Excess PLAC8 promotes an unconventional ERK2-dependent EMT in colon cancer

Journal of Clinical Investigation

Volumn 124, Issue 5, 2014, Pages 2172-2187

  Li, Cunxi ^a,f   Ma, Haiting ^b   Wang, Yang ^a   Cao, Zheng ^a   Graves Deal, Ramona ^a   Powell, Anne E ^a   Starchenko, Alina ^c   Ayers, Gregory D ^a   Washington, Mary Kay ^a   Kamath, Vidya ^d   Desai, Keyur ^d   Gerdes, Michael J ^d   Solnica Krezel, Lila ^b   Coffey, Robert J ^a,c,e  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GE GLOBAL RESEARCH   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

^f Beijing Jiaen Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OCCLUDIN; P CADHERIN; PLACENTA SPECIFIC 8; PROTEIN; PROTEIN ZO1; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ANIMAL CELL; ARTICLE; CANCER CELL LINE; CANCER GRADING; CANCER GROWTH; CELL DIFFERENTIATION; CELL MOTILITY; CELL SURFACE; COLON CANCER; COLON MUCOSA; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GASTRULATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; TISSUE MICROARRAY; TUMOR GROWTH; TUMOR INVASION; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; CADHERINS; CELL LINE, TUMOR; COLONIC NEOPLASMS; DUAL SPECIFICITY PHOSPHATASE 6; EPITHELIAL-MESENCHYMAL TRANSITION; HEK293 CELLS; HUMANS; INTESTINAL MUCOSA; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PROTEINS; VIMENTIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84899768764     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71103     Document Type: Article

References (89)

