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Science 14 February 1997:
Vol. 275. no. 5302, pp. 973 - 977
DOI: 10.1126/science.275.5302.973
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Reports

A Mammalian Telomerase-Associated Protein

Lea Harrington, * Timothy McPhail, Vernon Mar, Wen Zhou, Rena Oulton, Amgen EST Program, Mike B. Bass, Isabel Arruda, Murray O. Robinson *

The telomerase ribonucleoprotein catalyzes the addition of new telomeres onto chromosome ends. A gene encoding a mammalian telomerase homolog called TP1 (telomerase-associated protein 1) was identified and cloned. TP1 exhibited extensive amino acid similarity to the Tetrahymena telomerase protein p80 and was shown to interact specifically with mammalian telomerase RNA. Antiserum to TP1 immunoprecipitated telomerase activity from cell extracts, suggesting that TP1 is associated with telomerase in vivo. The identification of TP1 suggests that telomerase-associated proteins are conserved from ciliates to humans.

L. Harrington, R. Oulton, I. Arruda, Ontario Cancer Institute-Amgen Institute, Department of Medical Biophysics, University of Toronto, 620 University Avenue, Toronto, Ontario M5G 2C1, Canada.
T. McPhail, V. Mar, W. Zhou, Amgen EST Program, M. B. Bass, M. O. Robinson, Amgen, Inc., 1840 DeHavilland Drive, Thousand Oaks, CA 91320, USA.
*   To whom correspondence should be addressed.

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V. Anantharaman, E. V. Koonin, and L. Aravind (2002)
Nucleic Acids Res. 30, 1427-1464
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Analysis of the structure of human telomerase RNA in vivo.
M. Antal, E. Boros, F. Solymosy, and T. Kiss (2002)
Nucleic Acids Res. 30, 912-920
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Functional Multimerization of Human Telomerase Requires an RNA Interaction Domain in the N Terminus of the Catalytic Subunit.
T. J. Moriarty, S. Huard, S. Dupuis, and C. Autexier (2002)
Mol. Cell. Biol. 22, 1253-1265
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Functional Analysis of Conserved Residues in the Putative "Finger" Domain of Telomerase Reverse Transcriptase.
D. Bosoy and N. F. Lue (2001)
J. Biol. Chem. 276, 46305-46312
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Potent Inhibition of Telomerase by Small-Molecule Pentacyclic Acridines Capable of Interacting with G-Quadruplexes.
S. M. Gowan, R. Heald, M. F. G. Stevens, and L. R. Kelland (2001)
Mol. Pharmacol. 60, 981-988
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Regulation of Telomerase Activity by Alternate Splicing of Human Telomerase Reverse Transcriptase mRNA in a Subset of Neuroblastomas.
M. Krams, A. Claviez, K. Heidorn, G. Krupp, R. Parwaresch, D. Harms, and P. Rudolph (2001)
Am. J. Pathol. 159, 1925-1932
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Tetrahymena proteins p80 and p95 are not core telomerase components.
D. X. Mason, C. Autexier, and C. W. Greider (2001)
PNAS
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Regulation of Human Telomerase Activity: Repression by Normal Chromosome 3 Abolishes Nuclear Telomerase Reverse Transcriptase Transcripts but Does Not Affect c-Myc Activity.
A.-L. Ducrest, M. Amacker, Y. D. Mathieu, A. P. Cuthbert, D. A. Trott, R. F. Newbold, M. Nabholz, and J. Lingner (2001)
Cancer Res. 61, 7594-7602
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Elevated Expression of hTERT Is Associated with Dysplastic Cell Transformation during Human Oral Carcinogenesis in Situ.
H.-R. Kim, R. Christensen, N.-H. Park, P. Sapp, M. K. Kang, and N.-H. Park (2001)
Clin. Cancer Res. 7, 3079-3086
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Functional Multimerization of the Human Telomerase Reverse Transcriptase.
T. L. Beattie, W. Zhou, M. O. Robinson, and L. Harrington (2001)
Mol. Cell. Biol. 21, 6151-6160
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Human telomerase RNA-protein interactions.
