14
Views
34
CrossRef citations to date
0
Altmetric
Article

Doubles Game: Src-Stat3 versus p53-PTEN in Cellular Migration and Invasion

, , , , &
Pages 4980-4995 | Received 04 Jan 2010, Accepted 02 Aug 2010, Published online: 20 Mar 2023

REFERENCES

  • Abdulghani, J., L. Gu, A. Dagvadorj, J. Lutz, B. Leiby, G. Bonuccelli, M. P. Lisanti, T. Zellweger, K. Alanen, T. Mirtti, T. Visakorpi, L. Bubendorf, and M. T. Nevalainen. 2008. Stat3 promotes metastatic progression of prostate cancer. Am. J. Pathol. 172:1717–1728.
  • Artym, V. V., Y. Zhang, F. Seillier-Moiseiwitsch, K. M. Yamada, and S. C. Mueller. 2006. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 66:3034–3043.
  • Aylon, Y., and M. Oren. 2007. Living with p53, dying of p53. Cell 130:597–600.
  • Bowman, T., M. A. Broome, D. Sinibaldi, W. Wharton, W. J. Pledger, J. M. Sedivy, R. Irby, T. Yeatman, S. A. Courtneidge, and R. Jove. 2001. Stat3-mediated Myc expression is required for Src transformation and PDGF-induced mitogenesis. Proc. Natl. Acad. Sci. U. S. A. 98:7319–7324.
  • Brisbin, S., J. Liu, J. Boudreau, J. Peng, M. Evangelista, and I. Chin-Sang. 2009. A role for C. elegans Eph RTK signaling in PTEN regulation. Dev. Cell 17:459–469.
  • Bromberg, J. F., C. M. Horvath, D. Besser, W. W. Lathem, and J. E. Darnell, Jr. 1998. Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18:2553–2558.
  • Bromberg, J. F., M. H. Wrzeszczynska, G. Devgan, Y. Zhao, R. G. Pestell, C. Albanese, and J. E. Darnell, Jr. 1999. Stat3 as an oncogene. Cell 98:295–303.
  • Buccione, R., G. Caldieri, and I. Ayala. 2009. Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev. 28:137–149.
  • Buccione, R., J. D. Orth, and M. A. McNiven. 2004. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat. Rev. Mol. Cell Biol. 5:647–657.
  • Campisi, J. 2005. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120:513–522.
  • Chalhoub, N., and S. J. Baker. 2009. PTEN and the PI3-kinase pathway in cancer. Annu. Rev. Pathol. 4:127–150.
  • de la Iglesia, N., G. Konopka, S. V. Puram, J. A. Chan, R. M. Bachoo, M. J. You, D. E. Levy, R. A. DePinho, and A. Bonni. 2008. Identification of a PTEN-regulated STAT3 brain tumor suppressor pathway. Genes Dev. 22:449–462.
  • de Stanchina, E., E. Querido, M. Narita, R. V. Davuluri, P. P. Pandolfi, G. Ferbeyre, and S. W. Lowe. 2004. PML is a direct p53 target that modulates p53 effector functions. Mol. Cell 13:523–535.
  • Devarajan, E., and S. Huang. 2009. STAT3 as a central regulator of tumor metastases. Curr. Mol. Med. 9:626–633.
  • Dey, N., H. E. Crosswell, P. De, R. Parsons, Q. Peng, J. D. Su, and D. L. Durden. 2008. The protein phosphatase activity of PTEN regulates SRC family kinases and controls glioma migration. Cancer Res. 68:1862–1871.
  • Efeyan, A., and M. Serrano. 2007. p53: guardian of the genome and policeman of the oncogenes. Cell Cycle 6:1006–1010.
  • Eves, R., B. A. Webb, S. T. Zhou, and A. S. Mak. 2006. Caldesmon is an integral component of podosomes in smooth muscle cells. J. Cell Sci. 119:1691–1702.
