Focal adhesion kinase protein levels in gut epithelial motility

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 291, Issue 3, 2006, Pages

  Basson, Marc D ^a,b   Sanders, Matthew A ^a   Gomez, Ruben ^a   Hatfield, James ^a   VanderHeide, Richard ^a   Thamilselvan, Vijayalakshmi ^a   Zhang, Jianhu ^a   Walsh, Mary F ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Healing; Migration; Restitution; Ulcer

Indexed keywords

CELL PROTEIN; CYCLOHEXIMIDE; FOCAL ADHESION KINASE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; BIOLOGICAL MODEL; CANCER CELL; CELL MIGRATION; CELL MOTILITY; COLON CANCER; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM; MUCOSAL BLEEDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CACO-2 CELLS; CELL ADHESION; CELL MOVEMENT; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GASTROINTESTINAL MOTILITY; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; RATS;

EID: 33748300743     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00292.2005     Document Type: Article

References (56)

1. Agochiya M, Brunton VG, Owens DW, Parkinson EK, Paraskeva C, Keith WN, and Frame MC. Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene 18: 5646-5653, 1999.
2. Basson MD, Modlin IM, and Madri JA. Human enterocyte (Caco-2) migration is modulated in vitro by extracellular matrix composition and epidermal growth factor. J Clin Invest 90: 15-23, 1992.
3. Cao Y, Baig MR, Hamm LL, Wu K, and Simon EE. Growth factors stimulate kidney proximal tubule cell migration independent of augmented tyrosine phosphorylation of focal adhesion kinase. Biochem Biophys Res Commun 328: 560-566, 2005.
4. Gatti A. Nerve growth factor (NGF) induces a rapid and sustained downregulation of the focal adhesion kinase (FAK). Cell Mol Neurobiol 24: 461-475, 2004.
5. Gilmore AP and Romer LH. Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol Biol Cell 7: 1209-1224, 1996.
6. Golubovskaya V, Finch R, and Cance WG. Direct interaction of the N-terminal domain of focal adhesion kinase with the N-terminal transactivation domain of p53. J Biol Chem 280: 25008-25021, 2005.
7. Han EK, McGonigal T, Wang J, Giranda VL, and Luo Y. Functional analysis of focal adhesion kinase (FAK) reduction by small inhibitory RNAs. Anticancer Res 24: 3899-3905, 2004.
8. Hauck CR, Sieg DJ, Hsia DA, Loftus JC, Gaarde WA, Monia BP, and Schlaepfer DD. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res 61: 7079-7090, 2001.
9. Hsia DA, Mitra SK, Hauck CR, Streblow DN, Nelson JA, Ilic D, Huang S, Li E, Nemerow GR, Leng J, Spencer KS, Cheresh DA, and Schlaepfer DD. Differential regulation of cell motility and invasion by FAK. J Cell Biol 160: 753-767, 2003.
10. Hunger-Glaser I, Fan RS, Perez-Salazar E, and Rozengurt E. PDGF and FGF induce focal adhesion kinase (FAK) phosphorylation at Ser-910: dissociation from Tyr-397 phosphorylation and requirement for ERK activation. J Cell Physiol 200: 213-222, 2004.
11. Iliâc D, Genbacev O, Jin F, Caceres E, Almeida EA, Bellingard-Dubouchaud V, Schaefer EM, Damsky CH, and Fisher SJ. Plasma membrane-associated pY397FAK is a marker of cytotrophoblast invasion in vivo and in vitro. Am J Pathol 159: 93-108, 2001.
12. Ilic D, Kovacic B, Johkura K, Schlaepfer DD, Tomasevic N, Han Q, Kim JB, Howerton K, Baumbusch C, Ogiwara N, Streblow DN, Nelson JA, Dazin P, Shino Y, Sasaki K, and Damsky CH. FAK promotes organization of fibronectin matrix and fibrillar adhesions. J Cell Sci 117: 177-187, 2004.
13. Jones G, Machado J, and Merlo A. Loss of focal adhesion kinase (FAK) inhibits epidermal growth factor receptor-dependent migration and induces aggregation of NH2-terminal FAK in the nuclei of apoptotic glioblastoma cells. Cancer Res 61: 4978-4981, 2001.
14. Jones G and Stewart G. Nuclear import of N-terminal FAK by activation of the FcepsilonR1 receptor in RBL-2H3 cells. Biochem Biophys Res Commun 314: 39-45, 2004.
15. Jones MK, Tomikawa M, Mohajer B, and Tarnawski AS. Gastrointestinal mucosal regeneration: role of growth factors. Front Biosci 4: D303-309, 1999.