F. Bachand, I. Triki, and C. Autexier (2001)
Nucleic Acids Res. 29, 3385-3393
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Complex Regulation of Telomerase Activity : Implications for Cancer Therapy.
K. S. J. Elenitoba-Johnson (2001)
Am. J. Pathol. 159, 405-410
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Down-Regulation of Telomerase Activity in Malignant Lymphomas by Radiation and Chemotherapeutic Agents.
Z. Lin, S. Lim, M. A. Viani, M. Sapp, and M. S. Lim (2001)
Am. J. Pathol. 159, 711-719
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E2F-1 represses transcription of the human telomerase reverse transcriptase gene.
D. L. Crowe, D. C. Nguyen, K. J. Tsang, and S. Kyo (2001)
Nucleic Acids Res. 29, 2789-2794
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Telomerase Inhibition in RenCa, a Murine Tumor Cell Line with Short Telomeres, by Overexpression of a Dominant Negative mTERT Mutant, Reveals Fundamental Differences in Telomerase Regulation between Human and Murine Cells.
J. Sachsinger, E. Gonzalez-Suarez, E. Samper, R. Heicappell, M. Muller, and Maria. A. Blasco (2001)
Cancer Res. 61, 5580-5586
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hnRNP A1 may interact simultaneously with telomeric DNA and the human telomerase RNA in vitro.
S. Fiset and B. Chabot (2001)
Nucleic Acids Res. 29, 2268-2275
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A Novel Mechanism for Chaperone-mediated Telomerase Regulation during Prostate Cancer Progression.
A. Akalin, L. W. Elmore, H. L. Forsythe, B. A. Amaker, E. D. McCollum, P. S. Nelson, J. L. Ware, and S. E. Holt (2001)
Cancer Res. 61, 4791-4796
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Retinoids down-regulate telomerase and telomere length in a pathway distinct from leukemia cell differentiation.
F. Pendino, M. Flexor, F. Delhommeau, D. Buet, M. Lanotte, and E. Ségal-Bendirdjian (2001)
PNAS
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Telomerase activation and p53 mutations in urethane-induced A/J mouse lung tumor development.
J. Ohno, Y. Horio, Y. Sekido, Y. Hasegawa, M. Takahashi, J.-i. Nishizawa, H. Saito, F. Ishikawa, and K. Shimokata (2001)
Carcinogenesis 22, 751-756
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Identification of human telomerase reverse transcriptase-derived peptides that induce HLA-A24-restricted antileukemia cytotoxic T lymphocytes.
J. Arai, M. Yasukawa, H. Ohminami, M. Kakimoto, A. Hasegawa, and S. Fujita (2001)
Blood 97, 2903-2907
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Telomerase and cancer.
J. W. Shay, Y. Zou, E. Hiyama, and W. E. Wright (2001)
Hum. Mol. Genet. 10, 677-685
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Autocrine Transforming Growth Factor {beta} Suppresses Telomerase Activity and Transcription of Human Telomerase Reverse Transcriptase in Human Cancer Cells.
H. Yang, S. Kyo, M. Takatura, and L. Sun (2001)
Cell Growth Differ. 12, 119-127
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The Telomerase/Vault-Associated Protein Tep1 Is Required for Vault RNA Stability and Its Association with the Vault Particle.
V. A. Kickhoefer, Y. Liu, L. B. Kong, B. E. Snow, P. L. Stewart, L. Harrington, and L. H. Rome (2001)
J. Cell Biol. 152, 157-164
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Heterogeneous Nuclear Ribonucleoproteins C1 and C2 Associate with the RNA Component of Human Telomerase.
L. P. Ford, J. M. Suh, W. E. Wright, and J. W. Shay (2000)
Mol. Cell. Biol. 20, 9084-9091
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Telomerase-Associated Protein TEP1 Is Not Essential for Telomerase Activity or Telomere Length Maintenance In Vivo.
Y. Liu, B. E. Snow, M. P. Hande, G. Baerlocher, V. A. Kickhoefer, D. Yeung, A. Wakeham, A. Itie, D. P. Siderovski, P. M. Lansdorp, et al. (2000)
Mol. Cell. Biol. 20, 8178-8184
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Progesterone Regulates Human Telomerase Reverse Transcriptase Gene Expression via Activation of Mitogen-activated Protein Kinase Signaling Pathway.
