Telomerase in breast cancer: A critical evaluation

Advances in Anatomic Pathology

Volumn 11, Issue 5, 2004, Pages 262-268

  Baykal, Atac ^a   Rosen, Daniel ^a   Zhou, Chenyi ^a   Liu, Jinsong ^a   Sahin, Aysegul A ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Breast cancer; Ductal carcinoma in situ; Telomerase; TRAP assay

Indexed keywords

TELOMERASE;

BREAST TUMOR; ENZYMOLOGY; HUMAN; METABOLISM; PAGET NIPPLE DISEASE; REVIEW; TELOMERE;

BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; HUMANS; TELOMERASE; TELOMERE;

EID: 16644398654     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/01.pap.0000138145.19258.64     Document Type: Review

References (89)

1. Moyzis RK, Buckingham JM, Cram LS, et al. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA. 1988;85:6622-6626.
2. Blackburn EH. Structure and function of telomeres. Nature. 1991;350:569-573. (Pubitemid 21912269)
3. Greider CW. Telomeres. Curr Opin Cell Biol. 1991;3:444-451. (Pubitemid 121006106)
4. Greider CW, Blackburn EH. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985;43:405-413. (Pubitemid 16213265)
5. Shore D. Telomerase and telomere-binding proteins: controlling the endgame. Trends Biochem Sci. 1997;22:233-235. (Pubitemid 27310941)
6. Blackburn EH. Telomere states and cell fates. Nature. 2000;408:53-56.
7. Gasser SM. A sense of the end. Science. 2000;288:1377-1379. (Pubitemid 30366316)
8. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature. 1990;345:458-460.
9. Harley CB. Telomere loss: mitotic clock or genetic time bomb? Mutat Res. 1991;256:271-282.
10. Lindsey J, McGill NI, Lindsey LA, et al. In vivo loss of telomeric repeats with age in humans. Mutat Res. 1991;256:45-48.
11. Vaziri H, Dragowska W, Allsopp RC, et al. Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age. Proc Natl Acad Sci USA. 1994;91:9857-9860. (Pubitemid 24311907)
12. Nakamura TM, Morin GB, Chapman KB, et al. Telomerase catalytic subunit homologs from fission yeast and human. Science. 1997;277:955-959. (Pubitemid 27366681)
13. Feng J, Funk WD, Wang SS, et al. The RNA component of human telomerase. Science. 1995;269:1236-1241.
14. Avilion AA, Piatyszek MA, Gupta J, et al. Human telomerase RNA and telomerase activity in immortal cell lines and tumor tissues. Cancer Res. 1996;56:645-650. (Pubitemid 26043667)
15. Counter CM, Avilion AA, LeFeuvre CE, et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 1992;11:1921-1929.
16. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266:2011-2015.
17. Kilian A, Bowtell DD, Abud HE, et al. Isolation of a candidate human telomerase catalytic subunit gene, which reveals complex splicing patterns in different cell types. Hum Mol Genet. 1997;6:2011-2019. (Pubitemid 27477942)
18. Meyerson M, Counter CM, Eaton EN, et al. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell. 1997;90:785-795. (Pubitemid 27357969)
19. Ducrest AL, Amacker M, Mathieu YD, et al. Regulation of human telomerase activity: repression by normal chromosome 3 abolishes nuclear telomerase reverse transcriptase transcripts but does not affect c-Myc activity. Cancer Res. 2001;61:7594-7602. (Pubitemid 32995053)
20. Takakura M, Kyo S, Kanaya T, et al. Expression of human telomerase subunits and correlation with telomerase activity in cervical cancer. Cancer Res. 1998;58:1558-1561. (Pubitemid 28193624)
21. Kolquist KA, Ellisen LW, Counter CM, et al. Expression of TERT in early premalignant lesions and a subset of cells in normal tissues. Nat Genet. 1998;19:182-186. (Pubitemid 28248803)
22. Wan M, Li WZ, Duggan BD, et al. Telomerase activity in benign and malignant epithelial ovarian tumors. J Natl Cancer Inst. 1997;89:437-441. (Pubitemid 27136735)
23. Murakami J, Nagai N, Ohama K, et al. Telomerase activity in ovarian tumors. Cancer. 1997;80:1085-1092. (Pubitemid 27427608)
24. Kyo S, Takakura M, Tanaka M, et al. Quantitative differences in telomerase activity among malignant, premalignant, and benign ovarian lesions. Clin Cancer Res. 1998;4:399-405. (Pubitemid 28122755)
