Cooperative signaling between Wnt1 and integrin-linked kinase induces accelerated breast tumor development

Breast Cancer Research

Volumn 12, Issue 3, 2010, Pages

  Oloumi, Arusha ^a   Maidan, Mykola ^a   Lock, Frances E ^a   Tearle, Howard ^b   McKinney, Steven ^a   Muller, William J ^d   Aparicio, Samuel A J R ^a   Dedhar, Shoukat ^a,b,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b JACK BELL RESEARCH CENTRE   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIN D1; INTEGRIN LINKED KINASE; MOLECULAR MARKER; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXA1; UNCLASSIFIED DRUG; WNT1 PROTEIN; INTEGRIN-LINKED KINASE; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; TUMOR MARKER; WNT1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; BREAST EPITHELIUM; BREAST HYPERPLASIA; BREAST TUMOR; CARCINOGENESIS; GENE EXPRESSION PROFILING; MAMMARY GLAND; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TUMOR GROWTH; UPREGULATION; ANIMAL; CELL TRANSFORMATION; DNA MICROARRAY; EPITHELIUM CELL; EXPERIMENTAL NEOPLASM; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; MALE; METABOLISM; MOUSE MAMMARY TUMOR ONCOVIRUS; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HUMANS; MALE; MAMMARY NEOPLASMS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; WNT1 PROTEIN;

EID: 77956584844     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2592     Document Type: Article

References (62)

1. Hanahan D, Wagner EF, Palmiter RD. The origins of oncomice: a history of the first transgenic mice genetically engineered to develop cancer. Genes Dev 2007, 21:2258-2270. 10.1101/gad.1583307, 17875663.
2. Veeck J, Niederacher D, An H, Klopocki E, Wiesmann F, Betz B, Galm O, Camara O, Durst M, Kristiansen G, Huszka C, Knuchel R, Dahl E. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene 2006, 25:3479-3488. 10.1038/sj.onc.1209386, 16449975.
3. Sims AH, Howell A, Howell SJ, Clarke RB. Origins of breast cancer subtypes and therapeutic implications. Nat Clin Pract Oncol 2007, 4:516-525. 10.1038/ncponc0908, 17728710.
4. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480. 10.1016/j.cell.2006.10.018, 17081971.
5. Cowin P. Unraveling the cytoplasmic interactions of the cadherin superfamily. Proc Natl Acad Sci USA 1994, 91:10759-10761. 10.1073/pnas.91.23.10759, 45104, 7971957.
6. Huang H, He X. Wnt/beta-catenin signaling: new (and old) players and new insights. Curr Opin Cell Biol 2008, 20:119-125. 10.1016/j.ceb.2008.01.009, 2390924, 18339531.
7. Klopocki E, Kristiansen G, Wild PJ, Klaman I, Castanos-Velez E, Singer G, Stohr R, Simon R, Sauter G, Leibiger H, Essers L, Weber B, Hermann K, Rosenthal A, Hartmann A, Dahl E. Loss of SFRP1 is associated with breast cancer progression and poor prognosis in early stage tumors. Int J Oncol 2004, 25:641-649.
8. Vaillant F, Asselin-Labat ML, Shackleton M, Forrest NC, Lindeman GJ, Visvader JE. The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res 2008, 68:7711-7717. 10.1158/0008-5472.CAN-08-1949, 18829523.
9. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, Rowlands T, Egeblad M, Cowin P, Werb Z, Tan LK, Rosen JM, Varmus HE. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci USA 2003, 100:15853-15858. 10.1073/pnas.2136825100, 307657, 14668450.
10. Liu S, Dontu G, Wicha MS. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res 2005, 7:86-95. 10.1186/bcr1021, 1143566, 15987436.
11. Lin SY, Xia W, Wang JC, Kwong KY, Spohn B, Wen Y, Pestell RG, Hung MC. Beta-catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc Natl Acad Sci USA 2000, 97:4262-4266. 10.1073/pnas.060025397, 18221, 10759547.
12. Ryo A, Nakamura M, Wulf G, Liou YC, Lu KP. Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nature Cell Biol 2001, 3:793-801. 10.1038/ncb0901-793, 11533658.
13. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 2005, 5:51-63. 10.1038/nrc1524, 15630415.
14. McDonald PC, Fielding AB, Dedhar S. Integrin-linked kinase: essential roles in physiology and cancer biology. J Cell Sci 2008, 121:3121-3132. 10.1242/jcs.017996, 18799788.
15. Oloumi A, McPhee T, Dedhar S. Regulation of E-cadherin expression and beta-catenin/Tcf transcriptional activity by the integrin-linked kinase. Biochim Biophys Acta 2004, 1691:1-15. 10.1016/j.bbamcr.2003.12.002, 15053919.
16. Bravou V, Klironomos G, Papadaki E, Taraviras S, Varakis J. ILK over-expression in human colon cancer progression correlates with activation of beta-catenin, down-regulation of E-cadherin and activation of the Akt-FKHR pathway. J Pathol 2006, 208:91-99. 10.1002/path.1860, 16278819.
17. Oloumi A, Syam S, Dedhar S. Modulation of Wnt3a-mediated nuclear beta-catenin accumulation and activation by integrin-linked kinase in mammalian cells. Oncogene 2006, 25:7747-7757. 10.1038/sj.onc.1209752, 16799642.
18. Cho RW, Wang X, Diehn M, Shedden K, Chen GY, Sherlock G, Gurney A, Lewicki J, Clarke MF. Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells 2008, 26:364-371. 10.1634/stemcells.2007-0440, 17975224.
19. Li Y, Hively WP, Varmus HE. Use of MMTV-Wnt-1 transgenic mice for studying the genetic basis of breast cancer. Oncogene 2000, 19:1002-1009. 10.1038/sj.onc.1203273, 10713683.
20. D'Amico M, Hulit J, Amanatullah DF, Zafonte BT, Albanese C, Bouzahzah B, Fu M, Augenlicht LH, Donehower LA, Takemaru K, Moon RT, Davis R, Lisanti MP, Shtutman M, Zhurinsky J, Ben-Ze'ev A, Troussard AA, Dedhar S, Pestell RG. The integrin-linked kinase regulates the cyclin D1 gene through glycogen synthase kinase 3beta and cAMP-responsive element-binding protein-dependent pathways. J Biol Chem 2000, 275:32649-32657. 10.1074/jbc.M000643200, 10915780.
21. White DE, Cardiff RD, Dedhar S, Muller WJ. Mammary epithelial-specific expression of the integrin-linked kinase (ILK) results in the induction of mammary gland hyperplasias and tumors in transgenic mice. Oncogene 2001, 20:7064-7072. 10.1038/sj.onc.1204910, 11704830.
22. Ahmed N, Oliva K, Rice GE, Quinn MA. Cell-free 59 kDa immunoreactive integrin-linked kinase: a novel marker for ovarian carcinoma. Clin Cancer Res 2004, 10:2415-2420. 10.1158/1078-0432.CCR-03-0042, 15073119.
23. Bravou V, Klironomos G, Papadaki E, Stefanou D, Varakis J. Integrin-linked kinase (ILK) expression in human colon cancer. Br J Cancer 2003, 89:2340-2341. 10.1038/sj.bjc.6601482, 2395290, 14676816.
24. Goulioumis AK, Bravou V, Varakis J, Goumas P, Papadaki H. Integrin-linked kinase cytoplasmic and nuclear expression in laryngeal carcinomas. Virchows Arch 2008, 453:511-519. 10.1007/s00428-008-0668-8, 18813944.
25. Lin TP, Guzman RC, Osborn RC, Thordarson G, Nandi S. Role of endocrine, autocrine, and paracrine interactions in the development of mammary hyperplasia in Wnt-1 transgenic mice. Cancer Res 1992, 52:4413-4419.
26. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989, 24:148-154. 10.1007/BF00300234, 2544306.
27. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, Filmus J, Bell JC, Dedhar S. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996, 379:91-96. 10.1038/379091a0, 8538749.