  • Freeman, D. J., A. G. Li, G. Wei, H. H. Li, N. Kertesz, R. Lesche, A. D. Whale, H. Martinez-Diaz, N. Rozengurt, R. D. Cardiff, X. Liu, and H. Wu. 2003. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell 3:117–130.
  • Gadea, G., M. de Toledo, C. Anguille, and P. Roux. 2007. Loss of p53 promotes RhoA-ROCK-dependent cell migration and invasion in 3D matrices. J. Cell Biol. 178:23–30.
  • Gadéa, G., L. Lapasset, C. Gauthier-Rouviere, and P. Roux. 2002. Regulation of Cdc42-mediated morphological effects: a novel function for p53. EMBO J. 21:2373–2382.
  • Gao, S. P., and J. F. Bromberg. 2006. Touched and moved by STAT3. Sci. STKE 2006:pe30.
  • Garcia, R., T. L. Bowman, G. Niu, H. Yu, S. Minton, C. A. Muro-Cacho, C. E. Cox, R. Falcone, R. Fairclough, S. Parsons, A. Laudano, A. Gazit, A. Levitzki, A. Kraker, and R. Jove. 2001. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20:2499–2513.
  • Geletu, M., C. Chaize, R. Arulanandam, A. Vultur, C. Kowolik, A. Anagnostopoulou, R. Jove, and L. Raptis. 2009. Stat3 activity is required for gap junctional permeability in normal rat liver epithelial cells. DNA Cell Biol. 28:319–327.
  • Gimona, M., R. Buccione, S. A. Courtneidge, and S. Linder. 2008. Assembly and biological role of podosomes and invadopodia. Curr. Opin. Cell Biol. 20:235–241.
  • Hollstein, M., D. Sidransky, B. Vogelstein, and C. C. Harris. 1991. p53 mutations in human cancers. Science 253:49–53.
  • Itoh, M., T. Murata, T. Suzuki, M. Shindoh, K. Nakajima, K. Imai, and K. Yoshida. 2006. Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells. Oncogene 25:1195–1204.
  • Kruse, J. P., and W. Gu. 2009. Modes of p53 regulation. Cell 137:609–622.
  • Ku, T. K., D. C. Nguyen, M. Karaman, P. Gill, J. G. Hacia, and D. L. Crowe. 2007. Loss of p53 expression correlates with metastatic phenotype and transcriptional profile in a new mouse model of head and neck cancer. Mol. Cancer Res. 5:351–362.
  • Leslie, N. R., H. Maccario, L. Spinelli, and L. Davidson. 2009. The significance of PTEN′s protein phosphatase activity. Adv. Enzyme Regul. 49:190–196.
  • Leslie, N. R., X. Yang, C. P. Downes, and C. J. Weijer. 2005. The regulation of cell migration by PTEN. Biochem. Soc. Trans. 33:1507–1508.
  • Leslie, N. R., X. Yang, C. P. Downes, and C. J. Weijer. 2007. PtdIns(3,4,5)P(3)-dependent and -independent roles for PTEN in the control of cell migration. Curr. Biol. 17:115–125.
  • Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323–331.
  • Lewis, B. C., D. S. Klimstra, N. D. Socci, S. Xu, J. A. Koutcher, and H. E. Varmus. 2005. The absence of p53 promotes metastasis in a novel somatic mouse model for hepatocellular carcinoma. Mol. Cell. Biol. 25:1228–1237.
  • Li, A. G., L. G. Piluso, X. Cai, G. Wei, W. R. Sellers, and X. Liu. 2006. Mechanistic insights into maintenance of high p53 acetylation by PTEN. Mol. Cell 23:575–587.
  • Li, G. H., H. Wei, Z. T. Chen, S. Q. Lv, C. L. Yin, and D. L. Wang. 2009. STAT3 silencing with lentivirus inhibits growth and induces apoptosis and differentiation of U251 cells. J. Neurooncol. 91:165–174.
  • Lin, J., X. Jin, K. Rothman, H. J. Lin, H. Tang, and W. Burke. 2002. Modulation of signal transducer and activator of transcription 3 activities by p53 tumor suppressor in breast cancer cells. Cancer Res. 62:376–380.