25. Kyo S, Kanaya T, Takakura M, et al. Expression of human telomerase subunits in ovarian malignant, borderline and benign tumors. Int J Cancer. 1999;80:804-809. (Pubitemid 29108852)
26. Baykal A, Thompson JA, Xu X-C, et al. In situ human telomerase reverse transcriptase expression pattern in normal and neoplastic ovarian tissues. Oncol Rep. 2004;11:297-302.
27. Hahn WC, Counter CM, Lundberg AS, et al. Creation of human tumour cells with defined genetic elements. Nature. 1999;400:464-468. (Pubitemid 29361801)
28. Herbert B, Pitts AE, Baker SI, et al. Inhibition of human telomerase in immortal human cells leads to progressive telomere shortening and cell death. Proc Natl Acad Sci USA. 1999;96:14276-14281. (Pubitemid 30000641)
29. Kanaya T, Kyo S, Takakura M, et al. hTERT is a critical determinant of telomerase activity in renal-cell carcinoma. Int J Cancer. 1998;78:539-543. (Pubitemid 28507174)
30. Counter CM, Meyerson M, Eaton EN, et al. Telomerase activity is restored in human cells by ectopic expression of hTERT (hEST2), the catalytic subunit of telomerase. Oncogene. 1998;16:1217-1222. (Pubitemid 28127521)
31. Weinrich SL, Pruzan R, Ma L, et al. Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat Genet. 1997;17:498-502. (Pubitemid 27518407)
32. Bodnar AG, Ouellette M, Frolkis M, et al. Extension of life-span by introduction of telomerase into normal human cells. Science. 1998;279:349-352. (Pubitemid 28063364)
33. Hiyama E, Gollahon L, Kataoka T, et al. Telomerase activity in human breast tumors. J Natl Cancer Inst. 1996;88:116-122. (Pubitemid 26020100)
34. Sugino T, Yoshida K, Bolodeoku J, et al. Telomerase activity in human breast cancer and benign breast lesions: diagnostic applications in clinical specimens, including fine needle aspirates. Int J Cancer. 1996;69:301-306. (Pubitemid 26298295)
35. Nawaz S, Hashizumi TL, Markham NE, et al. Telomerase expression in human breast cancer with and without lymph node metastases. Am J Clin Pathol. 1997;107:542-547. (Pubitemid 27183986)
36. Clark GM, Osborne CK, Levitt D, et al. Telomerase activity and survival of patients with node-positive breast cancer. J Natl Cancer Inst. 1997;89:1874-1881. (Pubitemid 28009823)
37. Roos G, Nilsson P, Cajander S, et al. Telomerase activity in relation to p53 status and clinico-pathological parameters in breast cancer. Int J Cancer. 1998;79:343-348. (Pubitemid 28359730)
38. Hoos A, Hepp HH, Kaul S, et al. Telomerase activity correlates with tumor aggressiveness and reflects therapy effect in breast cancer. Int J Cancer. 1998;79:8-12. (Pubitemid 28157718)
39. Mokbel K, Parris CN, Ghilchik M, et al. The association between telomerase, histopathological parameters, and Ki-67 expression in breast cancer. Am J Surg. 1999;178:69-72. (Pubitemid 29375068)
40. Umbricht CB, Sherman ME, Dome J, et al. Telomerase activity in ductal carcinoma in situ and invasive breast cancer. Oncogene. 1999;18:3407-3414. (Pubitemid 29286987)
41. Li H, Cao Y, Berndt MC, et al. Molecular interactions between telomerase and the tumor suppressor protein p53 in vitro. Oncogene. 1999;18:6785-6794.
42. Xu D, Wang Q, Gruber A, et al. Downregulation of telomerase reverse transcriptase mRNA expression by wild-type p53 in human tumor cells. Oncogene. 2000;19:5123-5133.
43. Greenberg RA,O'Hagan RC, Deng H, et al. Telomerase reverse transcriptase gene is a direct target of c-Myc but is not functionally equivalent in cellular transformation. Oncogene. 1999;18:1219-1226. (Pubitemid 29085995)
44. Wu KJ, Grandori C, Amacker M, et al. Direct activation of TERT transcription by c-Myc. Nat Genet. 1999;21:220-224. (Pubitemid 29070372)
45. Kyo S, Takakura M, Taira T, et al. Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res. 2000;28:669-677. (Pubitemid 30068249)
