AF1q is a novel TCF7 co-factor which activates CD44 and promotes breast cancer metastasis

Oncotarget

Volumn 6, Issue 24, 2015, Pages 20697-20710

  Park, Jino ^a   Schlederer, Michaela ^b,c   Schreiber, Martin ^c   Ice, Ryan ^d,e   Merkel, Olaf ^f   Bilban, Martin ^c   Hofbauer, Sebastian ^c   Kim, Soojin ^a   Addison, Joseph ^d,e   Zou, Jie ^g   Ji, Chunyan ^g   Bunting, Silvia T ^h   Wang, Zhengqi ^h   Shoham, Menachem ⁱ   Huang, Gang ^j   Bago Horvath, Zsuzsanna ^c   Gibson, Laura F ^d   Rojanasakul, Yon ^d,e   Remick, Scot ^d   Ivanov, Alexey ^d,e   Pugacheva, Elena ^d,e   Bunting, Kevin D ^h   Moriggl, Richard ^b,k   Kenner, Lukas ^b,c,k   Tse, William ^a   more..

^a University of Louisville School of Medicine   (United States)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d WEST VIRGINIA UNIVERSITY   (United States)

^e WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g SHANDONG UNIVERSITY   (China)

^h EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^j CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^k UNIVERSITY OF VETERINARY MEDICINE   (Austria)

more..

Author keywords

AF1q; CD44; Metastasis; TCF7; Wnt

Indexed keywords

AF1Q PROTEIN; HERMES ANTIGEN; LYMPHOID ENHANCER FACTOR 1; MIXED LINEAGE LEUKEMIA PROTEIN; TRANSCRIPTION FACTOR 7; UNCLASSIFIED DRUG; CD44 PROTEIN, HUMAN; MLLT11 PROTEIN, HUMAN; ONCOPROTEIN; TCF7 PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOLOGICAL FUNCTIONS; BRAIN METASTASIS FREE SURVIVAL; BREAST CANCER; BREAST CELL; CANCER CELL LINE; CANCER GROWTH; CANCER PATIENT; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LIVER METASTASIS; LUNG METASTASIS; MAJOR CLINICAL STUDY; MAMMOSPHERE; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN BINDING; SURVIVAL; THERAPY RESISTANCE; TRANSCRIPTION INITIATION; TUMOR XENOGRAFT; WNT SIGNALING PATHWAY; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; BREAST TUMOR; CELL GROWTH; CELL MOTION; CHEMISTRY; GENETIC TRANSFECTION; GENETICS; METABOLISM; METASTASIS; MOLECULAR GENETICS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; TUMOR CELL LINE; TUMOR INVASION; XENOGRAFT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD44; BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; HETEROGRAFTS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PROTO-ONCOGENE PROTEINS; T CELL TRANSCRIPTION FACTOR 1; TRANSFECTION; WNT SIGNALING PATHWAY;

EID: 84940199679     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4136     Document Type: Article

References (47)

