Enhanced expression of 14-3-3sigma in pancreatic cancer and its role in cell cycle regulation and apoptosis

Carcinogenesis

Volumn 25, Issue 9, 2004, Pages 1575-1585

  Guweidhi, Ahmed ^a   Kleeff, Jörg ^a   Giese, Nathalia ^a   El Fitori, Jamael ^a   Ketterer, Knut ^a,b   Giese, Thomas ^a   Büchler, Markus W ^a   Korc, Murray ^b   Friess, Helmut ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN 14 3 3; PROTEIN BAD; PROTEIN BAX;

ADULT; AGED; APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE; CELL CYCLE G2 PHASE; CONTROLLED STUDY; DNA MICROARRAY; EPIGENETICS; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LASER CAPTURE MICRODISSECTION; MAJOR CLINICAL STUDY; MALE; MITOSIS; PANCREAS ADENOCARCINOMA; PANCREAS DUCT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-ASSOCIATED DEATH PROTEIN; BLOTTING, SOUTHERN; BLOTTING, WESTERN; CARCINOMA, PANCREATIC DUCTAL; CARRIER PROTEINS; CASE-CONTROL STUDIES; CDC2 PROTEIN KINASE; CELL CYCLE; EXONUCLEASES; FEMALE; HUMANS; LASERS; MALE; MIDDLE AGED; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREAS; PANCREATIC NEOPLASMS; PRECIPITIN TESTS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR MARKERS, BIOLOGICAL;

EID: 4544269166     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgh159     Document Type: Article

References (63)

