Quantitative expression analysis and prognostic significance of the novel apoptosis-related gene BCL2L12 in colon cancer

Biological Chemistry

Volumn 389, Issue 12, 2008, Pages 1467-1475

  Kontos, Christos K ^a   Papadopoulos, Iordanis N ^b   Scorilas, Andreas ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b NATIONAL AND KAPODISTRIAN UNIVERSITY OF ATHENS   (Greece)

Author keywords

Apoptosis; BCL2 (Bcl 2) family; BCL2L12; Real time PCR; Tumor biomarkers

Indexed keywords

BIOLOGICAL MARKER; COMPLEMENTARY DNA; MESSENGER RNA; PROTEIN BCL 2; RNA;

ADULT; AGED; APOPTOSIS; ARTICLE; BCL2L12 GENE; CANCER SURVIVAL; COLON CANCER; CONTROLLED STUDY; GENE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MULTIGENE FAMILY; PRIORITY JOURNAL; PROGNOSIS;

ADULT; AGED; AGED, 80 AND OVER; ANALYSIS OF VARIANCE; COLON; COLONIC NEOPLASMS; DNA, COMPLEMENTARY; FEMALE; FLUORESCENT DYES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MIDDLE AGED; MUSCLE PROTEINS; ORGANIC CHEMICALS; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, NEOPLASM; SURVIVAL ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 57649131064     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2008.173     Document Type: Article

References (81)

