Tiam1-regulated osteopontin in senescent fibroblasts contributes to the migration and invasion of associated epithelial cells

Journal of Cell Science

Volumn 125, Issue 2, 2012, Pages 376-386

  Liu, Jiewei ^a,b   Xu, Kun ^a   Chase, Maya ^a,c   Ji, Yuxin ^a   Logan, Jennifer K ^a,d   Buchsbaum, Rachel J ^a,d  

^a TUFTS MEDICAL CENTER   (United States)

^b SICHUAN UNIVERSITY   (China)

^c BUCKNELL UNIVERSITY   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Invasion; Migration; Osteopontin; Senescence; Tiam1; Tumor microenvironment

Indexed keywords

INITIATION FACTOR; MESSENGER RNA; OSTEOPONTIN; TIAM1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BREAST EPITHELIUM; CANCER CELL CULTURE; CANCER INVASION; CELL INVASION; CELL MIGRATION; CELL STRESS; CONTROLLED STUDY; EPITHELIUM CELL; EPITHELIUM TUMOR; FIBROBLAST; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; SENESCENCE; TUMOR CELL; TUMOR MICROENVIRONMENT;

CALPAIN; CELL AGING; CELL LINE; CELL MOVEMENT; EPITHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; OSTEOPONTIN; STRESS, PHYSIOLOGICAL;

EID: 84863249949     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.089466     Document Type: Article

References (48)

