Wnt-beta-catenin pathway signals metastasis-associated tumor cell phenotypes in triple negative breast cancers

Oncotarget

Volumn 7, Issue 28, 2016, Pages 43124-43149

  De, Pradip ^a,b   Carlson, Jennifer H ^a   Wu, Hui ^c   Marcus, Adam ^c   Leyland Jones, Brian ^a,b   Dey, Nandini ^a,b  

^a Avera Research Institute   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain metastasis specific TNBC cells; Integrin directed migration; LWnt3ACM stimulation; Matrigel invasion; Wnt pathway modulators

Indexed keywords

7,8 DIHYDRO 2 [4 (TRIFLUOROMETHYL)PHENYL] 5H THIOPYRANO[4,3 D]PYRIMIDIN 4 OL; APC PROTEIN; BETA CATENIN; CASEIN; DISHEVELLED 1; FIBRONECTIN; INTEGRIN; MATRIGEL; MATRILYSIN; PICTILISIB; SMALL INTERFERING RNA; SULINDAC SULFIDE; 2-(1H-INDAZOL-4-YL)-6-(4-METHANESULFONYLPIPERAZIN-1-YLMETHYL)-4-MORPHOLIN-4-YLTHIENO(3,2-D)PYRIMIDINE; APC PROTEIN, HUMAN; CTNNB1 PROTEIN, HUMAN; DISHEVELLED PROTEIN; DVL1 PROTEIN, HUMAN; FUSED HETEROCYCLIC RINGS; INDAZOLE DERIVATIVE; MMP7 PROTEIN, HUMAN; SULFONAMIDE; SULINDAC; WNT PROTEIN;

ACTIN FILAMENT; ARTICLE; BRAIN METASTASIS; BREAST CANCER CELL LINE; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CLONOGENESIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; METASTASIS; PHENOTYPE; TRIPLE NEGATIVE BREAST CANCER; TUMOR CELL; VIDEO MICROSCOPY; WNT SIGNALING PATHWAY; ZYMOGRAPHY; ANALOGS AND DERIVATIVES; BRAIN TUMOR; CARCINOMA; CELL MOTION; DRUG EFFECTS; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PATHOLOGY; RNA INTERFERENCE; SECONDARY; TUMOR CELL LINE; UPREGULATION; WNT SIGNALING;

ADENOMATOUS POLYPOSIS COLI PROTEIN; BETA CATENIN; BRAIN NEOPLASMS; CARCINOMA; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISHEVELLED PROTEINS; FEMALE; FIBRONECTINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; INDAZOLES; INTEGRINS; MATRIX METALLOPROTEINASE 7; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROSCOPY, VIDEO; MUTATION; PHENOTYPE; RNA INTERFERENCE; RNA, SMALL INTERFERING; SULFONAMIDES; SULINDAC; TRIPLE NEGATIVE BREAST NEOPLASMS; UP-REGULATION; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84978761872     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8988     Document Type: Article

References (56)

1. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, et al. Molecular portraits of human breast tumours. Nature. 2000; 406:747-752
2. Carey L, Winer E, Viale G, Cameron D and Gianni L. Triple-negative breast cancer: disease entity or title of convenience? Nature reviews Clinical oncology. 2010; 7:683-692
3. Reis-Filho JS and Tutt AN. Triple negative tumours: a critical review. Histopathology. 2008; 52:108-118
4. Dent R, Hanna WM, Trudeau M, Rawlinson E, Sun P and Narod SA. Pattern of metastatic spread in triple-negative breast cancer. Breast cancer research and treatment. 2009; 115:423-428
5. Carey LA. Directed therapy of subtypes of triple-negative breast cancer. The oncologist. 2011; 16 Suppl 1:71-78
6. Badve S, Dabbs DJ, Schnitt SJ, Baehner FL, Decker T, Eusebi V, Fox SB, Ichihara S, Jacquemier J, Lakhani SR, Palacios J, Rakha EA, Richardson AL, Schmitt FC, Tan PH, Tse GM, et al. Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod Pathol. 2011; 24:157-167
7. Hurvitz S and Mead M. Triple-negative breast cancer: advancements in characterization and treatment approach. Current opinion in obstetrics & gynecology. 2016; 28:59-69
8. Le Du F, Eckhardt BL, Lim B, Litton JK, Moulder S, Meric-Bernstam F, Gonzalez-Angulo AM and Ueno NT. Is the future of personalized therapy in triple-negative breast cancer based on molecular subtype? Oncotarget. 2015; 6:12890-12908. doi: 10.18632/oncotarget.3849
9. Lawrence RT, Perez EM, Hernandez D, Miller CP, Haas KM, Irie HY, Lee SI, Blau CA and Villen J. The proteomic landscape of triple-negative breast cancer. Cell reports. 2015; 11:630-644
10. Andreopoulou E, Schweber SJ, Sparano JA and McDaid HM. Therapies for triple negative breast cancer. Expert opinion on pharmacotherapy. 2015; 16:983-998
11. Peddi PF, Ellis MJ and Ma C. Molecular basis of triple negative breast cancer and implications for therapy. International journal of breast cancer. 2012; 2012:217185
12. Marme F and Schneeweiss A. Targeted Therapies in Triple-Negative Breast Cancer. Breast care. 2015; 10:159-166
13. Dey N, Smith BR and Leyland-Jones B. Targeting basal-like breast cancers. Current drug targets. 2012; 13:1510-1524
14. Mathe A, Wong-Brown M, Morten B, Forbes JF, Braye SG, Avery-Kiejda KA and Scott RJ. Novel genes associated with lymph node metastasis in triple negative breast cancer. Scientific reports. 2015; 5:15832
15. Pal SK, Childs BH and Pegram M. Triple negative breast cancer: unmet medical needs. Breast cancer research and treatment. 2011; 125:627-636
16. Nusse R and Varmus HE. Wnt genes. Cell. 1992; 69:1073-1087
17. Nusse R. The Wnt gene family in tumorigenesis and in normal development. The Journal of steroid biochemistry and molecular biology. 1992; 43:9-12
18. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell. 2006; 127:469-480
19. Geyer FC, Lacroix-Triki M, Savage K, Arnedos M, Lambros MB, MacKay A, Natrajan R and Reis-Filho JS. beta-Catenin pathway activation in breast cancer is associated with triple-negative phenotype but not with CTNNB1 mutation. Mod Pathol. 2011; 24:209-231
20. Dey N, Barwick BG, Moreno CS, Ordanic-Kodani M, Chen Z, Oprea-Ilies G, Tang W, Catzavelos C, Kerstann KF, Sledge GW, Jr., Abramovitz M, Bouzyk M, De P and Leyland-Jones BR. Wnt signaling in triple negative breast cancer is associated with metastasis. BMC cancer. 2013; 13:537
21. Khramtsov AI, Khramtsova GF, Tretiakova M, Huo D, Olopade OI and Goss KH. Wnt/beta-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. The American journal of pathology. 2010; 176:2911-2920