1. Tse W, Zhu W, Chen HS and Cohen A. A novel gene, AF1q, fused to MLL in t(1;11) (q21;q23), is specifically expressed in leukemic and immature hematopoietic cells. Blood. 1995; 85:650-656.
2. Xiong Y, Li Z, Ji M, Tan AC, Bemis J, Tse JV, Huang G, Park J, Ji C, Chen J, Bemis LT, Bunting KD and Tse W. MIR29B regulates expression of MLLT11 (AF1Q), an MLL fusion partner, and low MIR29B expression associates with adverse cytogenetics and poor overall survival in AML. British journal of haematology. 2011; 153:753-757.
3. Tiberio P, Cavadini E, Callari M, Daidone MG and Appierto V. AF1q: a novel mediator of basal and 4-HPR-induced apoptosis in ovarian cancer cells. PloS one. 2012; 7:e39968.
4. Co NN, Tsang WP, Tsang TY, Yeung CL, Yau PL, Kong SK and Kwok TT. AF1q enhancement of gamma irradiation-induced apoptosis by up-regulation of BAD expression via NF-kappaB in human squamous carcinoma A431 cells. Oncology reports. 2010; 24:547-554.
5. Jacques C, Baris O, Prunier-Mirebeau D, Savagner F, Rodien P, Rohmer V, Franc B, Guyetant S, Malthiery Y and Reynier P. Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. The Journal of clinical endocrinology and metabolism. 2005; 90:2314-2320.
6. Strunk CJ, Platzbecker U, Thiede C, Schaich M, Illmer T, Kang Z, Leahy P, Li C, Xie X, Laughlin MJ, Lazarus HM, Gerson SL, Bunting KD, Ehninger G and Tse W. Elevated AF1q expression is a poor prognostic marker for adult acute myeloid leukemia patients with normal cytogenetics. American journal of hematology. 2009; 84:308-309.
7. Tse W, Meshinchi S, Alonzo TA, Stirewalt DL, Gerbing RB, Woods WG, Appelbaum FR and Radich JP. Elevated expression of the AF1q gene, an MLL fusion partner, is an independent adverse prognostic factor in pediatric acute myeloid leukemia. Blood. 2004; 104:3058-3063.
8. Tse W, Deeg HJ, Stirewalt D, Appelbaum FR, Radich J and Gooley T. Increased AF1q gene expression in high-risk myelodysplastic syndrome. British journal of haematology. 2005; 128:218-220.
9. Parcelier A, Maharzi N, Delord M, Robledo-Sarmiento M, Nelson E, Belakhdar-Mekid H, Pla M, Kuranda K, Parietti V, Goodhardt M, Legrand N, Bernstein ID, Gluckman JC, Sigaux F and Canque B. AF1q/MLLT11 regulates the emergence of human prothymocytes through cooperative interaction with the Notch signaling pathway. Blood. 2011; 118:1784-1796.
10. Li DQ, Hou YF, Wu J, Chen Y, Lu JS, Di GH, Ou ZL, Shen ZZ, Ding J and Shao ZM. Gene expression profile analysis of an isogenic tumour metastasis model reveals a functional role for oncogene AF1Q in breast cancer metastasis. European journal of cancer (Oxford, England: 1990). 2006; 42:3274-3286.
11. Yang S, Dong Q, Yao M, Shi M, Ye J, Zhao L, Su J, Gu W, Xie W, Wang K, Du Y, Li Y and Huang Y. Establishment of an experimental human lung adenocarcinoma cell line SPC-A-1BM with high bone metastases potency by (99m)Tc-MDP bone scintigraphy. Nuclear medicine and biology. 2009; 36:313-321.
12. Chang XZ, Li DQ, Hou YF, Wu J, Lu JS, Di GH, Jin W, Ou ZL, Shen ZZ and Shao ZM. Identification of the functional role of AF1Q in the progression of breast cancer. Breast cancer research and treatment. 2008; 111:65-78.
13. Skotheim RI, Autio R, Lind GE, Kraggerud SM, Andrews PW, Monni O, Kallioniemi O and Lothe RA. Novel genomic aberrations in testicular germ cell tumors by array-CGH, and associated gene expression changes. Cellular oncology: the official journal of the International Society for Cellular Oncology. 2006; 28:315-326.
14. Co NN, Tsang WP, Wong TW, Cheung HH, Tsang TY, Kong SK and Kwok TT. Oncogene AF1q enhances doxorubicin-induced apoptosis through BAD-mediated mitochondrial apoptotic pathway. Molecular cancer therapeutics. 2008; 7:3160-3168.
15. Chou J, Lin JH, Brenot A, Kim JW, Provot S and Werb Z. GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nature cell biology. 2013; 15:201-213.
16. van de Wetering M, Oosterwegel M, Dooijes D and Clevers H. Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. The EMBO journal. 1991; 10:123-132.
17. Travis A, Amsterdam A, Belanger C and Grosschedl R. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function [corrected]. Genes & development. 1991; 5:880-894.
18. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F and Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nature medicine. 2006; 12:1167-1174.
19. Wielenga VJ, Smits R, Korinek V, Smit L, Kielman M, Fodde R, Clevers H and Pals ST. Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway. The American journal of pathology. 1999; 154:515-523.
20. Tiemessen MM, Baert MR, Schonewille T, Brugman MH, Famili F, Salvatori DC, Meijerink JP, Ozbek U, Clevers H, van Dongen JJ and Staal FJ. The nuclear effector of Wnt-signaling, Tcf1, functions as a T-cell-specific tumor suppressor for development of lymphomas. PLoS biology. 2012; 10:e1001430.
21. Montgomery N, Hill A, McFarlane S, Neisen J, O'Grady A, Conlon S, Jirstrom K, Kay EW and Waugh DJ. CD44 enhances invasion of basal-like breast cancer cells by upregulating serine protease and collagen-degrading enzymatic expression and activity. Breast cancer research: BCR. 2012; 14:R84.