1. Adams, J.M. and Cory, S. (1998). The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322-1326.
2. Altman, D.G., Lausen, B., Sauerbrei, W., and Schumacher, M. (1994). Dangers of using 'optimal' cutpoints in the evaluation of prognostic factors. J. Natl. Cancer Inst. 86, 829-835.
3. Bairey, O., Zimra, Y., Shaklai, M., Okon, E., and Rabizadeh, E. (1999). Bcl-2, Bcl-X, Bax, and Bak expression in short- and long-lived patients with diffuse large B-cell lymphomas. Clin. Cancer Res. 5, 2860-2866.
4. Bargou, R.C., Daniel, P.T., Mapara, M.Y., Bommert, K., Wagener, C., Kallinich, B., Royer, H.D., and Dorken, B. (1995). Expression of the bcl-2 gene family in normal and malignant breast tissue: low bax-a expression in tumor cells correlates with resistance towards apoptosis. Int. J. Cancer 60, 854-859.
5. Biroccio, A., Benassi, B., D'Agnano, I., D'Angelo, C., Buglioni, S., Mottolese, M., Ricciotti, A., Citro, G., Cosimelli, M., Ramsay, R.G., et al. (2001). c-Myb and Bcl-x overexpression predicts poor prognosis in colorectal cancer: clinical and experimental findings. Am. J. Pathol. 158, 1289-1299.
6. Blum, C., Graham, A., Yousefzadeh, M., Shrout, J., Benjamin, K., Krishna, M., Hoda, R., Cole, D.J., Garrett-Mayer, E., Reed, C., et al. (2008). The expression ratio of Map7/B2M is prognostic for survival in patients with stage II colon cancer. Int. J. Oncol. 33, 579-584.
7. Camp, R.L., Dolled-Filhart, M., and Rimm, D.L. (2004). X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin. Cancer Res. 10, 7252-7259.
8. Campos, L., Rouault, J.P., Sabido, O., Oriol, P., Roubi, N., Vasselon, C., Archimbaud, E., Magaud, J.P., and Guyotat, D. (1993). High expression of bcl-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Blood 81, 3091-3096.
9. Compton, C.C. and Greene, F.L. (2004). The staging of colorectal cancer: 2004 and beyond. CA Cancer J. Clin. 54, 295-308.
10. Cox, D.R. (1972). Regression models and life tables. R. Stat. Soc. B 34, 187-202.
11. de Jong, D., Prins, F.A., Mason, D.Y., Reed, J.C., van Ommen, G.B., and Kluin, P.M. (1994). Subcellular localization of the bcl-2 protein in malignant and normal lymphoid cells. Cancer Res. 54, 256-260.
12. Duffy, M.J. (2001). Carcinoembryonic antigen as a marker for colorectal cancer: is it clinically useful? Clin. Chem. 47, 624-630.
13. Evan, G.I. and Vousden, K.H. (2001). Proliferation, cell cycle and apoptosis in cancer. Nature 411, 342-348.
14. Ferlay, J., Autier, P., Boniol, M., Heanue, M., Colombet, M., and Boyle, P. (2007). Estimates of the cancer incidence and mortality in Europe in 2006. Ann. Oncol. 18, 581-592.
15. Filella, X., Molina, R., Grau, J.J., Pique, J.M., Garcia-Valdecasas, J.C., Astudillo, E., Biete, A., Bordas, J.M., Novell, A., Campo, E., et al. (1992). Prognostic value of CA 19.9 levels in colorectal cancer. Ann. Surg. 216, 55-59.
16. Flohil, C.C., Janssen, P.A., and Bosman, F.T. (1996). Expression of Bcl-2 protein in hyperplastic polyps, adenomas, and carcinomas of the colon. J. Pathol. 178, 393-397.
17. Floros, K.V., Thomadaki, H., Lallas, G., Katsaros, N., Talieri, M., and Scorilas, A. (2003). Cisplatin-induced apoptosis in HL-60 human promyelocytic leukemia cells: differential expression of BCL2 and novel apoptosis-related gene BCL2L12. Ann. NY Acad. Sci. 1010, 153-158.
18. Floros, K.V., Thomadaki, H., Katsaros, N., Talieri, M., and Scorilas, A. (2004). mRNA expression analysis of a variety of apoptosis-related genes, including the novel gene of the BCL2-family, BCL2L12, in HL-60 leukemia cells after treatment with carboplatin and doxorubicin. Biol. Chem. 385, 1099-1103.
19. Floros, K.V., Talieri, M., and Scorilas, A. (2006a). Topotecan and methotrexate alter expression of the apoptosis-related genes BCL2, FAS and BCL2L12 in leukemic HL-60 cells. Biol. Chem. 387, 1629-1633.
20. Floros, K.V., Thomadaki, H., Florou, D., Talieri, M., and Scorilas, A. (2006b). Alterations in mRNA expression of apoptosis-related genes BCL2, BAX, FAS, caspase-3, and the novel member BCL2L12 after treatment of human leukemic cell line HL60 with the antineoplastic agent etoposide. Ann. NY Acad. Sci. 1090, 89-97.
