.
18. Fletcher SJ, Rappoport JZ. 2009. The role of vesicle trafficking in epithelial cell motility. Biochem Soc Trans 37: 1072-1076.
19. Gort EH, Groot AJ, van der Wall E, van Diest PJ, Vooijs MA. 2008. Hypoxic regulation of metastasis via hypoxia-inducible factors. Curr Mol Med 8: 60-67.
20. Grant BD, Donaldson JG. 2009. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10: 597-608.
21. Hajdin K, D'Alessandro V, Niggli FK, Schafer BW, Bernasconi M. 2010. Furin targeted drug delivery for treatment of rhabdomyosarcoma in a mouse model. PLoS One 5: e10445.
22. Hobson JP, Liu S, Rono B, Leppla SH, Bugge TH. 2006. Imaging specific cell-surface proteolytic activity in single living cells. Nat Method 3: 259-261.
23. Hotary K, Allen E, Punturieri A, Yana I, Weiss SJ. 2000. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J Cell Biol 149: 1309-1323.
24. Jones BG, Thomas L, Molloy SS, Thulin CD, Fry MD, Walsh KA, Thomas G. 1995. Intracellular trafficking of furin is modulated by the phosphorylation state of a casein kinase II site in its cytoplasmic tail. EMBO J 14: 5869-5883.
25. Khatib AM, Bassi D, Siegfried G, Klein-Szanto AJ, Ouafik L. 2005. Endo/exo-proteolysis in neoplastic progression and metastasis. J Mol Med 83: 856-864.
26. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, Iyer N, LaRusch J, Pak B, Taghavi P, Semenza GL. 2003. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 63: 1138-1143.
27. Labrecque L, Nyalendo C, Langlois S, Durocher Y, Roghi C, Murphy G, Gingras D, Beliveau R. 2004. Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase. J Biol Chem 279: 52132-52140.
28. Le QT, Denko NC, Giaccia AJ. 2004. Hypoxic gene expression and metastasis. Cancer Metastasis Rev 23: 293-310.
29. Lissitzky JC, Luis J, Munzer JS, Benjannet S, Parat F, Chretien M, Marvaldi J, Seidah NG. 2000. Endoproteolytic processing of integrin pro-alpha subunits involves the redundant function of furin and proprotein convertase (PC) 5A, but not paired basic amino acid converting enzyme (PACE) 4, PC5B or PC7. Biochem J 346: 133-138.
30. Liu G, Thomas L, Warren RA, Enns CA, Cunningham CC, Hartwig JH, Thomas G. 1997. Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J Cell Biol 139: 1719-1733.
31. Lunt SJ, Chaudary N, Hill RP. 2009. The tumor microenvironment and metastatic disease. Clin Exp Metastasis 26: 19-34.
32. Manders EMM, Verbeek FJ, Aten. JA. 1993. Measurement of of objects in dual-color confocal images. J Microsc 169: 375-382.
33. Mayer G, Boileau G, Bendayan M. 2003. Furin interacts with proMT1-MMP and integrin alphaV at specialized domains of renal cell plasma membrane. J Cell Sci 116: 1763-1773.
34. McMahon S, Grondin F, McDonald PP, Richard DE, Dubois CM. 2005. Hypoxia-enhanced expression of the proprotein convertase furin is mediated by hypoxia-inducible factor-1: Impact on the bioactivation of proproteins. J Biol Chem 280: 6561-6569.
35. McMahon S, Laprise MH, Dubois CM. 2003. Alternative pathway for the role of furin in tumor cell invasion process. Enhanced MMP-2 levels through bioactive TGFbeta. Exp Cell Res 291: 326-339.
36. Molloy SS, Thomas L, Kamibayashi C, Mumby MC, Thomas G. 1998. Regulation of endosome sorting by a specific PP2A isoform. J Cell Biol 142: 1399-1411.
37. Molloy SS, Thomas L, VanSlyke JK, Stenberg PE, Thomas G. 1994. Intracellular trafficking and activation of the furin proprotein convertase: Localization to the TGN and recycling from the cell surface. EMBO J 13: 18-33.
38. Park SJ, Kim HY, Kim H, Park SM, Joe EH, Jou I, Choi YH. 2009. Oxidative stress induces lipid-raft-mediated activation of Src homology 2 domain-containing protein-tyrosine phosphatase 2 in astrocytes. Free Radic Biol Med 46: 1694-1702.
