Dysregulation of cell polarity proteins synergize with oncogenes or the microenvironment to induce invasive behavior in epithelial cells

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Chatterjee, Samit ^a,b   Seifried, Laurie ^a   Feigin, Michael E ^b   Gibbons, Don L ^c   Scuoppo, Claudio ^b   Lin, Wei ^c   Rizvi, Zain H ^c   Lind, Evan ^a   Dissanayake, Dilan ^a   Kurie, Jonathan ^c   Ohashi, Pam ^a   Muthuswamy, Senthil K ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COLLAGEN TYPE 1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; INTERLEUKIN 6; PROTEIN AF 6; PROTEIN DLG1; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN PAR6; SCRIBBLE PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CELL INVASION; CELL MIGRATION; CELL POLARITY; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; FEMALE; LUNG TUMOR; MALE; MOUSE; NONHUMAN; ONCOGENE; PHENOTYPIC PLASTICITY; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE; CELL MOVEMENT; CELL POLARITY; CELLULAR MICROENVIRONMENT; CYTOKINES; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; KINESIN; MALE; MEMBRANE PROTEINS; MICE; MICE, 129 STRAIN; MYOSINS; ONCOGENES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2;

EID: 84860015579     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034343     Document Type: Article

References (45)

1. Macara IG, Mili S, (2008) Polarity and differential inheritance-universal attributes of life? Cell 135: 801-812.
2. Huang L, Muthuswamy SK, (2010) Polarity protein alterations in carcinoma: a focus on emerging roles for polarity regulators. Curr Opin Genet Dev 20: 41-50.
3. Lee M, Vasioukhin V, (2008) Cell polarity and cancer - cell and tissue polarity as a non-canonical tumor suppressor. J Cell Sci 121: 1141-1150.
4. Joshi A, Cao D, (2010) TGF-beta signaling, tumor microenvironment and tumor progression: the butterfly effect. Front Biosci 15: 180-194.
5. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, et al. (2005) Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307: 1603-1609.
6. Dow LE, Elsum IA, King CL, Kinross KM, Richardson HE, et al. (2008) Loss of human Scribble cooperates with H-Ras to promote cell invasion through deregulation of MAPK signalling. Oncogene 27: 5988-6001.
7. Pagliarini RA, Xu T, (2003) A genetic screen in Drosophila for metastatic behavior. Science 302: 1227-1231.
8. Thiery JP, Acloque H, Huang RY, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
9. Spaderna S, Schmalhofer O, Wahlbuhl M, Dimmler A, Bauer K, et al. (2008) The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 68: 537-544.
10. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS, (2001) ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 3: 785-792.
11. Schoenenberger CA, Zuk A, Kendall D, Matlin KS, (1991) Multilayering and loss of apical polarity in MDCK cells transformed with viral K-ras. J Cell Biol 112: 873-889.
12. Lu J, Guo H, Treekitkarnmongkol W, Li P, Zhang J, et al. (2009) 14-3-3zeta Cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell 16: 195-207.
13. Andrechek ER, Hardy WR, Siegel PM, Rudnicki MA, Cardiff RD, et al. (2000) Amplification of the neu/erbB-2 oncogene in a mouse model of mammary tumorigenesis. Proc Natl Acad Sci U S A 97: 3444-3449.
14. Karreth FA, Tuveson DA, (2009) Modelling oncogenic Ras/Raf signalling in the mouse. Curr Opin Genet Dev 19: 4-11.
15. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
16. Joyce JA, Pollard JW, (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239-252.
17. Aranda V, Haire T, Nolan ME, Calarco JP, Rosenberg AZ, et al. (2006) Par6-aPKC uncouples ErbB2 induced disruption of polarized epithelial organization from proliferation control. Nat Cell Biol 8: 1235-1245.
18. Humbert PO, Dow LE, Russell SM, (2006) The Scribble and Par complexes in polarity and migration: friends or foes? Trends Cell Biol 16: 622-630.
