Stathmin overexpression cooperates with p53 mutation and osteopontin overexpression, and is associated with tumour progression, early recurrence, and poor prognosis in hepatocellular carcinoma

Journal of Pathology

Volumn 209, Issue 4, 2006, Pages 549-558

  Yuan, R H ^a,b   Jeng, Y M ^a,b   Chen, H L ^a   Lai, P L ^a   Pan, H W ^b   Hsieh, F J ^a,b   Lin, C Y ^b   Lee, P H ^a,b   Hsu, H C ^a,b  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Hepatocellular carcinoma; Osteopontin; P53 mutation; Prognosis; Stathmin

Indexed keywords

ALPHA FETOPROTEIN; MESSENGER RNA; OSTEOPONTIN; PROTEIN P53; STATHMIN;

ADOLESCENT; ADULT; AGED; ARTICLE; CANCER GRADING; CANCER GROWTH; CANCER INVASION; CANCER RECURRENCE; CANCER SIZE; CANCER STAGING; CANCER SURGERY; CELL CYCLE PROGRESSION; CELL MOTILITY; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER CELL CARCINOMA; LIVER METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTASIS POTENTIAL; PORTAL VEIN; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SURVIVAL RATE; TUMOR THROMBUS;

CARCINOMA, HEPATOCELLULAR; CHI-SQUARE DISTRIBUTION; DISEASE PROGRESSION; DNA MUTATIONAL ANALYSIS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, P53; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; OSTEOPONTIN; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIALOGLYCOPROTEINS; STATHMIN; TUMOR MARKERS, BIOLOGICAL;

EID: 33746884331     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2011     Document Type: Article

References (69)

