CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression

Journal of Clinical Investigation

Volumn 121, Issue 3, 2011, Pages 1064-1074

  Brown, Rhonda L ^a   Reinke, Lauren M ^a   Damerow, Marin S ^a   Perez, Denise ^b   Chodosh, Lewis A ^b   Yang, Jing ^c   Cheng, Chonghui ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD44V ANTIGEN; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER GROWTH; CONTROLLED STUDY; EPITHELIUM; FEMALE; HUMAN; HUMAN CELL; MESENCHYME; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ALTERNATIVE SPLICING; ANIMALS; ANTIGENS, CD44; BREAST NEOPLASMS; CADHERINS; CELL LINE; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; EPITHELIUM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MESODERM; MICE; PROTEIN ISOFORMS;

EID: 79952227361     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44540     Document Type: Article

References (44)

1. Moody SE, et al. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell. 2005;8(3):197-209.
2. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol. 2006;7(2):131-142. (Pubitemid 43278296)
3. Yang J, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927-939. (Pubitemid 38798858)
4. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008;14(6):818-829. (Pubitemid 351757205)
5. Bolos V, Peinado H, Perez-Moreno MA, Fraga MF, Esteller M, Cano A. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci. 2003; 116(pt 3):499-511. (Pubitemid 36231290)
6. Comijn J, et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell. 2001;7(6):1267-1278. (Pubitemid 32607360)
7. Eger A, et al. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene. 2005; 24(14):2375-2385. (Pubitemid 40546696)
8. Gregory PA, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008; 10(5):593-601. (Pubitemid 351627379)
9. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008;22(7):894-907. (Pubitemid 351482843)
10. Kong W, et al. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol. 2008;28(22):6773-6784.
11. Ma L, et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010;12(3):247-256.
12. Wang ET, et al. Alternative isoform regulation in human tissue transcriptomes. Nature. 2008; 456(7221):470-476. (Pubitemid 352759009)
13. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet. 2008;40(12):1413-1415.
14. Brickell PM, Latchman DS, Murphy D, Willison K, Rigby PW. Activation of a Qa/Tla class I major histocompatibility antigen gene is a general feature of oncogenesis in the mouse. Nature. 1983; 306(5945):756-760. (Pubitemid 14206038)
15. Sharma S, Lichtenstein A. Aberrant splicing of the E-cadherin transcript is a novel mechanism of gene silencing in chronic lymphocytic leukemia cells. Blood. 2009;114(19):4179-4185.
16. Shtivelman E, Lifshitz B, Gale RP, Roe BA, Canaani E. Alternative splicing of RNAs transcribed from the human abl gene and from the bcr-abl fused gene. Cell. 1986;47(2):277-284. (Pubitemid 17181545)
17. Venables JP. Unbalanced alternative splicing and its significance in cancer. Bioessays. 2006;28(4):378-386.
18. Cheng C, Yaffe MB, Sharp PA. A positive feedback loop couples Ras activation and CD44 alternative splicing. Genes Dev. 2006;20(13):1715-1720. (Pubitemid 43992879)
19. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P, Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev. 2002; 16(23):3074-3086. (Pubitemid 35424194)
20. Sherman LS, Rizvi TA, Karyala S, Ratner N. CD44 enhances neuregulin signaling by Schwann cells. J Cell Biol. 2000;150(5):1071-1084.
21. Bourguignon LY, Zhu H, Chu A, Iida N, Zhang L, Hung MC. Interaction between the adhesion receptor, CD44, and the oncogene product, p185HER2, promotes human ovarian tumor cell activation. J Biol Chem. 1997;272(44):27913- 27918. (Pubitemid 27473595)
22. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol. 2003;4(1):33-45. (Pubitemid 36077255)
23. Mani SA, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704-715. (Pubitemid 351636299)
24. Godar S, et al. Growth-inhibitory and tumor- suppressive functions of p53 depend on its repression of CD44 expression. Cell. 2008;134(1):62-73. (Pubitemid 351905743)
25. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell. 2009;33(5):591-601.
26. Grille SJ, et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 2003;63(9):2172-2178. (Pubitemid 36538623)
27. Larue L, Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3′ kinase/AKT pathways. Oncogene. 2005; 24(50):7443-7454. (Pubitemid 41637984)
28. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem. 2000; 275(47):36803-36810. (Pubitemid 32002090)
29. Julien S, et al. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene. 2007; 26(53):7445-7456. (Pubitemid 350158710)
30. Nath AK, Brown RM, Michaud M, Sierra-Honigmann MR, Snyder M, Madri JA. Leptin affects endocardial cushion formation by modulating EMT and migration via Akt signaling cascades. J Cell Biol. 2008;181(2):367-380. (Pubitemid 351574559)
31. Testa JR, Tsichlis PN. AKT signaling in normal and malignant cells. Oncogene. 2005;24(50):7391-7393. (Pubitemid 41637978)
32. Feng Q, et al. PDK1 regulates vascular remodeling and promotes epithelial-mesenchymal transition in cardiac development. Mol Cell Biol. 2010; 30(14):3711-3721.
33. Moody SE, et al. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell. 2002;2(6):451-461.
34. Batsche E, Yaniv M, Muchardt C. The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol. 2006;13(1):22-29. (Pubitemid 43049398)
35. Cheng C, Sharp PA. Regulation of CD44 alternative splicing by SRm160 and its potential role in tumor cell invasion. Mol Cell Biol. 2006;26(1):362-370.
36. Matter N, Herrlich P, Konig H. Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature. 2002;420(6916):691-695. (Pubitemid 36764503)
37. Barrallo-Gimeno A, Nieto MA. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 2005; 132(14):3151-3161. (Pubitemid 41167144)
38. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer. 2007; 7(6):415-428. (Pubitemid 46809165)
39. Protin U, Schweighoffer T, Jochum W, Hilberg F. CD44-deficient mice develop normally with changes in subpopulations and recirculation of lymphocyte subsets. J Immunol. 1999;163(9):4917-4923. (Pubitemid 29501257)
40. Schmits R, et al. CD44 regulates hematopoietic progenitor distribution, granuloma formation, and tumorigenicity. Blood. 1997;90(6):2217-2233. (Pubitemid 27392706)
41. Weber GF, Bronson RT, Ilagan J, Cantor H, Schmits R, Mak TW. Absence of the CD44 gene prevents sarcoma metastasis. Cancer Res. 2002;62(8):2281-2286. (Pubitemid 34411705)
42. Lopez JI, Camenisch TD, Stevens MV, Sands BJ, McDonald J, Schroeder JA. CD44 attenuates metastatic invasion during breast cancer progression. Cancer Res. 2005;65(15):6755-6763. (Pubitemid 41060713)
43. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell. 2009;136(4):777-793.
44. Srebrow A, Kornblihtt AR. The connection between splicing and cancer. J Cell Sci. 2006; 119(pt 13):2635-2641. (Pubitemid 44184000)