Heparanase-induced GEF-H1 signaling regulates the cytoskeletal dynamics of brain metastatic breast cancer cells

Molecular Cancer Research

Volumn 10, Issue 6, 2012, Pages 689-702

  Ridgway, Lon D ^a   Wetzel, Michael D ^a   Ngo, Jason A ^a   Erdreich Epstein, Anat ^b   Marchetti, Dario ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HEPARANASE; PROTEIN KINASE C ALPHA; PROTEOHEPARAN SULFATE; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR H1; SYNDECAN 4; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN METASTASIS; BREAST CANCER; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; DOWNSTREAM PROCESSING; HUMAN; HUMAN CELL; HYPOTHESIS; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPINDLE CELL; TUMOR CELL; VASCULAR ENDOTHELIUM;

ANTIGENS, CD29; BLOTTING, WESTERN; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; CYTOSKELETON; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONIDASE; GTP PHOSPHOHYDROLASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SYNDECAN-4; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84862518274     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0534     Document Type: Article

References (51)

1. Gavrilovic IT, Posner JB. Brain metastases: epidemiology and pathophysiology. J Neurooncol 2005;75:5-14. (Pubitemid 41548673)
2. Steeg PS, Camphausen KA, Smith QR. Brain metastases as preventive and therapeutic targets. Nat Rev Cancer 2011;11:352-63.
3. Eichler AF, Chung E, Kodack DP, Loeffler JS, Fukumura D, Jain RK. The biology of brain metastases-translation to new therapies. Nat Rev Clin Oncol 2011;8:344-56.
4. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, et al. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Ann Rev Cell Biol 1992;8:365-93. (Pubitemid 23001002)
5. Iozzo RV. Heparan sulfate proteoglycans: intricate molecules with intriguing functions. J Clin Invest 2001;108:165-7. (Pubitemid 32656237)
6. O'Connell MP, Fiori JL, Kershner EK, Frank BP, Indig FE, Taub DD, et al. Heparan sulfate proteoglycan modulation of Wnt5A signal transduction in metastatic melanoma cells. J Biol Chem 2009;284:28704-12.
7. Sanderson RD, Yang Y. Syndecan-1: a dynamic regulator of the myeloma microenvironment. Clin Exp Metastasis 2008;25:149-59.
8. Reiland J, Kempf D, Roy M, Denkins Y, Marchetti D. FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells. Neoplasia 2006;8:596-606. (Pubitemid 44061315)
9. Ilan N, Elkin M, Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol 2006;38:2018-39. (Pubitemid 44397619)
10. Vreys V, David G. Mammalian heparanase: what is the message? J Cell Mol Med 2007;11:427-52. (Pubitemid 47153456)
11. Ridgway LD, Wetzel MD, Marchetti D. Modulation of GEF-H1 induced signaling by heparanase in brain metastatic melanoma cells. J Cell Biochem 2010;111:1299-309.
12. Zetser A, Bashenko Y, Miao HQ, Vlodavsky I, Ilan N. Heparanase affects adhesive and tumorigenic potential of human glioma cells. Cancer Res 2003;63:7733-41. (Pubitemid 37466704)
13. Cohen-Kaplan V, Doweck I, Naroditsky I, Vlodavsky I, Ilan N. Heparanase augments epidermal growth factor receptor phosphorylation: correlation with head and neck tumor progression. Cancer Res 2008;68:10077-85.
14. Zhang L, Sullivan PS, Goodman JC, Gunaratne PH, Marchetti D. MicroRNA-1258 suppresses breast cancer brain metastasis by targeting heparanase. Cancer Res 2011;71:645-54.
15. Nalbant P, Chang YC, Birkenfeld J, Chang ZF, Bokoch GM. Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol Biol Cell 2009;20: 4070-82.
16. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992;70:389-99.
17. Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, et al. Rac activation and inactivation control plasticity of tumor cell movement. Cell 2008;135:510-23.
18. Sanz-Moreno V, Marshall CJ. Rho-GTPase signaling drives melanoma cell plasticity. Cell Cycle 2009;8:1484-7.
19. Symons M, Segall JE. Rac and Rho driving tumor invasion: who's at the wheel? Genome Biol 2009;10:213.
20. Heasman SJ, Carlin LM, Cox S, Ng T, Ridley AJ. Coordinated RhoA signaling at the leading edge and uropod is required for T cell transendothelial migration. J Cell Biol 2010;190:553-63.
21. Birkenfeld J, Nalbant P, Yoon SH, Bokoch GM. Cellular functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered GEF-H1 activity a crucial determinant of disease pathogenesis? Trends Cell Biol 2008;18:210-9.
22. Lorger M, Felding-Habermann B. Capturing changes in the brain micro-environment during initial steps of breast cancer brain metastasis. Am J Pathol 2010;176:2958-71.
23. Zhang L, Sullivan P, Suyama J, Marchetti D. Epidermal growth factor-induced heparanase nucleolar localization augments DNA topoisomerase I activity in brain metastatic breast cancer. Mol Cancer Res 2010;8:278-90.