22. Pelengaris S, Khan M and Evan G. c-MYC: more than just a matter of life and death. Nature reviews Cancer. 2002; 2:764-776.
23. Tanaka S, Akiyoshi T, Mori M, Wands JR and Sugimachi K. A novel frizzled gene identified in human esophageal carcinoma mediates APC/beta-catenin signals. Proceedings of the National Academy of Sciences of the United States of America. 1998; 95:10164-10169.
24. Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, Robker RL, Richards JS, McGinnis LK, Biggers JD, Eppig JJ, Bronson RT, Elledge SJ and Weinberg RA. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature. 1996; 384:470-474.
25. Sanyal S, Sandstrom DJ, Hoeffer CA and Ramaswami M. AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature. 2002; 416:870-874.
26. Lee JH and Welch DR. Identification of highly expressed genes in metastasis-suppressed chromosome 6/human malignant melanoma hybrid cells using subtractive hybridization and differential display. International journal of cancer Journal international du cancer. 1997; 71:1035-1044.
27. Lee JH and Welch DR. Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1. Cancer research. 1997; 57:2384-2387.
28. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature. 2001; 411:613-617.
29. Cho SG, Li D, Tan K, Siwko SK and Liu M. KiSS1 and its G-protein-coupled receptor GPR54 in cancer development and metastasis. Cancer metastasis reviews. 2012; 31:585-591.
30. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, French AD, Shah KV, Hewitt KJ, Rosenthal DT, Indig FE, Jiang Y, Nickoloff BJ, Taub DD, Trent JM, Moon RT, Bittner M, et al. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. The Journal of biological chemistry. 2007; 282:17259-17271.
31. Siegert JL, Rushton JJ, Sellers WR, Kaelin WG, Jr. and Robbins PD. Cyclin D1 suppresses retinoblastoma protein-mediated inhibition of TAFII250 kinase activity. Oncogene. 2000; 19:5703-5711.
32. Semenov MV, Tamai K, Brott BK, Kuhl M, Sokol S and He X. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Current biology: CB. 2001; 11:951-961.
33. Collins VP, Loeffler RK and Tivey H. Observations on growth rates of human tumors. The American journal of roentgenology, radium therapy, and nuclear medicine. 1956; 76:988-1000.
34. Stoecklein NH and Klein CA. Genetic disparity between primary tumours, disseminated tumour cells, and manifest metastasis. International journal of cancer Journal international du cancer. 2010; 126:589-598.
35. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
36. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nature reviews Cancer. 2003; 3:453-458.
37. Nguyen DX, Bos PD and Massague J. Metastasis: from dissemination to organ-specific colonization. Nature reviews Cancer. 2009; 9:274-284.
38. Barker N and Clevers H. Mining the Wnt pathway for cancer therapeutics. Nature reviews Drug discovery. 2006; 5:997-1014.
39. Walia V, Yu Y, Cao D, Sun M, McLean JR, Hollier BG, Cheng J, Mani SA, Rao K, Premkumar L and Elble RC. Loss of breast epithelial marker hCLCA2 promotes epithelial-to-mesenchymal transition and indicates higher risk of metastasis. Oncogene. 2012; 31:2237-2246.
40. 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.
41. Holden NS and Tacon CE. Principles and problems of the electrophoretic mobility shift assay. Journal of pharmacological and toxicological methods. 2011; 63:7-14.
42. Ozeki T, Takahashi Y, Kume T, Nakayama K, Yokoi T, Nunoya K, Hara A and Kamataki T. Co-operative regulation of the transcription of human dihydrodiol dehydrogenase (DD)4/aldo-keto reductase (AKR)1C4 gene by hepatocyte nuclear factor (HNF)-4alpha/gamma and HNF-1alpha. The Biochemical journal. 2001; 355:537-544.
43. Laimer D, Dolznig H, Kollmann K, Vesely PW, Schlederer M, Merkel O, Schiefer AI, Hassler MR, Heider S, Amenitsch L, Thallinger C, Staber PB, Simonitsch-Klupp I, Artaker M, Lagger S, Turner SD, et al. PDGFR blockade is a rational and effective therapy for NPM-ALK-driven lymphomas. Nature medicine. 2012; 18:1699-1704.
44. Vinatzer U, Dampier B, Streubel B, Pacher M, Seewald MJ, Stratowa C, Kaserer K and Schreiber M. Expression of HER2 and the coamplified genes GRB7 and MLN64 in human breast cancer: quantitative real-time reverse transcription-PCR as a diagnostic alternative to immunohistochemistry and fluorescence in situ hybridization. Clinical cancer research: an official journal of the American Association for Cancer Research. 2005; 11:8348-8357.
45. Waerner T, Alacakaptan M, Tamir I, Oberauer R, Gal A, Brabletz T, Schreiber M, Jechlinger M and Beug H. ILEI: a cytokine essential for EMT, tumor formation, and late events in metastasis in epithelial cells. Cancer cell. 2006; 10:227-239.
46. Team RDC. (2009). R: A language and environment for statistical computing: R Foundation for Statistical Computing).
47. Harrington DP and Fleming TR. A Class of Rank Test Procedures for Censored Survival-Data. Biometrics. 1981; 37:613-613.