46. Zhou C, Liu J. Inhibition of human telomerase reverse transcriptase gene expression by BRCA1 in human ovarian cancer cells. Biochem Biophys Res Commun. 2003;303:130-136. (Pubitemid 36338217)
47. Kyo S, Takakura M, Kanaya T, et al. Estrogen activates telomerase. Cancer Res. 1999;59:5917-5921. (Pubitemid 30004951)
48. Wang Z, Kyo S, Maida Y, et al. Tamoxifen regulates human telomerase reverse transcriptase (hTERT) gene expression differently in breast and endometrial cancer cells. Oncogene. 2002;21:3517-3524. (Pubitemid 34587683)
49. Morales CP, Holt SE, Ouellette M, et al. Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat Genet. 1999;21:115-118. (Pubitemid 29036296)
50. Jiang XR, Jimenez G, Chang E, et al. Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype. Nat Genet. 1999;21:111-114.
51. Hahn WC, Stewart SA, Brooks MW, et al. Inhibition of telomerase limits the growth of human cancer cells. Nat Med. 1999;5:1164-1170. (Pubitemid 29474421)
52. Toouli CD, Huschtscha LI, Neumann AA, et al. Comparison of human mammary epithelial cells immortalized by simian virus 40 T-Antigen or by the telomerase catalytic subunit. Oncogene. 2002;21:128-139. (Pubitemid 34076385)
53. Seger YR, Garcia-Cao M, Piccinin S, et al. Transformation of normal human cells in the absence of telomerase activation. Cancer Cell. 2002;2:401-413. (Pubitemid 41039106)
54. Soder AI, Going JJ, Kaye SB, et al. Tumour specific regulation of telomerase RNA gene expression visualized by in situ hybridization. Oncogene. 1998;16:979-983. (Pubitemid 28107935)
55. Ramakrishnan S, Eppenberger U, Mueller H, et al. Expression profile of the putative catalytic subunit of the telomerase gene. Cancer Res. 1998;58:622-625. (Pubitemid 28099468)
56. Hiyama E, Hiyama K, Yokoyama T, et al. Correlating telomerase activity levels with human neuroblastoma outcomes. Nat Med. 1995;1:249-255.
57. Wright WE, Piatyszek MA, Rainey WE, et al. Telomerase activity in human germline and embryonic tissues and cells. Dev Genet. 1996;18:173-179. (Pubitemid 26116862)
58. Yashima K, Milchgrub S, Gollahon LS, et al. Telomerase enzyme activity and RNA expression during the multistage pathogenesis of breast carcinoma. Clin Cancer Res. 1998;4:229-234. (Pubitemid 28062901)
59. Hiyama E, Hiyama K, Yokoyama T, et al. Immunohistochemical detection of telomerase (hTERT) protein in human cancer tissues and a subset of cells in normal tissues. Neoplasia. 2001;3:17-26. (Pubitemid 32201606)
60. Ulaner GA, Hu JF, Vu TH, et al. Telomerase activity in human development is regulated by human telomerase reverse transcriptase (hTERT) transcription and by alternate splicing of hTERT transcripts. Cancer Res. 1998;58:4168-4172. (Pubitemid 28440575)
61. Beckmann MW, Niederacher D, Schnurch HG, et al. Multistep carcinogenesis of breast cancer and tumour heterogeneity. J Mol Med. 1997;75:429-439. (Pubitemid 27297013)
62. Silverstein MJ. Ductal carcinoma in situ of the breast. Br J Surg. 1997;84:145-146.
63. Medina D, Kittrell FS, Shepard A, et al. Biological and genetic properties of the p53 null preneoplastic mammary epithelium. FASEB J. 2002;16:881-883.
64. Tsao J, Zhao Y, Lukas J, et al. Telomerase activity in normal and neoplastic breast. Clin Cancer Res. 1997;3:627-631. (Pubitemid 27211843)
65. Poremba C, Bocker W, Willenbring H, et al. Telomerase activity in human proliferative breast lesions. Int J Oncol. 1998;12:641-648. (Pubitemid 28097295)
66. Pearson AS, Gollahon LS, O'Neal NC, et al. Detection of telomerase activity in breast masses by fine-needle aspiration. Ann Surg Oncol. 1998;5:186-193. (Pubitemid 29071289)
67. Kassim SK, Fawzy H, El Rassad MM, et al. Telomerase activity, and tissue polypeptide specific antigen (TPS) in Egyptian breast cancer patients. Clin Biochem. 2001;34:499-504. (Pubitemid 33001320)
68. Bednarek AK, Sahin A, Brenner AJ, et al. Analysis of telomerase activity levels in breast cancer: positive detection at the in situ breast carcinoma stage. Clin Cancer Res. 1997;3:11-16. (Pubitemid 27079438)
