The CD44s splice isoform is a central mediator for invadopodia activity

Journal of Cell Science

Volumn 129, Issue 7, 2016, Pages 1355-1365

  Zhao, Pu ^a,c   Xu, Yilin ^a   Wei, Yong ^b   Qiu, Qiong ^b   Chew, Teng Leong ^a,d   Kang, Yibin ^b   Cheng, Chonghui ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c NORTHEASTERN UNIVERSITY   (China)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Breast cancer; CD44s; Invadopodia; Metastasis; Splice isoform

Indexed keywords

CORTACTIN; HERMES ANTIGEN; SHORT HAIRPIN RNA; CD44 PROTEIN, HUMAN; ISOPROTEIN; MATRIX METALLOPROTEINASE 14; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER; CONTROLLED STUDY; HUMAN; HUMAN CELL; METASTASIS; PODOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA SPLICING; ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; FEMALE; GENETICS; LUNG TUMOR; MCF-7 CELL LINE; METABOLISM; MOUSE; NIH 3T3 CELL LINE; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; SECONDARY; TUMOR CELL LINE; TUMOR INVASION; XENOGRAFT;

ANIMALS; ANTIGENS, CD44; BREAST NEOPLASMS; CELL LINE, TUMOR; CORTACTIN; FEMALE; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 14; MCF-7 CELLS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NIH 3T3 CELLS; PHOSPHORYLATION; PODOSOMES; PROTEIN ISOFORMS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSPLANTATION, HETEROLOGOUS;

EID: 84964063270     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.171959     Document Type: Article

References (46)