21. Gee, J.M., Robertson, J.F., Ellis, I.O., Willsher, P., McClelland, R.A., Hoyle, H.B., Kyme, S.R., Finlay, P., Blamey, R.W., and Nicholson, R.I. (1994). Immunocytochemical localization of BCL-2 protein in human breast cancers and its relationship to a series of prognostic markers and response to endocrine therapy. Int. J. Cancer 59, 619-628.
22. Gil, J., Yamamoto, H., Zapata, J.M., Reed, J.C., and Perucho, M. (1999). Impairment of the proapoptotic activity of Bax by missense mutations found in gastrointestinal cancers. Cancer Res. 59, 2034-2037.
23. Giulietti, A., Overbergh, L., Valckx, D., Decallonne, B., Bouillon, R., and Mathieu, C. (2001). An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25, 386-401.
24. Gonzalez-Garcia, M., Perez-Ballestero, R., Ding, L., Duan, L., Boise, L.H., Thompson, C.B., and Nunez, G. (1994). bcl-XL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development 120, 3033-3042.
25. Gosens, M.J., Moerland, E., Lemmens, V.P., Rutten, H.T., Tan-Go, I., and van den Brule, A.J. (2008). Thymidylate synthase genotyping is more predictive for therapy response than immunohistochemistry in patients with colon cancer. Int. J. Cancer 123, 1941-1949.
26. Greenlee, R.T., Hill-Harmon, M.B., Murray, T., and Thun, M. (2001). Cancer statistics, 2001. CA Cancer J. Clin. 51, 15-36.
27. Gryfe, R., Kim, H., Hsieh, E.T., Aronson, M.D., Holowaty, E.J., Bull, S.B., Redston, M., and Gallinger, S. (2000). Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N. Engl. J. Med. 342, 69-77.
28. L with Bax and Bad in colorectal cancer. Acta Oncol. 39, 495-500.
29. Jen, J., Kim, H., Piantadosi, S., Liu, Z.F., Levitt, R.C., Sistonen, P., Kinzler, K.W., Vogelstein, B., and Hamilton, S.R. (1994). Allelic loss of chromosome 18q and prognosis in colorectal cancer. N. Engl. J. Med. 331, 213-221.
30. Johnston, P.G., Fisher, E.R., Rockette, H.E., Fisher, B., Wolmark, N., Drake, J.C., Chabner, B.A., and Allegra, C.J. (1994). The role of thymidylate synthase expression in prognosis and outcome of adjuvant chemotherapy in patients with rectal cancer. J. Clin. Oncol. 12, 2640-2647.
31. Kaplan, E.L. and Meier, P. (1958). Nonparametric observation from incomplete observations. J. Am. Stat. Assoc. 53, 457-481.
32. Karakas, T., Maurer, U., Weidmann, E., Miething, C.C., Hoelzer, D., and Bergmann, L. (1998). High expression of bcl-2 mRNA as a determinant of poor prognosis in acute myeloid leukemia. Ann. Oncol. 9, 159-165.
33. Kerr, J.F., Wyllie, A.H., and Currie, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
34. Kitamura, S., Kondo, S., Shinomura, Y., Kanayama, S., Miyazaki, Y., Kiyohara, T., Hiraoka, S., and Matsuzawa, Y. (2000). Met/HGF receptor modulates bcl-w expression and inhibits apoptosis in human colorectal cancers. Br. J. Cancer 83, 668-673.
35. Koch, C.A., Anderson, D., Moran, M.F., Ellis, C., and Pawson, T. (1991). SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252, 668-674.
36. Korsmeyer, S.J. (1999). BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 59, 1693s-1700s.
37. Krajewska, M., Moss, S.F., Krajewski, S., Song, K., Holt, P.R., and Reed, J.C. (1996). Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas. Cancer Res. 56, 2422-2427.
38. Krajewski, S., Blomqvist, C., Franssila, K., Krajewska, M., Wasenius, V.M., Niskanen, E., Nordling, S., and Reed, J.C. (1995). Reduced expression of proapoptotic gene BAX is associated with poor response rates to combination chemotherapy and shorter survival in women with metastatic breast adenocarcinoma. Cancer Res. 55, 4471-4478.
39. Krajewski, S., Tanaka, S., Takayama, S., Schibler, M.J., Fenton, W., and Reed, J.C. (1993). Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53, 4701-4714.
40. Li, Q., Dashwood, W.M., Zhong, X., Nakagama, H., and Dashwood, R.H. (2007). Bcl-2 overexpression in PhIP-induced colon tumors: cloning of the rat Bcl-2 promoter and characterization of a pathway involving β-catenin, c-Myc and E2F1. Oncogene 26, 6194-6202.
