Urokinase plasminogen activator receptor induced non-small cell lung cancer invasion and metastasis requires NHE1 transporter expression and transport activity

Cellular Oncology

Volumn 35, Issue 2, 2012, Pages 95-110

  Provost, J J ^a   Rastedt, D ^a   Canine, J ^a   Ngyuen, T ^a   Haak, A ^a   Kutz, C ^a   Berthelsen, N ^a   Slusser, A ^a   Anderson, K ^a   Dorsam, G ^b   Wallert, M A ^a  

^a MINNESOTA STATE UNIVERSITY MOORHEAD   (United States)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

5 (N ethyl N isopropyl) amiloride; NCI H460; Non small cell lung cancer; Nude mice; Sodium hydrogen exchanger; Stress fiber; Tumor progression; Urokinase; Urokinase plasminogen activator; Urokinase plasminogen activator receptor

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; GELATINASE B; SODIUM PROTON EXCHANGE PROTEIN 1; UROKINASE RECEPTOR;

AMINO TERMINAL SEQUENCE; ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CANCER MORTALITY; CARCINOGENIC ACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; STRESS FIBER; TUMOR GROWTH; TUMOR VOLUME;

EID: 84870013632     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-011-0068-y     Document Type: Article

References (58)

1. Johnson DH, B.W., Carbone DP, et al. Johnson DH, Blot WJ, Carbone DP, et al., Clinical Oncology. 4 ed. Cancer of the Lung: non-small cell lung cancer and small cell lung cancer, ed. A.J. Abeloff MD, Niederhuber JE, Kastan MB, McKena WG. 2008, Philadelphia: Churchill Livingstone Elsevier. Chapter 76.
2. D. Hanahan, R.A.Weinberg, Hallmarks of cancer: the next generation. Cell 144(5), 646-74 (2011)
3. M.V. Carriero et al., Structure-based design of an urokinase-type plasminogen activator receptor-derived peptide inhibiting cell migration and lung metastasis. Molecular cancer therapeutics 8(9), 2708-17 (2009)
4. J.S. Rao et al., Inhibition of invasion, angiogenesis, tumor growth, and metastasis by adenovirus-mediated transfer of antisense uPAR and MMP-9 in non-small cell lung cancer cells. Mol Cancer Ther 4 (9), 1399-408 (2005)
5. A.K. Nalla et al., Targeting MMP-9, uPAR, and cathepsin B inhibits invasion, migration and activates apoptosis in prostate cancer cells. Cancer gene therapy 17(9), 599-613 (2010)
6. F. Blasi, P. Carmeliet, uPAR: a versatile signalling orchestrator. Nature reviews. Molecular cell biology 3(12), 932-43 (2002) (Pubitemid 35477371)
7. F. Blasi, N. Sidenius, The urokinase receptor: focused cell surface proteolysis, cell adhesion and signaling. FEBS letters 584(9), 1923-30 (2010)
8. H.W. Smith, C.J. Marshall, Regulation of cell signalling by uPAR. Nature reviews. Molecular cell biology 11(1), 23-36 (2010)
9. D. Veale, G. Needham, A.L. Harris, Urokinase receptors in lung cancer and normal lung. Anticancer research 10(2A), 417-21 (1990) (Pubitemid 20187287)
10. G. Liu, M.A. Shuman, R.L. Cohen, Co-expression of urokinase, urokinase receptor and PAI-1 is necessary for optimum invasiveness of cultured lung cancer cells. International journal of cancer. Journal international du cancer 60(4), 501-6 (1995)
11. A.E. Dear, R.L. Medcalf, The urokinase-type-plasminogen-activator receptor (CD87) is a pleiotropic molecule. European journal of bioChemistry/FEBS 252(2), 185-93 (1998) (Pubitemid 28101992)
12. G.J. Steffens et al., The complete amino acid sequence of low molecular mass urokinase from human urine. Hoppe-Seyler's Zeitschrift fur physiologische Chemie 363(9), 1043-58 (1982) (Pubitemid 13205409)
13. L. Ossowski, J.A. Aguirre-Ghiso, Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth. Current opinion in cell biology 12(5), 613-20 (2000)
14. K. Dass et al., Evolving role of uPA/uPAR system in human cancers. Cancer treatment reviews 34(2), 122-36 (2008)
15. C. Martin et al., Intracellular pH gradients in migrating cells. American journal of physiology. Cell physiology 300(3), C490-5 (2011)
16. S.K. Parks, J. Chiche, J. Pouyssegur, pH control mechanisms of tumor survival and growth. Journal of cellular physiology 226(2), 299-308 (2011)
