Focal adhesion assembly in myofibroblasts fosters a microenvironment that promotes tumor growth

American Journal of Pathology

Volumn 177, Issue 4, 2010, Pages 1888-1900

  Kang, Ningling ^a   Yaqoob, Usman ^a   Geng, Zhimin ^a   Bloch, Kenneth ^c   Liu, Chunsheng ^a   Gomez, Timothy ^b   Billadeau, Daniel ^b   Shah, Vijay ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAC1 PROTEIN; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL SPREADING; CELL TRANSFORMATION; CONTROLLED STUDY; FOCAL ADHESION; HUMAN; HUMAN CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL; TUMOR; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

EID: 77957356733     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100187     Document Type: Article

References (55)

1. Kalluri R, Zeisberg M: Fibroblasts in cancer. Nat Rev Cancer 2006, 6:392-401
2. Mitra SK, Hanson DA, Schlaepfer DD: Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005, 6:56-68
3. Wehrle-Haller B, Imhof B: The inner lives of focal adhesions. Trends Cell Biol 2002, 12:382-389
4. Kwiatkowski AV, Gertler FB, Loureiro JJ: Function and regulation of Ena/VASP proteins. Trends Cell Biol 2003, 13:386-392
5. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB: Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 2003, 19:541-564
6. Smolenski A, Poller W, Walter U, Lohmann SM: Regulation of human endothelial cell focal adhesion sites and migration by cGMP-dependent protein kinase I. J Biol Chem 2000, 275:25723-25732
7. Galler AB, Garcia Arguinzonis MI, Baumgartner W, Kuhn M, Smolenski A, Simm A, Reinhard M: VASP-dependent regulation of actin cytoskeleton rigidity, cell adhesion, and detachment. Histochem Cell Biol 2006, 125:457-474
8. Schlegel N, Waschke J: Impaired integrin-mediated adhesion contributes to reduced barrier properties in VASP-deficient microvascular endothelium. J Cell Physiol 2009, 220:357-366
9. Xu L, Hui A, Albanis E, Arther M, O'Byrne S, Blaner W, Mukherjee P, Friedman S, Eng F: Human hepatic stellate cell lines. LX-1 and LX-2: new tools for analysis of hepatic fibrosis, Gut 2005, 54:142-151
10. Decker NK, Abdelmoneim SS, Yaqoob U, Hendrickson H, Hormes J, Bentley M, Pitot H, Urrutia R, Gores GJ, Shah VH: Nitric oxide regulates tumor cell cross-talk with stromal cells in the tumor microenvironment of the liver. Am J Pathol 2008, 173:1002-1012
11. Kang-Decker NCS, Chatterjee S, Yao J, Egan J, Semela D, Mukhopadhyay D, Shah V: Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2. J Cell Sci 2007, 120:492-501
12. de la Taille A, Katz AE, Bagiella E, Buttyan R, Sharir S, Olsson CA, Burchardt T, Ennis RD, Rubin MA: Microvessel density as a predictor of PSA recurrence after radical prostatectomy. A comparison of CD34 and CD31, Am J Clin Pathol 2000, 113:555-562
13. Das A, Yaqoob U, Mehta D, Shah VH: FXR Promotes Endothelial Cell Motility Through Coordinated Regulation of FAK and MMP-9. Arterioscler Thromb Vasc Biol 2009, 29:562-570
14. Huttelmaier S, Mayboroda O, Harbeck B, Jarchau T, Jockusch BM, Rudiger M: The interaction of the cell-contact proteins VASP and vinculin is regulated by phosphatidylinositol-4,5-bisphosphate. Curr Biol 1998, 8:479-488
15. Lee J, Decker N, Chatterjee S, Yao J, Friedman S, Shah V: Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am J Pathol 2005, 166:1861-1870
16. Semela D, Das A, Langer DA, Kang N, Leof E, Shah VH: Platelet-derived growth factor signaling through ephrin-B2 regulates hepatic vascular structure and function Gastroenterology 2008, 135:671-679
