MUC4 Overexpression Augments Cell Migration and Metastasis through EGFR Family Proteins in Triple Negative Breast Cancer Cells

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Mukhopadhyay, Partha ^a   Lakshmanan, Imayavaramban ^a   Ponnusamy, Moorthy P ^a   Chakraborty, Subhankar ^a   Jain, Maneesh ^a   Pai, Priya ^a   Smith, Lynette M ^b   Lele, Subodh M ^a   Batra, Surinder K ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUCIN 4; PROTEIN KINASE C GAMMA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST; CANCER CELL; CANCER INVASION; CANCER TISSUE; CARCINOGENICITY; CELL CYCLE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION;

ANIMALS; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; MUCIN-4; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84873682464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054455     Document Type: Article

References (63)

1. Reis-Filho JS, Tutt AN, (2008) Triple negative tumours: a critical review. Histopathology 52: 108-118.
2. Nofech-Mozes S, Trudeau M, Kahn HK, Dent R, Rawlinson E, et al. (2009) Patterns of recurrence in the basal and non-basal subtypes of triple-negative breast cancers. Breast Cancer Res Treat 118: 131-137.
3. Kaplan HG, Malmgren JA, Atwood M, (2009) T1N0 triple negative breast cancer: risk of recurrence and adjuvant chemotherapy. Breast J 15: 454-460.
4. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, et al. (2008) Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 26: 1275-1281.
5. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, et al. (2009) Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 361: 123-134.
6. Chaturvedi P, Singh AP, Batra SK, (2008) Structure, evolution, and biology of the MUC4 mucin. FASEB J 22: 966-981.
7. Chaturvedi P, Singh AP, Moniaux N, Senapati S, Chakraborty S, et al. (2007) MUC4 mucin potentiates pancreatic tumor cell proliferation, survival, and invasive properties and interferes with its interaction to extracellular matrix proteins. Mol Cancer Res 5 309-320: 1541-7786.
8. Singh PK, Hollingsworth MA, (2006) Cell surface-associated mucins in signal transduction. Trends Cell Biol 16: 467-476.
9. Bafna S, Singh AP, Moniaux N, Eudy JD, Meza JL, et al. (2008) MUC4, a multifunctional transmembrane glycoprotein, induces oncogenic transformation of NIH3T3 mouse fibroblast cells. Cancer Res 68: 9231-9238.
10. Ponnusamy MP, Singh AP, Jain M, Chakraborty S, Moniaux N, et al. (2008) MUC4 activates HER2 signalling and enhances the motility of human ovarian cancer cells. Br J Cancer 99: 520-526.
11. Mukhopadhyay P, Chakraborty S, Ponnusamy MP, Lakshmanan I, Jain M, et al. (2011) Mucins in the pathogenesis of breast cancer: implications in diagnosis, prognosis and therapy. Biochim Biophys Acta 1815: 224-240.
12. Singh AP, Moniaux N, Chauhan SC, Meza JL, Batra SK, (2004) Inhibition of MUC4 expression suppresses pancreatic tumor cell growth and metastasis. Cancer Res 64: 622-630.
13. Bafna S, Kaur S, Momi N, Batra SK, (2009) Pancreatic cancer cells resistance to gemcitabine: the role of MUC4 mucin. Br J Cancer 101: 1155-1161.
14. Mimeault M, Johansson SL, Senapati S, Momi N, Chakraborty S, et al. (2010) MUC4 down-regulation reverses chemoresistance of pancreatic cancer stem/progenitor cells and their progenies. Cancer Lett 295: 69-84.
15. Rakha EA, Boyce RW, Bd El-Rehim D, Kurien T, Green AR, et al. (2005) Expression of mucins (MUC1, MUC2, MUC3, MUC4, MUC5AC and MUC6) and their prognostic significance in human breast cancer. Mod Pathol 18: 1295-1304.
16. Workman HC, Miller JK, Ingalla EQ, Kaur RP, Yamamoto DI, et al. (2009) The membrane mucin MUC4 is elevated in breast tumor lymph node metastases relative to matched primary tumors and confers aggressive properties to breast cancer cells. Breast Cancer Res 11: R70.
