Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading

Molecular Biology of the Cell

Volumn 9, Issue 8, 1998, Pages 2287-2303

  Tominaga, Tomoko ^a   Barber, Diane L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; GROWTH FACTOR; GUANOSINE TRIPHOSPHATASE; INTEGRIN; INTEGRIN RECEPTOR; PAXILLIN; PLATELET DERIVED GROWTH FACTOR; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL PH; CELL SPREADING; CELL VOLUME; ENZYME INACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTON SODIUM EXCHANGE; SIGNAL TRANSDUCTION;

EID: 0031878095     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.8.2287     Document Type: Article

References (68)

1. An, X.L., Takauwa, Y., Nunomura, W., Manno, S., and Mohandas, N. (1996). Modulation of band 3-ankyrin interaction by protein 4.1. Functional implications in regulation of erythrocyte membrane mechanical properties. J. Biol. Chem. 271, 33187-33191.
2. Barry, S.T., Flinn, H.M., Humphries, M.J., Critchley, D.R., and Ridley, A.J. (1997). Requirement for Rho in integrin signalling. Cell Adhes. Commun. 4, 387-398.
3. Bendori, R., Salomon, D., and Geiger, B. (1987). Contact-dependent regulation of vinculin expression in cultured fibroblasts: a study with vinculin-specific cDNA probes. EMBO J. 6, 2897-2905.
4. Brown, P.J., and Juliano, R.L. (1985). Selective inhibition of fibronectin-mediated cell adhesion by monoclonal antibodies to a cell-surface glycoprotein. Science 228, 1448-1451.
5. Brown, P.J., and Juliano, R.L. (1988). Monoclonal antibodies to distinctive epitopes on the α and β subunits of the fibronectin receptor. Exp. Cell Res. 177, 303-318.
6. Burridge, K., and Chrzanowska-Wodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518.
7. Burridge, K., Turner, C.E., and Romer, L.H. (1992). Tyrosine phosphorylation of paxillin and Pp 125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
8. Chen, Q., Kinch, M.S., Lin, T.H., Burridge, K., and Juliano, R.L. (1994). Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J. Biol. Chem. 269, 26602-26605.
9. Chihara, K., Amano, M., Nakamura, N., Yano, T., Shibata, M., Tokui, T., Ichikawa, H., Ikebe, R., and Kaibuchi, K. (1997). Cytoskeletal rearrangements and transcriptional activation of c-fos serum response element by rho-kinase. J. Biol. Chem. 272, 25121-25127.
10. Chong, L.D., Traynor-Kaplan, A., Bokoch, G.M., and Schwartz, M.A. (1994). The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79, 507-513.
11. Chrzanowska-Wodnicka, M., and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
12. Clark, E.A., and Brugge, J.S. (1995). Integrins and signal transduction pathways: the road taken. Science 268, 233-239.
13. Coll, J.L., Ben-Ze'ev, A., Ezzell, R.M., Rodriguez Fernandez, J.L., Baribault, H., Oshima, R.G., and Adamson, E.D. (1995). Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion. Proc. Natl. Acad. Sci. USA 92, 9161-9165.
14. Craig, S.W., and Johnson, R.P. (1996). Assembly of focal adhesions: progress, paradigms, and portents. Curr. Opin. Cell Biol. 8, 74-85.
15. Demaurex, N., Downey, G.P., Waddell, T.K., and Grinstein, S. (1996). Intracellular pH regulation during spreading of human neutrophils. J. Cell Biol. 133, 1391-1402.
16. Ding, Y., Kobayashi, S., and Kopito, R. (1996). Mapping of ankyrin binding determinations on the erythroid anion exchanger, AE1. J. Biol. Chem. 271, 22494-22498.
17. Gillies, R.J., Martinez-Zaguilan, R., Martinez, G.M., Serrano, R., and Perona, R. (1990). Tumorigenic 3T3 cells maintain an alkaline intracellular pH under physiological conditions. Proc. Natl. Acad. Sci. USA 87, 7414-7418.
18. Grinstein, S., Woodside, M., Waddell, T.K., Downey, G.P., Orlowski, J., Pouyssegur, J., Wong, D.C., and Foskett, J.K. (1993). Focal localization of the NHE-1 isoform of the Na+/H+ antiport: assessment of effects on intracellular pH. EMBO J. 12, 5209-5218.
19. Guan, J.L., and Shalloway, D. (1992). Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 358, 690-692.
20. Gumbiner, B.M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357.
21. Hooley, R., Yu, C.-Y., Symons, M., and Barber, D.L. (1996). Ga13 stimulates Na-H exchange through distinct Cdc42-dependent and Rho-dependent pathways. J. Biol. Chem. 271, 6152-6158.