24. Xu J, Millard M, Ren X, Cox OT, Erdreich-Epstein A. C-Abl mediates endothelial apoptosis induced by inhibition of integrins alphavbeta3 and alphavbeta5 and by disruption of actin. Blood 2010;115: 2709-18.
25. Stins MF, Shen Y, Huang SH, Gilles F, Kalra VK, Kim KS. Gp120 activates children's brain endothelial cells via CD4. J Neurovirol 2001;7:125-34. (Pubitemid 32685246)
26. Ridgway LD, Kim EY, Dryer SE. MAGI-1 interacts with Slo1 channel proteins and suppresses Slo1 expression on the cell surface. Am J Physiol Cell Physiol 2009;297:C55-65.
27. Eugenin EA, Berman JW. Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 2003;29:351-61. (Pubitemid 36513434)
28. Roy M, Reiland J, Murry BP, Chouljenko V, Kousoulas KG, Marchetti D. Antisense-mediated suppression of heparanase gene inhibits melanoma cell invasion. Neoplasia 2005;7:253-62. (Pubitemid 40411637)
29. Naggi A, Casu B, Perez M, Torri G, Cassinelli G, Penco S, et al. Modulation of the heparanase-inhibiting activity of heparin through selective desulfation, graded N-acetylation, and gycol splitting. J Biol Chem 2005;280:12103-13.
30. Ritchie JP, Ramani VC, Ren Y, Naggi A, Torri G, Casu B, et al. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clin Cancer Res 2001;17:1382-93.
31. Minard ME, Kim LS, Price JE, Gallick GE. The role of the guanine nucleotide exchange factor Tiam1 in cellular migration, invasion, adhesion and tumor progression. Breast Cancer Res Treat 2004;84: 21-32. (Pubitemid 38388857)
32. Batzer AG, Rotin D, Urena JM, Skolnik EY, Schlessinger J. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol Cell Biol 1994;14:5192-201.
33. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW. Ligand binding to integrins. J Biol Chem 2000;275:21785-8. (Pubitemid 30621742)
34. Guo F, Debidda M, Yang L, Williams DA, Zheng Y. Genetic deletion of Rac1 GTPase reveals its critical role in actin stress fiber formation and focal adhesion complex assembly. J Biol Chem 2006;281:18652-9. (Pubitemid 44035525)
35. Burbach BJ, Friedl A, Mundhenke C, Rapraeger AC. Syndecan-1 accumulates in lysosomes of poorly differentiated breast carcinoma cells. Matrix Biol 2003;22:163-77. (Pubitemid 36627474)
36. Dokmanovic M, Hirsch DS, Shen Y, Wu WJ. Rac1 contributes to trastuzumab resistance of breast cancer cells: Rac1 as a potential therapeutic target for the treatment of trastuzumab-resistant breast cancer. Mol Cancer Ther 2009;8:1557-69.
37. Birkenfeld J, Nalbant P, Bohl BP, Pertz O, Hahn KM, Bokoch GM. GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev Cell 2007;12:699-712. (Pubitemid 46671149)
38. Ren Y, Li R, Zheng Y, Busch H. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J Biol Chem 1998;273:34954-60. (Pubitemid 29028193)
39. Guilluy C, Swaminathan V, Garcia-Mata R, O'Brien ET, Superfine R, Burridge K. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 2011;13:722-7.
40. Levy-Adam F, Feld S, Suss-Toby E, Vlodavsky I, Ilan N. Heparanase facilitates cell adhesion and spreading by clustering of cell surface heparan sulfate proteoglycans. PLoS One 2008;3:e2319.
41. Palmieri D, Bronder JL, Herring JM, Yoneda T, Weil RJ, Stark AM, et al. Her-2 overexpression increases the metastatic outgrowth of breast cancer cells in the brain. Cancer Res 2007;67:4190-8. (Pubitemid 46815065)
42. Schwartz BR, Wayner EA, Carlos TM, Ochs HD, Harlan JM. Identification of surface proteins mediating adherence of CD11/CD18-deficient lymphoblastoid cells to cultured human endothelium. J Clin Invest 1990;85:2019-22. (Pubitemid 20192982)
43. Haataja L, Groffen J, Heisterkamp N. Characterization of RAC3, a novel member of the Rho family. J Biol Chem 1997;272:20384-8. (Pubitemid 27355588)
44. Mira JP, Benard V, Groffen J, Sanders LC, Knaus UG. Endogenous, hyperactive Rac3 controls proliferation of breast cancer cells by a p21-activated kinase-dependent pathway. Proc Natl Acad Sci U S A 2000;97:185-9. (Pubitemid 30055805)
45. Lim ST, Longley RL, Couchman JR, Woods A. Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha. J Biol Chem 2003;278:13795-802. (Pubitemid 36799917)
46. Dovas A, Yoneda A, Couchman JR. PKCbeta-dependent activation of RhoA by syndecan-4 during focal adhesion formation. J Cell Sci 2006;119:2837-46. (Pubitemid 44184020)
47. Beauvais DM, Rapraeger AC. Syndecans in tumor cell adhesion and signaling. Reprod Biol Endocrinol 2004;2:3.
48. Oh ES, Woods A, Couchman JR. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem 1997;272:8133-6. (Pubitemid 27147760)
49. Horowitz A, Simons M. Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Calpha. J Biol Chem 1998;273:25548-51. (Pubitemid 28475771)
50. Horowitz A, Simons M. Regulation of syndecan-4 phosphorylation in vivo. J Biol Chem 1998;273:10914-8. (Pubitemid 28204929)
51. Ridgway LD, Wetzel MD, Marchetti D. Heparanase modulates Shh and Wnt3a signaling in human medulloblastoma cells. Exp Ther Med 2011;2:229-38.