17. Knox P: Kinetics of cell spreading in the presence of different concentrations of serum or fibronectin-depleted serum. J Cell Sci 1984, 71:51-59
18. Runyan RB, Versalovic J, Shur BD: Functionally distinct laminin receptors mediate cell adhesion and spreading: the requirement for surface galactosyltransferase in cell spreading. J Cell Biol 1988, 107:1863-1871
19. Cao S, Yao Y, McCabe T, Yao Q, Katusic Z, Sessa W, Shah V: Direct interaction between eNOS and dynamin-2:Implications for NOS function. J Biol Chem 2001, 276:14249-14256
20. Hautekeete ML, Geerts A: The hepatic stellate (Ito) cell: its role in human liver disease. Virchows Arch 1997, 430:195-207
21. Friedman SL: Mechanisms of disease: mechanisms of hepatic fibrosis and therapeutic implications. Nat Clin Pract Gastroenterol Hepatol 2004, 1:98-105
22. Olaso E, Salado C, Egilegor E, Gutierrez V, Santisteban A, Sancho-Bru P, Friedman S, Vidal-Vanaclocha F: Proangiogenic role of tumor-activated hepatic stellate cells in experimental melanoma metastasis. Hepatology 2003, 37:674-685
23. Kaimori A, Potter J, Kaimori JY, Wang C, Mezey E, Koteish A: Transforming growth factor-beta1 induces an epithelial-to-mesenchymal transition state in mouse hepatocytes in vitro. J Biol Chem 2007, 282:22089-22101
24. Reinhard M, Rudiger M, Jockusch BM, Walter U: VASP interaction with vinculin: a recurring theme of interactions with proline-rich motifs. FEBS Lett 1996, 399:103-107
25. Bear JE, Loureiro JJ, Libova I, Fassler R, Wehland J, Gertler FB: Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 2000, 101:717-728
26. Hoffman LM, Jensen CC, Kloeker S, Wang CL, Yoshigi M, Beckerle MC: Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling. J Cell Biol 2006, 172:771-782
27. Lynch PM, Schmid-Schonbein GW: Literature watch. Parker LH, Schmidt M, Jin S-W, Gray AM, Beis D, Pham T, Frantz G, Paliert S, Hillan K, Stainier DYR, de Sauvage FJ, Ye W: The endothelial-cell-derived secreted factor Egf17 regulates vascular tube formation. Nature 2004; 428:754-758.
28. Lymphat Res Biol 2004, 2:96-100
29. Niebuhr K, Ebel F, Frank R, Reinhard M, Domann E, Carl UD, Walter U, Gertler FB, Wehland J, Chakraborty T: A novel proline-rich motif present in ActA of Listeria monocytogenes and cytoskeletal proteins is the ligand for the EVH1 domain, a protein module present in the Ena/VASP family. EMBO J 1997, 16:5433-5444
30. Gertler FB, Niebuhr K, Reinhard M, Wehland J, Soriano P: Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 1996, 87:227-239
31. Reinhard M, Giehl K, Abel K, Haffner C, Jarchau T, Hoppe V, Jockusch BM, Walter U: The proline-rich focal adhesion and microfilament protein VASP is a ligand for profilins. EMBO J 1995, 14:1583-1589
32. Bachmann C, Fischer L, Walter U, Reinhard M: The EVH2 domain of the vasodilator-stimulated phosphoprotein mediates tetramerization. F-actin binding, and actin bundle formation, J Biol Chem 1999, 274:23549-23557
33. Grosse R, Copeland JW, Newsome TP, Way M, Treisman R: A role for VASP in RhoA-Diaphanous signalling to actin dynamics and SRF activity. EMBO J 2003, 22:3050-3061
34. Haffner C, Jarchau T, Reinhard M, Hoppe J, Lohmann SM, Walter U: Molecular cloning, structural analysis and functional expression of the proline-rich focal adhesion and microfilament-associated protein VASP. EMBO J 1995, 14:19-27
35. Brindle NP, Holt MR, Davies JE, Price CJ, Critchley DR: The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin, Biochem J 1996, 318:753-757
36. Schlegel N, Burger S, Golenhofen N, Walter U, Drenckhahn D, Waschke J: The role of VASP in regulation of cAMP- and Rac 1-mediated endothelial barrier stabilization. Am J Physiol Cell Physiol 2008, 294:C178-C188
