Molecular basis of S100 proteins interacting with the p53 homologs p63 and p73

Oncogene

Volumn 29, Issue 14, 2010, Pages 2024-2035

  Van Dieck, J ^a   Brandt, T ^a   Teufel, D P ^a   Veprintsev, D B ^a   Joerger, A C ^a   Fersht, A R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

P63; P73; Protein?protein interaction; S100; Tumor suppressor

Indexed keywords

CALCIUM; CALCYCLIN; CALVASCULIN; PROTEIN P53; PROTEIN P63; PROTEIN P73; PROTEIN S 100; PROTEIN S100A1; PROTEIN S100A2; PROTEIN S100B; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; GEL FILTRATION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; TRANSACTIVATION; ULTRACENTRIFUGATION;

ANIMALS; CALCIUM; CHROMATOGRAPHY, GEL; DNA-BINDING PROTEINS; FLUORESCENCE POLARIZATION; HUMANS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; S100 PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; ULTRACENTRIFUGATION;

EID: 77950858234     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.490     Document Type: Article

References (56)

1. Baudier J, Delphin C, Grunwald D, Khochbin S, Lawrence JJ. (1992). Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc Natl Acad Sci USA 89: 11627-11631.
2. Boldrup L, Coates PJ, Gu X, Nylander K. (2009). DeltaNp63 isoforms differentially regulate gene expression in squamous cell carcinoma: identification of Cox-2 as a novel p63 target. J Pathol 218: 428-436.
3. Brandt T, Petrovich M, Joerger AC, Veprintsev DB. (2009). Conservation of DNA-binding specificity and oligomerisation properties within the p53 family. BMC Genomics 10: 628.
4. Buckiova D, Syka J. (2009). Calbindin and S100 protein expression in the developing inner ear in mice. J Comp Neurol 513: 469-482.
5. Burge S, Teufel DP, Townsley FM, Freund SM, Bycroft M, Fersht AR. (2009). Molecular basis of the interactions between the p73 N terminus and p300: effects on transactivation and modulation by phosphorylation. Proc Natl Acad Sci USA 106: 3142-3147.
6. Chan WY, Xia CL, Dong DC, Heizmann CW, Yew DT. (2003). Differential expression of S100 proteins in the developing human hippocampus and temporal cortex. Microsc Res Tech 60: 600-613.
7. Danilova N, Sakamoto KM, Lin S. (2008). p53 family in development. Mech Dev 125: 919-931.
8. Dean B, Gray L, Scarr E. (2006). Regionally specific changes in levels of cortical S100beta in bipolar 1 disorder but not schizophrenia. Aust N Z J Psychiatry 40: 217-224.
9. Deyoung MP, Ellisen LW. (2007). p63 and p73 in human cancer: defining the network. Oncogene 26: 5169-5183.
10. Donato R. (2003). Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60: 540-551.
11. Dotto JE, Glusac EJ. (2006). p63 is a useful marker for cutaneous spindle cell squamous cell carcinoma. J Cutan Pathol 33: 413-417.
12. Fano G, Biocca S, Fulle S, Mariggio MA, Belia S, Calissano P. (1995). The S-100: a protein family in search of a function. Prog Neurobiol 46: 71-82.
13. Fernandez-Fernandez MR, Rutherford TJ, Fersht AR. (2008). Members of the S100 family bind p53 in two distinct ways. Protein Sci 17: 1663-1670.
14. Fernandez-Fernandez MR, Veprintsev DB, Fersht AR. (2005). Proteins of the S100 family regulate the oligomerization of p53 tumor suppressor. Proc Natl Acad Sci USA 102: 4735-4740.
15. Finlan LE, Hupp TR. (2007). p63: the phantom of the tumor suppressor. Cell Cycle 6: 1062-1071.