19. Ebnet K, Schulz CU, Meyer Zu Brickwedde MK, Pendl GG, Vestweber D, (2000) Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 275: 27979-27988.
20. Mandai K, Nakanishi H, Satoh A, Obaishi H, Wada M, et al. (1997) Afadin: A novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction. J Cell Biol 139: 517-528.
21. Gibbons DL, Lin W, Creighton CJ, Zheng S, Berel D, et al. (2009) Expression signatures of metastatic capacity in a genetic mouse model of lung adenocarcinoma. PLoS One 4: e5401.
22. Grivennikov SI, Greten FR, Karin M, (2010) Immunity, inflammation, and cancer. Cell 140: 883-899.
23. Mantovani A, Allavena P, Sica A, Balkwill F, (2008) Cancer-related inflammation. Nature 454: 436-444.
24. Pollard JW, (2008) Macrophages define the invasive microenvironment in breast cancer. J Leukoc Biol 84: 623-630.
25. Krieg AM, (2002) CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20: 709-760.
26. Benoy I, Salgado R, Colpaert C, Weytjens R, Vermeulen PB, et al. (2002) Serum interleukin 6, plasma VEGF, serum VEGF, and VEGF platelet load in breast cancer patients. Clin Breast Cancer 2: 311-315.
27. Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, et al. (2003) Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer 103: 642-646.
28. Miles DW, Happerfield LC, Naylor MS, Bobrow LG, Rubens RD, et al. (1994) Expression of tumour necrosis factor (TNF alpha) and its receptors in benign and malignant breast tissue. Int J Cancer 56: 777-782.
29. Leek RD, Landers R, Fox SB, Ng F, Harris AL, et al. (1998) Association of tumour necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma. Br J Cancer 77: 2246-2251.
30. Debnath J, Muthuswamy SK, Brugge JS, (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30: 256-268.
31. Kondapaka SB, Singh SS, Dasmahapatra GP, Sausville EA, Roy KK, (2003) Perifosine, a novel alkylphospholipid, inhibits protein kinase B activation. Mol Cancer Ther 2: 1093-1103.
32. Hennessy BT, Lu Y, Poradosu E, Yu Q, Yu S, et al. (2007) Pharmacodynamic markers of perifosine efficacy. Clin Cancer Res 13: 7421-7431.
33. Reischauer S, Levesque MP, Nusslein-Volhard C, Sonawane M, (2009) Lgl2 executes its function as a tumor suppressor by regulating ErbB signaling in the zebrafish epidermis. PLoS Genet 5: e1000720.
34. Wang SC, Hung MC, (2001) HER2 overexpression and cancer targeting. Semin Oncol 28: 115-124.
35. Nofech-Mozes S, Spayne J, Rakovitch E, Hanna W, (2005) Prognostic and predictive molecular markers in DCIS: a review. Adv Anat Pathol 12: 256-264.
36. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, et al. (2008) Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 68: 989-997.
37. Damonte P, Gregg JP, Borowsky AD, Keister BA, Cardiff RD, (2007) EMT tumorigenesis in the mouse mammary gland. Lab Invest 87: 1218-1226.
38. Hennessy BT, Gonzalez-Angulo AM, Stemke-Hale K, Gilcrease MZ, Krishnamurthy S, et al. (2009) Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res 69: 4116-4124.
39. Nelson WJ, (2009) Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. Cold Spring Harb Perspect Biol 1: a000513.
40. Suzuki A, Ohno S, (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119: 979-987.
41. Etienne-Manneville S, (2008) Polarity proteins in migration and invasion. Oncogene 27: 6970-6980.
42. Miyata M, Ogita H, Komura H, Nakata S, Okamoto R, et al. (2009) Localization of nectin-free afadin at the leading edge and its involvement in directional cell movement induced by platelet-derived growth factor. J Cell Sci 122: 4319-4329.
43. Gibbons DL, Lin W, Creighton CJ, Rizvi ZH, Gregory PA, et al. (2009) Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression. Genes Dev 23: 2140-2151.
44. Xiang B, Muthuswamy SK, (2006) Using three-dimensional acinar structures for molecular and cell biological assays. Methods Enzymol 406: 692-701.
45. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.