1. Jemal,A., Murray,T., Samuels,A., Ghafoor,A., Ward,E. and Thun,M.J. (2003) Cancer statistics, 2003. CA Cancer J. Clin., 53, 5-26.
2. Gudjonsson,B. (1987) Cancer of the pancreas. 50 years of surgery. Cancer, 60, 2284-2303.
3. Beger,H.G., Buchler,M.W. and Friess,H. (1994) [Surgical results and indications for adjuvant measures in pancreatic cancer]. Chirurg, 65, 246-252.
4. Warshaw,A.L. and Fernandez-del Castillo,C. (1992) Pancreatic carcinoma. N. Engl. J. Med., 326, 455-465.
5. Ungefroren,H., Voss,M., Jansen,M., Roeder,C., Henne-Bruns,D., Kremer,B. and Kalthoff,H. (1998) Human pancreatic adenocarcinomas express Fas and Fas ligand yet are resistant to Fas-mediated apoptosis. Cancer Res., 58, 1741-1749.
6. Raitano,A.B., Scuderi,P. and Korc,M. (1990) Binding and biological effects of tumor necrosis factor and gamma interferon in human pancreatic carcinoma cells. Pancreas, 5, 267-277.
7. Friess,H., Lu,Z., Graber,H.U., Zimmermann,A., Adler,G., Korc,M., Schmid,R.M. and Buchler,M.W. (1998) bax, but not bcl-2, influences the prognosis of human pancreatic cancer. Gut, 43, 414-421.
8. Korc,M. (1998) Role of growth factors in pancreatic cancer. Surg. Oncol. Clin. N. Am., 7, 25-41.
9. Paulovich,A.G., Toczyski,D.P. and Hartwell,L.H. (1997) When checkpoints fail. Cell, 88, 315-321.
10. Stewart,Z.A. and Pietenpol,J.A. (1999) Cell cycle checkpoints as therapeutic targets. J. Mammary Gland Biol. Neoplasia, 4, 389-400.
11. Hartwell,L.H. and Kastan,M.B. (1994) Cell cycle control and cancer. Science, 266, 1821-1828.
12. Aitken,A., Collinge,D.B., van Heusden,B.P., Isobe,T., Roseboom,P.H., Rosenfeld,G. and Soll,J. (1992) 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins. Trends Biochem. Sci., 17, 498-501.
13. Aitken,A. (1995) 14-3-3 proteins on the MAP. Trends Biochem. Sci., 20, 95-97.
14. Martens,G.J., Piosik,P.A. and Danen,E.H. (1992) Evolutionary conservation of the 14-3-3 protein. Biochem. Biophys. Res. Commun., 184, 1456-1459.
15. Swanson,K.D. and Ganguly,R. (1992) Characterization of a Drosophila melanogaster gene similar to the mammalian genes encoding the tyrosine/tryptophan hydroxylase activator and protein kinase C inhibitor proteins. Gene, 113, 183-190.
16. Wang,W. and Shakes,D.C. (1994) Isolation and sequence analysis of a Caenorhabditis elegans cDNA which encodes a 14-3-3 homologue. Gene, 147, 215-218.
17. van Heusden,G.P., Griffiths,D.J., Ford,J.C., Chin,A.W.T.F., Schrader,P.A., Carr,A.M. and Steensma,H.Y. (1995) The 14-3-3 proteins encoded by the BMH1 and BMH2 genes are essential in the yeast Saccharomyces cerevisiae and can be replaced by a plant homologue. Eur. J. Biochem., 229, 45-53.
18. Wang,W. and Shakes,D.C. (1996) Molecular evolution of the 14-3-3 protein family. J. Mol. Evol., 43, 384-398.
19. Rosenquist,M., Alsterfjord,M., Larsson,C. and Sommarin,M. (2001) Data mining the Arabidopsis genome reveals fifteen 14-3-3 genes. Expression is demonstrated for two out of five novel genes. Plant Physiol., 127, 142-149.
20. Rittinger,K., Budman,J., Xu,J., Volinia,S., Cantley,L.C., Smerdon,S.J., Gamblin,S.J. and Yaffe,M.B. (1999) Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell, 4, 153-166.
21. Yaffe,M.B., Rittinger,K., Volinia,S., Caron,P.R., Aitken,A., Leffers,H., Gamblin,S.J., Smerdon,S.J. and Cantley,L.C. (1997) The structural basis for 14-3-3: phosphopeptide binding specificity. Cell, 91, 961-971.
22. Yaffe,M.B. (2002) How do 14-3-3 proteins work? Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett., 513, 53-57.
23. Xiao,B., Smerdon,S.J., Jones,D.H., Dodson,G.G., Soneji,Y., Aitken,A. and Gamblin,S.J. (1995) Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature, 376, 188-191.
24. Chung,H.J., Sehnke,P.C. and Ferl,R.J. (1999) The 14-3-3 proteins: cellular regulators of plant metabolism. Trends Plant Sci., 4, 367-371.