16. Grigorian M, Andresen S, Tulchinsky E, Kriajevska M, Carlberg C, Kruse C et al., (2001). Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction. J Biol Chem 276: 22699-22708.
17. Hibi K, Trink B, Patturajan M, Westra WH, Caballero OL, Hill DE et al., (2000). AIS is an oncogene amplified in squamous cell carcinoma. Proc Natl Acad Sci USA 97: 5462-5467.
18. Ilg EC, Schafer BW, Heizmann CW. (1996). Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 68: 325-332.
19. Joerger AC, Fersht AR. (2007). Structure-function-rescue: the diverse nature of common p53 cancer mutants. Oncogene 26: 2226-2242.
20. Joerger AC, Rajagopalan S, Natan E, Veprintsev DB, Robinson CV, Fersht AR. (2009). Structural evolution of p53, p63, and p73: implication for heterotetramer formation. Proc Natl Acad Sci USA 106: 17705-17710.
21. Kirschner RD, Sanger K, Muller GA, Engeland K. (2008). Transcriptional activation of the tumor suppressor and differentiation gene S100A2 by a novel p63-binding site. Nucleic Acids Res 36: 2969-2980.
22. Langenbacher A, Chen JN. (2008). Calcium signaling: a common thread in vertebrate left-right axis development. Dev Dyn 237: 3491-3496.
23. Lapi E, Iovino A, Fontemaggi G, Soliera AR, Iacovelli S, Sacchi A et al., (2006). S100A2 gene is a direct transcriptional target of p53 homologues during keratinocyte differentiation. Oncogene 25: 3628-3637.
24. Lauriola L, Michetti F, Maggiano N, Galli J, Cadoni G, Schafer BW et al., (2000). Prognostic significance of the Ca(2+) binding protein S100A2 in laryngeal squamous-cell carcinoma. Int J Cancer 89: 345-349.
25. Lin J, Blake M, Tang C, Zimmer D, Rustandi RR, Weber DJ et al., (2001). Inhibition of p53 transcriptional activity by the S100B calcium-binding protein. J Biol Chem 276: 35037-35041.
26. Lin J, Yang Q, Yan Z, Markowitz J, Wilder PT, Carrier F et al., (2004). Inhibiting S100B restores p53 levels in primary malignant melanoma cancer cells. J Biol Chem 279: 34071-34077.
27. MacGregor IK, Anderson AL, Laue TM. (2004). Fluorescence detection for the XLI analytical ultracentrifuge. Biophys Chem 108: 165-185.
28. Melino G, Lu X, Gasco M, Crook T, Knight RA. (2003). Functional regulation of p73 and p63: development and cancer. Trends Biochem Sci 28: 663-670.
29. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. (1999). p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398: 708-713.
30. Moll UM, Slade N. (2004). p63 and p73: roles in development and tumor formation. Mol Cancer Res 2: 371-386.
31. Mrak RE, Griffinbc WS. (2001). The role of activated astrocytes and of the neurotrophic cytokine S100B in the pathogenesis of Alzheimer's disease. Neurobiol Aging 22: 915-922.
32. Mueller A, Schafer BW, Ferrari S, Weibel M, Makek M, Hochli M et al., (2005). The calcium-binding protein S100A2 interacts with p53 and modulates its transcriptional activity. J Biol Chem 280: 29186-29193.
33. Pelosi G, Pasini F, Olsen Stenholm C, Pastorino U, Maisonneuve P, Sonzogni A et al., (2002). p63 immunoreactivity in lung cancer: yet another player in the development of squamous cell carcinomas? J Pathol 198: 100-109.
34. Pruneri G, Pignataro L, Manzotti M, Carboni N, Ronchetti D, Neri A et al., (2002). p63 in laryngeal squamous cell carcinoma: evidence for a role of TA-p63 down-regulation in tumorigenesis and lack of prognostic implications of p63 immunoreactivity. Lab Invest 82: 1327-1334.