Z. Wang, S. Kyo, M. Takakura, M. Tanaka, N. Yatabe, Y. Maida, M. Fujiwara, J. Hayakawa, M. Ohmichi, K. Koike, et al. (2000)
Cancer Res. 60, 5376-5381
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Polymerization Defects within Human Telomerase Are Distinct from Telomerase RNA and TEP1 Binding.
T. L. Beattie, W. Zhou, M. O. Robinson, and L. Harrington (2000)
Mol. Biol. Cell 11, 3329-3340
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Characterization of the Interaction between the Nuclease and Reverse Transcriptase Activity of the Yeast Telomerase Complex.
H. Niu, J. Xia, and N. F. Lue (2000)
Mol. Cell. Biol. 20, 6806-6815
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Expression of human telomerase subunit genes in primary lung cancer and its clinical significance.
M. Arinaga, S. Shimizu, K. Gotoh, N. Haruki, T. Takahashi, T. Takahashi, and T. Mitsudomi (2000)
Ann. Thorac. Surg. 70, 401-405
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2-5A Antisense Telomerase RNA Therapy for Intracranial Malignant Gliomas.
S. Mukai, Y. Kondo, S. Koga, T. Komata, B. P. Barna, and S. Kondo (2000)
Cancer Res. 60, 4461-4467
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Identification of Functionally Important Domains in the N-Terminal Region of Telomerase Reverse Transcriptase.
J. Xia, Y. Peng, I. S. Mian, and N. F. Lue (2000)
Mol. Cell. Biol. 20, 5196-5207
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Identification and characterization of negative regulatory elements of the human telomerase catalytic subunit (hTERT) gene promoter: possible role of MZF-2 in transcriptional repression of hTERT.
K. Fujimoto, S. Kyo, M. Takakura, T. Kanaya, Y. Kitagawa, H. Itoh, M. Takahashi, and M. Inoue (2000)
Nucleic Acids Res. 28, 2557-2562
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Demethylating Reagent 5-Azacytidine Inhibits Telomerase Activity in Human Prostate Cancer Cells through Transcriptional Repression of hTERT.
Y. Kitagawa, S. Kyo, M. Takakura, T. Kanaya, K. Koshida, M. Namiki, and M. Inoue (2000)
Clin. Cancer Res. 6, 2868-2875
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Interference Footprinting Analysis of Telomerase Elongation Complexes.
S. Benjamin, N. Baran, and H. Manor (2000)
Mol. Cell. Biol. 20, 4224-4237
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Expression of the hTERT Gene Is Regulated at the Level of Transcriptional Initiation and Repressed by Mad1.
C. Günes, S. Lichtsteiner, A. P. Vasserot, and C. Englert (2000)
Cancer Res. 60, 2116-2121
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Adenoviral Expression of p53 Represses Telomerase Activity through Down-Regulation of Human Telomerase Reverse Transcriptase Transcription.
T. Kanaya, S. Kyo, K. Hamada, M. Takakura, Y. Kitagawa, H. Harada, and M. Inoue (2000)
Clin. Cancer Res. 6, 1239-1247
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The Est1 Subunit of Yeast Telomerase Binds the Tlc1 Telomerase RNA.
J. Zhou, K. Hidaka, and B. Futcher (2000)
Mol. Cell. Biol. 20, 1947-1955
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The role of senescence and immortalization in carcinogenesis.
R. R. Reddel (2000)
Carcinogenesis 21, 477-484
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Identification of Two RNA-binding Proteins Associated with Human Telomerase RNA.
S. Le, R. Sternglanz, and C. W. Greider (2000)
Mol. Biol. Cell 11, 999-1010
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Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT).
S. Kyo, M. Takakura, T. Taira, T. Kanaya, H. Itoh, M. Yutsudo, H. Ariga, and M. Inoue (2000)
Nucleic Acids Res. 28, 669-677
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Positive and negative regulation of telomerase access to the telomere.
S. Evans and V Lundblad (2000)
J. Cell Sci. 113, 3357-3364
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Functional Reconstitution of Human Telomerase Expressed in Saccharomyces cerevisiae.