1. Rissoan MC, et al. Subtractive hybridization reveals the expression of immunoglobulin-like transcript 7, Eph-B1, granzyme B, and 3 novel transcripts in human plasmacytoid dendritic cells. Blood. 2002;100(9):3295-3303.
2. Galaviz-Hernandez C, et al. Plac8 and Plac9, novel placental-enriched genes identified through microarray analysis. Gene. 2003;309(2):81-89.
3. Ledford JG, Kovarova M, Koller BH. Impaired host defense in mice lacking ONZIN. J Immunol. 2007;178(8):5132-5143.
4. Ledford JG, Kovarova M, Jania LA, Nguyen M, Koller BH. ONZIN deficiency attenuates contact hypersensitivity responses in mice. Immunol Cell Biol. 2012;90(7):733-742.
5. Jimenez-Preitner M, et al. Plac8 is an inducer of C/ EBPbeta required for brown fat differentiation, thermoregulation, and control of body weight. Cell Metab. 2011;14(5):658-670.
6. Jimenez-Preitner M, Berney X, Thorens B. Plac8 is required for white adipocyte differentiation in vitro and cell number control in vivo. PLoS One. 2012;7(11):e48767.
7. McMurray HR, et al. Synergistic response to oncogenic mutations defines gene class critical to cancer phenotype. Nature. 2008;453(7198):1112-1116.
8. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial- mesenchymal transitions in development and disease. Cell. 2009;139(5):871-90.
9. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest. 2009; 119(6):1420-1428.
10. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744-749.
11. Nieto MA. Epithelial plasticity: a common theme in embryonic and cancer cells. Science. 2013; 342(6159):1234850.
12. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147(2):275-292.
13. Smith SC, Theodorescu D. Learning therapeutic lessons from metastasis suppressor proteins. Nat Rev Cancer. 2009;9(4):253-264.
14. Nieto MA, Sargent MG, Wilkinson DG, Cooke J. Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science. 1994; 264(5160):835-839.
15. Brabletz T, et al. Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal- epithelial transition, stem cells and betacatenin. Cells Tissues Organs. 2005;179(1-2):56-65.
16. Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell. 2004;118(3):277-279.
17. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial- mesenchymal transitions. Nat Rev Mol Cell Biol. 2006;7(2):131-142.
18. Baum B, Settleman J, Quinlan MP. Transitions between epithelial and mesenchymal states in development and disease. Semin Cell Dev Biol. 2008;19(3):294-308.
19. Park J, et al. Down-regulation of P-cadherin with PF-03732010 inhibits cell migration and tumor growth in gastric cancer. Invest New Drugs. 2012; 30(4):1404-1412.
20. Sun L, et al. P-cadherin promotes liver metastasis and is associated with poor prognosis in colon cancer. Am J Pathol. 2011;179(1):380-390.
21. Hardy RG, et al. Aberrant P-cadherin expression is an early event in hyperplastic and dysplastic transformation in the colon. Gut. 2002;50(4):513-519.
22. Shin S, Dimitri CA, Yoon SO, Dowdle W, Blenis J. ERK2 but not ERK1 induces epithelial-to-mesenchymal transformation via DEF motif-dependent signaling events. Mol Cell. 2010;38(1):114-127.
23. Muda M, et al. MKP-3, a novel cytosolic proteintyrosine phosphatase that exemplifies a new class of mitogen-activated protein kinase phosphatase. J Biol Chem. 1996;271(8):4319-4326.
24. Powell AE, et al. The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell. 2012;149(1):146-158.
25. Leibovitz A, et al. Classification of human colorectal adenocarcinoma cell lines. Cancer Res. 1976;36(12):4562-4569.
26. Kitadai Y, et al. Regulation of carcinoembryonic antigen expression in human colon carcinoma cells by the organ microenvironment. Am J Pathol. 1996;149(4):1157-1166.
27. Drewinko B, Romsdahl MM, Yang LY, Ahearn MJ, Trujillo JM. Establishment of a human carcinoembryonic antigen-producing colon adenocarcinoma cell line. Cancer Res. 1976;36(2 pt 1):467-475.
28. Santoriello C, Zon LI. Hooked! Modeling human disease in zebrafish. J Clin Invest. 2012;122(7):2337-2343.
29. Moreno-Hagelsieb G, Latimer K. Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics. 2008;24(3):319-324.
30. Woods IG, et al. A comparative map of the zebrafish genome. Genome Res. 2000;10(12):1903-1914.
31. Concha ML, Adams RJ. Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development. 1998;125(6):983-994.
32. Sepich DS, Usmani M, Pawlicki S, Solnica-Krezel L. Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements. Development. 2011;138(3):543-552.
33. Schulte-Merker S, van Eeden FJ, Halpern ME, Kimmel CB, Nusslein-Volhard C. no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development. 1994;120(4):1009-1015.
34. Lin F, et al. G12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J Cell Biol. 2009;184(6):909-921.
35. Babb SG, Marrs JA. E-cadherin regulates cell movements and tissue formation in early zebrafish embryos. Dev Dyn. 2004;230(2):263-277.
36. Shimizu T, et al. E-cadherin is required for gastrulation cell movements in zebrafish. Mech Dev. 2005;122(6):747-763.
37. Kane DA, McFarland KN, Warga RM. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development. 2005;132(5):1105-1116.
38. McFarland KN, Warga RM, Kane DA. Genetic locus half baked is necessary for morphogenesis of the ectoderm. Dev Dyn. 2005;233(2):390-406.
39. Ashby WJ, Zijlstra A. Established and novel methods of interrogating two-dimensional cell migration. Integr Biol (Camb). 2012;4(11):1338-1350.
40. Piepenhagen PA, Nelson WJ. Defining E-cadherinassociated protein complexes in epithelial cells: plakoglobin, and catenin are distinct components. J Cell Sci. 1993;104(pt 3):751-762.
41. Soini Y. Tight junctions in lung cancer and lung metastasis: a review. Int J Clin Exp Pathol. 2012; 5(2):126-136.
42. Masuda R, Semba S, Mizuuchi E, Yanagihara K, Yokozaki H. Negative regulation of the tight junction protein tricellulin by snail-induced epithelialmesenchymal transition in gastric carcinoma cells. Pathobiology. 2010;77(2):106-113.
43. Ohkubo T, Ozawa M. The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J Cell Sci. 2004;117(pt 9):1675-1685.
44. Javle MM, et al. Epithelial-mesenchymal transition (EMT) and activated extracellular signal-regulated kinase (p-Erk) in surgically resected pancreatic cancer. Ann Surg Oncol. 2007;14(12):3527-3533.
45. Larue L, Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3'kinase/AKT pathways. Oncogene. 2005;24(50):7443-7454.
46. Grille SJ, et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 2003;63(9):2172-2178.