1. El-Serag HB. Hepatocellular carcinoma: an epidemiologic view. J Clin Gastroenterol 2002;35:S72-S78.
2. Befeler AS, Di Bisceglie AM. Hepatocellular carcinoma: diagnosis and treatment. Gastroenterology 2002;122:1609-1619.
3. Pan HW, Ou YH, Peng SY, Liu SH, Lai PL, Lee PH, et al. Overexpression of osteopontin is associated with intrahepatic metastasis, early recurrence, and poorer prognosis of surgically resected hepatocellular carcinoma. Cancer 2003;98:119-127.
4. Katoh H, Shibata T, Kokubu A, Ojima H, Loukopoulos P, Kanai Y, et al. Genetic profile of hepatocellular carcinoma revealed by array-based comparative genomic hybridization: identification of genetic indicators to predict patient outcome. J Hepatol 2005;43:863-874.
5. Fang W, Piao Z, Simon D, Sheu JC, Huang S. Mapping of a minimal deleted region in human hepatocellular carcinoma to lp36.13-p36.23 and mutational analysis of the RIZ (PRDM2) gene localized to the region. Genes Chromosomes Cancer 2000;28:269-275.
6. Leung TH, Wong N, Lai PB, Chan A, To KF, Liew CT, et al. Identification of four distinct regions of allelic imbalances on chromosome I by the combined comparative genomic hybridization and microsatellite analysis on hepatocellular carcinoma. Mod Pathol 2002;15:1213-1220.
7. Koshikawa K, Nomoto S, Yamashita K, Ishigure K, Takeda. S, Nakao A. Allelic imbalance at Ip36 in the pathogenesis of human hepatocellular carcinoma. Hepatogastroenterology 2004;51:186-191.
8. Nishimura T, Nishida N, Itoh T, Komeda T, Fukuda Y, Ikai I, et al. Discrete breakpoint mapping and shortest region of overlap of chromosome arm 1q gain and 1p loss in human hepatocellular carcinoma detected by semiquantitative microsatellite analysis. Genes Chromosomes Cancer 2005;42:34-43.
9. Okazaki T, Yoshida BN, Avraham KB, Wang H, Wuenschell CW, Jenkins NA, et al. Molecular diversity of the SCG10/stathmin gene family in the mouse. Genomics 1993;18:360-373.
10. Ferrari AC, Seuanez HN, Hanash SM, Atweh GF. A gene that encodes for a leukemia-associated phosphoprotein (p18) maps to chromosome bands 1p35-36.1. Genes Chromosomes Cancer 1990;2:125-129.
11. Sun M, Eshleman JR, Ferrell LD, Jacobs G, Sudilovsky EC, Tuthill R, et al. An early lesion in hepatic carcinogenesis: loss of heterozygosity in human cirrhotic livers and dysplastic nodules at the 1p36-p34 region. Hepatology 2001;33:1415-1424.
12. Ozon S, Byk T, Sobel A. SCLIP: a novel SCG10-like protein of the stathmin family expressed in the nervous system. J Neurochem 1998;70:2386-2396.
13. Ozon S, Maucuer A, Sobel A. The stathmin family - molecular and biological characterization of novel mammalian proteins expressed in the nervous system. Ear J Biochem 1997;248:794-806.
14. Cassimeris L. The oncoprotein 18/stathmin family of microtubule destabilizers. Curr Opin Cell Biol 2002;14:18-24.
15. Belmont LD, Mitchison TJ. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 1996;84:623-631.
16. Curmi PA, Andersen SS, Lachkar S, Gavet O, Karsenti E, Knossow M, et al. The stathmin/tubulin interaction in vitro. J Biol Chem 1997;272:25029-25036.
17. Charbaut E, Curmi PA, Ozon S, Lachkar S, Redeker V, Sobel A. Stathmin family proteins display specific molecular and tubulin binding properties. J Biol Chem 2001;276:16146-16154.
18. Curmi PA, Gavet O, Charbaut E, Ozon S, Lachkar-Colmerauer S, Manceau V, et al. Stathmin and its phosphoprotein family: general properties, biochemical and functional interaction with tubulin. Cell Struct Funct 1999;24:345-357.
19. Brattsand G, Marklund U, Nylander K, Roos G, Gullberg M. Cell-cycle-regulated phosphorylation of oncoprotein 18 on Ser16, Ser25 and Ser38. Ear J Biochem 1994;220:359-368.
20. Luo XN, Mookerjee B, Ferrari A, Mistry S, Atweh GF. Regulation of phosphoprotein p18 in leukemic cells. Cell cycle regulated phosphorylation by p34cdc2 kinase. J Biol Chem 1994;269:10312-10318.
21. Howell B, Larsson N, Gullberg M, Cassimeris L. Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/stathmin Mol Biol Cell 1999;10:105-118.
22. Rubin CI, Atweh GF. The role of stathmin in the regulation of the cell cycle. J Cell Biochem 2004;93:242-250.
23. Larsson N, Melander H, Marklund U, Osterman O, Gullberg M. G2/M transition requires multisite phosphorylation of oncoprotein 18 by two distinct protein kinase systems. J Biol Chem 1995;270:14 175-14 183.
24. Iancu C, Mistry SJ, Arkin S, Wallenstein S, Atweh GF. Effects of stathmin inhibition on the mitotic spindle. J Cell Sci 2001;114:909-916.