35. Rajagopalan S, Jaulent AM, Wells M, Veprintsev DB, Fersht AR. (2008). 14-3-3 activation of DNA binding of p53 by enhancing its association into tetramers. Nucleic Acids Res 36: 5983-5991.
36. Rosenbluth JM, Pietenpol JA. (2008). The jury is in: p73 is a tumor suppressor after all. Genes Dev 22: 2591-2595.
37. Rustandi RR, Baldisseri DM, Weber DJ. (2000). Structure of the negative regulatory domain of p53 bound to S100B(betabeta). Nat Struct Biol 7: 570-574.
38. Salama I, Malone PS, Mihaimeed F, Jones JL. (2008). A review of the S100 proteins in cancer. Eur J Surg Oncol 34: 357-364.
39. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. (2006). Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 396: 201-214.
40. Schuck P. (2000). Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
41. Scotto C, Deloulme JC, Rousseau D, Chambaz E, Baudier J. (1998). Calcium and S100B regulation of p53-dependent cell growth arrest and apoptosis. Mol Cell Biol 18: 4272-4281.
42. Scotto C, Delphin C, Deloulme JC, Baudier J. (1999). Concerted regulation of wild-type p53 nuclear accumulation and activation by S100B and calcium-dependent protein kinase C. Mol Cell Biol 19: 7168-7180.
43. Scoumanne A, Harms KL, Chen X. (2005). Structural basis for gene activation by p53 family members. Cancer Biol Ther 4: 1178-1185.
44. Sedaghat F, Notopoulos A. (2008). S100 protein family and its application in clinical practice. Hippokratia 12: 198-204.
45. Serber Z, Lai HC, Yang A, Ou HD, Sigal MS, Kelly AE et al., (2002). A C-terminal inhibitory domain controls the activity of p63 by an intramolecular mechanism. Mol Cell Biol 22: 8601-8611.
46. Slomnicki LP, Nawrot B, Lesniak W. (2009). S100A6 binds p53 and affects its activity. Int J Biochem Cell Biol 41: 784-790.
47. Teufel DP, Freund SM, Bycroft M, Fersht AR. (2007). Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53. Proc Natl Acad Sci USA 104: 7009-7014.
48. van Dieck J, Fernandez-Fernandez MR, Veprintsev DB, Fersht AR. (2009). Modulation of the oligomerization state of p53 by differential binding of proteins of the S100 family to p53 monomers and tetramers. J Biol Chem 284: 13804-13811.
49. Vigliano FA, Bermudez R, Nieto JM, Quiroga MI. (2009). Development of rodlet cells in the gut of turbot (Psetta maxima L.): relationship between their morphology and S100 protein immunoreactivity. Fish Shellfish Immunol 26: 146-153.
50. Vilgelm A, El-Rifai W, Zaika A. (2008). Therapeutic prospects for p73 and p63: rising from the shadow of p53. Drug Resist Update 11: 152-163.
51. Whitaker M. (2008). Calcium signalling in early embryos. Philos Trans R Soc Lond B Biol Sci 363: 1401-1418.
52. Yamaguchi K, Wu L, Caballero OL, Hibi K, Trink B, Resto V et al., (2000). Frequent gain of the p40/p51/p63 gene locus in primary head and neck squamous cell carcinoma. Int J Cancer 86: 684-689.
53. Yang A, Schweitzer R, Sun D, Kaghad M, Walker N, Bronson RT et al., (1999). p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398: 714-718.
54. Yang A, Walker N, Bronson R, Kaghad M, Oosterwegel M, Bonnin J et al., (2000). p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404: 99-103.
55. Zimmer DB, Cornwall EH, Landar A, Song W. (1995). The S100 protein family: history, function, and expression. Brain Res Bull 37: 417-429.
56. Zimmer DB, Wright Sadosky P, Weber DJ. (2003). Molecular mechanisms of S100-target protein interactions. Microsc Res Tech 60: 552-559.