69. Mueller C, Riese U, Kosmehl H, et al. Telomerase activity in microdissected human breast cancer tissues: association with p53, p21 and outcome. Int J Oncol. 2002;20:385-390.
70. Shpitz B, Zimlichman S, Zemer R, et al. Telomerase activity in ductal carcinoma in situ of the breast. Breast Cancer Res Treat. 1999;58:65-69. (Pubitemid 30003872)
71. Rha SY, Park KH, Kim TS, et al. Changes of telomerase and telomere lengths in paired normal and cancer tissues of breast. Int J Oncol. 1999;15:839-845.
72. Carey LA, Hedican CA, Henderson GS, et al. Careful histological confirmation and microdissection reveal telomerase activity in otherwise telomerase-negative breast cancers. Clin Cancer Res. 1998;4:435-440. (Pubitemid 28122760)
73. Carey LA, Kim NW, Goodman S, et al. Telomerase activity and prognosis in primary breast cancers. J Clin Oncol. 1999;17:3075-3081. (Pubitemid 29470635)
74. Mokbel KM, Parris CN, Ghilchik M, et al. Telomerase activity and lymphovascular invasion in breast cancer. Eur J Surg Oncol. 2000;26:30-33. (Pubitemid 30102819)
75. Hiyama E, Saeki T, Hiyama K, et al. Telomerase activity as a marker of breast carcinoma in fine-needle aspirate samples. Cancer. 2000;90:235-238. (Pubitemid 30660111)
76. Poremba C, Shroyer KR, Frost M, et al. Telomerase is a highly sensitive and specific molecular marker in fine-needle aspirates of breast lesions. J Clin Oncol. 1999;17:2020-2026. (Pubitemid 29318830)
77. Poremba C, Heine B, Diallo R, et al. Telomerase as a prognostic marker in breast cancer: high-throughput tissue microarray analysis of hTERT and hTR. J Pathol. 2002;198:181-189. (Pubitemid 35251756)
78. Mokbel K, Ghilchik M, Williams G, et al. The association between telomerase activity and hormone receptor status and p53 expression in breast cancer. Int J Surg Investig. 2000;1:509-516.
79. Simickova M, Nekulova M, Pecen L, et al. Quantitative determination of telomerase activity in breast cancer and benign breast diseases. Neoplasma. 2001;48:267-273. (Pubitemid 32802437)
80. Minev B, Hipp J, Firat H, et al. Cytotoxic T cell immunity against telomerase reverse transcriptase in humans. Proc Natl Acad Sci USA. 2000;97:4796-4801. (Pubitemid 30238637)
81. Nair SK, Heiser A, Boczkowski D, et al. Induction of cytotoxic T cell responses and tumor immunity against unrelated tumors using telomerase reverse transcriptase RNA transfected dendritic cells. Nat Med. 2000;6:1011-1017.
82. Schroers R, Huang XF, Hammer J, et al. Identification of HLA DR7-restricted epitopes from human telomerase reverse transcriptase recognized by CD4+ T-helper cells. Cancer Res. 2002;62:2600-2605. (Pubitemid 34462740)
83. Gowan SM, Harrison JR, Patterson L, et al. A G-quadruplex-interactive potent small-molecule inhibitor of telomerase exhibiting in vitro and in vivo antitumor activity. Mol Pharmacol. 2002;61:1154-1162. (Pubitemid 34441781)
84. Saito K, Yagihashi A, Nasu S, et al. Gene expression for suppressors of telomerase activity (telomeric-repeat binding factors) in breast cancer. Jpn J Cancer Res. 2002;93:253-258. (Pubitemid 34464360)
85. Herbert BS, Pongracz K, Shay JW, et al. Oligonucleotide N3′→P5′ phosphoramidates as efficient telomerase inhibitors. Oncogene. 2002;21:638-642. (Pubitemid 34146265)
86. Kaur H, Richardson E, Murty L. Preparation of monoclonal antibodies against human telomerase. Hybridoma. 2001;20:183-188. (Pubitemid 32881313)
87. Kim MM, Rivera MA, Botchkina IL, et al. A low threshold level of expression of mutant-template telomerase RNA inhibits human tumor cell proliferation. Proc Natl Acad Sci USA. 2001;98:7982-7987. (Pubitemid 32642673)
88. Herbert BS, Wright AC, Passons CM, et al. Effects of chemopreventive and antitelomerase agents on the spontaneous immortalization of breast epithelial cells. J Natl Cancer Inst. 2001;93:39-45. (Pubitemid 32060888)
89. Masutomi K, Yu EY, Khurts S, et al. Telomerase maintains telomere structure in normal human cells. Cell. 2003;114:241-253. (Pubitemid 36936917)