Heparin co-factor II enhances cell motility and promotes metastasis in non-small cell lung cancer

Journal of Pathology

Volumn 235, Issue 1, 2015, Pages 50-64

  Liao, Wei Yu ^a,b   Ho, Chao Chi ^b   Hou, Hsin Han ^b   Hsu, Tsi Hsuan ^c   Tsai, Meng Feng ^d   Chen, Kuan Yu ^b   Chen, Hsuan Yu ^e   Lee, Yung Chie ^b   Yu, Chong Jen ^b   Lee, Chau Hwang ^c,f   Yang, Pan Chyr ^b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d DA YEH UNIVERSITY   (Taiwan)

^e INSTITUTE OF STATISTICAL SCIENCE   (Taiwan)

^f RESEARCH CENTER FOR APPLIED SCIENCES   (Taiwan)

Author keywords

Cell motility; Heparin co factor II; Metastasis; Non small cell lung cancer

Indexed keywords

HEPARIN COFACTOR II; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; RAC1 PROTEIN; THROMBIN; SERPIND1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PATIENT; CANCER RECURRENCE; CANCER SURGERY; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; FILOPODIUM; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG CANCER CELL LINE; MAJOR CLINICAL STUDY; METASTASIS; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; OVERALL SURVIVAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SERIAL ANALYSIS OF GENE EXPRESSION; UPREGULATION; ADULT; AGED; CELL MOTION; CELL PROLIFERATION; FEMALE; GENETICS; LUNG TUMOR; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; PATHOLOGY; PHYSIOLOGY; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, NON-SMALL-CELL LUNG; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; HEPARIN COFACTOR II; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASM RECURRENCE, LOCAL; PHOSPHATIDYLINOSITOL 3-KINASES;

EID: 84916233102     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4421     Document Type: Article