39. Pluemsampant S, Safronova OS, Nakahama K, Morita I. 2008. Protein kinase CK2 is a key activator of histone deacetylase in hypoxia-associated tumors. Int J Cancer 122: 333-341.
40. Remacle AG, Gawlik K, Golubkov VS, Cadwell GW, Liddington RC, Cieplak P, Millis SZ, Desjardins R, Routhier S, Yuan XW, Neugebauer WA, Day R, Strongin AY. 2010. Selective and potent furin inhibitors protect cells from anthrax without significant toxicity. Int J Biochem Cell Biol 42: 987-995.
41. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K. 1999. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10: 961-974.
42. Sato H, Okada Y, Seiki M. 1997. Membrane-type matrix metalloproteinases (MT-MMPs) in cell invasion. Thromb Haemost 78: 497-500.
43. Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, Seiki M. 1994. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370: 61-65.
44. Schafer W, Stroh A, Berghofer S, Seiler J, Vey M, Kruse ML, Kern HF, Klenk HD, Garten W. 1995. Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J 14: 2424-2435.
45. Shapiro J, Sciaky N, Lee J, Bosshart H, Angeletti RH, Bonifacino JS. 1997. Localization of endogenous furin in cultured cell lines. J Histochem Cytochem 45: 3-12.
46. Siegfried G, Basak A, Cromlish JA, Benjannet S, Marcinkiewicz J, Chretien M, Seidah NG, Khatib AM. 2003. The secretory proprotein convertases furin, PC5, and PC7 activate VEGF-C to induce tumorigenesis. J Clin Invest 111: 1723-1732.
47. Siegfried G, Basak A, Prichett-Pejic W, Scamuffa N, Ma L, Benjannet S, Veinot JP, Calvo F, Seidah N, Khatib AM. 2005. Regulation of the stepwise proteolytic cleavage and secretion of PDGF-B by the proprotein convertases. Oncogene 24: 6925-6935.
48. Sternlicht MD, Werb Z. 2001. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463-516.
49. Sverdlov M, Shinin V, Place AT, Castellon M, Minshall RD. 2009. Filamin A regulates caveolae internalization and trafficking in endothelial cells. Mol Biol Cell 20: 4531-4540.
50. Sweeney MC, Wavreille AS, Park J, Butchar JP, Tridandapani S, Pei D. 2005. Decoding protein-protein interactions through combinatorial chemistry: Sequence specificity of SHP-1, SHP-2, and SHIP SH2 domains. Biochemistry 44: 14932-14947.
51. Teuchert M, Berghofer S, Klenk HD, Garten W. 1999. Recycling of furin from the plasma membrane. Functional importance of the cytoplasmic tail sorting signals and interaction with the AP-2 adaptor medium chain subunit. J Biol Chem 274: 36781-36789.
52. Theriault C, aRochdi MD, Parent JL. 2004. Role of the Rab11-associated intracellular pool of receptors formed by constitutive endocytosis of the beta isoform of the thromboxane A2 receptor (TP beta). Biochemistry 43: 5600-5607.
53. Thomas G. 2002. Furin at the cutting edge: From protein traffic to embryogenesis and disease. Nat Rev Mol Cell Biol 3: 753-766.
54. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135: 913-924.
55. Van Elzen R, Ghesquiere B, Timmerman E, Vandamme S, Moens L, Gevaert K, Dewilde S. 2010. Integrated proteomic analysis reveals a substantial enrichment of protein trafficking processes in hippocampus tissue after hypoxic stress. J Proteome Res 9: 204-215.
56. Wan L, Molloy SS, Thomas L, Liu G, Xiang Y, Rybak SL, Thomas G. 1998. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 94: 205-216.
57. Wang LH, Rothberg KG, Anderson RG. 1993. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117.
58. Watanabe K, Nagaoka T, Lee JM, Bianco C, Gonzales M, Castro NP, Rangel MC, Sakamoto K, Sun Y, Callahan R, Salomon DS. 2009. Enhancement of Notch receptor maturation and signaling sensitivity by Cripto-1. J Cell Biol 187: 343-353.
59. White DP, Caswell PT, Norman JC. 2007. Alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J Cell Biol 177: 515-525.
60. Yoon SO, Shin S, Mercurio AM. 2005. Hypoxia stimulates carcinoma invasion by stabilizing microtubules and promoting the Rab11 trafficking of the alpha6beta4 integrin. Cancer Res 65: 2761-2769.