25. Marklund U, Osterman O, Melander H, Bergh A, Gullberg M. The phenotype of a "Cdc2 kinase target site-deficient" mutant of oncoprotein 18 reveals a role of this protein in cell cycle control. J Biol Chem 1994;269:30 626-30 635.
26. Koppel J, Loyer P, Maucuer A, Rehak P, Manceau V, Guguen-Guillouzo C, et al. Induction of stathmin expression during liver regeneration. FEBS Lett 1993;331:65-70.
27. Barone S, Okaya T, Rudich S, Petrovic S, Tenram K, Wang Z, et al. Distinct and sequential upregulation of genes regulating cell growth and cell cycle progression during hepatic ischemia-reperfusion injury. Am J Physiol Cell Physiol 2005;289:C826-C835.
28. Melhem RF, Strahler JR, Hailat N, Zhu XX, Hanash SM. Involvement of OP18 in cell proliferation. Biochem Biophys Res Commun 1991;179:1649-1655.
29. Rubin CI, French DL, Atweh GF. Stathmin expression and megakaryocyte differentiation: a potential role in polyploidy. Exp Hematol 2003;31:389-397.
30. Bieche I, Maucuer A, Laurendeau I, Lachkar S, Spano AJ, Frankfurter A, et al. Expression of stathmin family genes in human tissues: non-neural-restricted expression for SCLIP. Genomics 2003;81:400-410.
31. Feurestein N, Cooper HL. Rapid protein phosphorylation induced by phorbol ester in HL-60 cells. Unique alkali-stable phosphorylation of a 17,000-dalton protein detected by two-dimensional gel electrophoresis. J Biol Chem 1983;258:10 786-10 793.
32. Hanash SM, Strahler JR, Kuick R, Chu EH, Nichols D. Identification of a polypeptide associated with the malignant phenotype in acute leukemia. J Biol Chem 1988;263:12813-12815.
33. Nylander K, Marklund U, Brattsand G, Gullberg M, Roos G. Immunohistochemical detection of oncoprotein 18 (Op18) in malignant lymphomas. Histochem J 1995;27:155-160.
34. Price DK, Ball JR, Bahrani-Mostafavi Z, Vachris JC, Kaufman JS, Naumann RW, et al. The phosphoprotein Op18/stathmin is differentially expressed in ovarian cancer. Cancer Invest 2000;18:722-730.
35. Brattsand G. Correlation of oncoprotein 18/stathmin expression in human breast cancer with established prognostic factors. Br J Cancer 2000;83:311-318.
36. Curmi PA, Nogues C, Lachkar S, Carelle N, Gonthier MP, Sobel A, et al. Overexpression of stathmin in breast carcinomas points out to highly proliferative tumours. Br J Cancer 2000;82:142-150.
37. Friedrich B, Gronberg H, Landstrom M, Gullberg M, Bergh A. Differentiation-stage specific expression of oncoprotein 18 in human and rat prostatic adenocarcinoma. Prostate 1995;27:102-109.
38. Peng SY, Lai PL, Chu JS, Lee PH, Tsung PT, Chen DS, et al. Expression and hypomethylation of alpha-fetoprotein gene in unicentric and multicentric human hepatocellular carcinomas. Hepatology 1993;17:35-41.
39. Hsu HC, Chiou TJ, Chen JY, Lee CS, Lee PH, Peng SY. Clonality and clonal evolution of hepatocellular carcinoma with multiple nodules. Hepatology 1991;13:923-928.
40. Yuan RH, Jeng YM, Chen HL, Hsieh FJ, Yang CY, Lee PH, et al. Opposite roles of human PAP and REG1A expression in hepatocellular carcinoma (HCC): association of PAP expression with low-stage HCC. β-catenin mutation, and favorable prognosis. Clin Cancer Res 2005;11:2568-2575.
41. Hsu HC, Wu TT, Wu MZ, Sheu JC, Lee CS, Chen DS. Tumor invasiveness and prognosis in resected hepatocellular carcinoma. Clinical and pathogenetic implications. Cancer 1988;61:2095-2099.
42. Peng SY, Chen WJ, Lai PL, Jeng YM, Sheu JC, Hsu HC. High alpha-fetoprotein level correlates with high stage, early recurrence and poor prognosis of hepatocellular carcinoma: significance of hepatitis virus infection, age, p53 and beta-catenin mutations. Int J Cancer 2004;112:44-50.
43. Liu SH, Lin CY, Peng SY, Jeng YM, Pan HW, Lai PL, et al. Down-regulation of annexin A10 in hepatocellular carcinoma is associated with vascular invasion, early recurrence, and poor prognosis in synergy with p53 mutation. Am J Pathol 2002;160:1831-1837.
44. Vincent S, Marty L, Fort P. S26 ribosomal protein RNA: an invariant control for gene regulation experiments in eucaryotic cells and tissues. Nucleic Acids Res 1993;21:1498.
45. Hsu HC, Jeng YM, Mao TL, Chu JS, Lai PL, Peng SY. Beta-catenin mutations are associated with a subset of low-stage hepatocellular carcinoma negative for hepatitis B virus and with favorable prognosis. Am J Pathol 2000;157:763-770.
46. Hsu HC, Huang AM, Lai PL, Chien WM, Peng SY, Lin SW. Genetic alterations at the splice junction of p53 gene in human hepatocellular carcinoma. Hepatology 1994;19:122-128.