22. Hotchin, N.A., and Hall, A. (1995). The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J. Cell Biol. 131, 1857-1865.
23. Ingber, D.E., Prusty, D., Frangioni, J.V., Cragoe, E.J., Lechene, C., and Schwartz, M.A. (1990). Control of intracellular pH and growth by fibronectin in capillary endothelial cells. J. Cell Biol. 110, 1803-1811.
24. Ishizaki, T., Naito, M., Fujisawa, K., Maekawa, M., Watanabe, N., Saito, Y., and Narumiya, S. (1997). p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 404, 118-124.
25. Kapus, A., Grinstein, S., Wasan, S., Kandasamy, R., and Orlowski, O. (1994). Functional characterization of three isoforms of the Na+/H+ exchanger stably expressed in Chinese hamster ovary cells. ATP dependence, osmotic sensitivity, and role in cell proliferation. J. Biol. Chem. 269, 23544-23552.
26. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K.K. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
27. 3. Curr. Opin. Cell Biol. 9, 725-731.
28. Kornberg, L., Earp, H.S., Parsons, J.T., Schaller, M., and Juliano, R.L. (1992). Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267, 23439-23442.
29. Krump, E., Nikitas, K., and Grinstein, S. (1997). Induction of tyrosine phosphorylation and Na+/H+ exchanger activation during shrinkage of human neutrophils. J. Biol. Chem. 272, 17303-17311.
30. Kumagai, N., Morii, N., Fujisawa, K., Nemoto, Y., and Narumiya, S. (1993). ADP-ribosylation of rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells. J. Biol. Chem. 268, 24535-24538.
31. Laudanna, C., Campbell, J.J., and Butcher, E.C. (1996). Role of rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271, 981-983.
32. Lee, S.W., and Otto, J.J. (1996). Differences in turnover rates of vinculin and talin caused by viral transformation and cell density. Exp. Cell Res. 227, 352-359.
33. Leung, T., Manser, E., Tan, L., and Lim, L. (1995). A novel serine/ threonine kinase binding the ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 27, 29051-29054.
34. Lin, X., and Barber, D.L. (1996). A calcineurin homologous protein inhibits GTPase-stimulated Na-H exchange. Proc. Natl. Acad. Sci. USA 93, 12631-12636.
35. Lin, X., Voyno-Yasenetskaya, T., Hooley, R., Lin, C., Orlowski, J., and Barber, D.L. (1996). Ga12 differentially regulates Na-H exchanger isoforms. J. Biol. Chem. 271, 22604-22610.
36. Matsui, T., Amano, M., Yamamoto, T., Chihara, K., Nakafuku, M., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP binding protein Rho. EMBO J. 15, 2208-2216.
37. Miyamoto, S., Teramoto, H., Coso, O.A., Gutkind, J.S., Burbelo, P.D., Akiyama, S.K., and Yamada, K.M. (1995). Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 231, 791-807.
38. Morii, N., and Narumiya, S. (1995). Preparation of native and recombinant Clostridium botulinum C3 ADP-ribosyltransferase and identification of Rho proteins by ADP-ribosylation. Methods Enzymol. 256, 196-206.
39. Morii, N., Teru-uchi, T., Tominaga, T., Kumagai, N., Kozaki, S., Ushikubi, F., and Narumiya, S. (1992). A rho gene product in human blood platelets. J. Biol. Chem. 267, 20921-20926.
40. Morino, N., Mimura, T., Hamasaki, K., Tobe, K., Ueki, K., Kikuchi, K., Takehara, K., Kadowaki, T., Yazaki, Y., and Nojima, Y. (1995). Matrix/integrin interaction activates the mitogen-activated protein kinase, p44erk-1 and p42erk-2. J. Biol. Chem. 270, 269-273.
41. Nobes, C.D., and Hall, A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
42. Parsons, J.T. (1996). Integrin-mediated signalling: regulation by protein tyrosine kinases and small GTP-binding proteins. Curr. Opin. Cell Biol. 8, 146-152.
43. Peter, K., and O'Toole, T.E. (1995). Modulation of cell adhesion by changes in alpha L beta 2 (LFA-1, CD11a/CD18) cytoplasmic domain/cytoskeleton interaction. J. Exp. Med. 18, 315-326.
44. Plopper, G.E., McNamee, H.P., Dike, L.E., Bojanowski, K., and Ingber, D.E. (1995). Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6, 1349-1365.
45. Pouyssegur, J., Sardet, C., Franchi, A., Allemain, G., and Paris, A. (1984). A specific mutation abolishing Na+/H+ antiport activity in hamster fibroblasts precludes growth at neutral and acidic pH. Proc. Natl. Acad. Sci. USA 81, 4833-4837.
