Phosphoinositide 3-kinase d regulates migration and invasion of synoviocytes in rheumatoid arthritis

Journal of Immunology

Volumn 192, Issue 5, 2014, Pages 2063-2070

  Bartok, Beatrix ^a   Hammaker, Deepa ^a   Firestein, Gary S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE DELTA; PLATELET DERIVED GROWTH FACTOR; PROTEIN FAK; PROTEIN JNK; PROTEIN PAK; RAC1 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CELL INVASION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LAMELLIPODIUM; MIGRATION INHIBITION; PRIORITY JOURNAL; PROTEIN FUNCTION; RHEUMATOID ARTHRITIS; SYNOVIOCYTE;

ACTIN CYTOSKELETON; ARTHRITIS, RHEUMATOID; CELL MOVEMENT; CELL SURVIVAL; ENZYME ACTIVATION; FEMALE; FIBROBLASTS; FOCAL ADHESION KINASE 1; HUMANS; MALE; MAP KINASE KINASE 4; PHOSPHATIDYLINOSITOL 3-KINASES; PLATELET-DERIVED GROWTH FACTOR; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; SYNOVIAL MEMBRANE;

EID: 84896514909     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300950     Document Type: Article

References (52)

1. Bartok, B., and G. S. Firestein. 2010. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol. Rev. 233: 233-255.
2. Bottini, N., and G. S. Firestein. 2013. Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors. Nat. Rev. Rheumatol. 9: 24-33.
3. Lefévre, S., A. Knedla, C. Tennie, A. Kampmann, C. Wunrau, R. Dinser, A. Korb, E. M. Schnäker, I. H. Tarner, P. D. Robbins, et al. 2009. Synovial fibroblasts spread rheumatoid arthritis to unaffected joints. Nat. Med. 15: 1414-1420.
4. Ridley, A. J., M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, and A. R. Horwitz. 2003. Cell migration: integrating signals from front to back. Science 302: 1704-1709.
5. Parsons, J. T., A. R. Horwitz, and M. A. Schwartz. 2010. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11: 633-643.
6. Vanhaesebroeck, B., J. Guillermet-Guibert, M. Graupera, and B. Bilanges. 2010. The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11: 329-341.
7. Vanhaesebroeck, B., L. Stephens, and P. Hawkins. 2012. PI3K signalling: the path to discovery and understanding. Nat. Rev. Mol. Cell Biol. 13: 195-203.
8. Foster, J. G., M. D. Blunt, E. Carter, and S. G. Ward. 2012. Inhibition of PI3K signaling spurs new therapeutic opportunities in inflammatory/autoimmune diseases and hematological malignancies. Pharmacol. Rev. 64: 1027-1054.
9. Chen, Y., B. C. Wang, and Y. Xiao. 2012. PI3K: a potential therapeutic target for cancer. J. Cell. Physiol. 227: 2818-2821.
10. Rommel, C., M. Camps, and H. Ji. 2007. PI3K delta and PI3K gamma: partners in crime in inflammation in rheumatoid arthritis and beyond? Nat. Rev. Immunol. 7: 191-201.
11. Blajecka, K., A. Borgström, and A. Arcaro. 2011. Phosphatidylinositol 3-kinase isoforms as novel drug targets. Curr. Drug Targets 12: 1056-1081.
12. Bartok, B., D. L. Boyle, Y. Liu, P. Ren, S. T. Ball, W. D. Bugbee, C. Rommel, and G. S. Firestein. 2012. PI3 kinase d is a key regulator of synoviocyte function in rheumatoid arthritis. Am. J. Pathol. 180: 1906-1916.
13. Alvaro-Gracia, J. M., N. J. Zvaifler, C. B. Brown, K. Kaushansky, and G. S. Firestein. 1991. Cytokines in chronic inflammatory arthritis. VI. Analysis of the synovial cells involved in granulocyte-macrophage colony-stimulating factor production and gene expression in rheumatoid arthritis and its regulation by IL-1 and tumor necrosis factor-Alpha. J. Immunol. 146: 3365-3371.