1. Aoshiba, K., Tsuji, T. and Nagai, A. (2003). Bleomycin induces cellular senescence in alveolar epithelial cells. Eur. Respir. J. 22, 436-443.
2. Bavik, C., Coleman, I., Dean, J. P., Knudsen, B., Plymate, S. and Nelson, P. S. (2006). The gene expression program of prostate fibroblast senescence modulates neoplastic epithelial cell proliferation through paracrine mechanisms. Cancer Res. 66, 794-802.
3. Belizario, J. E., Alves, J., Garay-Malpartida, M. and Occhiucci, J. M. (2008). Coupling caspase cleavage and proteasomal degradation of proteins carrying PEST motif. Curr. Protein Pept. Sci. 9, 210-220.
4. Ben-Porath, I. and Weinberg, R. A. (2005). The signals and pathways activating cellular senescence. Int. J. Biochem. Cell Biol. 37, 961-976.
5. Buchsbaum, R., Telliez, J. B., Goonesekera, S. and Feig, L. A. (1996). The N-terminal pleckstrin, coiled-coil, and IQ domains of the exchange factor Ras-GRF act cooperatively to facilitate activation by calcium. Mol. Cell. Biol. 16, 4888-4896.
6. Buchsbaum, R. J., Connolly, B. A. and Feig, L. A. (2002). Interaction of Rac exchange factors Tiam1 and Ras-GRF1 with a scaffold for the p38 mitogen-activated protein kinase cascade. Mol. Cell. Biol. 22, 4073-4085.
7. Buchsbaum, R. J., Connolly, B. A. and Feig, L. A. (2003). Regulation of p70 S6 kinase by complex formation between the Rac guanine nucleotide exchange factor (Rac-GEF) Tiam1 and the scaffold spinophilin. J. Biol. Chem. 278, 18833-18841.
8. Campisi, J. (2005). Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120, 513-522.
9. Campisi, J. and d'Adda di Fagagna, F. (2007). Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell. Biol. 8, 729-740.
10. Castro, P., Giri, D., Lamb, D. and Ittmann, M. (2003). Cellular senescence in the pathogenesis of benign prostatic hyperplasia. Prostate 55, 30-38.
11. Chen, Q., Fischer, A., Reagan, J. D., Yan, L. J. and Ames, B. N. (1995). Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc. Natl. Acad. Sci. USA 92, 4337-4341.
12. Connolly, B. A., Rice, J., Feig, L. A. and Buchsbaum, R. J. (2005). Tiam1-IRSp53 complex formation directs specificity of rac-mediated actin cytoskeleton regulation. Mol. Cell. Biol. 25, 4602-4614.
13. Coppe, J. P., Kauser, K., Campisi, J. and Beausejour, C. M. (2006). Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J. Biol. Chem. 281, 29568-29574.
14. Coppe, J. P., Patil, C. K., Rodier, F., Sun, Y., Munoz, D. P., Goldstein, J., Nelson, P. S., Desprez, P. Y. and Campisi, J. (2008). Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868.
15. d'Adda di Fagagna, F., Reaper, P. M., Clay-Farrace, L., Fiegler, H., Carr, P., Von Zglinicki, T., Saretzki, G., Carter, N. P. and Jackson, S. P. (2003). A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198.
16. Davalos, A. R., Coppe, J. P., Campisi, J. and Desprez, P. Y. (2010). Senescent cells as a source of inflammatory factors for tumor progression. Cancer Metastasis Rev. 29, 273-283.
17. Demarchi, F., Cataldo, F., Bertoli, C. and Schneider, C. (2010). DNA damage response links calpain to cellular senescence. Cell Cycle 9, 755-760.
18. Dilley, T. K., Bowden, G. T. and Chen, Q. M. (2003). Novel mechanisms of sublethal oxidant toxicity: induction of premature senescence in human fibroblasts confers tumor promoter activity. Exp. Cell Res. 290, 38-48.
19. Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., Pereira-Smith, O. et al. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92, 9363-9367.
20. Franco, S. J. and Huttenlocher, A. (2005). Regulating cell migration: calpains make the cut. J. Cell Sci. 118, 3829-3838.
21. Hayflick, L. (1965). The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636.
22. Hornsby, P. J. (2007). Senescence as an anticancer mechanism. J. Clin. Oncol. 25, 1852-1857.
23. Itahana, K., Campisi, J. and Dimri, G. P. (2004). Mechanisms of cellular senescence in human and mouse cells. Biogerontology 5, 1-10.
24. Janzen, V., Forkert, R., Fleming, H. E., Saito, Y., Waring, M. T., Dombkowski, D. M., Cheng, T., DePinho, R. A., Sharpless, N. E. and Scadden, D. T. (2006). Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 443, 421-426.
25. Juo, P., Kuo, C. J., Yuan, J. and Blenis, J. (1998). Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr. Biol. 8, 1001-1008.
26. Kang, J., Chen, W., Xia, J., Li, Y., Yang, B., Chen, B., Sun, W., Song, X., Xiang, W., Wang, X. et al. (2008). Extracellular matrix secreted by senescent fibroblasts induced by UVB promotes cell proliferation in HaCaT cells through PI3K/AKT and ERK signaling pathways. Int. J. Mol. Med. 21, 777-784.
27. Krishnamurthy, J., Ramsey, M. R., Ligon, K. L., Torrice, C., Koh, A., Bonner-Weir, S. and Sharpless, N. E. (2006). p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 443, 453-457.
28. Krtolica, A. and Campisi, J. (2002). Cancer and aging: a model for the cancer promoting effects of the aging stroma. Int. J. Biochem. Cell. Biol. 34, 1401-1414.
29. Krtolica, A., Parrinello, S., Lockett, S., Desprez, P. Y. and Campisi, J. (2001). Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging. Proc. Natl. Acad. Sci. USA 98, 12072-12077.
30. Li, H., Bergeron, L., Cryns, V., Pasternack, M. S., Zhu, H., Shi, L., Greenberg, A. and Yuan, J. (1997). Activation of caspase-2 in apoptosis. J. Biol. Chem. 272, 21010-21017.
31. Mertens, A. E., Roovers, R. C. and Collard, J. G. (2003). Regulation of Tiam1-Rac signalling. FEBS Lett. 546, 11-16.
32. Molofsky, A. V., Slutsky, S. G., Joseph, N. M., He, S., Pardal, R., Krishnamurthy, J., Sharpless, N. E. and Morrison, S. J. (2006). Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443, 448-452.
33. Narita, M., Nunez, S., Heard, E., Lin, A. W., Hearn, S. A., Spector, D. L., Hannon, G. J. and Lowe, S. W. (2003). Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113, 703-716.
34. Parrinello, S., Coppe, J. P., Krtolica, A. and Campisi, J. (2005). Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation. J. Cell Sci. 118, 485-496.
35. Pazolli, E., Luo, X., Brehm, S., Carbery, K., Chung, J. J., Prior, J. L., Doherty, J., Demehri, S., Salavaggione, L., Piwnica-Worms, D. et al. (2009). Senescent stromal-derived osteopontin promotes preneoplastic cell growth. Cancer Res. 69, 1230-1239.
36. Qi, H., Juo, P., Masuda-Robens, J., Caloca, M. J., Zhou, H., Stone, N., Kazanietz, M. G. and Chou, M. M. (2001). Caspase-mediated cleavage of the TIAM1 guanine nucleotide exchange factor during apoptosis. Cell Growth Differ. 12, 603-611.
37. Rajagopal, S., Ji, Y., Xu, K., Li, Y., Wicks, K., Liu, J., Wong, K. W., Herman, I. M., Isberg, R. R. and Buchsbaum, R. J. (2010). Scaffold proteins IRSp53 and spinophilin regulate localized Rac activation by T-lymphocyte invasion and metastasis protein 1 (TIAM1). J. Biol. Chem. 285, 18060-18071.
38. Rechsteiner, M. and Rogers, S. W. (1996). PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271.
39. Rodier, F., Coppe, J. P., Patil, C. K., Hoeijmakers, W. A., Munoz, D. P., Raza, S. R., Freund, A., Campeau, E., Davalos, A. R. and Campisi, J. (2009). Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat. Cell Biol. 11, 973-979.
40. Toussaint, O., Medrano, E. E. and von Zglinicki, T. (2000). Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp. Gerontol. 35, 927-945.
41. Wai, P. Y. and Kuo, P. C. (2004). The role of osteopontin in tumor metastasis. J. Surg. Res. 121, 228-241.
42. Wai, P. Y. and Kuo, P. C. (2008). Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev. 27, 103-118.
43. Weber, G. F. (2008). Molecular mechanisms of metastasis. Cancer Lett. 270, 181-190.
44. Woodcock, S. A., Rooney, C., Liontos, M., Connolly, Y., Zoumpourlis, V., Whetton, A. D., Gorgoulis, V. G. and Malliri, A. (2009). SRC-induced disassembly of adherens junctions requires localized phosphorylation and degradation of the rac activator tiam1. Mol. Cell 33, 639-653.
45. Xu, K., Rajagopal, S., Klebba, I., Dong, S., Ji, Y., Liu, J., Kuperwasser, C., Garlick, J. A., Naber, S. P. and Buchsbaum, R. J. (2010). The role of fibroblast Tiam1 in tumor cell invasion and metastasis. Oncogene 29, 6533-6542.
46. Yang, G., Rosen, D. G., Zhang, Z., Bast, R. C., Jr., Mills, G. B., Colacino, J. A., Mercado-Uribe, I. and Liu, J. (2006). The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis. Proc. Natl. Acad. Sci. USA 103, 16472-16477.
47. Zhang, H. and Macara, I. G. (2006). The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis. Nat. Cell Biol. 8, 227-237.
48. Zindy, F., Quelle, D. E., Roussel, M. F. and Sherr, C. J. (1997). Expression of the p16INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene 15, 203-211.