22. Heitz F, Harter P, Lueck HJ, Fissler-EckhoffA, Lorenz-Salehi F, Scheil-Bertram S, Traut A and du Bois A. Triple-negative and HER2-overexpressing breast cancers exhibit an elevated risk and an earlier occurrence of cerebral metastases. European journal of cancer. 2009; 45:2792-2798
23. Smart D, Garcia-Glaessner A, Palmieri D, Wong-Goodrich SJ, Kramp T, Gril B, Shukla S, Lyle T, Hua E, Cameron HA, Camphausen K and Steeg PS. Analysis of radiation therapy in a model of triple-negative breast cancer brain metastasis. Clinical & experimental metastasis. 2015; 32:717-727
24. Pradip D, Bouzyk M, Dey N and Leyland-Jones B. Dissecting GRB7-mediated signals for proliferation and migration in HER2 overexpressing breast tumor cells: GTP-ase rules. American journal of cancer research. 2013; 3:173-195
25. Huguet EL, McMahon JA, McMahon AP, Bicknell R and Harris AL. Differential expression of human Wnt genes 2, 3, 4, and 7B in human breast cell lines and normal and disease states of human breast tissue. Cancer research. 1994; 54:2615-2621
26. De P, Sun Y, Carlson JH, Friedman LS, Leyland-Jones BR and Dey N. Doubling down on the PI3K-AKT-mTOR pathway enhances the antitumor efficacy of PARP inhibitor in triple negative breast cancer model beyond BRCA-ness. Neoplasia. 2014; 16:43-72
27. Dey N, Young B, Abramovitz M, Bouzyk M, Barwick B, De P and Leyland-Jones B. Differential activation of Wnt-beta-catenin pathway in triple negative breast cancer increases MMP7 in a PTEN dependent manner. PloS one. 2013; 8:e77425
28. Staal FJ, Noort Mv M, Strous GJ and Clevers HC. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO reports. 2002; 3:63-68
29. O'Connor R, O'Leary M, Ballot J, Collins CD, Kinsella P, Mager DE, Arnold RD, O'Driscoll L, Larkin A, Kennedy S, Fennelly D, Clynes M and Crown J. A phase I clinical and pharmacokinetic study of the multi-drug resistance protein-1 (MRP-1) inhibitor sulindac, in combination with epirubicin in patients with advanced cancer. Cancer chemotherapy and pharmacology. 2007; 59:79-87
30. Witta SE, Gustafson DL, Pierson AS, Menter A, Holden SN, Basche M, Persky M, O'Bryant CL, Zeng C, Baron A, Long ME, Gibbs A, Kelly K, Bunn PA, Jr., Chan DC, Pallansch P, et al. A phase I and pharmacokinetic study of exisulind and docetaxel in patients with advanced solid tumors. Clin Cancer Res. 2004; 10:7229-7237
31. Rice PL, KelloffJ, Sullivan H, Driggers LJ, Beard KS, Kuwada S, Piazza G and Ahnen DJ. Sulindac metabolites induce caspase-and proteasome-dependent degradation of beta-catenin protein in human colon cancer cells. Molecular cancer therapeutics. 2003; 2:885-892
32. Han A, Song Z, Tong C, Hu D, Bi X, Augenlicht LH and Yang W. Sulindac suppresses beta-catenin expression in human cancer cells. European journal of pharmacology. 2008; 583:26-31
33. Clapper ML, Coudry J and Chang WC. beta-catenin-mediated signaling: a molecular target for early chemopreventive intervention. Mutation research. 2004; 555:97-105
34. De P, Carlson JH, Leyland-Jones B and Dey N. Wnt-β-Catenin Pathway Regulates Vascular Mimicry in Triple Negative Breast Cancer. J Cytol Histol. 2013; 4
35. Dihlmann S and von Knebel Doeberitz M. Wnt/betacatenin-pathway as a molecular target for future anticancer therapeutics. International journal of cancer Journal international du cancer. 2005; 113:515-524
36. Qiao L, ShiffSJ and Rigas B. Sulindac sulfide inhibits the proliferation of colon cancer cells: diminished expression of the proliferation markers PCNA and Ki-67. Cancer letters. 1997; 115:229-234
37. Staal FJ, Luis TC and Tiemessen MM. WNT signalling in the immune system: WNT is spreading its wings. Nature reviews Immunology. 2008; 8:581-593