14. Arnett, F. C., S. M. Edworthy, D. A. Bloch, D. J. McShane, J. F. Fries, N. S. Cooper, L. A. Healey, S. R. Kaplan, M. H. Liang, H. S. Luthra, et al. 1988. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31: 315-324.
15. Rosengren, S., D. L. Boyle, and G. S. Firestein. 2007. Acquisition, culture, and phenotyping of synovial fibroblasts. Methods Mol. Med. 135: 365-375.
16. Aupperle, K. R., B. L. Bennett, D. L. Boyle, P. P. Tak, A. M. Manning, and G. S. Firestein. 1999. NF-kappa B regulation by I kappa B kinase in primary fibroblast-like synoviocytes. J. Immunol. 163: 427-433.
17. Inoue, T., D. Hammaker, D. L. Boyle, and G. S. Firestein. 2005. Regulation of p38 MAPK by MAPK kinases 3 and 6 in fibroblast-like synoviocytes. J. Immunol. 174: 4301-4306.
18. Sweeney, S. E., T. B.Kimbler, and G. S. Firestein. 2010. Synoviocyte innate immune responses. II. Pivotal role of IFN regulatory factor 3. J. Immunol. 184: 7162-7168.
19. Hammaker, D. R., D. L. Boyle, T. Inoue, and G. S. Firestein. 2007. Regulation of the JNK pathway by TGF-beta activated kinase 1 in rheumatoid arthritis synoviocytes. Arthritis Res. Ther. 9: R57.
20. Boyle, D. L., H. R. Kim, K. Topolewski, B. Bartok, and G. S. Firestein. 2014. Novel phosphoinositide 3-kinase d,g inhibitor: potent anti-inflammatory effects and joint protection in models of rheumatoid arthritis. J. Pharmacol. Exp. Ther. 348: 271-280.
21. Kaur, H., P. J. Phillips-Mason, S. M. Burden-Gulley, A. E. Kerstetter-Fogle, J. P. Basilion, A. E. Sloan, and S. M. Brady-Kalnay. 2012. Cadherin-11, a marker of the mesenchymal phenotype, regulates glioblastoma cell migration and survival in vivo. Mol. Cancer Res. 10: 293-304.
22. Petrie, R. J., A. D. Doyle, and K. M. Yamada. 2009. Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10: 538-549.
23. Meima, M. E., B. A. Webb, H. E. Witkowska, and D. L. Barber. 2009. The sodium-hydrogen exchanger NHE1 is an Akt substrate necessary for actin filament reorganization by growth factors. J. Biol. Chem. 284: 26666-26675.
24. Andrae, J., R. Gallini, and C. Betsholtz. 2008. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22: 1276-1312.
25. Huttenlocher, A., and A. R. Horwitz. 2011. Integrins in cell migration. Cold Spring Harb. Perspect. Biol. 3: a005074.
26. Cain, R. J., and A. J. Ridley. 2009. Phosphoinositide 3-kinases in cell migration. Biol. Cell 101: 13-29.
27. Kazlauskas, A., and J. A. Cooper. 1989. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58: 1121-1133.
28. Huang, C., K. Jacobson, and M. D. Schaller. 2004. A role for JNK-paxillin signaling in cell migration. Cell Cycle 3: 4-6.
29. Sieg, D. J., C. R. Hauck, D. Ilic, C. K. Klingbeil, E. Schaefer, C. H. Damsky, and D. D. Schlaepfer. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2: 249-256.
30. Noss, E. H., and M. B. Brenner. 2008. The role and therapeutic implications of fibroblast-like synoviocytes in inflammation and cartilage erosion in rheumatoid arthritis. Immunol. Rev. 223: 252-270.
31. Lee, D. M., H. P. Kiener, S. K. Agarwal, E. H. Noss, G. F. Watts, O. Chisaka, M. Takeichi, and M. B. Brenner. 2007. Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315: 1006-1010.
32. Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