17. Dixit M, Yang JL, Poirier MC, Price JO, Andrews PA, et al. (1997) Abrogation of cisplatin-induced programmed cell death in human breast cancer cells by epidermal growth factor antisense RNA. J Natl Cancer Inst 89: 365-373.
18. Masuda A, Kondo M, Saito T, Yatabe Y, Kobayashi T, et al. (1997) Establishment of human peripheral lung epithelial cell lines (HPL1) retaining differentiated characteristics and responsiveness to epidermal growth factor, hepatocyte growth factor, and transforming growth factor beta1. Cancer Res 57: 4898-4904.
19. Moniaux N, Varshney GC, Chauhan SC, Copin MC, Jain M, et al. (2004) Generation and characterization of anti-MUC4 monoclonal antibodies reactive with normal and cancer cells in humans. J Histochem Cytochem 52: 253-261.
20. Jain M, Venkatraman G, Moniaux N, Kaur S, Kumar S, et al. (2011) Monoclonal antibodies recognizing the non-tandem repeat regions of the human mucin MUC4 in pancreatic cancer. PLoS One 6: e23344.
21. 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.
22. 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.
23. Baine MJ, Chakraborty S, Smith LM, Mallya K, Sasson AR, et al. (2011) Transcriptional profiling of peripheral blood mononuclear cells in pancreatic cancer patients identifies novel genes with potential diagnostic utility. PLoS One 6: e17014.
24. Moniaux N, Chakraborty S, Yalniz M, Gonzalez J, Shostrom VK, et al. (2008) Early diagnosis of pancreatic cancer: neutrophil gelatinase-associated lipocalin as a marker of pancreatic intraepithelial neoplasia. Br J Cancer 98: 1540-1547.
25. Chaturvedi P, Singh AP, Chakraborty S, Chauhan SC, Bafna S, et al. (2008) MUC4 mucin interacts with and stabilizes the HER2 oncoprotein in human pancreatic cancer cells. Cancer Res 68: 2065-2070.
26. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL, (2002) p38 mitogen-activated protein kinase is required for TGFbeta-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 115: 3193-3206.
27. Ma L, Teruya-Feldstein J, Weinberg RA, (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688.
28. Sun Y, Turbin DA, Ling K, Thapa N, Leung S, et al. (2010) Type I gamma phosphatidylinositol phosphate kinase modulates invasion and proliferation and its expression correlates with poor prognosis in breast cancer. Breast Cancer Res 12: R6.
29. Simon R, Lam A, Li MC, Ngan M, Menenzes S, et al. (2007) Analysis of gene expression data using BRB-ArrayTools. Cancer Inform 3: 11-17.
30. Viloria-Petit AM, David L, Jia JY, Erdemir T, Bane AL, et al. (2009) A role for the TGFbeta-Par6 polarity pathway in breast cancer progression. Proc Natl Acad Sci U S A 106: 14028-14033.
31. Whipple RA, Balzer EM, Cho EH, Matrone MA, Yoon JR, et al. (2008) Vimentin filaments support extension of tubulin-based microtentacles in detached breast tumor cells. Cancer Res 68: 5678-5688.
32. Evan GI, Vousden KH, (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411: 342-348.
33. Hoadley KA, Weigman VJ, Fan C, Sawyer LR, He X, et al. (2007) EGFR associated expression profiles vary with breast tumor subtype. BMC Genomics 8: 258.
34. Wong ES, Fong CW, Lim J, Yusoff P, Low BC, et al. (2002) Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signalling. EMBO J 21: 4796-4808.
35. Bissell MJ, Radisky D, (2001) Putting tumours in context. Nat Rev Cancer 1: 46-54.
36. Inman JL, Bissell MJ, (2010) Apical polarity in three-dimensional culture systems: where to now? J Biol 9: 2.
37. Jain M, Venkatraman G, Moniaux N, Kaur S, Kumar S, et al. (2011) Monoclonal Antibodies Recognizing the Non-Tandem Repeat Regions of the Human Mucin MUC4 in Pancreatic Cancer. PLoS ONE 6: e23344.
38. Bafna S, Kaur S, Batra SK, (2010) Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 29: 2893-2904.
39. Hynes NE, Lane HA, (2005) ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 5: 341-354.
40. Suo Z, Nesland JM, (2000) Phyllodes tumor of the breast: EGFR family expression and relation to clinicopathological features. Ultrastruct Pathol 24: 371-381.