37. Schlegel N, Waschke J: VASP is involved in cAMP-mediated Rac 1 activation in microvascular endothelial cells. Am J Physiol Cell Physiol 2009, 296:C453-C462
38. 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, 281:18652-18659
39. Abramsson A, Lindblom P, Betsholtz C: Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest 2003, 112:1142-1151
40. Abramsson A, Berlin O, Papayan H, Paulin D, Shani M, Betsholtz C: Analysis of mural cell recruitment to tumor vessels. Circulation 2002, 105:112-117
41. Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, Parker NR, Toi CS, Pirola RC, Wilson JS, Goldstein D, Apte MV: Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res 2008, 68:2085-2093
42. Philippar U, Roussos ET, Oser M, Yamaguchi H, Kim HD, Giampieri S, Wang Y, Goswami S, Wyckoff JB, Lauffenburger DA, Sahai E, Condeelis JS, Gertler FB: A Mena invasion isoform potentiates EGF-induced carcinoma cell invasion and metastasis. Dev Cell 2008, 15:813-828
43. Han G, Fan B, Zhang Y, Zhou X, Wang Y, Dong H, Wei Y, Sun S, Hu M, Zhang J, Wei L: Positive regulation of migration and invasion by vasodilator- stimulated phosphoprotein via Rac1 pathway in human breast cancer cells. Oncol Rep 2008, 20:929-939
44. Hu LD, Zou HF, Zhan SX, Cao KM: EVL (Ena/VASP-like) expression is up-regulated in human breast cancer and its relative expression level is correlated with clinical stages. Oncol Rep 2008, 19:1015-1020
45. Toyoda A, Kawana H, Azuhata K, Yu J, Omata A, Kishi H, Higashi M, Harigaya K: Aberrant expression of human ortholog of mammalian enabled (hMena) in human colorectal carcinomas: implications for its role in tumor progression. Int J Oncol 2009, 34:53-60
46. Theret N, Musso O, Turlin B, Lotrian D, Bioulac-Sage P, Campion JP, Boudjema K, Clement B: Increased extracellular matrix remodeling is associated with tumor progression in human hepatocellular carcinomas. Hepatology 2001, 34:82-88
47. Vidal-Vanaclocha F: The prometastatic microenvironment of the liver. Cancer Microenviron 2008, 1:113-129
48. Antoine M, Tag CG, Gressner AM, Hellerbrand C, Kiefer P: Expression of E-selectin ligand-1 (CFR/ESL-1) on hepatic stellate cells: implications for leukocyte extravasation and liver metastasis. Oncol Rep 2009, 21:357-362
49. Amann T, Bataille F, Spruss T, Muhlbauer M, Gabele E, Scholmerich J, Kiefer P, Bosserhoff AK, Hellerbrand C: Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Cancer Sci 2009, 100:646-653
50. Matsusue R, Kubo H, Hisamori S, Okoshi K, Takagi H, Hida K, Nakano K, Itami A, Kawada K, Nagayama S, Sakai Y: Hepatic stellate cells promote liver metastasis of colon cancer cells by the action of SDF-1/CXCR4 axis. Ann Surg Oncol 2009, 16:2645-2653
51. Cukierman E, Pankov R, Stevens DR, Yamada KM: Taking cell-matrix adhesions to the third dimension. Science 2001, 294:1708-1712
52. Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ: ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 2003, 163:583-595
53. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ: Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 2009, 28:4326-4343
54. Kwiatkowski AV, Rubinson DA, Dent EW, Edward van Veen J, Leslie JD, Zhang J, Mebane LM, Philippar U, Pinheiro EM, Burds AA, Bronson RT, Mori S, Fassler R, Gertler FB: Ena/VASP Is Required for neuritogenesis in the developing cortex. Neuron 2007, 56:441-455
55. Higashi M, Ishikawa C, Yu J, Toyoda A, Kawana H, Kurokawa K, Matsuda M, Kitagawa M, Harigaya K: Human Mena associates with Rac1 small GTPase in glioblastoma cell lines. PLoS One 2009, 4:e4765