28. Muskhelishvili L, Latendresse JR, Kodell RL, Henderson EB. Evaluation of cell proliferation in rat tissues with BrdU, PCNA, Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. J Histochem Cytochem 2003, 51:1681-1688.
29. Hinck L, Nelson WJ, Papkoff J. Wnt-1 modulates cell-cell adhesion in mammalian cells by stabilizing beta-catenin binding to the cell adhesion protein cadherin. J Cell Biol 1994, 124:729-741. 10.1083/jcb.124.5.729, 2119963, 8120095.
30. van Leeuwen F, Samos CH, Nusse R. Biological activity of soluble wingless protein in cultured Drosophila imaginal disc cells. Nature 1994, 368:342-344. 10.1038/368342a0, 8127369.
31. Bauer A, Huber O, Kemler R. Pontin52, an interaction partner of beta-catenin, binds to the TATA box binding protein. Proc Natl Acad Sci USA 1998, 95:14787-14792. 10.1073/pnas.95.25.14787, 24527, 9843967.
32. Bauer A, Chauvet S, Huber O, Usseglio F, Rothbacher U, Aragnol D, Kemler R, Pradel J. Pontin52 and reptin52 function as antagonistic regulators of beta-catenin signalling activity. EMBO J 2000, 19:6121-6130. 10.1093/emboj/19.22.6121, 305835, 11080158.
33. Dobreva I, Fielding A, Foster LJ, Dedhar S. Mapping the integrin-linked kinase interactome using SILAC. J Proteome Res 2008, 7:1740-1749. 10.1021/pr700852r, 18327965.
34. Zhao H, Cui Y, Dupont J, Sun H, Hennighausen L, Yakar S. Overexpression of the tumor suppressor gene phosphatase and tensin homologue partially inhibits wnt-1-induced mammary tumorigenesis. Cancer Res 2005, 65:6864-6873. 10.1158/0008-5472.CAN-05-0181, 16061670.
35. Yu Q, Geng Y, Sicinski P. Specific protection against breast cancers by cyclin D1 ablation. Nature 2001, 411:1017-1021. 10.1038/35082500, 11429595.
36. Lanzino M, De Amicis F, McPhaul MJ, Marsico S, Panno ML, Ando S. Endogenous coactivator ARA70 interacts with estrogen receptor alpha (ERalpha) and modulates the functional ERalpha/androgen receptor interplay in MCF-7 cells. J Biol Chem 2005, 280:20421-20430. 10.1074/jbc.M413576200, 15772083.
37. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970. 10.1016/j.cell.2008.01.018, 2323438, 18358809.
38. Takata T, Ishikawa F. Human Sir2-related protein SIRT1 associates with the bHLH repressors HES1 and HEY2 and is involved in HES1- and HEY2-mediated transcriptional repression. Biochem Biophys Res Commun 2003, 301:250-257. 10.1016/S0006-291X(02)03020-6, 12535671.
39. Tanno M, Sakamoto J, Miura T, Shimamoto K, Horio Y. Nucleocytoplasmic shuttling of the NAD+-dependent histone deacetylase SIRT1. J Biol Chem 2007, 282:6823-6832. 10.1074/jbc.M609554200, 17197703.
40. Bouras T, Pal B, Vaillant F, Harburg G, Asselin-Labat ML, Oakes SR, Lindeman GJ, Visvader JE. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 2008, 3:429-441. 10.1016/j.stem.2008.08.001, 18940734.
41. Raouf A, Zhao Y, To K, Stingl J, Delaney A, Barbara M, Iscove N, Jones S, McKinney S, Emerman J, Aparicio S, Marra M, Eaves C. Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 2008, 3:109-118. 10.1016/j.stem.2008.05.018, 18593563.
42. Carroll JS, Brown M. Estrogen receptor target gene: an evolving concept. Mol Endocrinol 2006, 20:1707-1714. 10.1210/me.2005-0334, 16396959.
43. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122:33-43. 10.1016/j.cell.2005.05.008, 16009131.
44. Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006, 127:1041-1055. 10.1016/j.cell.2006.09.048, 2646406, 17129787.
