Identification of the receptor tyrosine kinase AXL in breast cancer as a target for the human miR-34a microRNA

Breast Cancer Research and Treatment

Volumn 130, Issue 2, 2011, Pages 663-679

  MacKiewicz, Mark ^a   Huppi, Konrad ^a   Pitt, Jason J ^a   Dorsey, Tiffany H ^a   Ambs, Stefan ^a   Caplen, Natasha J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

AXL; Breast cancer; MicroRNAs; miR 34a; Triple negative

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; LUCIFERASE; MESSENGER RNA; MICRORNA 34A; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

3' UNTRANSLATED REGION; ALGORITHM; ARTICLE; BINDING AFFINITY; BREAST CARCINOGENESIS; CANCER CELL CULTURE; CANCER GROWTH; CELL MIGRATION; CONTROLLED STUDY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE OVEREXPRESSION; GENE TARGETING; GENOTYPE PHENOTYPE CORRELATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA DEGRADATION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER;

3' UNTRANSLATED REGIONS; APOPTOSIS; BASE SEQUENCE; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; HUMANS; LUCIFERASES, RENILLA; MICRORNAS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 82955248085     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-011-1690-0     Document Type: Article

References (58)

1. Rakha EA, Ellis IO (2009) Triple-negative/basal-like breast cancer: review. Pathology 41:40-47
2. Venkitaraman R (2010) Triple-negative/basal-like breast cancer: clinical, pathologic and molecular features. Expert Rev. Anti-cancer Ther. 10:199-207
3. Charafe-Jauffret E, Ginestier C, Monville F, Finetti P, Adélǎ̈de J, Cervera N, Fekairi S, Xerri L, Jacquemier J, Birnbaum D, Bert-ucci F (2006) Gene expression profiling ofbreast cancer cell lines identifies potential new basal markers. Oncogene 25:2273-2284
4. Kao J, Salari K, Bocanegra M, Choi Y-L, Girard L, Gandhi J, Kwei KA, Hernandez-Boussard T, Wang P, Gazdar AF, Minna JD, Pollack JR (2009) Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLOS One 4:1-16
5. Kreike B, Van Kouwenhove M, Horlings H, Weigelt B, Peterse H, Bartelink H, Van de Vijver MJ (2007) Gene expression pro-filing and histopathological characterization of triple-negative/basal-like breast carcinomas. Breast Cancer Res 9:R65
6. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe J-P, Tong F, Speed T, Spellman PT, De Vries S, Lapuk A, Wang NJ, Kuo W-L, Stilwell JL, Pinkel D, Albertson DG, Waldman FM, Mc Cormick F, Dickson RB, Johnson MD, Lippman M, Ethier S, Gazdar A, Gray JW (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10:515-527 (Pubitemid 44854747)
7. Perou CM, Sørlie T, Eisen MB, Van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Aksien LA, Fluge Ø, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børre-sen-Dale A-L, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406:747-752
8. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, Van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lønning PE, Børresen-Dale A-L (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98:10869-10874 (Pubitemid 32878711)
9. Sørlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lønning PE, Brown PO, Børresen-Dale A-L, Botstein D (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 100: 8418-8423 (Pubitemid 36842560)
10. Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO (2007) Prognostic markers in triple-negative breast cancer. Cancer 109:25-32 (Pubitemid 46120191)
11. Gluz O, Liedtke C, Gottschalk N, Pusztai L, Nitz U, Harbeck N (2009) Triple-negative breast cancer-current status and future directions. Ann Oncol 20:1913-1927
12. Bartel DP (2004) Micro RNAs: genomics biogenesis, mechanism, and function. Cell 116:281-297
13. Babar IA, Slack FJ, Weidhaas JB (2008) Mi RNA modulation of the cellular stress response. Future Oncol 4:289-298 (Pubitemid 351715785)
14. Chang TC, Mendell JT (2007) Micro RNAs in vertebrate physi-ology and human disease. Annu Rev Genomics Hum Genet 8:215-239
15. Krutzfeldt J, Stoffel M (2006) Micro RNAs: a new class of reg-ulatory genes affecting metabolism. Cell Metabolism 4:9-12 (Pubitemid 43942256)
