ΔNp63α activates CD82 metastasis suppressor to inhibit cancer cell invasion

Cell Death and Disease

Volumn 5, Issue 6, 2014, Pages

  Wu, J ^a   Liang, S ^b   Bergholz, J ^b   He, H ^b   Walsh, E M ^c   Zhang, Y ^b   Xiao, Z X ^b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SICHUAN UNIVERSITY   (China)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

CD82; Cell invasion; GSK3 ; KAI1; P63; catenin

Indexed keywords

ANTIMETASTATIC AGENT; BETA CATENIN; CD82 ANTIGEN; DELTANP63ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; MATRIGEL; RNA; UNCLASSIFIED DRUG; CD82 PROTEIN, HUMAN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; TP63 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL INVASION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIAL CANCER CELL LINE; GAIN OF FUNCTION MUTATION; GENE EXPRESSION PROFILING; GENE SILENCING; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; METASTASIS INHIBITION; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SQUAMOUS CELL CARCINOMA CELL LINE; TRANSCRIPTION INITIATION; UPREGULATION; GENETICS; METABOLISM; METASTASIS; NEOPLASM; PATHOLOGY; TUMOR INVASION;

ANTIGENS, CD82; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84903787438     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.239     Document Type: Article

References (67)

1. Bergholz J, Xiao Z-X. Role of p63 in development, tumorigenesis and cancer progression. Cancer Microenviron 2012; 5: 311-322.
2. Candi E, Cipollone R, Rivetti di Val Cervo P, Gonfloni S, Melino G, Knight R. P63 in epithelial development. Cell Mol Life Sci 2008; 65: 3126-3133.
3. Celli J, Duijf P, Hamel BC, Bamshad M, Kramer B, Smits AP et al. Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome. Cell 1999; 99: 143-153.
4. McGrath JA, Duijf PH, Doetsch V, Irvine AD, de Waal R, Vanmolkot KR et al. Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum Mol Genet 2001; 10: 221-229.
5. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. P63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999; 398: 708-713.
6. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT et al. P63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999; 398: 714-718.
7. Gonfloni S, Di Tella L, Caldarola S, Cannata SM, Klinger FG, Di Bartolomeo C et al. Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nat Med 2009; 15: 1179-1185.
8. Suh E-K, Yang A, Kettenbach A, Bamberger C, Michaelis AH, Zhu Z et al. P63 protects the female germ line during meiotic arrest. Nature 2006; 444: 624-628.
9. Senoo M, Pinto F, Crum CP, McKeon F. P63 is essential for the proliferative potential of stem cells in stratified epithelia. Cell 2007; 129: 523-536.
10. Shalom-Feuerstein R, Lena AM, Zhou H, De La Forest Divonne S, Van Bokhoven H, Candi E et al. DNp63 is an ectodermal gatekeeper of epidermal morphogenesis. Cell Death Differ 2010; 18: 887-896.
11. Hagiwara K, McMenamin MG, Miura K, Harris CC. Mutational analysis of the p63/p73L/ p51/p40/CUSP/KET gene in human cancer cell lines using intronic primers. Cancer Res 1999; 59: 4165-4169.
12. Sunahara M, Shishikura T, Takahashi M, Todo S, Yamamoto N, Kimura H et al. Mutational analysis of p51A/TAp63gamma, a p53 homolog, in non-small cell lung cancer and breast cancer. Oncogene 1999; 18: 3761-3765.
13. Hibi K, Trink B, Patturajan M, Westra WH, Caballero OL, Hill DE et al. AIS is an oncogene amplified in squamous cell carcinoma. Proc Natl Acad Sci USA 2000; 97: 5462-5467.
14. Massion PP, Taflan PM, Jamshedur Rahman SM, Yildiz P, Shyr Y, Edgerton ME et al. Significance of p63 amplification and overexpression in lung cancer development and prognosis. Cancer Res 2003; 63: 7113-7121.
15. DeYoung MP, Johannessen CM, Leong C-O, Faquin W, Rocco JW, Ellisen LW. Tumor-specific p73 up-regulation mediates p63 dependence in squamous cell carcinoma. Cancer Res 2006; 66: 9362-9368.
16. Rocco JW, Leong C-O, Kuperwasser N, DeYoung MP, Ellisen LW. p63 mediates survival in squamous cell carcinoma by suppression of p73-dependent apoptosis. Cancer Cell 2006; 9: 45-56.
17. Keyes WM, Pecoraro M, Aranda V, Vernersson-Lindahl E, Li W, Vogel H et al. DNp63a is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell 2011; 8: 164-176.
18. Flores ER, Sengupta S, Miller JB, Newman JJ, Bronson R, Crowley D et al. Tumor predisposition in mice mutant for p63 and p73: evidence for broader tumor suppressor functions for the p53 family. Cancer Cell 2005; 7: 363-373.
