Knockdown of CD44 inhibits the invasion and metastasis of hepatocellular carcinoma both in vitro and in vivo by reversing epithelial-mesenchymal transition

Oncotarget

Volumn 6, Issue 10, 2015, Pages 7828-7837

  Gao, Yuan ^a   Ruan, Bai ^a   Liu, Weihui ^b   Wang, Jianlin ^a   Yang, Xisheng ^a   Zhang, Zhuochao ^a   Li, Xia ^a   Duan, Juanli ^a   Zhang, Fuqing ^a   Ding, Rui ^a   Tao, Kaishan ^a   Dou, Kefeng ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b CHENGDU MILITARY GENERAL HOSPITAL   (China)

Author keywords

CD44; Epithelial mesenchymal transition; Hepatocellular carcinoma; Snail

Indexed keywords

HERMES ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SNAIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; METASTASIS; MOUSE; NONHUMAN; TUMOR INVASION; ANIMAL; BAGG ALBINO MOUSE; GENETICS; HEP-G2 CELL LINE; LIVER TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIGENS, CD44; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HETEROGRAFTS; HUMANS; LIVER NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS;

EID: 84928390998     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3488     Document Type: Article

References (49)

1. Forner A, Llovet JM and Bruix J. Hepatocellular carcinoma. Lancet. 2012; 379(9822):1245-1255.
2. David F, Jacques F. The global and regional burden of cancer//Bernard WS, Christopher PD. World Cancer Report 2014. Paris: International Agency for Research on Cancer, 2014: 16-53.
3. Poon RT, Ng IO, Fan ST, Lai EC, Lo CM, Liu CL and Wong J. Clinicopathologic features of long-term survivors and disease-free survivors after resection of hepatocellular carcinoma: a study of a prospective cohort. J Clin Oncol. 2001; 19:3037-3044.
4. Chaffer CL, Marjanovic ND, Lee T, Bell G, Kleer CG, Reinhardt F, D'Alessio AC, Young RA and Weinberg RA. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell. 2013; 154:61-74.
5. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, Reichert M, Beatty GL, Rustgi AK, Vonderheide RH, Leach SD and Stanger BZ. EMT and dissemination precede pancreatic tumor formation. Cell. 2012; 148:349-361.
6. Gos M, Miloszewska J and Przybyszewska M. [Epithelialmesenchymal transition in cancer progression]. Postepy Biochem. 2009; 55:121-128.
7. Huang RY, Guilford P and Thiery JP. Early events in cell adhesion and polarity during epithelial-mesenchymal transition. J Cell Sci. 2012; 125:4417-4422.
8. Lamouille S, Xu J and Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Bio. 2014; 15:178-196.
9. Puisieux A, Brabletz T and Caramel J. Oncogenic roles of EMT-inducing transcription factors. Nat Cell Biol. 2014; 16:488-494.
10. Briegel KJ. Embryonic transcription factors in human breast cancer. Iubmb Life. 2006; 58:123-132.
11. Bhat-Nakshatri P, Appaiah H, Ballas C, Pick-Franke P, Goulet RJ, Badve S, Srour EF and Nakshatri H. SLUG/SNAI2 and tumor necrosis factor generate breast cells with CD44+/CD24-phenotype. Bmc Cancer. 2010; 10:411.
12. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J and Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133:704-715.
13. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S and Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One. 2008; 3:e2888.
14. Hiraga T, Ito S and Nakamura H. Cancer stem-like cell marker CD44 promotes bone metastases by enhancing tumorigenicity, cell motility, and hyaluronan production. Cancer Res. 2013; 73:4112-4122.
15. Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer. 2011; 11:254-267.
16. Su YJ, Lai HM, Chang YW, Chen GY and Lee JL. Direct reprogramming of stem cell properties in colon cancer cells by CD44. Embo J. 2011; 30:3186-3199.
17. Kimura Y, Goi T, Nakazawa T, Hirono Y, Katayama K, Urano T and Yamaguchi A. CD44variant exon 9 plays an important role in colon cancer initiating cells. Oncotarget. 2013; 4:785-791.
18. Wang D, Lu P, Zhang H, Luo M, Zhang X, Wei X, Gao J, Zhao Z and Liu C. Oct-4 and Nanog promote the epithelialmesenchymal transition of breast cancer stem cells and are associated with poor prognosis in breast cancer patients. Oncotarget. 2014; 5:10803-10815.
19. Tovuu LO, Imura S, Utsunomiya T, Morine Y, Ikemoto T, Arakawa Y, Mori H, Hanaoka J, Kanamoto M, Sugimoto K, Iwahashi S, Saito Y, Yamada S, Asanoma M, Miyake H and Shimada M. Role of CD44 expression in non-tumor tissue on intrahepatic recurrence of hepatocellular carcinoma. Int J Clin Oncol. 2013; 18:651-656.
20. Endo K and Terada T. Protein expression of CD44 (standard and variant isoforms) in hepatocellular carcinoma: relationships with tumor grade, clinicopathologic parameters, p53 expression, and patient survival. J Hepatol. 2000; 32:78-84.
21. Cufi S, Corominas-Faja B, Vazquez-Martin A, Oliveras-Ferraros C, Dorca J, Bosch-Barrera J, Martin-Castillo B and Menendez JA. Metformin-induced preferential killing of breast cancer initiating CD44+CD24-/low cells is sufficient to overcome primary resistance to trastuzumab in HER2+ human breast cancer xenografts. Oncotarget. 2012; 3:395-398.