16. Zhao Y, Srivastava D (2007) A developmental view of micro R-NA function. Trends Biochem Sci 32:189-197 (Pubitemid 46603281)
17. Croce CM (2009) Causes and consequences of micro RNA dys-regulation in cancer. Nat Rev Genet 10:704-714
18. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM (2005) A micro RNA polycistron as a potential human oncogene. Nature 435:828-833 (Pubitemid 40839734)
19. Garzon R, Calin GA, Croce CM (2009) Micro RNAs in cancer. Annu Rev Med 60:167-179
20. Linger RM, Keating AK, Earp HS, Graham DK (2008) TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 100:35-83 (Pubitemid 351932179)
21. Gjerdrum C, Tiron C, Høiby T, Stefansson I, Haugen H, Sandal T, Collett K, Li S, Mc Cormack E, Gjertsen BT, Micklem DR, Aksien LA, Glackin C, Lorens JB (2010) Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci USA 107:1124-1129
22. Corney DC, Hwang CL, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK, Kamat AA, Sood AK, Ellenson LH, Hermeking H, Nikitin AY (2010) Frequent downregulation of mi R-34 family in human ovarian cancers. Clin Cancer Res 16:1119-1128
23. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D, Purow B, Abounader R (2010) Micro RNA-34a is tumor sup-pressive in brain tumors and glioma stem cells. Cell Cycle 9:1031-1036
24. Hu Y, Correa AM, Hoque A, Guan B, Ye F, Huang J, Swisher SG, Wu TT, Ajani JA, Xu XC (2010) Prognostic significance of differentially expressed mi RNAs in esophageal cancer. Int J Cancer. doi:10.1002/ijc.25330.
25. Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y, Zheng X (2009) mi R-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 275:44-53
26. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E, Marcinkiewicz L, Jiang J, Yang Y, Schmittgen TD, Lopes B, Schiff D, Purow B, Abounader R (2009) Micro RNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 69:7569-7576
27. Yan D, Zhou X, Chen X, Hu DN, Dong XD, Wang J, Lu F, Tu L, Qu J (2009) Micro RNA-34a inhibits uveal melanoma cell pro-liferation and migration through downregulation of c-MET. Invest Ophthalmol Vis Sci 50:1559-1565
28. Prueitt RL, Boersma BJ, Howe TM, Goodman JE, Thomas DD, Ying L, Pfiester CM, Yfantis HG, Cottrell JR, Lee DH, Remaley AT, Hofseth LJ, Wink DA, Ambs S (2007) Inflammation and IGF-I activate the Akt pathway in breast cancer. Int J Cancer 120:796-805 (Pubitemid 46175399)
29. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, Akslen LA, Ragaz J, Gown AM, Gilks CB, Van de Rijn M, Perou CM (2004) Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 10:5367-5374 (Pubitemid 39100473)
30. Boersma BJ, Howe TM, Goodman JE, Yfantis HG, Lee DH, Chanock SJ, Ambs S (2006) Association of breast cancer out-come with status of p53 and MDM2 SNP309. J Natl Cancer Inst 98:911-919 (Pubitemid 44018921)
31. Saldanha AJ (2004) Java Treeview\-extensible visualization of microarray data. Bioinformatics 20:3246-3248 (Pubitemid 39619217)
32. Martin SE, Jones TL, Thomas CL, Lorenzi PL, Nguyen DA, Runfola T, Gunsior M, Weinstein JN, Goldsmith PK, Lader E, Huppi K, Caplen NJ (2007) Multiplexing si RNAs to compress RNAi-based screen size in human cells. Nucleic Acids Res 35:e57
33. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics Int 11:36-42
34. Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, Wells W, Kauppinen S, Cole CN (2007) Altered micro RNA expression confined to specific epithelial cell sub-populations in breast cancer. Cancer Res 67:11612-11620
35. Radojicic J, Zaravinos A, Vrekoussis T, Kafousi M, Spandidos DA, Stathopoulos EN (2011) Micro RNA expression analysis in triple-negative (ER, PR and Her2/neu) breast cancer. Cell Cycle 10:507-517
36. Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM, Atchison RE, Mc Laughlin J, Swift SE, Pali ES, Yam G, Wong S, Lasaga J, Shen MR, Yu S, Xu W, Hitoshi Y, Bogenberger J, Nör JE, Payan DG, Lorens JB (2005) Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 65:9294-9303 (Pubitemid 41507996)
37. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J, Kallop D, Lulam MJ, Pei L (2009) Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis, and angiogenesis. Oncogene 28:3442-3455
38. Zhang YX, Knyazev PG, Cheburkin YV, Sharma K, Knyazev YP, Orfi L, Szabadkai I, Daub H, Kéri G, Ullrich A (2008) AXL is a potential target for therapeutic intervention in breast cancer progressio. Cancer Res 68:1905-1915 (Pubitemid 351416577)
39. Meric F, Lee W-P, Sahin A, Zhang H, Kung H-J, Hung M-C (2002) Expression profile of tyrosine kinases in breast cancer. Clin Cancer Res 8:361-367 (Pubitemid 34193951)
40. Nagaraja GM, Othman M, Fox BP, Alsaber R, Pellegrino CM, Zeng Y, Khanna R, Tamburini P, Swaroop A, Kandpal RP (2006) Gene expression signatures and biomarkers of noninvasive and invasive breast cancer cells: comprehensive profiles by repre-sentational difference analysis, microarrays and proteomics. Oncogene 25:2328-2338
41. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB (2007) p53-med-iated activiation of mi RNA34 candidate tumor-suppressor genes. Curr Biol 17:1298-1307 (Pubitemid 47176893)
42. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, Arking DE, Beer MA, Maitra A, Mendell JT (2007) Trans-activation of mi R-34a by p53 broadly influences gene expression and promotes apoptosis. Molecular Cell 26(5):745-752.
43. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY (2007) Micro RNA-34b and Micro RNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-inde-pendent growth. Cancer Res 67:8433-8438 (Pubitemid 47437414)
44. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ (2007) A micro RNA compo-nent of the p53 tumour suppressor network. Nature 447:1130-1134 (Pubitemid 47014436)
45. He X, He L, Hannon GJ (2007) The guardian's little helper: micro RNAs in the p53 tumor suppressor network. Cancer Res 67:11099-11101 (Pubitemid 350248530)
46. Hermeking H (2007) p53 enters the micro RNA world. Cancer Cell 12:414-418 (Pubitemid 350046413)
47. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, Oren M (2007) Transcriptional acti-vation of mi R-34a contributes to p53-mediated apoptosis. Mol Cell 26:731-743 (Pubitemid 46856247)
48. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H (2007) Differential regu-lation of micro RNAs by p53 revealed by massively parallel sequencing: mi R-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6:1586-1593 (Pubitemid 47327945)
49. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M, Allgayer H (2011) Regulation of Axl receptor tyrosine kinase expression by mi R-34a and mi R-199a/b in solid cancer. Onco-gene 30:2888-2899
50. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of micro RNAs on protein output. Nature 455:64-71
51. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N (2008) Widespread changes in protein synthesis induced by micro RNAs. Nature 455:58-63
52. Fridell YW, Villa J Jr, Attar EC, Liu ET (1998) GAS6 induces Axl-mediated chemotaxis of vascular smooth muscle cells. J Biol Chem 273:7123-7126 (Pubitemid 28160384)
53. Hafizi S, Dahlbäck B (2006) Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev 17:295-304 (Pubitemid 44038616)
54. Koorstra J-B, Karikari CA, Feldmann G, Bisht S, Rojas PL, Offerhaus GJ, Alvarez H, Maitra A (2009) The Axl recptor tyrosine kinase confers an adverse prognostic influence in pan-creatic cancer and represents a new therapeutic target. Cancer Biol Ther 8:618-626
55. Pierce A, Bliesner B, Xu M, Nielsen-Preiss S, Lemke G, Tobet S, Wierman ME (2008) Axl and Tyro3 modulate female reproduc-tion by influencing gonadotropin-releasing hormone neuron sur-vival and migration. Mol Endocrinol 22:2481-2495
56. Forbes SA, Bhamra G, Bamford S, Dawson E, Kok C, Clements J, Menzies A, Teague JW, Futreal PA, Stratton MR (2008) The catalogue of somatic mutations in cancer (COSMIC). Curr Pro-tocols Hum Genet 10.11:1-26
57. Welch C, Chen Y, Stallings RL (2007) Micro RNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuro-blastoma cells. Oncogene 26:5017-5022 (Pubitemid 47172643)
58. Hermeking H (2010) The mi R-34 family in cancer and apoptosis. Cell Death Differ 17:193-199