16. Konturek PC, Konturek SJ, Brzozowski T, and Ernst H. Epidermal growth factor and transforming growth factor-alpha: role in protection and healing of gastric mucosal lesions. Eur J Gastroenterol Hepatol 7: 933-937, 1995.
17. Lark AL, Livasy CA, Calvo B, Caskey L, Moore DT, Yang X, and Cance WG. Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time PCR analyses. Clin Cancer Res 9: 215-222, 2003.
18. Levy P, Robin H, Kornprobst M, Capeau J, and Cherqui G. Enterocytic differentiation of the human Caco-2 cell line correlates with alterations in integrin signaling. J Cell Physiol 177: 618-627, 1998.
19. Lim Y, Han I, Jeon J, Park H, Bahk YY, and Oh ES. Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J Biol Chem 279: 29060-29065, 2004.
20. Liu YW, Sanders MA, and Basson MD. Human Caco-2 intestinal epithelial motility is associated with tyrosine kinase and cytoskeletal focal adhesion kinase signals. J Surg Res 77: 112-118, 1998.
21. Liu YW, Sanders MA, and Basson MD. Loss of matrix-dependent cytoskeletal tyrosine kinase signals may regulate intestinal epithelial differentiation during mucosal healing. J Gastrointest Surg 3: 82-94, 1999.
22. Lobo M and Zachary I. Nuclear localization and apoptotic regulation of an amino-terminal domain focal adhesion kinase fragment in endothelial cells. Biochem Biophys Res Commun 276: 1068-1073, 2000.
23. Ma A, Richardson A, Schaefer EM, and Parsons JT. Serine phosphorylation of focal adhesion kinase in interphase and mitosis: a possible role in modulating binding to p130(Cas). Mol Biol Cell 12: 1-12, 2001.
24. Martin W and Koonin EV. Introns and the origin of the nucleus-cytosol compartmentalization. Nature 440: 41-45, 2006.
25. Matkowskyj KA, Keller K, Glover S, Kornberg L, Tran-Son-Tay R, and Benya RV Expression of GRP and its receptor in well-differentiated colon cancer cells correlates with the presence of focal adhesion kinase phosphorylated at tyrosines 397 and 407. J Histochem Cytochem 51: 1041-1048, 2003.
26. Milani S and Calabro A. Role of growth factors and their receptors in gastric ulcer healing. Microsc Res Tech 53: 360-371, 2001.
27. Moissoglu K and Gelman IH. v-Src rescues actin-based cytoskeletal architecture and cell motility and induces enhanced anchorage independence during oncogenic transformation of focal adhesion kinase-null fibroblasts. J Biol Chem 278: 47946-47959, 2003.
28. Owen JD, Ruest PJ, Fry DW, and Hanks SK. Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol Cell Biol 19: 4806-4818, 1999.
29. Peterson MD, Bement WM, and Mooseker MS. An in vitro model for the analysis of intestinal brush border assembly. II. Changes in expression and localization of brush border proteins during cell contact-induced brush border assembly in Caco-2BBe cells. J Cell Sci 105: 461-472, 1993.
30. Peterson MD and Mooseker MS. An in vitro model for the analysis of intestinal brush border assembly. I. Ultrastructural analysis of cell contact-induced brush border assembly in Caco-2BBe cells. J Cell Sci 105: 445-460, 1993.
31. Polk DB and Tong W. Epidermal and hepatocyte growth factors stimulate chemotaxis in an intestinal epithelial cell line. Am J Physiol Cell Physiol 277: C1149-C1159, 1999.
32. Rankin S and Rozengurt E. Platelet-derived growth factor modulation of focal adhesion kinase (p125FAK) and paxillin tyrosine phosphorylation in Swiss 3T3 cells. Bell-shaped dose response and cross-talk with bombesin. J Biol Chem 269: 704-710, 1994.
33. Renshaw MW, Price LS, and Schwartz MA. Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J Cell Biol 147: 611-618, 1999.
34. Rhoads JM, Chen W, Gookin J, Wu GY, Fu Q, Blikslager AT, Rippe RA, Argenzio RA, Cance WG, Weaver EM, and Romer LH. Arginine stimulates intestinal cell migration through a focal adhesion kinase dependent mechanism. Gut 53: 514-522, 2004.
35. Salazar EP and Rozengurt E. Bombesin and platelet-derived growth factor induce association of endogenous focal adhesion kinase with Src in intact Swiss 3T3 cells. J Biol Chem 274: 28371-28378, 1999.