47. Hsu HC, Peng SY, Lai PL, Chu JS, Lee PH. Mutations of p53 gene in hepatocellular carcinoma (HCC) correlate with tumor progression and patient prognosis. Int J Oncoly 1994;4:1341-1347.
48. Marklund U, Brattsand G, Shingler V, Gullberg M. Serine 25 of oncoprotein 18 is a major cytosolic target for the mitogen-activated protein kinase. J Biol Chem 1993;268:15 039-15 047.
49. Jin K, Mao XO, Cottrell B, Schilling B, Xie L, Row RH, et al. Proteomic and immunochemical characterization of a role for stathmin in adult neurogenesis. FASEB J 2004;18:287-299.
50. Camoletto P, Peretto P, Bonfanti L, Manceau V, Sobel A, Fasolo A. The cytosolic stathmin is expressed in the olfactory system of the adult rat. Neuroreport 1997;8:2825-2829.
51. Niethammer P, Bastiaens P, Karsenti E. Stathmin-tubulin interaction gradients in motile and mitotic cells. Science 2004;303:1862-1866.
52. Wehrle-Haller B, Imhof BA. Actin, microtubules and focal adhesion dynamics during cell migration. Int J Biochem Cell Biol 2003;35:39-50.
53. Gavet O, Ozon S, Manceau V, Lawler S, Curmi P, Sobel A. The stathmin phosphoprotein family: intracellular localization and effects on the microtubule network. J Cell Sci 1998;111:3333-3346.
54. Holmfeldt P, Larsson N, Segerman B, Howell B, Morabito J, Cassimeris L, et al. The catastrophe-promoting activity of ectopic Op18/stathmin is required for disruption of mitotic spindles but not interphase microtubules. Mol Biol Cell 2001;12:73-83.
55. Giampietro C, Luzzati F, Gambarotta G, Giacobini P, Boda E, Fasolo A, et al. Stathmin expression modulates migratory properties of GN-11 neurons in vitro. Endocrinology 2005;146:1825-1834.
56. Baldassarre G, Belletti B, Nicoloso MS, Schiappacassi M, Vecchione A, Spessotto P, et al. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 2005;7:51-63.
57. Miyashita H, Kanemura M, Yamazaki T, Abe M, Sato Y. Vascular endothelial zinc finger 1 is involved in the regulation of angiogenesis: possible contribution of stathmin/OP18 as a downstream target gene. Arterioscler Thromb Vasc Biol 2004;24:878-884.
58. Lacoste-Collin L, Gomez-Brouchet A, Escourrou G, Delisle MB, Levade T, Uro-Coste E. Expression of p27(Kip1) in bladder cancers: immunchistochemical study and prognostic value in a series of 95 cases. Cancer Lett 2002;186:115-120.
59. Laurent-Puig P, Legoix P, Bluteau O, Belghiti J, Franco D, Binot F, et al. Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis. Gastroenterology 2001;120:1763-1773.
60. Oliveira AM, Nascimento AG, Okuno SH, Lloyd RV. p27(kip1) protein expression correlates with survival in myxoid and round-cell liposarcoma. J Clin Oncol 2000;18:2888-2893.
61. Hsu HC, Tseng HJ, Lai PL, Lee PH, Peng SY. Expression of p53 gene in 184 unifocal hepatocellular carcinomas: association with tumor growth and invasiveness. Cancer Res 1993;53:4691-4694.
62. Peng SY, Ou YH, Chen WJ, Li HY, Liu SH, Pan HW, et al. Aberrant expressions of annexin A10 short isoform, osteopontin and alpha-fetoprotein at chromosome 4q cooperatively contribute to progression and poor prognosis of hepatocellular carcinoma. Int J Oncol 2005;26:10 853-11061.
63. Sheen IS, Jeng KS, Wu JY. Is p53 gene mutation an indicator of the biological behaviors of recurrence of hepatocellular carcinoma? World J Gastroenterol 2003;9:1202-1207.
64. Oates AJ, Barraclough R, Rudland PS. The identification of osteopontin as a metastasis-related gene product in a rodent mammary tumour model. Oncogene 1996;13:97-104.
65. Tuck AB, Arsenault DM, O'Malley FP, Hota C, Ling MC, Wilson SM, et al. Osteopontin induces increased invasiveness and plasminogen activator expression of human mammary epithelia] cells. Oncogene 1999;18:4237-4246.
66. El-Tanani M, Barraclough R, Wilkinson MC, Rudland PS. Metastasis-inducing DNA regulates the expression of the osteopontin gene by binding the transcription factor tcf-4. Cancer Res 2001;61:5619-5629.
67. Tang ZY, Ye SL, Liu YK, Qin LX, Sun HC, Ye QH, et al. A decade's studies on metastasis of hepatocellular carcinoma. J Cancer Res Clin Oncol 2004;130:187-196.
68. Hu RH, Lee PH, Yu SC, Dai HC, Sheu JC, Lai MY, et al. Surgical resection for recurrent hepatocellular carcinoma: prognosis and analysis of risk factors. Surgery 1996;120:23-29.
69. Poon RT, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Different risk factors and prognosis for early and late intrahepatic recurrence after resection of hepatocellular carcinoma. Cancer 2000;89:500-507.