47. Guarino M. Src signaling in cancer invasion. J Cell Physiol. 2010;223(1):14-26.
48. Rogulski K, et al. Onzin, a c-Myc-repressed target, promotes survival and transformation by modulating the Akt-Mdm2-p53 pathway. Oncogene. 2005;24(51):7524-7541.
49. Kwak SP, Dixon JE. Multiple dual specificity protein tyrosine phosphatases are expressed and regulated differentially in liver cell lines. J Biol Chem. 1995;270(3):1156-1160.
50. Todd JL, Tanner KG, Denu JM. Extracellular regulated kinases (ERK) 1 and ERK2 are authentic substrates for the dual-specificity protein-tyrosine phosphatase VHR. A novel role in down-regulating the ERK pathway. J Biol Chem. 1999;274(19):13271-13280.
51. Keyse SM. Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev. 2008;27(2):253-261.
52. Camps M, et al. Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science. 1998;280(5367):1262-1265.
53. Nelson DA, et al. Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation. Biol Open. 2013;2(5):439-447.
54. Gerdes MJ, et al. Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue. Proc Natl Acad Sci U S A. 2013;110(29):11982-11987.
55. Libault M, Stacey G. Evolution of FW2.2-like (FWL) and PLAC8 genes in eukaryotes. Plant Signal Behav. 2010;5(10):1226-1228.
56. Song WY, Hortensteiner S, Tomioka R, Lee Y, Martinoia E. Common functions or only phylogenetically related? The large family of PLAC8 motifcontaining/ PCR genes. Mol Cells. 2011;31(1):1-7.
57. Guo M, et al. Cell Number Regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. Plant Cell. 2010;22(4):1057-1073.
58. Hughes L, O'Brien SL, Gallagher WM, McDonnell S. DNA microarray-based transcriptomic profiling of an isogenic cell culture model of breast tumour cell invasion. Anticancer Res. 2007; 27(3A):1353-1359.
59. Uehara H, Takahashi T, Izumi K. Induction of retinol-binding protein 4 and placenta-specific 8 expression in human prostate cancer cells remaining in bone following osteolytic tumor growth inhibition by osteoprotegerin. Int J Oncol. 2013; 43(2):365-374.
60. Abdel-Rahman WM, et al. Spectral karyotyping suggests additional subsets of colorectal cancers characterized by pattern of chromosome rearrangement. Proc Natl Acad Sci U S A. 2001;98(5):2538-2543.
61. Paredes J, et al. Epithelial E- and P-cadherins: role and clinical significance in cancer. Biochim Biophys Acta. 2012;1826(2):297-311.
62. Mandeville JA, et al. P-cadherin as a prognostic indicator and a modulator of migratory behaviour in bladder carcinoma cells. BJU Int. 2008; 102(11):1707-1714.
63. Paredes J, Correia AL, Ribeiro AS, Milanezi F, Cameselle- Teijeiro J, Schmitt FC. Breast carcinomas that co-express E- and P-cadherin are associated with p120-catenin cytoplasmic localisation and poor patient survival. J Clin Pathol. 2008;61(7):856-862.
64. Taniuchi K, et al. Overexpressed P-cadherin/CDH3 promotes motility of pancreatic cancer cells by interacting with p120ctn and activating rho-family GTPases. Cancer Res. 2005;65(8):3092-3099.
65. Paredes J, et al. P-cadherin is up-regulated by the antiestrogen ICI 182,780 and promotes invasion of human breast cancer cells. Cancer Res. 2004;64(22):8309-8317.
66. Cheung LW, Leung PC, Wong AS. Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene. 2010;29(16):2427-2440.
67. Ireton RC, et al. A novel role for p120 catenin in E-cadherin function. J Cell Biol. 2002;159(3):465-476.
68. Ji H, et al. EGF-induced ERK activation promotes CK2-mediated disassociation of catenin from catenin and transactivation of catenin. Mol Cell. 2009;36(4):547-559.
69. Fang D, et al. Phosphorylation of catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem. 2007;282(15):11221-11229.
70. Fujita Y, et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol. 2002;4(3):222-231.
71. Sepich DS, Solnica-Krezel L. Analysis of cell movements in zebrafish embryos: morphometrics and measuring movement of labeled cell populations in vivo. Methods Mol Biol. 2005;294:211-33.
72. Lin F, et al. Essential roles of G12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements. J Cell Biol. 2005;169(5):777-787.
73. Speirs CK, et al. Prostaglandin G signaling stimulates gastrulation movements by limiting cell adhesion through Snai1a stabilization. Development. 2010;137(8):1327-1337.
74. von der Hardt S, et al. The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr Biol. 2007; 17(6):475-487.
75. Barone V, Heisenberg CP. Cell adhesion in embryo morphogenesis. Curr Opin Cell Biol. 2012; 24(1):148-153.
76. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol. 2004;16(1):14-23.
77. Hall HG, Farson DA, Bissell MJ. Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture. Proc Natl Acad Sci U S A. 1982;79(15):4672-4676.
78. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer. 2005;5(9):675-688.
79. Jaffe AB, Kaji N, Durgan J, Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J Cell Biol. 2008;183(4):625-633.
80. Coffey RJ, et al. Epidermal growth factor receptor activation induces nuclear targeting of cyclooxygenase-2, basolateral release of prostaglandins, and mitogenesis in polarizing colon cancer cells. Proc Natl Acad Sci U S A. 1997;94(2):657-662.
81. Meylan E, et al. Requirement for NF-B signalling in a mouse model of lung adenocarcinoma. Nature. 2009;462(7269):104-107.
82. Topczewska JM, Topczewski J, Shostak A, Kume T, Solnica-Krezel L, Hogan BL. The winged helix transcription factor Foxc1a is essential for somitogenesis in zebrafish. Genes Dev. 2001;15(18):2483-93.
83. Euhus DM, Hudd C, LaRegina MC, Johnson FE. Tumor measurement in the nude mouse. J Surg Oncol. 1986;31(4):229-234.
84. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol. 1989;24(3):148-154.
85. Thisse C, Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc. 2008;3(1):59-69.
86. Sepich DS, Calmelet C, Kiskowski M, Solnica-Krezel L. Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation. Dev Dyn. 2005;234(2):279-292.
87. Hinnen A, Hicks JB, Fink GR. Transformation of yeast. Proc Natl Acad Sci U S A. 1978;75(4):1929-1933.
88. Lazo JS, et al. Discovery and biological evaluation of a new family of potent inhibitors of the dual specificity protein phosphatase Cdc25. J Med Chem. 2001;44(24):4042-4049.
89. Lazo JS, Nunes R, Skoko JJ, Queiroz de Oliveira PE, Vogt A, Wipf P. Novel benzofuran inhibitors of human mitogen-activated protein kinase phosphatase-1. Bioorg Med Chem. 2006;14(16):5643-5650.