36. Schlaepfer DD, Hauck CR, and Sieg DJ. Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478, 1999.
37. Schlaepfer DD, Mitra SK, and Ilic D. Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta 1692: 77-102, 2004.
38. Schneider GB, Kurago Z, Zaharias R, Gruman LM, Schaller MD, and Hendrix MJ. Elevated focal adhesion kinase expression facilitates oral tumor cell invasion. Cancer 95: 2508-2515, 2002.
39. Seufferlein T, Withers DJ, Mann D, and Rozengurt E. Dissociation of mitogen-activated protein kinase activation from p125 focal adhesion kinase tyrosine phosphorylation in Swiss 3T3 cells stimulated by bombesin, lysophosphatidic acid, and platelet-derived growth factor. Mol Biol Cell 7: 1865-1875, 1996.
40. Stewart A, Ham C, and Zachary I. The focal adhesion kinase aminoterminal domain localises to nuclei and intercellular junctions in HEK293 and MDCK cells independently of tyrosine 397 and the carboxy-terminal domain. Biochem Biophys Res Commun 299: 62-66, 2002.
41. Szabo IL, Pai R, Jones MK, Ehring GR, Kawanaka H, and Tarnawski AS. Indomethacin delays gastric restitution: association with the inhibition of focal adhesion kinase and tensin phosphorylation and reduced actin stress fibers. Exp Biol Med (Maywood) 227: 412-424, 2002.
42. Tangkijvanich P, Melton AC, Chitapanarux T, Han J, and Yee HF. Platelet-derived growth factor-BB and lysophosphatidic acid distinctly regulate hepatic myofibroblast migration through focal adhesion kinase. Exp Cell Res 281: 140-147, 2002.
43. Tarnawski A, Szabo IL, Husain SS, and Soreghan B. Regeneration of gastric mucosa during ulcer healing is triggered by growth factors and signal transduction pathways. J Physiol 95: 337-344, 2001.
44. Tarnawski AS and Jones MK. The role of epidermal growth factor (EGF) and its receptor in mucosal protection, adaptation to injury, and ulcer healing: involvement of EGF-R signal transduction pathways. J Clin Gastroenterol 27, Suppl 1: S12-S20, 1998.
45. Thamiselvan V and Basson MD. Pressure activates colon cancer cell adhesion by inside-out focal adhesion complex and cytoskeletal signaling. Gastroenterology 126: 8-18, 2004.
46. Tremblay L, Hauck W, Nguyen LT, Allard P, Landry F, Chapdelaine A, and Chevalier S. Regulation and activation of focal adhesion kinase and paxillin during the adhesion, proliferation, and differentiation of prostatic epithelial cells in vitro and in vivo. Mol Endocrinol 10: 1010-1020, 1996.
47. Westhoff MA, Serrels B, Fincham VJ, Frame MC, and Carragher NO. SRC-mediated phosphorylation of focal adhesion kinase couples actin and adhesion dynamics to survival signaling. Mol Cell Biol 24: 8113-8133, 2004.
48. Whitney GS, Chan PY, Blake J, Cosand WL, Neubauer MG, Aruffo A, and Kanner SB. Human T and B lymphocytes express a structurally conserved focal adhesion kinase, pp125FAK. DNA Cell Biol 12: 823-830, 1993.
49. Withers BE, Hanks SK, and Fry DW. Correlations between the expression, phosphotyrosine content and enzymatic activity of focal adhesion kinase, pp125FAK, in tumor and nontransformed cells. Cancer Biochem Biophys 15: 127-139, 1996.
50. Wozniak MA, Modzelewska K, Kwong L, and Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692: 103-119, 2004.
51. 2+, PKC, and Rho kinase. Am J Physiol Cell Physiol 282: C1432-C1444, 2002.
52. Yano H, Mazaki Y, Kurokawa K, Hanks SK, Matsuda M, and Sabe H. Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J Cell Biol 166: 283-295, 2004.
53. Yi X, Wang X, Gerdes AM, and Li F. Subcellular distribution of focal adhesion kinase and its related nonkinase in hypertrophic myocardium. Hypertension 41: 1317-1323, 2003.
54. Yu CF and Basson MD. Matrix-specific FAK and MAPK reorganization during Caco-2 cell motility. Microsc Res Tech 51: 191-203, 2000.
55. Yu CF, Sanders MA, and Basson MD. Human caco-2 motility redistributes FAK and paxillin and activates p38 MAPK in a matrix-dependent manner. Am J Physiol Gastrointest Liver Physiol 278: G952-G966, 2000.
56. Zachary I. Focal adhesion kinase. Int J Biochem Cell Biol 29: 929-934, 1997.