P63 regulates tubular formation via epithelial-to-mesenchymal transition

Oncogene

Volumn 33, Issue 12, 2014, Pages 1548-1557

  Zhang, Y ^a   Yan, W ^a   Chen, X ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell proliferation; Epithelial to mesenchymal transition; Migration and invasion; P63; The p53 family; Tubular formation

Indexed keywords

BETA CATENIN; CADHERIN; KALININ; MESSENGER RNA; PROTEIN BAX; PROTEIN P21; PROTEIN P63; PUMA PROTEIN; SCATTER FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR TWIST; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL STRUCTURE; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; MDCK CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THREE DIMENSIONAL IMAGING; UPREGULATION; WESTERN BLOTTING;

MUS;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; DOGS; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE KNOCKDOWN TECHNIQUES; MADIN DARBY CANINE KIDNEY CELLS; PROTEIN ISOFORMS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84897082826     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.101     Document Type: Article

References (58)

1. Osada M, Ohba M, Kawahara C, Ishioka C, Kanamaru R, Katoh I et al. Cloning and functional analysis of human p51, which structurally and functionally resembles p53. Nat Med 1998; 4: 839-843.
2. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V et al. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, deathinducing, and dominant-negative activities. Mol Cell 1998; 2: 305-316.
3. Vanbokhoven H, Melino G, Candi E, Declercq W. p63, a story of mice and men. J Invest Dermatol 2011; 131: 1196-1207.
4. Dohn M, Zhang S, Chen X. p63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 2001; 20: 3193-3205.
5. Westfall MD, Mays DJ, Sniezek JC, Pietenpol JA. The Delta Np63 alpha phosphoprotein binds the p21 and 14-3-3 sigma promoters in vivo and has transcriptional repressor activity that is reduced by Hay-Wells syndrome-derived mutations. Mol Cell Biol 2003; 23: 2264-2276.
6. Sasaki Y, Ishida S, Morimoto I, Yamashita T, Kojima T, Kihara C et al. The p53 family member genes are involved in the Notch signal pathway. J Biol Chem 2002; 277: 719-724.
7. Lo Iacono M, Di Costanzo A, Calogero RA, Mansueto G, Saviozzi S, Crispi S et al. The Hay Wells syndrome-derived TAp63alphaQ540L mutant has impaired transcriptional and cell growth regulatory activity. Cell Cycle 2006; 5: 78-87.
8. Park BJ, Lee SJ, Kim JI, Lee CH, Chang SG, Park JH et al. Frequent alteration of p63 expression in human primary bladder carcinomas. Cancer Res 2000; 60: 3370-3374.
9. Sniezek JC, Matheny KE, Westfall MD, Pietenpol JA. Dominant negative p63 isoform expression in head and neck squamous cell carcinoma. Laryngoscope 2004; 114: 2063-2072.
10. 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.
11. 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.
12. 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.
13. Su X, Paris M, Gi YJ, Tsai KY, Cho MS, Lin YL et al. TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 2009; 5: 64-75.
14. Keyes WM, Wu Y, Vogel H, Guo X, Lowe SW, Mills AA. p63 deficiency activates a program of cellular senescence and leads to accelerated aging. Genes Dev 2005; 19: 1986-1999.
15. Bakkers J, Hild M, Kramer C, Furutani-Seiki M, Hammerschmidt M. Zebrafish DeltaNp63 is a direct target of Bmp signaling and encodes a transcriptional repressor blocking neural specification in the ventral ectoderm. Dev Cell 2002; 2: 617-627.
16. Lee H, Kimelman D. A dominant-negative form of p63 is required for epidermal proliferation in zebrafish. Dev Cell 2002; 2: 607-616.
17. Brunner HG, Hamel BC, Bokhoven HvH. P63 gene mutations and human developmental syndromes. Am J Med Genet 2002; 112: 284-290.
18. 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.
19. Allen LM, Maestri MJ. Three-dimensional sonographic findings associated with ectrodactyly ectodermal dysplasia clefting syndrome. J Ultrasound Med 2008; 27: 149-154.
20. Rinne T, Hamel B, van Bokhoven H, Brunner HG. Pattern of p63 mutations and their phenotypes-update. Am J Med Genet 2006; 140: 1396-1406.
21. van Bokhoven H, Hamel BC, Bamshad M, Sangiorgi E, Gurrieri F, Duijf PH et al. p63 Gene mutations in EEC syndrome, limb-mammary syndrome, and isolated split hand-split foot malformation suggest a genotype-phenotype correlation. Am J Hum Genet 2001; 69: 481-492.
22. Lindsay J, McDade SS, Pickard A, McCloskey KD, McCance DJ. Role of DeltaNp63-gamma in epithelial to mesenchymal transition. J Biol Chem 2011; 286: 3915-3924.
23. Zhang Y, Yan W, Chen X. Mutant p53 disrupts MCF-10A cell polarity in threedimensional culture via epithelial-to-mesenchymal transitions. J Biol Chem 2011; 286: 16218-16228.
24. Simons K, Fuller SD. Cell surface polarity in epithelia. Annu Rev Cell Biol 1985; 1: 243-288.