46. Rankin, S., Morii, N., Narumiya, S., and Rozengurt, E. (1994). Botulinum C3 exoenzyme blocks the tyrosine phosphorylation of p125FAK and paxillin induced by bombesin and endothelin. FEBS Lett. 354, 315-319.
47. Rao, G.N., Sardet, C., Pouyssegur, J., and Berk, B.C. (1992). Na+/H+ antiporter gene expression increases during retinoic acid-induced granulocytic differentiation of HL60 cells. J. Cell. Physiol. 151, 361-366.
48. Ridley, A.J., and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
49. Sardet, C., Franchi, A., and Pouyssegur, J. (1989). Molecular cloning, primary structure, and expression of the human growth factor-activatable Na+/H+ antiporter. Cell 56, 271-280.
50. Schwartz, M.A., Both, G., and Lechene, C. (1989). Effect of cell spreading on cytoplasmic pH in normal and transformed fibroblasts. Proc. Natl. Acad Sci. USA 86, 4525-4529.
51. Schwartz, M.A., Lechene, C., and Ingber, D.E. (1991). Insoluble fibronectin activates the Na/H antiporter by clustering and immobilizing integrin α5β1, independent of cell shape. Proc. Natl. Acad. Sci. USA 88, 7849-7853.
52. Schwartz, M.A., Toksoz, D., and Khosravi-Far, R. (1996). Transformation by Rho exchange factor oncogenes is mediated by activation of an integrin-dependent pathway. EMBO J. 15, 6524-6530.
53. Shrode, L.D., Klein, J.D., O'Neill, W.C., and Putnam, R.W. (1995). Shrinkage-induced activation of Na+/H+ exchange in primary rat astrocytes: role of myosin light-chain kinase. Am. J. Physiol. 269, C257-C266.
54. Thomas, J.A., Buchsbaum, R.N., Zimniak, A., and Racker, E. (1979). Intracellular pH measurement in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18, 2210-2218.
55. 2+-mobilizing H1 receptors. J. Cell Biol. 110, 1211-1215.
56. Tominaga, T., Ishizaki, T., Narymiya, S., and Barber, D. (1998). p160 ROCK mediates RhoA activation of Na-H exchange. EMBO J. (in press).
57. Tominaga, T., Sugie, K., Hirata, M., Morii, N., Fukata, J., Uchida, A., Imura, H., and Narumiya, S. (1993). Inhibition of PMA-induced, LFA-1-dependent lymphocyte aggregation by ADP ribosylation of the small molecular weight GTP binding protein, rho. J. Cell Biol. 120, 1529-1537.
58. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M., et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
59. Vexler, Z.S., Symons, M., and Barber, D.L. (1996). Activation of Na+-H+ exchange is necessary for rhoA-induced stress fiber formation. J. Biol. Chem. 271, 22281-22284.
60. Voyno-Yasenetskaya, T., Conklin, B.R., Gilbert, R.L., Hooley, R., Bourne, H.R., and Barber, D.L. (1994). Ga13 stimulates Na-H exchange. J. Biol. Chem. 269, 4721-4724.
61. Vuori, K., and Ruoslahti, E. (1993). Activation of protein kinase C precedes alpha 5 beta 1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268, 21459-21462.
62. Wakabayashi, S., Bertrand, B., Shigekawa, M., Fafournoux, P., and Pouyssegu, J. (1994). Growth factor activation and "H+-sensing" of the Na+/H+ exchanger isoform 1 (NHE1). J. Biol. Chem. 269, 5583-5588.
63. Wakabayashi, S., Fafournoux, P., Sardet, C., and Pouyssegur, J. (1992). The Na+/H+ antiporter cytoplasmic domain mediates growth factor signals and controls "H+-sensing." Proc. Natl. Acad. Sci. USA 89, 2424-2428.
64. Watson, A.L., Levine, S., Donowitz, M., and Montrose, M.H. (1992). Serum regulates Na+/H+ exchange in Coco-2 cells by a mechanism which is dependent on F-actin. J. Biol. Chem. 267, 956-962.
65. Werb, Z., Tremble, P.M., Behrendtson, O., Crowley, E., and Damsky, C.H. (1989). Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J. Cell Biol. 109, 877-889.
66. Wong, P. (1994). Mechanism of control of erythrocyte cell shape: a possible relationship to band 3. J. Theor. Biol. 171, 197-205.
67. Ylänne, J., Chen, Y., O'Toole, T.E., Loftus, J.C., Takada, Y., and Ginsberg, M.H. (1993). Distinct functions of integrin alpha and beta subunit cytoplasmic domains in cell spreading and formation of focal adhesions. J. Cell Biol. 122, 223-233.
68. Zhang, Z., Vuori, K., Wang, H.-G., Reed, J.C., and Ruoslahti, R. (1996). Integrin activation by R-ras. Cell 85, 61-69.