19. Su X, Chakravarti D, Cho MS, Liu L, Gi YJ, Lin Y-L et al. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 2010; 467: 986-990.
20. Barbieri CE, Tang LJ, Brown KA, Pietenpol JA. Loss of p63 leads to increased cell migration and up-regulation of genes involved in invasion and metastasis. Cancer Res 2006; 66: 7589-7597.
21. Fukushima H, Koga F, Kawakami S, Fujii Y, Yoshida S, Ratovitski E et al. Loss of DeltaNp63alpha promotes invasion of urothelial carcinomas via N-cadherin/Src homology and collagen/extracellular signal-regulated kinase pathway. Cancer Res 2009; 69: 9263-9270.
22. Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 2005; 6: 801-811.
23. Dong JT, Lamb PW, Rinker-Schaeffer CW, Vukanovic J, Ichikawa T, Isaacs JT et al. KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 1995; 268: 884-886.
24. Zhang XA, He B, Zhou B, Liu L. Requirement of the p130CAS-Crk coupling for metastasis suppressor KAI1/CD82-mediated inhibition of cell migration. J Biol Chem 2003; 278: 27319-27328.
25. Odintsova E, Sugiura T, Berditchevski F. Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin CD82/KAI-1. Curr Biol 2000; 10: 1009-1012.
26. Odintsova E, Voortman J, Gilbert E, Berditchevski F. Tetraspanin CD82 regulates compartmentalisation and ligand-induced dimerization of EGFR. J Cell Sci 2003; 116(Part 22): 4557-4566.
27. Marreiros A, Dudgeon K, Dao V, Grimm M-O, Czolij R, Crossley M et al. KAI1 promoter activity is dependent on p53, junB and AP2: evidence for a possible mechanism underlying loss of KAI1 expression in cancer cells. Oncogene 2005; 24: 637-649.
28. Mashimo T, Watabe M, Hirota S, Hosobe S, Miura K, Tegtmeyer PJ et al. The expression of the KAI1 gene, a tumor metastasis suppressor, is directly activated by p53. Proc Natl Acad Sci USA 1998; 95: 11307-11311.
29. Jacobs KM, Bhave SR, Ferraro DJ, Jaboin JJ, Hallahan DE, Thotala D. GSK-3b: a bifunctional role in cell death pathways. Int J Cell Biol 2012; 2012: 930710.
30. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat Rev Genet 2004; 5: 691-701.
31. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M et al. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 2004; 6: 931-940.
32. Batlle E, Sancho E, FrancíC, Domínguez D, Monfar M, Baulida J et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000; 2: 84-89.
33. Candi E, Rufini A, Terrinoni A, Dinsdale D, Ranalli M, Paradisi A et al. Differential roles of p63 isoforms in epidermal development: selective genetic complementation in p63 null mice. Cell Death Differ 2006; 13: 1037-1047.
34. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dötsch V et al. Pp63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 1998; 2: 305-316.
35. Fu SW, Schwartz A, Stevenson H, Pinzone JJ, Davenport GJ, Orenstein JM et al. Correlation of expression of BP1, a homeobox gene, with estrogen receptor status in breast cancer. Breast Cancer Res 2003; 5: R82-R87.
36. Miranti CK. Controlling cell surface dynamics and signaling: how CD82/KAI1 suppresses metastasis. Cell Signal 2009; 21: 196-211.
37. Carroll DK, Carroll JS, Leong C-O, Cheng F, Brown M, Mills AA et al. P63 regulates an adhesion programme and cell survival in epithelial cells. Nat Cell Biol 2006; 8: 551-561.
38. Kim JH, Kim B, Cai L, Choi HJ, Ohgi KA, Tran C et al. Transcriptional regulation of a metastasis suppressor gene by Tip60 and beta-catenin complexes. Nature 2005; 434: 921-926.
39. Helton ES, Zhu J, Chen X. The unique NH2-terminally deleted (DeltaN) residues, the PXXP motif, and the PPXY motif are required for the transcriptional activity of the DeltaN variant of p63. J Biol Chem 2006; 281: 2533-2542.
40. Browne G, Cipollone R, Lena AM, Serra V, Zhou H, van Bokhoven H et al. Differential altered stability and transcriptional activity of DNp63 mutants in distinct ectodermal dysplasias. J Cell Sci 2011; 124(Part 13): 2200-2207.
41. Freed-Pastor WA, Prives C. Mutant p53: one name, many proteins. Genes Dev 2012; 26: 1268-1286.
42. Duijf PHG, Vanmolkot KRJ, Propping P, Friedl W, Krieger E, McKeon F et al. Gain-offunction mutation in ADULT syndrome reveals the presence of a second transactivation domain in p63. Hum Mol Genet 2002; 11: 799-804.
43. Chung J, Grant RI, Kaplan DR, Irwin MS. Special AT-rich binding protein-2 (SATB2) differentially affects disease-causing p63 mutant proteins. J Biol Chem 2011; 286: 40671-40680.