1. Artym, V. V., Zhang, Y., Seillier-Moiseiwitsch, F., Yamada, K. M. and Mueller, S. C. (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.
2. Bourguignon, L. Y. W., Zhu, H., Shao, L. and Chen, Y.-W. (2001). CD44 interaction with c-Src kinase promotes cortactin-mediated cytoskeleton function and hyaluronic acid-dependent ovarian tumor cell migration. J. Biol. Chem. 276, 7327-7336.
3. Boyle, S. N., Michaud, G. A., Schweitzer, B., Predki, P. F. and Koleske, A. J. (2007). A critical role for cortactin phosphorylation by Abl-family kinases in PDGF-induced dorsal-wave formation. Curr. Biol. 17, 445-451.
4. Brown, R. L., Reinke, L. M., Damerow, M. S., Perez, D., Chodosh, L. A., Yang, J. and Cheng, C. (2011). CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J. Clin. Invest. 121, 1064-1074.
5. Chabadel, A., Banon-Rodriguez, I., Cluet, D., Rudkin, B. B., Wehrle-Haller, B., Genot, E., Jurdic, P., Anton, I. M. and Saltel, F. (2007). CD44 and beta3 integrin organize two functionally distinct actin-based domains in osteoclasts. Mol. Biol. Cell 18, 4899-4910.
6. Chaffer, C. L. and Weinberg, R. A. (2011). A perspective on cancer cell metastasis. Science 331, 1559-1564.
7. Chakrabarti, R., Hwang, J., Andres Blanco, M., Wei, Y., Lukačišin, M., Romano, R.-A., Smalley, K., Liu, S., Yang, Q., Ibrahim, T. et al. (2012). Elf5 inhibits the epithelial-mesenchymal transition in mammary gland development and breast cancer metastasis by transcriptionally repressing Snail2. Nat. Cell Biol. 14, 1212-1222.
8. Courtneidge, S. A., Azucena, E. F., Pass, I., Seals, D. F. and Tesfay, L. (2005). The SRC substrate Tks5, podosomes (invadopodia), and cancer cell invasion. Cold Spring Harb. Symp. Quant. Biol. 70, 167-171.
9. DesMarais, V., Macaluso, F., Condeelis, J. and Bailly, M. (2004). Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J. Cell Sci. 117, 3499-3510.
10. Diaz, L. K., Zhou, X., Wright, E. T., Cristofanilli, M., Smith, T., Yang, Y., Sneige, N., Sahin, A. and Gilcrease, M. Z. (2005). CD44 expression is associated with increased survival in node-negative invasive breast carcinoma. Clin. Cancer Res. 11, 3309-3314.
11. Eckert, M. A., Lwin, T. M., Chang, A. T., Kim, J., Danis, E., Ohno-Machado, L. and Yang, J. (2011). Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19, 372-386.
12. Grass, G. D., Tolliver, L. B., Bratoeva, M. and Toole, B. P. (2013). CD147, CD44, and the epidermal growth factor receptor (EGFR) signaling pathway cooperate to regulate breast epithelial cell invasiveness. J. Biol. Chem. 288, 26089-26104.
13. Head, J. A., Jiang, D., Li, M., Zorn, L. J., Schaefer, E. M., Parsons, J. T. and Weed, S. A. (2003). Cortactin tyrosine phosphorylation requires Rac1 activity and association with the cortical actin cytoskeleton. Mol. Biol. Cell 14, 3216-3229.
14. Hiraga, T., Ito, S. and Nakamura, H. (2013). Cancer stem-like cell marker CD44 promotes bone metastases by enhancing tumorigenicity, cell motility, and hyaluronan production. Cancer Res. 73, 4112-4122.
15. Hotary, K., Li, X.-Y., Allen, E., Stevens, S. L. and Weiss, S. J. (2006). A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 20, 2673-2686.
16. Huang, C., Liu, J., Haudenschild, C. C. and Zhan, X. (1998). The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J. Biol. Chem. 273, 25770-25776.
17. Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H. and Seiki, M. (2001). Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153, 893-904.
18. Kanner, S. B., Reynolds, A. B., Vines, R. R. and Parsons, J. T. (1990). Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc. Natl. Acad. Sci. USA 87, 3328-3332.
19. Li, C.-M., Chen, G., Dayton, T. L., Kim-Kiselak, C., Hoersch, S., Whittaker, C. A., Bronson, R. T., Beer, D. G., Winslow, M. M. and Jacks, T. (2013). Differential Tks5 isoform expression contributes to metastatic invasion of lung adenocarcinoma. Genes Dev. 27, 1557-1567.
20. Liu, S. and Cheng, C. (2013). Alternative RNA splicing and cancer. Wiley Interdiscip. Rev. RNA 4, 547-566.
21. Liu, Y.-J., Yan, P.-S., Li, J. and Jia, J.-F. (2005). Expression and significance of CD44s, CD44v6, and nm23 mRNA in human cancer. World J. Gastroenterol. 11, 6601-6606.
22. Lou, W., Krill, D., Dhir, R., Becich, M. J., Dong, J. T., Frierson, H. F., Jr, Isaacs, W. B., Isaacs, J. T. and Gao, A. C. (1999). Methylation of the CD44 metastasis suppressor gene in human prostate cancer. Cancer Res. 59, 2329-2331.