  • Lin, J., H. Tang, X. Jin, G. Jia, and J. T. Hsieh. 2002. p53 regulates Stat3 phosphorylation and DNA binding activity in human prostate cancer cells expressing constitutively active Stat3. Oncogene 21:3082–3088.
  • Linder, S. 2007. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17:107–117.
  • Lund, T. C., C. Coleman, E. Horvath, B. M. Sefton, R. Jove, M. M. Medveczky, and P. G. Medveczky. 1999. The Src-family kinase Lck can induce STAT3 phosphorylation and DNA binding activity. Cell. Signal. 11:789–796.
  • Marx, J. 2006. Cell biology—podosomes and invadopodia help mobile cells step lively. Science 312:1868–1869.
  • Meek, D. W. 2009. Tumour suppression by p53: a role for the DNA damage response? Nat. Rev. Cancer 9:714–723.
  • Morton, J. P., D. S. Klimstra, M. E. Mongeau, and B. C. Lewis. 2008. Trp53 deletion stimulates the formation of metastatic pancreatic tumors. Am. J. Pathol. 172:1081–1087.
  • Moskovits, N., A. Kalinkovich, J. Bar, T. Lapidot, and M. Oren. 2006. p53 attenuates cancer cell migration and invasion through repression of SDF-1/CXCL12 expression in stromal fibroblasts. Cancer Res. 66:10671–10676.
  • Mukhopadhyay, U. K., R. Eves, L. Jia, P. Mooney, and A. S. Mak. 2009. p53 suppresses Src-induced podosome and rosette formation and cellular invasiveness through the upregulation of caldesmon. Mol. Cell. Biol. 29:3088–3098.
  • Muller, P. A., P. T. Caswell, B. Doyle, M. P. Iwanicki, E. H. Tan, S. Karim, N. Lukashchuk, D. A. Gillespie, R. L. Ludwig, P. Gosselin, A. Cromer, J. S. Brugge, O. J. Sansom, J. C. Norman, and K. H. Vousden. 2009. Mutant p53 drives invasion by promoting integrin recycling. Cell 139:1327–1341.
  • Myers, M. P., I. Pass, I. H. Batty, J. Van der Kaay, J. P. Stolarov, B. A. Hemmings, M. H. Wigler, C. P. Downes, and N. K. Tonks. 1998. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc. Natl. Acad. Sci. U. S. A. 95:13513–13518.
  • Myers, M. P., J. P. Stolarov, C. Eng., J. Li, S. I. Wang, M. H. Wigler, R. Parsons, and N. K. Tonks. 1997. P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc. Natl. Acad. Sci. U. S. A. 94:9052–9057.
  • Ng, D. C., B. H. Lin, C. P. Lim, G. Huang, T. Zhang, V. Poli, and X. Cao. 2006. Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin. J. Cell Biol. 172:245–257.
  • Niu, G., T. Bowman, M. Huang, S. Shivers, D. Reintgen, A. Daud, A. Chang, A. Kraker, R. Jove, and H. Yu. 2002. Roles of activated Src and Stat3 signaling in melanoma tumor cell growth. Oncogene 21:7001–7010.
  • Niu, G., K. L. Wright, Y. Ma, G. M. Wright, M. Huang, R. Irby, J. Briggs, J. Karras, W. D. Cress, D. Pardoll, R. Jove, J. Chen, and H. Yu. 2005. Role of Stat3 in regulating p53 expression and function. Mol. Cell. Biol. 25:7432–7440.
  • Oikawa, T., T. Itoh, and T. Takenawa. 2008. Sequential signals toward podosome formation in NIH-src cells. J. Cell Biol. 182:157–169.
  • Paddison, P. J., M. Cleary, J. M. Silva, K. Chang, N. Sheth, R. Sachidanandam, and G. J. Hannon. 2004. Cloning of short hairpin RNAs for gene knockdown in mammalian cells. Nat. Methods 1:163–167.
