Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell

Nature Communications

Volumn 3, Issue , 2012, Pages

  Yae, Toshifumi ^a,b   Tsuchihashi, Kenji ^a   Ishimoto, Takatsugu ^a   Motohara, Takeshi ^a   Yoshikawa, Momoko ^a   Yoshida, Go J ^a   Wada, Takeyuki ^a   Masuko, Takashi ^c   Mogushi, Kaoru ^d   Tanaka, Hiroshi ^d   Osawa, Tsuyoshi ^e   Kanki, Yasuharu ^e   Minami, Takashi ^e   Aburatani, Hiroyuki ^e   Ohmura, Mitsuyo ^a   Kubo, Akiko ^a   Suematsu, Makoto ^a,f   Takahashi, Kazuhisa ^b   Saya, Hideyuki ^a,f   Nagano, Osamu ^a  

^a KEIO UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY   (Japan)

^c KINKI UNIVERSITY   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD44V ANTIGEN; EPITHELIAL SPLICING REGULATORY PROTEIN 1; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; HERMES ANTIGEN; RNA BINDING PROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CELL; CANCER CELL; CANCER STEM CELL; CELL ISOLATION; CELL SUBPOPULATION; CELL SURFACE; CONTROLLED STUDY; EMBRYONIC STEM CELL; EPIGENETICS; FEMALE; FIBROBLAST; LUNG METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TUMOR VOLUME; ANIMAL; BAGG ALBINO MOUSE; BREAST TUMOR; CHROMATIN IMMUNOPRECIPITATION; FLOW CYTOMETRY; GENETICS; IMMUNOBLOTTING; LUNG TUMOR; METABOLISM; METASTASIS; TUMOR CELL LINE;

MUS;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, CD44; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; FEMALE; FLOW CYTOMETRY; IMMUNOBLOTTING; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84863321158     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1892     Document Type: Article

References (55)