38. Guillen-Ahlers H, Buechler SA, Suckow MA, Castellino FJ and Ploplis VA. Sulindac treatment alters collagen and matrilysin expression in adenomas of ApcMin/+ mice. Carcinogenesis. 2008; 29:1421-1427
39. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P and Smith A. The ground state of embryonic stem cell self-renewal. Nature. 2008; 453:519-523
40. Bao R, Christova T, Song S, Angers S, Yan X and Attisano L. Inhibition of tankyrases induces Axin stabilization and blocks Wnt signalling in breast cancer cells. PloS one. 2012; 7:e48670
41. Lin NU, Amiri-Kordestani L, Palmieri D, Liewehr DJ and Steeg PS. CNS metastases in breast cancer: old challenge, new frontiers. Clin Cancer Res. 2013; 19:6404-6418
42. Karagoz K, Sinha R and Arga KY. Triple negative breast cancer: a multi-omics network discovery strategy for candidate targets and driving pathways. OMICS. 2015; 19:115-130
43. Weigelt B, Pusztai L, Ashworth A and Reis-Filho JS. Challenges translating breast cancer gene signatures into the clinic. Nature reviews Clinical oncology. 2012; 9:58-64
44. Martinez-Revollar G, Garay E, Martin-Tapia D, Nava P, Huerta M, Lopez-Bayghen E, Meraz-Cruz N, Segovia J and Gonzalez-Mariscal L. Heterogeneity between triple negative breast cancer cells due to differential activation of Wnt and PI3K/AKT pathways. Experimental cell research. 2015; 339:67-80
45. Angers S and Moon RT. Proximal events in Wnt signal transduction. Nature reviews Molecular cell biology. 2009; 10:468-477
46. Matsuda Y, Schlange T, Oakeley EJ, Boulay A and Hynes NE. WNT signaling enhances breast cancer cell motility and blockade of the WNT pathway by sFRP1 suppresses MDA-MB-231 xenograft growth. Breast Cancer Res. 2009; 11:R32
47. Pollack AL, Barth AI, Altschuler Y, Nelson WJ and Mostov KE. Dynamics of beta-catenin interactions with APC protein regulate epithelial tubulogenesis. The Journal of cell biology. 1997; 137:1651-1662
48. Semb H and Christofori G. The tumor-suppressor function of E-cadherin. American journal of human genetics. 1998; 63:1588-1593
49. Sommers CL, Gelmann EP, Kemler R, Cowin P and Byers SW. Alterations in beta-catenin phosphorylation and plakoglobin expression in human breast cancer cells. Cancer research. 1994; 54:3544-3552
50. Fedor-Chaiken M, Meigs TE, Kaplan DD and Brackenbury R. Two regions of cadherin cytoplasmic domains are involved in suppressing motility of a mammary carcinoma cell line. The Journal of biological chemistry. 2003; 278:52371-52378
51. van de Wetering M, Barker N, Harkes IC, van der Heyden M, Dijk NJ, Hollestelle A, Klijn JG, Clevers H and Schutte M. Mutant E-cadherin breast cancer cells do not display constitutive Wnt signaling. Cancer research. 2001; 61:278-284
52. Zhang L, Zhang S, Yao J, Lowery FJ, Zhang Q, Huang WC, Li P, Li M, Wang X, Zhang C, Wang H, Ellis K, Cheerathodi M, McCarty JH, Palmieri D, Saunus J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015; 527:100-104
53. Martins FC, De S, Almendro V, Gonen M, Park SY, Blum JL, Herlihy W, Ethington G, Schnitt SJ, Tung N, Garber JE, Fetten K, Michor F and Polyak K. Evolutionary pathways in BRCA1-associated breast tumors. Cancer discovery. 2012; 2:503-511
54. Ellis MJ and Perou CM. The genomic landscape of breast cancer as a therapeutic roadmap. Cancer discovery. 2013; 3:27-34
55. Lague MN, Paquet M, Fan HY, Kaartinen MJ, Chu S, Jamin SP, Behringer RR, Fuller PJ, Mitchell A, Dore M, Huneault LM, Richards JS and Boerboom D. Synergistic effects of Pten loss and WNT/CTNNB1 signaling pathway activation in ovarian granulosa cell tumor development and progression. Carcinogenesis. 2008; 29:2062-2072
56. Sidaway P. Breast cancer: Antipsychotic agent supresses metastatic TNBC. Nature reviews Clinical oncology. 2015