22. Dalerba P, Cho RW and Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med. 2007; 58:267-284.
23. Orian-Rousseau V and Sleeman J. CD44 is a multidomain signaling platform that integrates extracellular matrix cues with growth factor and cytokine signals. Adv Cancer Res. 2014; 123:231-254.
24. Zhou L, Wang DS, Li QJ, Sun W, Zhang Y and Dou KF. The down-regulation of Notch1 inhibits the invasion and migration of hepatocellular carcinoma cells by inactivating the cyclooxygenase-2/Snail/E-cadherin pathway in vitro. Dig Dis Sci. 2013; 58:1016-1025.
25. Yilmaz M and Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009; 28(1-2):15-33.
26. Polyak K and Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009; 9:265-273.
27. Eger A, Aigner K, Sonderegger S, Dampier B, Oehler S, Schreiber M, Berx G, Cano A, Beug H and Foisner R. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene. 2005; 24:2375-2385.
28. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A and Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004; 117:927-939.
29. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J and Garcia DHA. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2000; 2:84-89.
30. Sundaram MV. Canonical RTK-Ras-ERK signaling and related alternative pathways. WormBook. 2013:1-38.
31. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EWT, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A, Stivala F, Libra M, Basecke J, Evangelisti C, Martelli AM and Franklin RA. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2007; 1773:1263-1284.
32. Hsu YL, Hou MF, Kuo PL, Huang YF and Tsai EM. Breast tumor-associated osteoblast-derived CXCL5 increases cancer progression by ERK/MSK1/Elk-1/snail signaling pathway. Oncogene. 2013; 32:4436-4447.
33. Makrodouli E, Oikonomou E, Koc M, Andera L, Sasazuki T, Shirasawa S and Pintzas A. BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: a comparative study. Mol Cancer. 2011; 10:118.
34. Kong C, Wang C, Wang L, Ma M, Niu C, Sun X, Du J, Dong Z, Zhu S, Lu J and Huang B. NEDD9 is a positive regulator of epithelial-mesenchymal transition and promotes invasion in aggressive breast cancer. PLoS One. 2011; 6:e22666.
35. Barbera MJ, Puig I, Dominguez D, Julien-Grille S, Guaita-Esteruelas S, Peiro S, Baulida J, Franci C, Dedhar S, Larue L and Garcia DHA. Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells. Oncogene. 2004; 23:7345-7354.
36. Chaffer CL and Weinberg RA. A Perspective on Cancer Cell Metastasis. Science. 2011; 331:1559-1564.
37. Hou Y, Zou Q, Ge R, Shen F and Wang Y. The critical role of CD133(+)CD44(+/high) tumor cells in hematogenous metastasis of liver cancers. Cell Res. 2012; 22:259-272.
38. Blick T, Hugo H, Widodo E, Waltham M, Pinto C, Mani SA, Weinberg RA, Neve RM, Lenburg ME and Thompson EW. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia. 2010; 15:235-252.
39. Shang Z, Cai Q, Zhang M, Zhu S, Ma Y, Sun L, Jiang N, Tian J, Niu X, Chen J, Sun Y and Niu Y. A switch from CD44+ cell to EMT cell drives the metastasis of prostate cancer. Oncotarget. 2015; 6:1202-1216.
40. Liu J, Xiao Z, Wong SK, Tin VP, Ho KY, Wang J, Sham MH and Wong MP. Lung cancer tumorigenicity and drug resistance are maintained through ALDH(hi)CD44(hi) tumor initiating cells. Oncotarget. 2013; 4:1698-1711.
41. Takahashi E, Nagano O, Ishimoto T, Yae T, Suzuki Y, Shinoda T, Nakamura S, Niwa S, Ikeda S, Koga H, Tanihara H and Saya H. Tumor necrosis factor-alpha regulates transforming growth factor-beta-dependent epithelialmesenchymal transition by promoting hyaluronan-CD44-moesin interaction. J Biol Chem. 2010; 285:4060-4073.
42. Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, Watanabe M, Beppu T, Tamada M, Nagano O, Saya H and Baba H. CD44s Regulates the TGF-Mediated Mesenchymal Phenotype and Is Associated with Poor Prognosis in Patients with Hepatocellular Carcinoma. Cancer Res. 2012; 72:3414-3423.
43. Yang MH, Chen CL, Chau GY, Chiou SH, Su CW, Chou TY, Peng WL and Wu JC. Comprehensive analysis of the independent effect of twist and snail in promoting metastasis of hepatocellular carcinoma. Hepatology. 2009; 50:1464-1474.
44. Katsuno Y, Lamouille S and Derynck R. TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol. 2013; 25:76-84.
45. Zhang Q, Yu N and Lee C. Mysteries of TGF-β Paradox in Benign and Malignant Cells. Frontiers in Oncology. 2014; 4:94.
46. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P and Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev. 2002; 16:3074-3086.
47. Orian-Rousseau V, Morrison H, Matzke A, Kastilan T, Pace G, Herrlich P and Ponta H. Hepatocyte growth factorinduced Ras activation requires ERM proteins linked to both CD44v6 and F-actin. Mol Biol Cell. 2007; 18:76-83.
48. Bourguignon LY, Gilad E, Rothman K and Peyrollier K. Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression. J Biol Chem. 2005; 280:11961-11972.
49. Lee JL, Wang MJ and Chen JY. Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. J Cell Biol. 2009; 185:949-957.