1. Weigelt, B., Peterse, J. L. & van 't Veer, L. J. Breast cancer metastasis: markers and models. Nat. Rev. Cancer 5, 591-602 (2005). (Pubitemid 41081385)
2. Fidler, I. J. The biology of cancer metastasis. Semin. Cancer Biol. 21, 71 (2011).
3. Mehlen, P. & Puisieux, A. Metastasis: a question of life or death. Nat. Rev. Cancer 6, 449-458 (2006).
4. Liu, H. et al. Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models. Proc. Natl Acad. Sci. USA 107, 18115-18120 (2010).
5. Chaffer, C. L. & Weinberg, R. A. A perspective on cancer cell metastasis. Science 331, 1559-1564 (2011).
6. Croker, A. K. et al. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J. Cell. Mol. Med. 13, 2236-2252 (2009).
7. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983-3988 (2003). (Pubitemid 36418143)
8. Collins, A. T., Berry, P. A., Hyde, C., Stower, M. J. & Maitland, N. J. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65, 10946-10951 (2005). (Pubitemid 41713363)
9. Dalerba, P. et al. Phenotypic characterization of human colorectal cancer stem cells. Proc. Natl Acad. Sci. USA 104, 10158-10163 (2007). (Pubitemid 47175279)
10. Gunthert, U. et al. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65, 13-24 (1991). (Pubitemid 121001209)
11. Yu, Q., Toole, B. P. & Stamenkovic, I. Induction of apoptosis of metastatic mammary carcinoma cells in vivo by disruption of tumor cell surface CD44 function. J.Exp. Med. 186, 1985-1996 (1997). (Pubitemid 28013682)
12. Nagano, O. & Saya, H. Mechanism and biological significance of CD44 cleavage. Cancer Sci. 95, 930-935 (2004). (Pubitemid 40089583)
13. Ponta, H., Sherman, L. & Herrlich, P. A. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4, 33-45 (2003). (Pubitemid 36077255)
14. Warzecha, C. C., Sato, T. K., Nabet, B., Hogenesch, J. B. & Carstens, R. P. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol. Cell 33, 591-601 (2009).
15. Screaton, G. R., Bell, M. V., Bell, J. I. & Jackson, D. G. The identification of a new alternative exon with highly restricted tissue expression in transcripts encoding the mouse Pgp-1 (CD44) homing receptor. Comparison of all 10 variable exons between mouse, human, and rat. J. Biol. Chem. 268, 12235-12238 (1993). (Pubitemid 23182367)
16. Bennett, K. L. et al. CD44 isoforms containing exon V3 are responsible for the presentation of heparin-binding growth factor. J. Cell Biol. 128, 687-698 (1995).
17. Orian-Rousseau, V., Chen, L., Sleeman, J. P., Herrlich, P. & Ponta, H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev. 16, 3074-3086 (2002). (Pubitemid 35424194)
18. Ishimoto, T. et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19, 387-400 (2011).
19. Chiang, A. C. & Massague, J. Molecular basis of metastasis. N. Engl. J. Med. 359, 2814-2823 (2008).
20. Gupta, G. P. & Massague, J. Cancer metastasis: building a framework. Cell 127, 679-695 (2006). (Pubitemid 44781029)
21. Granot, Z. et al. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20, 300-314 (2011).
22. Sato, H. et al. Redox imbalance in cystine/glutamate transporter- deficient mice. J. Biol. Chem. 280, 37423-37429 (2005). (Pubitemid 41642349)
23. Huang, Y., Dai, Z., Barbacioru, C. & Sadee, W. Cystine-glutamate transporter SLC7A11 in cancer chemosensitivity and chemoresistance. Cancer Res. 65, 7446-7454 (2005). (Pubitemid 41161279)
24. Calvert, P., Yao, K. S., Hamilton, T. C. & O'Dwyer, P. J. Clinical studies of reversal of drug resistance based on glutathione. Chem. Biol. Interact. 111-112, 213-224 (1998). (Pubitemid 28271946)
25. Goto, S. et al. Augmentation of transport for cisplatin-glutathione adduct in cisplatin-resistant cancer cells. Cancer Res. 55, 4297-4301 (1995).
26. Bannai, S. & Ishii, T. Transport of cystine and cysteine and cell growth in cultured human diploid fibroblasts: effect of glutamate and homocysteate. J. Cell. Physiol. 112, 265-272 (1982). (Pubitemid 12097396)
27. Lo, M., Wang, Y. Z. & Gout, P. W. The x(c)-cystine/glutamate antiporter: a potential target for therapy of cancer and other diseases. J. Cell. Physiol. 215, 593-602 (2008). (Pubitemid 351632680)
28. Heppner, G. H., Miller, F. R. & Shekhar, P. M. Nontransgenic models of breast cancer. Breast Cancer Res. 2, 331-334 (2000). (Pubitemid 32223615)
29. Ishimoto, T. et al. CD44+ slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci. 101, 673-678 (2010).
30. Motohara, T. et al. Transient depletion of p53 followed by transduction of c-Myc and K-Ras converts ovarian stem-like cells into tumor-initiating cells. Carcinogenesis 32, 1597-1606 (2011).
31. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005). (Pubitemid 41528093)
32. Ben-Porath, I. et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40, 499-507 (2008). (Pubitemid 351601215)
33. Pawitan, Y. et al. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res. 7, R953-R964 (2005).
34. Kubo, A. et al. Semi-quantitative analyses of metabolic systems of human colon cancer metastatic xenografts in livers of superimmunodeficient NOG mice. Anal. Bioanal. Chem. 400, 1895-1904 (2011).
35. Morikawa, T. et al. Hypoxic regulation of the cerebral microcirculation is mediated by a carbon monoxide-sensitive hydrogen sulfide pathway. Proc. Natl Acad. Sci. USA 109, 1293-1298 (2012).
36. Griffith, O. W. & Meister, A. Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 254, 7558-7560 (1979). (Pubitemid 10230219)
37. Diehn, M. et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458, 780-783 (2009).
38. Ginestier, C. et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1, 555-567 (2007). (Pubitemid 350056407)
39. Gout, P. W., Buckley, A. R., Simms, C. R. & Bruchovsky, N. Sulfasalazine, a potent suppressor of lymphoma growth by inhibition of the x(c)-cystine transporter: a new action for an old drug. Leukemia 15, 1633-1640 (2001). (Pubitemid 32994684)
40. Warzecha, C. C. et al. An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO J. 29, 3286-3300 (2010).
41. Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939 (2004). (Pubitemid 38798858)
42. Saint-Andre, V., Batsche, E., Rachez, C. & Muchardt, C. Histone H3 lysine 9 trimethylation and HP1gamma favor inclusion of alternative exons. Nat. Struct. Mol. Biol. 18, 337-344 (2011).
43. Wagner, E. J. & Carpenter, P. B. Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell. Biol. 13, 115-126 (2012).
44. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. & Young, R. A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 (2007). (Pubitemid 47031323)
45. Cao, R. et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043 (2002). (Pubitemid 35247314)
46. Klingbeil, P. et al. CD44 variant isoforms promote metastasis formation by a tumor cell-matrix cross-talk that supports adhesion and apoptosis resistance. Mol. Cancer Res. 7, 168-179 (2009).
47. Wallach-Dayan, S. B. et al. CD44-dependent lymphoma cell dissemination: a cell surface CD44 variant, rather than standard CD44, supports in vitro lymphoma cell rolling on hyaluronic acid substrate and its in vivo accumulation in the peripheral lymph nodes. J. Cell. Sci. 114, 3463-3477 (2001). (Pubitemid 33019763)
48. Pani, G., Galeotti, T. & Chiarugi, P. Metastasis: cancer cell's escape from oxidative stress. Cancer Metastasis Rev. 29, 351-378 (2010).
49. Chen, R. S. et al. Disruption of xCT inhibits cancer cell metastasis via the caveolin-1/beta-catenin pathway. Oncogene 28, 599-609 (2009).
50. Brown, R. L. et al. 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 (2011).
51. Sahin, M., Sahin, E., Gumuslu, S., Erdogan, A. & Gultekin, M. DNA methylation or histone modification status in metastasis and angiogenesis-related genes: a new hypothesis on usage of DNMT inhibitors and S-adenosylmethionine for genome stability. Cancer Metastasis Rev. 29, 655-676 (2010).
52. Ishimoto, T. et al. CD44+ slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci. 101, 673-678 (2010).
53. Nagano, O. et al. Cell-matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca2+ influx and PKC activation. J. Cell Biol. 165, 893-902 (2004). (Pubitemid 38821979)
54. Tozawa, H. et al. Genome-wide approaches reveal functional interleukin-4-inducible STAT6 binding to the vascular cell adhesion molecule 1 promoter. Mol. Cell. Biol. 31, 2196-2209 (2011).
55. Nicol, J. W., Helt, G. A., Blanchard, S. G. Jr., Raja, A. & Loraine, A. E. The integrated genome browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25, 2730-2731 (2009).