25. Finnie,C., Borch,J. and Collinge,D.B. (1999) 14-3-3 proteins: eukaryotic regulatory proteins with many functions. Plant Mol. Biol., 40, 545-554.
26. Fu,H., Subramanian,R.R. and Masters,S.C. (2000) 14-3-3 proteins: structure, function and regulation. Annu. Rev. Pharmacol. Toxicol., 40, 617-647.
27. van Hemert,M.J., Steensma,H.Y. and van Heusden,G.P. (2001) 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays, 23, 936-946.
28. Prasad,G.L., Valverius,E.M., McDuffie,E. and Cooper,H.L. (1992) Complementary DNA cloning of a novel epithelial cell marker protein, HME1, that may be down-regulated in neoplastic mammary cells. Cell Growth Differ., 3, 507-513.
29. Leffers,H., Madsen,P., Rasmussen,H.H., Honore,B., Andersen,A.H., Walbum,E., Vandekerckhove,J. and Celis,J.E. (1993) Molecular cloning and expression of the transformation sensitive epithelial marker stratifin. A member of a protein family that has been involved in the protein kinase C signalling pathway. J. Mol. Biol., 231, 982-998.
30. Vellucci,V.F., Germino,F.J. and Reiss,M. (1995) Cloning of putative growth regulatory genes from primary human keratinocytes by subtractive hybridization. Gene, 166, 213-220.
31. 2/M progression. Mol. Cell, 1, 3-11.
32. Chan,T.A., Hermeking,H., Lengauer,C., Kinzler,K.W. and Vogelstein,B. (1999) 14-3-3Sigma is required to prevent mitotic catastrophe after DNA damage. Nature, 401, 616-620.
33. Laronga,C., Yang,H.Y., Neal,C. and Lee,M.H. (2000) Association of the cyclin-dependent kinases and 14-3-3 sigma negatively regulates cell cycle progression. J. Biol. Chem., 275, 23106-23112.
34. Subramanian,R.R., Masters,S.C., Zhang,H. and Fu,H. (2001) Functional conservation of 14-3-3 isoforms in inhibiting bad-induced apoptosis. Exp. Cell Res., 271, 142-151.
35. 2/M regulator 14-3-3sigma prevents apoptosis through sequestration of Bax. J. Biol. Chem., 276, 45201-45206.
36. Ferguson,A.T., Evron,E., Umbricht,C.B. et al. (2000) High frequency of hypermethylation at the 14-3-3 sigma locus leads to gene silencing in breast cancer. Proc. Natl Acad. Sci. USA, 97, 6049-6054.
37. Umbricht,C.B., Evron,E., Gabrielson,E., Ferguson,A., Marks,J. and Sukumar,S. (2001) Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene, 20, 3348-3353.
38. Suzuki,H., Itoh,F., Toyota,M., Kikuchi,T., Kakiuchi,H. and Imai,K. (2000) Inactivation of the 14-3-3 sigma gene is associated with 5′ CpG island hypermethylation in human cancers. Cancer Res., 60, 4353-4357.
39. Iwata,N., Yamamoto,H., Sasaki,S. et al. (2000) Frequent hypermethylation of CpG islands and loss of expression of the 14-3-3 sigma gene in human hepatocellular carcinoma. Oncogene, 19, 5298-5302.
40. Gasco,M., Sullivan,A., Repellin,C., Brooks,L., Farrell,P.J., Tidy,J.A., Dunne,B., Gusterson,B., Evans,D.J. and Crook,T. (2002) Coincident inactivation of 14-3-3sigma and p16INK4a is an early event in vulval squamous neoplasia. Oncogene, 21, 1876-1881.
41. Gasco,M., Bell,A.K., Heath,V. et al. (2002) Epigenetic inactivation of 14-3-3 sigma in oral carcinoma: association with p16 (INK4a) silencing and human papillomavirus negativity. Cancer Res., 62, 2072-2076.
42. Nakanishi,K., Hashizume,S., Kato,M., Honjoh,T., Setoguchi,Y. and Yasumoto,K. (1997) Elevated expression levels of the 14-3-3 family of proteins in lung cancer tissues. Hum. Antibodies, 8, 189-194.
43. Villaret,D.B., Wang,T., Dillon,D., Xu,J., Sivam,D., Cheever,M.A. and Reed,S.G. (2000) Identification of genes overexpressed in head and neck squamous cell carcinoma using a combination of complementary DNA subtraction and microarray analysis. Laryngoscope, 110, 374-381.
44. Friess,H., Ding,J., Kleeff,J., Fenkell,L., Rosinski,J.A., Guweidhi,A., Reidhaar-Olson,J.F., Korc,M., Hammer,J. and Buchler,M.W. (2003) Microarray-based identification of differentially expressed growth- and metastasis-associated genes in pancreatic cancer. Cell Mol. Life Sci., 60, 1180-1199.