41. Lindmark, G., Kressner, U., Bergstrom, R., and Glimelius, B. (1996). Limited clinical significance of the serum tumour marker Ca 72-4 in colorectal cancer. Anticancer Res. 16, 895-898.
42. Lipponen, P., Pietilainen, T., Kosma, V.M., Aaltomaa, S., Eskelinen, M., and Syrjanen, K. (1995). Apoptosis suppressing protein bcl-2 is expressed in well-differentiated breast carcinomas with favourable prognosis. J. Pathol. 177, 49-55.
43. (-ΔΔCT) method. Methods 25, 402-408.
44. Loukola, A., Salovaara, R., Kristo, P., Moisio, A.L., Kaariainen, H., Ahtola, H., Eskelinen, M., Harkonen, N., Julkunen, R., Kangas, E., et al. (1999). Microsatellite instability in adenomas as a marker for hereditary nonpolyposis colorectal cancer. Am. J. Pathol. 155, 1849-1853.
45. Martin, B., Paesmans, M., Berghmans, T., Branle, F., Ghisdal, L., Mascaux, C., Meert, A.P., Steels, E., Vallot, F., Verdebout, J.M., et al. (2003). Role of Bcl-2 as a prognostic factor for survival in lung cancer: a systematic review of the literature with meta-analysis. Br. J. Cancer 89, 55-64.
46. Mathioudaki, K., Scorilas, A., Papadokostopoulou, A., Xynopoulos, D., Arnogianaki, N., Agnanti, N., and Talieri, M. (2004). Expression analysis of BCL2L12, a new member of apoptosis-related genes, in colon cancer. Biol. Chem. 385, 779-783.
47. Maurer, C.A., Friess, H., Buhler, S.S., Wahl, B.R., Graber, H., Zimmermann, A., and Buchler, M.W. (1998). Apoptosis inhibiting factor Bcl-xL might be the crucial member of the Bcl-2 gene family in colorectal cancer. Dig. Dis. Sci. 43, 2641-2648.
48. McLeod, H.L. and Murray, G.I. (1999). Tumour markers of prognosis in colorectal cancer. Br. J. Cancer 79, 191-203.
49. Newcomb, P.A., Norfleet, R.G., Storer, B.E., Surawicz, T.S., and Marcus, P.M. (1992). Screening sigmoidoscopy and colorectal cancer mortality. J. Natl. Cancer Inst. 84, 1572-1575.
50. Ogura, E., Senzaki, H., Yamamoto, D., Yoshida, R., Takada, H., Hioki, K., and Tsubura, A. (1999). Prognostic significance of Bcl-2, Bcl-xL/S, Bax and Bak expressions in colorectal carcinomas. Oncol. Rep. 6, 365-369.
51. Parkin, D.M., Pisani, P., and Ferlay, J. (1999). Estimates of the worldwide incidence of 25 major cancers in 1990. Int. J. Cancer 80, 827-841.
52. Persson, B.E., Stahle, E., Pahlman, L., Glimelius, B., and Holmgren, J. (1988). CA-50 as a tumour marker for monitoring colorectal cancer: antigen rises in patients postoperatively precede clinical manifestations of recurrence. Eur. J. Cancer Clin. Oncol. 24, 241-246.
53. Pisani, P., Parkin, D.M., Bray, F., and Ferlay, J. (1999). Estimates of the worldwide mortality from 25 cancers in 1990. Int. J. Cancer 83, 18-29.
54. Pokorny, R.M., Hunt, L., and Galandiuk, S. (2000). What's new with tumor markers for colorectal cancer? Dig. Surg. 17, 209-215.
55. Prandi, M., Lionetto, R., Bini, A., Francioni, G., Accarpio, G., Anfossi, A., Ballario, E., Becchi, G., Bonilauri, S., Carobbi, A., et al. (2002). Prognostic evaluation of stage B colon cancer patients is improved by an adequate lymphadenectomy: results of a secondary analysis of a large scale adjuvant trial. Ann. Surg. 235, 458-463.
56. Pritchard, D.M., Print, C., O'Reilly, L., Adams, J.M., Potten, C.S., and Hickman, J.A. (2000). Bcl-w is an important determinant of damage-induced apoptosis in epithelia of small and large intestine. Oncogene 19, 3955-3959.
57. Reed, J.C. (1994). Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124, 1-6.
58. Reed, J.C. (1996). Balancing cell life and death: bax, apoptosis, and breast cancer. J. Clin. Invest. 97, 2403-2404.
59. Reed, J.C. (1999). Dysregulation of apoptosis in cancer. J. Clin. Oncol. 17, 2941-2953.
60. Reed, J.C. (2000). Mechanisms of apoptosis. Am. J. Pathol. 157, 1415-1430.
61. Reed, J.C. (2002). Apoptosis-based therapies. Nat. Rev. Drug Discov. 1, 111-121.
62. Reed, J.C. (2003). Apoptosis-targeted therapies for cancer. Cancer Cell 3, 17-22.