23. Mader, C. C., Oser, M., Magalhaes, M. A. O., Bravo-Cordero, J. J., Condeelis, J., Koleske, A. J. and Gil-Henn, H. (2011). An EGFR-Src-Arg-cortactin pathway mediates functional maturation of invadopodia and breast cancer cell invasion. Cancer Res. 71, 1730-1741.
24. Monteiro, P., Rosse, C., Castro-Castro, A., Irondelle, M., Lagoutte, E., Paul-Gilloteaux, P., Desnos, C., Formstecher, E., Darchen, F., Perrais, D. et al. (2013). Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J. Cell Biol. 203, 1063-1079.
25. Mori, H., Tomari, T., Koshikawa, N., Kajita, M., Itoh, Y., Sato, H., Tojo, H., Yana, I. and Seiki, M. (2002). CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J. 21, 3949-3959.
26. Murphy, D. A. and Courtneidge, S. A. (2011). The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426.
27. Oser, M., Yamaguchi, H., Mader, C. C., Bravo-Cordero, J. J., Arias, M., Chen, X., DesMarais, V., van Rheenen, J., Koleske, A. J. and Condeelis, J. (2009). Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol. 186, 571-587.
28. Pan, Q., Shai, O., Lee, L. J., Frey, B. J. and Blencowe, B. J. (2008). Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 40, 1413-1415.
29. Paz, H., Pathak, N. and Yang, J. (2013). Invading one step at a time: the role of invadopodia in tumor metastasis. Oncogene. 33, 4193-4202.
30. Ponta, H., Sherman, L. and Herrlich, P. A. (2003). CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4, 33-45.
31. Rajadurai, C. V., Havrylov, S., Zaoui, K., Vaillancourt, R., Stuible, M., Naujokas, M., Zuo, D., Tremblay, M. L. and Park, M. (2012). Met receptor tyrosine kinase signals through a cortactin-Gab1 scaffold complex, to mediate invadopodia. J. Cell Sci. 125, 2940-2953.
32. Seals, D. F., Azucena, E. F., Jr., Pass, I., Tesfay, L., Gordon, R., Woodrow, M., Resau, J. H. and Courtneidge, S. A. (2005). The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 7, 155-165.
33. Steffen, A., Le Dez, G., Poincloux, R., Recchi, C., Nassoy, P., Rottner, K., Galli, T. and Chavrier, P. (2008). MT1-MMP-dependent invasion is regulated by TIVAMP/VAMP7. Curr. Biol. 18, 926-931.
34. Suenaga, N., Mori, H., Itoh, Y. and Seiki, M. (2005). CD44 binding through the hemopexin-like domain is critical for its shedding by membrane-type 1 matrix metalloproteinase. Oncogene 24, 859-868.
35. Tehrani, S., Tomasevic, N., Weed, S., Sakowicz, R. and Cooper, J. A. (2007). Src phosphorylation of cortactin enhances actin assembly. Proc. Natl. Acad. Sci. USA 104, 11933-11938.
36. Thiery, J. P. and Sleeman, J. P. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142.
37. Vikesaa, J., Hansen, T. V., Jønson, L., Borup, R., Wewer, U. M., Christiansen, J. and Nielsen, F. C. (2006). RNA-binding IMPs promote cell adhesion and invadopodia formation. EMBO J. 25, 1456-1468.
38. Wang, E. T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P. and Burge, C. B. (2008). Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476.
39. Weaver, A. M. (2008). Cortactin in tumor invasiveness. Cancer Lett. 265, 157-166.
40. Weed, S. A. and Parsons, J. T. (2001). Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20, 6418-6434.
41. Wiesner, C., Faix, J., Himmel, M., Bentzien, F. and Linder, S. (2010). KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 116, 1559-1569.
42. Woodson, K., O'Reilly, K. J., Ward, D. E., Walter, J., Hanson, J., Walk, E. L. and Tangrea, J. A. (2006). CD44 and PTGS2 methylation are independent prognostic markers for biochemical recurrence among prostate cancer patients with clinically localized disease. Epigenetics 1, 183-186.
43. Xu, Y., Gao, X. D., Lee, J.-H., Huang, H., Tan, H., Ahn, J., Reinke, L. M., Peter, M. E., Feng, Y., Gius, D. et al. (2014). Cell type-restricted activity of hnRNPM promotes breast cancer metastasis via regulating alternative splicing. Genes Dev. 28, 1191-1203.
44. Yamaguchi, H., Lorenz, M., Kempiak, S., Sarmiento, C., Coniglio, S., Symons, M., Segall, J., Eddy, R., Miki, H., Takenawa, T. et al. (2005). Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 168, 441-452.
45. Yang, J. and Weinberg, R. A. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829.
46. Zarrabi, K., Dufour, A., Li, J., Kuscu, C., Pulkoski-Gross, A., Zhi, J., Hu, Y., Sampson, N. S., Zucker, S. and Cao, J. (2011). Inhibition of matrix metalloproteinase 14 (MMP-14)-mediated cancer cell migration. J. Biol. Chem. 286, 33167-33177.