25. Leighton J, Estes LW, Mansukhani S, Brada Z. A cell line derived from normal dog kidney (MDCK) exhibiting qualities of papillary adenocarcinoma and of renal tubular epithelium. Cancer 1970; 26: 1022-1028.
26. McAteer JA, Evan AP, Gardner KD. Morphogenetic clonal growth of kidney epithelial cell line MDCK. Anat Rec 1987; 217: 229-239.
27. Montesano R, Schaller G, Orci L. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 1991; 66: 697-711.
28. Saxen L, Sariola H. Early organogenesis of the kidney. Pediatr Nephrol 1987; 1: 385-392.
29. Zhang J, Chen X, Kent MS, Rodriguez CO. Establishment of a dog model for the p53 family pathway and identification of a novel isoform of p21 cyclin-dependent kinase inhibitor. Mol Cancer Res 2009; 7: 67-78.
30. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009; 119: 1429-1437.
31. Carroll DK, Carroll JS, Leong CO, 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.
32. Zheng Z, Zhu H, Wan Q, Liu J, Xiao Z, Siderovski DP et al. LGN regulates mitotic spindle orientation during epithelial morphogenesis. J Cell Biol 2010; 189: 275-288.
33. Prindull G, Zipori D. Environmental guidance of normal and tumor cell plasticity: epithelial mesenchymal transitions as a paradigm. Blood 2004; 103: 2892-2899.
34. Kim D, Dressler GR. Nephrogenic factors promote differentiation of mouse embryonic stem cells into renal epithelia. J Am Soc Nephrol 2005; 16: 3527-3534.
35. Jia L, Liu F, Hansen SH, Ter Beest MB, Zegers MM. Distinct roles of cadherin-6 and E-cadherin in tubulogenesis and lumen formation. Mol Biol Cell 2011; 22: 2031-2041.
36. Tan M, Wang Y, Guan K, Y Sun. PTGF-beta, a type beta transforming growth factor (TGF-beta) superfamily member, is a p53 target gene that inhibits tumor cell growth via TGF-beta signaling pathway. Proc Natl Acad Sci USA 2000; 97: 109-114.
37. Lipschutz JH, Guo W, O'Brien LE, Nguyen YH, Novick P, Mostov KE. Exocyst is involved in cystogenesis and tubulogenesis and acts by modulating synthesis and delivery of basolateral plasma membrane and secretory proteins. Mol Biol Cell 2000; 11: 4259-4275.
38. Dressler G. Tubulogenesis in the developing mammalian kidney. Trends Cell Biol 2002; 12: 390-395.
39. Guo X, Keyes WM, Papazoglu C, Zuber J, Li W, Lowe SW et al. TAp63 induces senescence and suppresses tumorigenesis in vivo. Nat Cell Biol 2009; 11: 1451-1457.
40. Su X, Chakravarti D, Cho MS, Liu L, Gi YJ, Lin YL et al. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 2010; 467: 986-990.
41. Zeisberg M, Shah AA, Kalluri R. Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. J Biol Chem 2005; 280: 8094-8100.
42. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
43. Cook HT. The origin of renal fibroblasts and progression of kidney disease. Am J Pathol 2010; 176: 22-24.
44. Peinado H, Olmeda D, A Cano. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Revi Cancer 2007; 7: 415-428.
45. Ihrie RA, Marques MR, Nguyen BT, Horner JS, Papazoglu C, Bronson RT et al. Perp is a p63-regulated gene essential for epithelial integrity. Cell 2005; 120: 843-856.
46. 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.
47. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 2008; 22: 894-907.
48. 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.
49. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
50. 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.
51. O'Brien LE, Tang K, Kats ES, Schutz-Geschwender A, Lipschutz JH, KE Mostov. ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev Cell 2004; 7: 21-32.
52. Pollack AL, Runyan RB, Mostov KE. Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev Biol 1998; 204: 64-79.
53. Cao Y, Wang L, Nandy D, Zhang Y, Basu A, Radisky D et al. Neuropilin-1 upholds dedifferentiation and propagation phenotypes of renal cell carcinoma cells by activating Akt and sonic hedgehog axes. Cancer Res 2008; 68: 8667-8672.
54. Zimmers TA, Jin X, Hsiao EC, McGrath SA, Esquela AF, Koniaris LG. Growth differentiation factor-15/macrophage inhibitory cytokine-1 induction after kidney and lung injury. Shock 2005; 23: 543-548.
55. O'Brien LE, Yu W, Tang K, Jou TS, Zegers MM, Mostov KE. Morphological and biochemical analysis of Rac1 in three-dimensional epithelial cell cultures. Methods Enzymol 2006; 406: 676-691.
56. Liu G, Chen X. DNA polymerase eta, the product of the xeroderma pigmentosum variant gene and a target of p53, modulates the DNA damage checkpoint and p53 activation. Mol Cell Biol 2006; 26: 1398-1413.
57. Sensen CW, Charlebois RL, Chow C, Clausen IG, Curtis B, Doolittle WF et al. Completing the sequence of the Sulfolobus solfataricus P2 genome. Extremophiles 1998; 2: 305-312.
58. Zhang Y, Shu L, Chen X. Syntaxin 6, a regulator of the protein trafficking machinery and a target of the p53 family, is required for cell adhesion and survival. J Biol Chem 2008; 283: 30689-30698.