41. Abd El-Rehim DM, Pinder SE, Paish CE, Bell JA, Rampaul RS, et al. (2004) Expression and co-expression of the members of the epidermal growth factor receptor (EGFR) family in invasive breast carcinoma. Br J Cancer 91: 1532-1542.
42. Walker RA, Dearing SJ, (1999) Expression of epidermal growth factor receptor mRNA and protein in primary breast carcinomas. Breast Cancer Res Treat 53: 167-176.
43. Leibl S, Moinfar F, (2005) Metaplastic breast carcinomas are negative for Her-2 but frequently express EGFR (Her-1): potential relevance to adjuvant treatment with EGFR tyrosine kinase inhibitors? J Clin Pathol 58: 700-704.
44. Foulkes WD, Metcalfe K, Hanna W, Lynch HT, Ghadirian P, et al. (2003) Disruption of the expected positive correlation between breast tumor size and lymph node status in BRCA1-related breast carcinoma. Cancer 98: 1569-1577.
45. van de Rijn M, Perou CM, Tibshirani R, Haas P, Kallioniemi O, et al. (2002) Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am J Pathol 161: 1991-1996.
46. Siziopikou KP, Cobleigh M, (2007) The basal subtype of breast carcinomas may represent the group of breast tumors that could benefit from EGFR-targeted therapies. Breast 16: 104-107.
47. Wong ES, Fong CW, Lim J, Yusoff P, Low BC, et al. (2002) Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signalling. EMBO J 21: 4796-4808.
48. Freedman VH, Shin SI, (1974) Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 3: 355-359.
49. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
50. Stetler-Stevenson WG, Aznavoorian S, Liotta LA, (1993) Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol 9: 541-573.
51. Yamaguchi H, Wyckoff J, Condeelis J, (2005) Cell migration in tumors. Curr Opin Cell Biol 17: 559-564.
52. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, et al. (2006) Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9: 261-272.
53. Cance WG, Harris JE, Iacocca MV, Roche E, Yang X, et al. (2000) Immunohistochemical analyses of focal adhesion kinase expression in benign and malignant human breast and colon tissues: correlation with preinvasive and invasive phenotypes. Clin Cancer Res 6: 2417-2423.
54. Muller T, Choidas A, Reichmann E, Ullrich A, (1999) Phosphorylation and free pool of beta-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration. J Biol Chem 274: 10173-10183.
55. Simian M, Hirai Y, Navre M, Werb Z, Lochter A, et al. (2001) The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128: 3117-3131.
56. Wiseman BS, Werb Z, (2002) Stromal effects on mammary gland development and breast cancer. Science 296: 1046-1049.
57. Ponnusamy MP, Lakshmanan I, Jain M, Das S, Chakraborty S, et al. (2010) MUC4 mucin-induced epithelial to mesenchymal transition: a novel mechanism for metastasis of human ovarian cancer cells. Oncogene 29: 5741-5754.
58. Roland CL, Lynn KD, Toombs JE, Dineen SP, Udugamasooriya DG, et al. (2009) Cytokine levels correlate with immune cell infiltration after anti-VEGF therapy in preclinical mouse models of breast cancer. PLoS One 4: e7669.
59. Helfman DM, Kim EJ, Lukanidin E, Grigorian M, (2005) The metastasis associated protein S100A4: role in tumour progression and metastasis. Br J Cancer 92: 1955-1958.
60. Ilg EC, Schafer BW, Heizmann CW, (1996) Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 68: 325-332.
61. Yang G, Truong LD, Timme TL, Ren C, Wheeler TM, et al. (1998) Elevated expression of caveolin is associated with prostate and breast cancer. Clin Cancer Res 4: 1873-1880.
62. Pinilla SM, Honrado E, Hardisson D, Benitez J, Palacios J, (2006) Caveolin-1 expression is associated with a basal-like phenotype in sporadic and hereditary breast cancer. Breast Cancer Res Treat 99: 85-90.
63. Frank PG, Cheung MW, Pavlides S, Llaverias G, Park DS, et al. (2006) Caveolin-1 and regulation of cellular cholesterol homeostasis. Am J Physiol Heart Circ Physiol 291: H677-H686.