45. Sleeman KE, Kendrick H, Ashworth A, Isacke CM, Smalley MJ. CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res 2006, 8:R7. 10.1186/bcr1371, 1413978, 16417656.
46. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988. 10.1073/pnas.0530291100, 153034, 12629218.
47. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88. 10.1038/nature04372, 16397499.
48. Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, Hartley L, Robb L, Grosveld FG, van der Wees J, Lindeman GJ, Visvader JE. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nature Cell Biol 2007, 9:201-209. 10.1038/ncb1530, 17187062.
49. Persad S, Troussard AA, McPhee TR, Mulholland DJ, Dedhar S. Tumor suppressor PTEN inhibits nuclear accumulation of beta-catenin and T cell/lymphoid enhancer factor 1-mediated transcriptional activation. J Cell Biol 2001, 153:1161-1174. 10.1083/jcb.153.6.1161, 2192018, 11402061.
50. Sinner D, Rankin S, Lee M, Zorn AM. Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 2004, 131:3069-3080. 10.1242/dev.01176, 15163629.
51. Lin L, Miller CT, Contreras JI, Prescott MS, Dagenais SL, Wu R, Yee J, Orringer MB, Misek DE, Hanash SM, Glover TW, Beer DG. The hepatocyte nuclear factor 3 alpha gene, HNF3alpha (FOXA1), on chromosome band 14q13 is amplified and overexpressed in esophageal and lung adenocarcinomas. Cancer Res 2002, 62:5273-5279.
52. Laganiere J, Deblois G, Lefebvre C, Bataille AR, Robert F, Giguere V. From the cover: location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc Natl Acad Sci USA 2005, 102:11651-11656. 10.1073/pnas.0505575102, 1183449, 16087863.
53. Arnold A, Papanikolaou A. Cyclin D1 in breast cancer pathogenesis. J Clin Oncol 2005, 23:4215-4224. 10.1200/JCO.2005.05.064, 15961768.
54. Sutherland RL, Prall OW, Watts CK, Musgrove EA. Estrogen and progestin regulation of cell cycle progression. J Mammary Gland Biol Neoplasia 1998, 3:63-72. 10.1023/A:1018774302092, 10819505.
55. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999, 398:422-426. 10.1038/18884, 10201372.
56. Ando S, De Amicis F, Rago V, Carpino A, Maggiolini M, Panno ML, Lanzino M. Breast cancer: from estrogen to androgen receptor. Mol Cell Endocrinol 2002, 193:121-128. 10.1016/S0303-7207(02)00105-3, 12161011.
57. Thorat MA, Marchio C, Morimiya A, Savage K, Nakshatri H, Reis-Filho JS, Badve S. Forkhead box A1 expression in breast cancer is associated with luminal subtype and good prognosis. J Clin Pathol 2008, 61:327-332. 10.1136/jcp.2007.052431, 18037662.
58. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, Feleppa F, Huschtscha LI, Thorne HJ, Fox SB, Yan M, French JD, Brown MA, Smyth GK, Visvader JE, Lindeman GJ. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nature Med 2009, 15:907-913. 10.1038/nm.2000, 19648928.
59. Baumann P, Cremers N, Kroese F, Orend G, Chiquet-Ehrismann R, Uede T, Yagita H, Sleeman JP. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 2005, 65:10783-10793. 10.1158/0008-5472.CAN-05-0619, 16322224.
60. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, Eaves CJ. Purification and unique properties of mammary epithelial stem cells. Nature 2006, 439:993-997.
61. Tabe Y, Jin L, Tsutsumi-Ishii Y, Xu Y, McQueen T, Priebe W, Mills GB, Ohsaka A, Nagaoka I, Andreeff M, Konopleva M. Activation of integrin-linked kinase is a critical prosurvival pathway induced in leukemic cells by bone marrow-derived stromal cells. Cancer Res 2007, 67:684-694. 10.1158/0008-5472.CAN-06-3166, 17234779.
62. Badve S, Nakshatri H. Oestrogen-receptor-positive breast cancer: towards bridging histopathological and molecular classifications. J Clin Pathol 2009, 62:6-12. 10.1136/jcp.2008.059899, 18794199.