33. Roymans, D., and H. Slegers. 2001. Phosphatidylinositol 3-kinases in tumor progression. Eur. J. Biochem. 268: 487-498.
34. Samuels, Y., and K. Ericson. 2006. Oncogenic PI3K and its role in cancer. Curr. Opin. Oncol. 18: 77-82.
35. Whitehead, M. A., M. Bombardieri, C. Pitzalis, and B. Vanhaesebroeck. 2012. Isoform-selective induction of human p110d PI3K expression by TNFa: identification of a new and inducible PIK3CD promoter. Biochem. J. 443: 857-867.
36. Fung-Leung, W. P. 2011. Phosphoinositide 3-kinase delta (PI3Kd) in leukocyte signaling and function. Cell. Signal. 23: 603-608.
37. Tzenaki, N., and E. A. Papakonstanti. 2013. p110d PI3 kinase pathway: emerging roles in cancer. Front. Oncol. 3: 40.
38. Luk, S. K., R. P. Piekorz, B. Nurnberg, and S. S. Tony To. 2012. The catalytic phosphoinositol 3-kinase isoform p110d is required for glioma cell migration and invasion. Eur. J. Cancer 48: 149-157.
39. Sawyer, C., J. Sturge, D. C. Bennett, M. J. O'Hare, W. E. Allen, J. Bain, G. E. Jones, and B. Vanhaesebroeck. 2003. Regulation of breast cancer cell chemotaxis by the phosphoinositide 3-kinase p110delta. Cancer Res. 63: 1667-1675.
40. Campbell, I. G., S. E. Russell, D. Y. Choong, K. G. Montgomery, M. L. Ciavarella, C. S. Hooi, B. E. Cristiano, R. B. Pearson, and W. A. Phillips. 2004. Mutation of the PIK3CA gene in ovarian and breast cancer. Cancer Res. 64: 7678-7681.
41. Samuels, Y., and V. E. Velculescu. 2004. Oncogenic mutations of PIK3CA in human cancers. Cell Cycle 3: 1221-1224.
42. Yuan, T. L., and L. C. Cantley. 2008. PI3K pathway alterations in cancer: variations on a theme. Oncogene 27: 5497-5510.
43. Zhao, L., and P. K. Vogt. 2008. Class I PI3K in oncogenic cellular transformation. Oncogene 27: 5486-5496.
44. Kang, S., A. Denley, B. Vanhaesebroeck, and P. K. Vogt. 2006. Oncogenic transformation induced by the p110beta, -gamma, and -delta isoforms of class I phosphoinositide 3-kinase. Proc. Natl. Acad. Sci. USA 103: 1289-1294.
45. Ridley, A. J. 2011. Life at the leading edge. Cell 145: 1012-1022.
46. Welch, H. C., W. J. Coadwell, L. R. Stephens, and P. T. Hawkins. 2003. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett. 546: 93-97.
47. Schneider, I. C., and J. M. Haugh. 2005. Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts. J. Cell Biol. 171: 883-892.
48. Higuchi, M., N. Masuyama, Y. Fukui, A. Suzuki, and Y. Gotoh. 2001. Akt mediates Rac/Cdc42-regulated cell motility in growth factor-stimulated cells and in invasive PTEN knockout cells. Curr. Biol. 11: 1958-1962.
49. Kim, E. K., D. F. Tucker, S. J. Yun, K. H. Do, M. S. Kim, J. H. Kim, C. D. Kim, M. J. Birnbaum, and S. S. Bae. 2008. Linker region of Akt1/protein kinase Balpha mediates platelet-derived growth factor-induced translocation and cell migration. Cell. Signal. 20: 2030-2037.
50. Kim, D., S. Kim, H. Koh, S. O. Yoon, A. S. Chung, K. S. Cho, and J. Chung. 2001. Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J. 15: 1953-1962.
51. Manning, B. D., and L. C. Cantley. 2007. AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274.
52. Tolboom, T. C., A. H. Van der Helm-Van Mil, R. G. Nelissen, F. C. Breedveld, R. E. Toes, and T. W. Huizinga. 2005. Invasiveness of fibroblast-like synoviocytes is an individual patient characteristic associated with the rate of joint destruction in patients with rheumatoid arthritis. Arthritis Rheum. 52: 1999-2002.