45. Logsdon,C.D., Simeone,D.M., Binkley,C., Arumugam,T., Greenson,J.K., Giordano,T.J., Misek,D.E., Kuick,R. and Hanash,S. (2003) Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res., 63, 2649-2657.
46. Iacobuzio-Donahue,C.A., Maitra,A., Olsen,M. et al. (2003) Exploration of global gene expression patterns in pancreatic adenocarcinoma using cDNA microarrays. Am. J. Pathol., 162, 1151-1162.
47. Tureci,O., Ding,J., Hilton,H. et al. (2003) Computational dissection of tissue contamination for identification of colon cancer-specific expression profiles. FASEB J., 17, 376-385.
48. Giese,N.A., Raykov,Z., DeMartino,L., Vecchi,A., Sozzani,S., Dinsart,C., Cornelis,J.J. and Rommelaere,J. (2002) Suppression of metastatic hemangiosarcoma by a parvovirus MVMp vector transducing the IP-10 chemokine into immunocompetent mice. Cancer Gene Ther., 9, 432-442.
49. Emmert-Buck,M.R., Bonner,R.F., Smith,P.D., Chuaqui,R.F., Zhuang,Z., Goldstein,S.R., Weiss,R.A. and Liotta,L.A. (1996) Laser capture micro-dissection. Science, 274, 998-1001.
50. Sato,N., Maitra,A., Fukushima,N., van Heek,N.T., Matsubayashi,H., Iacobuzio-Donahue,C.A., Rosty,C. and Goggins,M. (2003) Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res., 63, 4158-4166.
51. Aprelikova,O., Pace,A.J., Fang,B., Koller,B.H. and Liu,E.T. (2001) BRCA1 is a selective co-activator of 14-3-3 sigma gene transcription in mouse embryonic stem cells. J. Biol. Chem., 276, 25647-25650.
52. Booher,R.N., Holman,P.S. and Fattaey,A. (1997) Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J. Biol. Chem., 272, 22300-22306.
53. Liu,F., Stanton,J.J., Wu,Z. and Piwnica-Worms,H. (1997) The human Myt1 kinase preferentially phosphorylates Cdc2 on threonine 14 and localizes to the endoplasmic reticulum and Golgi complex. Mol. Cell. Biol., 17, 571-583.
54. Zha,J., Harada,H., Yang,E., Jockel,J. and Korsmeyer,S.J. (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X (L). Cell, 87, 619-628.
55. Yang,E., Zha,J., Jockel,J., Boise,L.H., Thompson,C.B. and Korsmeyer,S.J. (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell, 80, 285-291.
56. Ottilie,S., Diaz,J.L., Horne,W., Chang,J., Wang,Y., Wilson,G., Chang,S., Weeks,S., Fritz,L.C. and Oltersdorf,T. (1997) Dimerization properties of human BAD. Identification of a BH-3 domain and analysis of its binding to mutant BCL-2 and BCL-XL proteins. J. Biol. Chem., 272, 30866-30872.
57. Zha,J., Harada,H., Osipov,K., Jockel,J., Waksman,G. and Korsmeyer,S.J. (1997) BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J. Biol. Chem., 272, 24101-24104.
58. Kelekar,A., Chang,B.S., Harlan,J.E., Fesik,S.W. and Thompson,C.B. (1997) Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol. Cell. Biol., 17, 7040-7046.
59. Kleeff,J., Kornmann,M., Sawhney,H. and Korc,M. (2000) Actinomycin D induces apoptosis and inhibits growth of pancreatic cancer cells. Int. J. Cancer, 86, 399-407.
60. 1 arrest in human cancer cells. Cancer Res., 55, 5187-5190.
61. Sinha,P., Hutter,G., Kottgen,E., Dietel,M., Schadendorf,D. and Lage,H. (1999) Increased expression of epidermal fatty acid binding protein, cofilin and 14-3-3-sigma (stratifin) detected by two-dimensional gel electrophoresis, mass spectrometry and microsequencing of drug-resistant human adenocarcinoma of the pancreas. Electrophoresis, 20, 2952-2960.
62. Courtois,S., de Fromentel,C.C. and Hainaut,P. (2004) p53 protein variants: structural and functional similarities with p63 and p73 isoforms. Oncogene, 23, 631-638.
63. Guo,J., Kleeff,J., Li,J., Ding,J., Hammer,J., Zhao,Y., Giese,T., Korc,M., Buchler,M.W. and Friess,H. (2004) Expression and functional significance of CDC25B in human pancreatic ductal adenocarcinoma. Oncogene, 23, 71-81.