44. Tucci P, Agostini M, Grespi F, Markert EK, Terrinoni A, Vousden KH et al. Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer. Proc Natl Acad Sci USA 2012; 109: 15312-15317.
45. Higashikawa K, Yoneda S, Tobiume K, Saitoh M, Taki M, Mitani Y et al. DeltaNp63alphadependent expression of Id-3 distinctively suppresses the invasiveness of human squamous cell carcinoma. Int J Cancer 2009; 124: 2837-2844.
46. Higashikawa K, Yoneda S, Tobiume K, Taki M, Shigeishi H, Kamata N. Snail-induced down-regulation of DeltaNp63alpha acquires invasive phenotype of human squamous cell carcinoma. Cancer Res 2007; 67: 9207-9213.
47. Herfs M, Hubert P, Suarez-Carmona M, Reschner A, Saussez S, Berx G et al. Regulation of p63 isoforms by Snail and Slug transcription factors in human squamous cell carcinoma. Am J Pathol 2010; 176: 1941-1949.
48. Koga F, Kawakami S, Fujii Y, Saito K, Ohtsuka Y, Iwai A et al. Impaired p63 expression associates with poor prognosis and uroplakin III expression in invasive urothelial carcinoma of the bladder. Clin Cancer Res 2003; 9: 5501-5507.
49. Urist MJ, Di Como CJ, Lu M-L, Charytonowicz E, Verbel D, Crum CP et al. Loss of p63 expression is associated with tumor progression in bladder cancer. Am J Pathol 2002; 161: 1199-1206.
50. Wang X, Mori I, Tang W, Nakamura M, Nakamura Y, Sato M et al. P63 expression in normal, hyperplastic and malignant breast tissues. Breast Cancer 2002; 9: 216-219.
51. Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, Hann B et al. A mutant-p53/ Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 2009; 137: 87-98.
52. Muller PAJ, Caswell PT, Doyle B, Iwanicki MP, Tan EH, Karim S et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 2009; 139: 1327-1341.
53. Tan EH, Morton JP, Timpson P, Tucci P, Melino G, Flores ER et al. Functions of TAp63 and p53 in restraining the development of metastatic cancer. Oncogene 2014; 33: 3325-3333.
54. Barbareschi M, Pecciarini L, Cangi MG, Macrì E, Rizzo A, Viale G et al. P63, a p53 homologue, is a selective nuclear marker of myoepithelial cells of the human breast. Am J Surg Pathol 2001; 25: 1054-1060.
55. Romano R-A, Ortt K, Birkaya B, Smalley K, Sinha S. An active role of the DeltaN isoform of p63 in regulating basal keratin genes K5 and K14 and directing epidermal cell fate. PLoS One 2009; 4: e5623.
56. Bergholz J, Zhang Y, Wu J, Meng L, Walsh EM, Rai A et al. DNp63a regulates Erk signaling via MKP3 to inhibit cancer metastasis. Oncogene 2014; 33: 212-224.
57. Liu F-S, Dong J-T, Chen J-T, Hsieh Y-T, Ho ES-C, Hung M-J et al. KAI1 metastasis suppressor protein is down-regulated during the progression of human endometrial cancer. Clin Cancer Res 2003; 9: 1393-1398.
58. Liu FS, Chen JT, Dong JT, Hsieh YT, Lin AJ, Ho ES et al. KAI1 metastasis suppressor gene is frequently down-regulated in cervical carcinoma. Am J Pathol 2001; 159: 1629-1634.
59. Liu FS, Dong JT, Chen JT, Hsieh YT, Ho ES, Hung MJ. Frequent down-regulation and lack of mutation of the KAI1 metastasis suppressor gene in epithelial ovarian carcinoma. Gynecol Oncol 2000; 78: 10-15.
60. Yang X, Wei L, Tang C, Slack R, Montgomery E, Lippman M. KAI1 protein is down-regulated during the progression of human breast cancer. Clin Cancer Res 2000; 6: 3424-3429.
61. Phillips KK, White AE, Hicks DJ, Welch DR, Barrett JC, Wei LL et al. Correlation between reduction of metastasis in the MDA-MB-435 model system and increased expression of the Kai-1 protein. Mol Carcinogen 1998; 21: 111-120.
62. Takaoka A, Hinoda Y, Sato S, Itoh F, Adachi M, Hareyama M et al. Reduced invasive and metastatic potentials of KAI1-transfected melanoma cells. Jpn J Cancer Res 1998; 89: 397-404.
63. Yang X, Welch DR, Phillips KK, Weissman BE, Wei LL. KAI1, a putative marker for metastatic potential in human breast cancer. Cancer Lett 1997; 119: 149-155.
64. Eicheler W, Zips D, Dörfler A, Grénman R, Baumann M. Splicing mutations in TP53 in human squamous cell carcinoma lines influence immunohistochemical detection. J Histochem Cytochem 2002; 50: 197-204.
65. Zhou B, Liu L, Reddivari M, Zhang XA. The palmitoylation of metastasis suppressor KAI1/ CD82 is important for its motility-and invasiveness-inhibitory activity. Cancer Res 2004; 64: 7455-7463.
66. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
67. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37: 1-13.