References (39)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013; 63: 11-30.
2. Dubey S, Powell CA. Update in lung cancer 2007. Am J Respir Crit Care Med 2008; 177: 941-946.
3. Molina JR, Yang P, Cassivi SD, et al. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc 2008; 83: 584-594.
4. Chen HY, Yu SL, Chen CH, et al. A five-gene signature and clinical outcome in non-small-cell lung cancer. N Engl J Med 2007; 356: 11-20.
5. Yanagisawa K, Tomida S, Shimada Y, et al. A 25-signal proteomic signature and outcome for patients with resected non-small-cell lung cancer. J Natl Cancer Inst 2007; 99: 858-867.
6. Untergasser G, Koch HB, Menssen A, et al. Characterization of epithelial senescence by serial analysis of gene expression: identification of genes potentially involved in prostate cancer. Cancer Res 2002; 62: 6255-6262.
7. Walter-Yohrling J, Cao X, Callahan M, et al. Identification of genes expressed inmalignant cells that promote invasion. Cancer Res 2003; 63: 8939-8947.
8. Boon K, Osorio EC, Greenhut SF, et al. An anatomy of normal and malignant gene expression. Proc Natl Acad Sci USA 2002; 99: 11287-11292.
9. Kim B, Lee HJ, Choi HY, et al. Clinical validity of the lung cancer biomarkers identified by bioinformatics analysis of public expression data. Cancer Res 2007; 67: 7431-7438.
10. Ossandon FJ, Villarroel C, Aguayo F, et al. In silico analysis of gastric carcinoma serial analysis of gene expression libraries reveals different profiles associated with ethnicity. Mol Cancer 2008; 7: 22-30.
11. Tollefsen DM, Majerus DW, Blank MK. Heparin cofactor II. Purification and properties of a heparin-dependent inhibitor of thrombin in human plasma. J Biol Chem 1982; 257: 2162-2169.
12. Pike RN, Buckle AM, le Bonniec BF, et al. Control of the coagulation system by serpins. Getting by with a little help from glycosaminoglycans. FEBS J 2005; 272: 4842-4851.
13. Tollefsen DM. Heparin cofactor II modulates the response to vascular injury. Arterioscler Thromb Vasc Biol 2007; 27: 454-460.
14. Kamp P, Strathmann A, Ragg H. Heparin cofactor II, antithrombin-β and their complexes with thrombin in human tissues. Thromb Res 2001; 101: 483-491.
15. Hoffman M, Loh KL, Bond VK, et al. Localization of heparin cofactor II in injured human skin: a potential role in wound healing. Exp Mol Pathol 2003; 75: 109-118.
16. Hoffman M, Pratt CW, Brown RL, et al. Heparin cofactor II-proteinase reaction products exhibit neutrophil chemoattractant activity. Blood 1989; 73: 1682-1685.
17. Ikeda Y, Aihara K, Yoshida S, Iwase T, et al. Heparin cofactor II, a serine protease inhibitor, promotes angiogenesis via activation of the AMP-activated protein kinase-endothelial nitric oxide synthase signaling pathway. J Biol Chem 2012; 287: 34256-34263.
18. Tsai MF, Wang CC, Chang GC, et al. A new tumor suppressor DNAJ-like heat shock protein, HLJ1, and survival of patients with non-small-cell lung carcinoma. J Natl Cancer Inst 2006; 98: 825-838.
19. Hsu TH, Liao WY, Yang PC, et al. Dynamics of cancer cell filopodia characterized by super-resolution brightfield optical microscopy. Opt Express 2007; 15: 76-82.
20. Hsu TH, Yen MH, Liao WY, et al. Label-free quantification of asymmetric cancer-cell filopodium activities in amulti-gradient chip. Lab Chip 2009; 9: 884-890.
21. Vignjevic D, Schoumacher M, Gavert N, et al. Fascin, a novel target of β-catenin-TCF signaling, is expressed at the invasive front of human colon cancer. Cancer Res 2007; 67: 6844-6853.
22. Dumstrei K, Mennecke R, Raz E. Signaling pathways controlling primordial germ cell migration in zebrafish. J Cell Sci 2004; 117: 4787-4795.
23. Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 2004; 265: 23-32.
24. O'Keeffe D, Olson ST, Gasiunas N, et al. The heparin binding properties of heparin cofactor II suggest an antithrombin-like activation mechanism. J Biol Chem 2004; 279: 50267-50273.
25. Blinder MA, Tollefsen DM. Site-directed mutagenesis of arginine 103 and lysine 185 in the proposed glycosaminoglycan-binding site of heparin cofactor II. J Biol Chem 1990; 265: 286-291.
26. Machesky LM. Lamellipodia and filopodia in metastasis and invasion. FEBS Lett 2008; 582: 2102-2111.
27. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420: 629-635.
28. Sahai E, Marshall CJ. RHO-GTPases and cancer. Nat Rev Cancer 2002; 2: 133-142.
29. Vega FM, Ridley AJ. Rho GTPases in cancer cell biology. FEBS Lett 2008; 582: 2093-2101.
30. Cain RJ, Ridley AJ. Phosphoinositide 3-kinases in cell migration. Biol Cell 2009; 101: 13-29.
31. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, et al. The emerging mechanisms of isoform-specific PI3K signaling. Nat Rev Mol Cell Biol 2010; 11: 329-341.
32. Kavanaugh WM, Klippel A, Escobedo JA, et al. Modification of the 85-kDa subunit of phosphatidylinositol-3 kinase in platelet-derived growth factor-stimulated cells. Mol Cell Biol 1992; 12: 3415-3424.
33. Cuevas BD, Lu Y, Mao M, et al. Tyrosine phosphorylation of p85 relieves its inhibitory activity on phosphatidylinositol 3-kinase. J Biol Chem 2001; 276: 27455-27461.
34. Lee SY, Meier R, Furuta S, et al. FAM83A confers EGFR-TKI resistance in breast cancer cells and in mice. J Clin Invest 2012; 122: 3211-3220.
35. Skokowa J, Klimiankou M, Klimenkova O, et al. Interactions among HCLS1 HAX1 and LEF-1 proteins are essential for G-CSF-triggered granulopoiesis. Nat Med 2012; 18: 1550-1559.
36. Nürnberg A, Kitzing T, Grosse R. Nucleating actin for invasion. Nat Rev Cancer 2011; 11: 177-187.
37. Borsig L. Antimetastatic activities of heparins andmodified heparins. Experimental evidence. Thromb Res 2010; 125(suppl 2): S66-71.
38. Saxena M, Christofori G. Rebuilding cancer metastasis in the mouse. Mol Oncol 2013; 7: 283-296.
39. van Doormaal FF, Nisio MD, Otten H-M, et al. Randomized trial of the effect of the low molecular weight heparin nadroparin on survival in patients with cancer. J Clin Oncol 2011; 29: 2071-2076.