63. Schorr, K., Li, M., Krajewski, S., Reed, J.C., and Furth, P.A. (1999). Bcl-2 gene family and related proteins in mammary gland involution and breast cancer. J. Mammary Gland Biol. Neoplasia 4, 153-164.
64. Scorilas, A., Kyriakopoulou, L., Yousef, G.M., Ashworth, L.K., Kwamie, A., and Diamandis, E.P. (2001). Molecular cloning, physical mapping, and expression analysis of a novel gene, BCL2L12, encoding a proline-rich protein with a highly conserved BH2 domain of the Bcl-2 family. Genomics 72, 217-221.
65. Selby, J.V., Friedman, G.D., Quesenberry, C.P. Jr., and Weiss, N.S. (1992). A case-control study of screening sigmoidoscopy and mortality from colorectal cancer. N. Engl. J. Med. 326, 653-657.
66. Shibata, D., Reale, M.A., Lavin, P., Silverman, M., Fearon, E.R., Steele, G. Jr., Jessup, J.M., Loda, M., and Summerhayes, I.C. (1996). The DCC protein and prognosis in colorectal cancer. N. Engl. J. Med. 335, 1727-1732.
67. 2microglobulin mRNA expression levels are prognostic for lymph node metastasis in colorectal cancer patients. Br. J. Cancer 98, 1999-2005.
68. Steinberg, S.M., Barkin, J.S., Kaplan, R.S., and Stablein, D.M. (1986). Prognostic indicators of colon tumors. The Gastrointestinal Tumor Study Group experience. Cancer 57, 1866-1870.
69. Sun, S.Y., Yue, P., Zhou, J.Y., Wang, Y., Choi Kim, H.R., Lotan, R., and Wu, G.S. (2001). Overexpression of BCL2 blocks TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in human lung cancer cells. Biochem. Biophys. Res. Commun. 280, 788-797.
70. Sun, X.F., Carstensen, J.M., Zhang, H., Stal, O., Wingren, S., Hatschek, T., and Nordenskjold, B. (1992). Prognostic significance of cytoplasmic p53 oncoprotein in colorectal adenocarcinoma. Lancet 340, 1369-1373.
71. Talieri, M., Diamandis, E.P., Katsaros, N., Gourgiotis, D., and Scorilas, A. (2003). Expression of BCL2L12, a new member of apoptosis-related genes, in breast tumors. Thromb. Haemost. 89, 1081-1088.
72. Tepper, J.E., O'Connell, M.J., Niedzwiecki, D., Hollis, D., Compton, C., Benson, A.B. 3rd, Cummings, B., Gunderson, L., Macdonald, J.S., and Mayer, R.J. (2001). Impact of number of nodes retrieved on outcome in patients with rectal cancer. J. Clin. Oncol. 19, 157-163.
73. Thomadaki, H. and Scorilas, A. (2006). BCL2 family of apoptosis-related genes: functions and clinical implications in cancer. Crit. Rev. Clin. Lab. Sci. 43, 1-67.
74. Thomadaki, H. and Scorilas, A. (2007). Breast cancer cells response to the antineoplastic agents cisplatin, carboplatin, and doxorubicin at the mRNA expression levels of distinct apoptosis-related genes, including the new member, BCL2L12. Ann. NY Acad. Sci. 1095, 35-44.
75. Thomadaki, H., Talieri, M., and Scorilas, A. (2006). Treatment of MCF-7 cells with taxol and etoposide induces distinct alterations in the expression of apoptosis-related genes BCL2, BCL2L12, BAX, CASPASE-9 and FAS. Biol. Chem. 387, 1081-1086.
76. Thomadaki, H., Talieri, M., and Scorilas, A. (2007). Prognostic value of the apoptosis related genes BCL2 and BCL2L12 in breast cancer. Cancer Lett. 247, 48-55.
77. Tothova, E., Fricova, M., Stecova, N., Kafkova, A., and Elbertova, A. (2002). High expression of Bcl-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Neoplasma 49, 141-144.
78. Tsourouflis, G., Theocharis, S.E., Sampani, A., Giagini, A., Kostakis, A., and Kouraklis, G. (2008). Prognostic and predictive value of thymidylate synthase expression in colon cancer. Dig. Dis. Sci. 53, 1289-1296.
79. Valassiadou, K.E., Stefanaki, K., Tzardi, M., Datseris, G., Georgoulias, V., Melissas, J., Tsiftsis, D.D., Delides, G., and Kanavaros, P. (1997). Immunohistochemical expression of p53, bcl-2, mdm2 and waf1/p21 proteins in colorectal adenocarcinomas. Anticancer Res. 17, 2571-2576.
80. van der Schouw, Y.T., Verbeek, A.L., Wobbes, T., Segers, M.F., and Thomas, C.M. (1992). Comparison of four serum tumour markers in the diagnosis of colorectal carcinoma. Br. J. Cancer 66, 148-154.
81. Wilson, J.W., Nostro, M.C., Balzi, M., Faraoni, P., Cianchi, F., Becciolini, A., and Potten, C.S. (2000). Bcl-w expression in colorectal adenocarcinoma. Br. J. Cancer 82, 178-185.