  • Poincloux, R., C. Cougoule, T. Daubon, I. Maridonneau-Parini, and V. Le Cabec. 2007. Tyrosine-phosphorylated STAT5 accumulates on podosomes in Hck-transformed fibroblasts and chronic myeloid leukemia cells. J. Cell. Physiol. 213:212–220.
  • Raftopoulou, M., S. Etienne-Manneville, A. Self, S. Nicholls, and A. Hall. 2004. Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science 303:1179–1181.
  • Salmena, L., A. Carracedo, and P. P. Pandolfi. 2008. Tenets of PTEN tumor suppression. Cell 133:403–414.
  • Schreiner, S. J., A. P. Schiavone, and T. E. Smithgall. 2002. Activation of STAT3 by the Src family kinase Hck requires a functional SH3 domain. J. Biol. Chem. 277:45680–45687.
  • Sharpless, N. E., and R. A. DePinho. 2002. p53: good cop/bad cop. Cell 110:9–12.
  • Stambolic, V., D. MacPherson, D. Sas, Y. Lin, B. Snow, Y. Jang, S. Benchimol, and T. W. Mak. 2001. Regulation of PTEN transcription by p53. Mol. Cell 8:317–325.
  • Stiles, B. L. 2009. Phosphatase and tensin homologue deleted on chromosome 10: extending its PTENtacles. Int. J. Biochem. Cell Biol. 41:757–761.
  • Stylli, S. S., A. H. Kaye, and P. Lock. 2008. Invadopodia: at the cutting edge of tumour invasion. J. Clin. Neurosci. 15:725–737.
  • Sun, S., and B. M. Steinberg. 2002. PTEN is a negative regulator of STAT3 activation in human papillomavirus-infected cells. J. Gen. Virol. 83:1651–1658.
  • Vogelstein, B., D. Lane, and A. J. Levine. 2000. Surfing the p53 network. Nature 408:307–310.
  • Wang, S. P., W. L. Wang, Y. L. Chang, C. T. Wu, Y. C. Chao, S. H. Kao, A. Yuan, C. W. Lin, S. C. Yang, W. K. Chan, K. C. Li, T. M. Hong, and P. C. Yang. 2009. p53 controls cancer cell invasion by inducing the MDM2-mediated degradation of Slug. Nat. Cell Biol. 11:694–704.
  • Weaver, A. M. 2006. Invadopodia: specialized cell structures for cancer invasion. Clin. Exp. Metastasis 23:97–105.
  • Webb, B. A., L. Jia, R. Eves, and A. S. Mak. 2007. Dissecting the functional domain requirements of cortactin in invadopodia formation. Eur. J. Cell Biol. 86:189–206.
  • Xia, M., and H. Land. 2007. Tumor suppressor p53 restricts Ras stimulation of RhoA and cancer cell motility. Nat. Struct. Mol. Biol. 14:215–223.
  • Yeatman, T. J. 2004. A renaissance for SRC. Nat. Rev. Cancer 4:470–480.
  • Yoshio, T., T. Morita, Y. Kimura, M. Tsujii, N. Hayashi, and K. Sobue. 2007. Caldesmon suppresses cancer cell invasion by regulating podosome/invadopodium formation. FEBS Lett. 581:3777–3782.
  • Yu, C. L., D. J. Meyer, G. S. Campbell, A. C. Larner, C. Carter-Su, J. Schwartz, and R. Jove. 1995. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269:81–83.
  • Zbuk, K. M., and C. Eng. 2007. Cancer phenomics: RET and PTEN as illustrative models. Nat. Rev. Cancer 7:35–45.
  • Zhou, J., J. Wulfkuhle, H. Zhang, P. Gu, Y. Yang, J. Deng, J. B. Margolick, L. A. Liotta, E. Petricoin III, and Y. Zhang. 2007. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc. Natl. Acad. Sci. U. S. A. 104:16158–16163.
  • Zhou, S. T., B. A. Webb, R. Eves, and A. S. Mak. 2006. Effects of tyrosine phosphorylation of cortactin on podosome formation in A7r5 vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 290:C463–C471.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.