17. M.E. Meima, J.R. Mackley, D.L. Barber, Beyond ion translocation: structural functions of the sodium-hydrogen exchanger isoform-1. Curr Opin Nephrol Hypertens 16(4), 365-72 (2007) (Pubitemid 46944336)
18. C. Stock, A. Schwab, Protons make tumor cells move like clockwork. Pflugers Archiv: European journal of physiology 458(5), 981-92 (2009)
19. BA Webb et al., Dysregulated pH: a perfect storm for cancer progression. Nature reviews. Cancer (2011)
20. MWallert et al., alpha-(1) adrenergic receptor-induced cytoskeletal organization and cell motility in CCL39 fibroblasts requires Phospholipase D1. Journal of cellular bioChemistry, (2011)
21. J. Taves et al., Sodium hydrogen exchanger and phospholipase D are required for alpha1-adrenergic receptor stimulation of metalloproteinase-9 and cellular invasion in CCL39 fibroblasts. Arch Biochem Biophys 477(1), 60-6 (2008)
22. S. Li et al., Inhibition of proliferation and apoptosis induced by a Na+/H+exchanger-1 (NHE-1) antisense gene on drug-resistant human small cell lung cancer cells. Oncology reports 21(5), 1243-9 (2009)
23. J. Pouyssegur et al., A specific mutation abolishing Na+/H+antiport activity in hamster fibroblasts precludes growth at neutral and acidic pH. Proceedings of the National Academy of Sciences of the United States of America 81(15), 4833-7 (1984) (Pubitemid 14066209)
24. J.A. Thomas et al., Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. BioChemistry 18(11), 2210-8 (1979) (Pubitemid 9191034)
25. M.A.Wallert, O. Frohlich, Na+-H+exchange in isolated myocytes from adult rat heart. Am J Physiol 257(2 Pt 1), C207-13 (1989)
26. E.E. Vomhof-DeKrey, J.S. Haring, G.P. Dorsam, Vasoactive intestinal peptide receptor 1 is downregulated during expansion of antigen-specific CD8 T cells following primary and secondary Listeria monocytogenes infections. Journal of neuroimmunology 234(1-2), 40-8 (2011)
27. C.W. Crowley et al., Prevention of metastasis by inhibition of the urokinase receptor. Proceedings of the National Academy of Sciences of the United States of America 90(11), 5021-5 (1993) (Pubitemid 23182967)
28. Y.X. Chen, E.R. O'Brien, Ethyl isopropyl amiloride inhibits smooth muscle cell proliferation and migration by inducing apoptosis and antagonizing urokinase plasminogen activator activity. Can J Physiol Pharmacol 81(7), 730-9 (2003)
29. H. Matthews, M. Ranson, M. J. Kelso, Anti-tumour/metastasis effects of the potassium-sparing diuretic amiloride: An orally active anti-cancer drug waiting for its call-of-duty? International journal of cancer. Journal international du cancer (2011)
30. S. Ghosh et al., Functional relevance of urinary-type plasminogen activator receptor-alpha3beta1 integrin association in proteinase regulatory pathways. The Journal of Biological Chemistry 281 (19), 13021-9 (2006) (Pubitemid 43855211)
31. C.H. Tang et al., Signaling through urokinase and urokinase receptor in lung cancer cells requires interactions with beta1 integrins. Journal of cell science 121(Pt 22), 3747-56 (2008)
32. S. Duriseti et al., Antagonistic anti-urokinase plasminogen activator receptor (uPAR) antibodies significantly inhibit uPAR-mediated cellular signaling and migration. The Journal of Biological Chemistry 285(35), 26878-88 (2010)
33. Y. Wei et al., Urokinase receptors are required for alpha 5 beta 1 integrin-mediated signaling in tumor cells. The Journal of Biological Chemistry 282(6), 3929-39 (2007) (Pubitemid 47084483)
34. M. Raftopoulou, A. Hall, Cell migration: Rho GTPases lead the way. Dev Biol 265(1), 23-32 (2004) (Pubitemid 38018819)
35. S. Pellegrin, H. Mellor, Actin stress fibres. Journal of cell science 120(Pt 20), 3491-9 (2007)
36. S.F. Yang et al., Increased plasma levels of urokinase plasminogen activator and matrix metalloproteinase-9 in nonsmall cell lung cancer patients. Clin Chim Acta 354(1-2), 91-9 (2005)
37. S.J. Reshkin et al., Phosphoinositide 3-kinase is involved in the tumor-specific activation of human breast cancer cell Na(+)/H(+) exchange, motility, and invasion induced by serum deprivation. J Biol Chem 275(8), 5361-9 (2000) (Pubitemid 30115166)
38. L. Kraus-Berthier et al., Histology and sensitivity to anticancer drugs of two human non-small cell lung carcinomas implanted in the pleural cavity of nude mice. Clinical cancer research: an official journal of the American Association for Cancer Research 6(1), 297-304 (2000) (Pubitemid 30065005)
39. A. Estreicher et al., The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. The Journal of cell biology 111(2), 783-92 (1990)
40. L.Y. Bourguignon et al., CD44 interaction with Na+-H+exchanger (NHE1) creates acidic microenvironments leading to haluronidase-2 and cathepsin B activation and breast tumor cell invasion. J Biol Chem 279(26), 16991-7007 (2004)
41. W. Yang et al., Inhibition of Na(+)/H(+) exchanger 1 by 5-(Nethyl-N-isopropyl) amiloride reduces hypoxia-induced hepatocellular carcinoma invasioin and motility. Cancer Lett 295(2), 198-204 (2010)
42. Y. Lin et al., NHE1 mediates MDA-MB-231 cells invasion through the regulation of MT1-MMP. Exp Cell Res 317(14), 2031-40 (2011)
43. H. Allgayer, Translational research on u-PAR. European journal of cancer 46(7), 1241-51 (2010)
44. D.A. Nikolova et al., Cetuximab attenuates metastasis and u-PAR expression in non-small cell lung cancer: u-PAR and E-cadherin are novel biomarkers of cetuximab sensitivity. Cancer research 69 (6), 2461-70 (2009)
45. S. Shetty, S. Idell, Posttranscriptional regulation of urokinase receptor gene expression in human lung carcinoma and mesothelioma cells in vitro. Molecular and cellular bioChemistry 199(1-2), 189-200 (1999) (Pubitemid 29476157)
46. R. Wang et al., Tumor-associated macrophages provide a suitable microenvironment for non-small lung cancer invasion and progression. Lung cancer, (2011)
47. J.B. Wyckoff et al., ROCK-and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Current biology: CB 16(15), 1515-23 (2006) (Pubitemid 44142977)
48. M. Baumgartner, H. Patel, D.L. Barber, Na(+)/H(+) exchanger NHE1 as plasma membrane scaffold in the assembly of signaling complexes. Am J Physiol Cell Physiol 287(4), C844-50 (2004) (Pubitemid 39238307)
49. S. Kunigal et al., SPARC-induced migration of glioblastoma cell lines via uPA-uPAR signaling and activation of small GTPase RhoA. International journal of oncology 29(6), 1349-57 (2006)
50. M. Jo et al., Cooperativity between the Ras-ERK and Rho-Rho kinase pathways in urokinase-type plasminogen activator-stimulated cell migration. The Journal of Biological Chemistry 277(14), 12479-85 (2002) (Pubitemid 34952823)
51. T. Mitsudomi et al., Mutations of ras genes distinguish a subset of non-small-cell lung cancer cell lines from small-cell lung cancer cell lines. Oncogene 6(8), 1353-62 (1991) (Pubitemid 21924231)
52. C. Legrand et al., uPA/plasmin system-mediated MMP-9 activation is implicated in bronchial epithelial cell migration. Experimental cell research 264(2), 326-36 (2001)
53. I. Henneke et al., Inhibition of urokinase activity reduces primary tumor growth and metastasis formation in a murine lung carcinoma model. American journal of respiratory and critical care medicine 181(6), 611-9 (2010)
54. M.J. Duffy, The urokinase plasminogen activator system: role in malignancy. Current pharmaceutical design 10(1), 39-49 (2004) (Pubitemid 38072742)
55. S. Linder, The matrix corroded: podosomes and invadopodia in extracellular matrix degredation. Trends in Cell Biology 17(3), 107-117 (2007) (Pubitemid 46341826)
56. G. Busco et al., NHE1 promotes invadopodial ECM proteolysis through acidification of the peri-invadopodial space. The FASEB Journal, 24(10): 3903-3915
57. L.K. Putney, D.L. Barber, Expression profile of genes regulated by activity of the Na-H exchanger NHE1. BMC Genomics 5(1), 46 (2004)
58. D. Zhou et al., Na+/H+exchanger 1 deficiency alters gene expression in mouse brain. Physiological genomics 18(3), 331-9 (2004) (Pubitemid 39319517)