F. Bachand and C. Autexier (1999)
J. Biol. Chem. 274, 38027-38031
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Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA.
M. S. Fitzgerald, K. Riha, F. Gao, S. Ren, T. D. McKnight, and D. E. Shippen (1999)
PNAS 96, 14813-14818
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Estrogen Activates Telomerase.
S. Kyo, M. Takakura, T. Kanaya, W. Zhuo, K. Fujimoto, Y. Nishio, A. Orimo, and M. Inoue (1999)
Cancer Res. 59, 5917-5921
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Studies of the molecular mechanisms in the regulation of telomerase activity.
J.-P. LIU (1999)
FASEB J 13, 2091-2104
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Vaults and Telomerase Share a Common Subunit, TEP1.
V. A. Kickhoefer, A. G. Stephen, L. Harrington, M. O. Robinson, and L. H. Rome (1999)
J. Biol. Chem. 274, 32712-32717
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Telomeres and telomerase.
M. A. Blasco, S. M. Gasser, and J. Lingner (1999)
Genes & Dev. 13, 2353-2359
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Telomere shortening and apoptosis in telomerase-inhibited human tumor cells.
X. Zhang, V. Mar, W. Zhou, L. Harrington, and M. O. Robinson (1999)
Genes & Dev. 13, 2388-2399
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The 193-Kd Vault Protein, Vparp, Is a Novel Poly(Adp-Ribose) Polymerase.
V. A. Kickhoefer, A. C. Siva, N. L. Kedersha, E. M. Inman, C. Ruland, M. Streuli, and L. H. Rome (1999)
J. Cell Biol. 146, 917-928
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Two Inactive Fragments of the Integral RNA Cooperate To Assemble Active Telomerase with the Human Protein Catalytic Subunit (hTERT) In Vitro.
V. M. Tesmer, L. P. Ford, S. E. Holt, B. C. Frank, X. Yi, D. L. Aisner, M. Ouellette, J. W. Shay, and W. E. Wright (1999)
Mol. Cell. Biol. 19, 6207-6216
   Abstract »    Full Text »    PDF »
The telomerase RNA pseudoknot is critical for the stable assembly of a catalytically active ribonucleoprotein.
D. Gilley and E. H. Blackburn (1999)
PNAS 96, 6621-6625
   Abstract »    Full Text »    PDF »
Human Telomerase Reverse Transcriptase (hTERT) Gene Expression in Thyroid Neoplasms.
M. Saji, S. Xydas, W. H. Westra, C.-K. Liang, D. P. Clark, R. Udelsman, C. B. Umbricht, S. Sukumar, and M. A. Zeiger (1999)
Clin. Cancer Res. 5, 1483-1489
   Abstract »    Full Text »    PDF »
Akt Protein Kinase Enhances Human Telomerase Activity through Phosphorylation of Telomerase Reverse Transcriptase Subunit.
S. S. Kang, T. Kwon, D. Y. Kwon, and S. I. Do (1999)
J. Biol. Chem. 274, 13085-13090
   Abstract »    Full Text »    PDF »
Telomerase RNA function in recombinant Tetrahymena telomerase.
J. D. Licht and K. Collins (1999)
Genes & Dev. 13, 1116-1125
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Expression of Mutated Paramecium Telomerase RNAs In Vivo Leads to Templating Errors That Resemble Those Made by Retroviral Reverse Transcriptase.
A. J. Ye, W. J. Haynes, and D. P. Romero (1999)
Mol. Cell. Biol. 19, 2887-2894
   Abstract »    Full Text »    PDF »
Functional requirement of p23 and Hsp90 in telomerase complexes.
S. E. Holt, D. L. Aisner, J. Baur, V. M. Tesmer, M. Dy, M. Ouellette, J. B. Trager, G. B. Morin, D. O. Toft, J. W. Shay, et al. (1999)
Genes & Dev. 13, 817-826
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Rapid Detection of MYCN Gene Amplification and Telomerase Expression in Neuroblastoma.
E. Hiyama, K. Hiyama, T. Yokoyama, I. Fukuba, H. Yamaoka, J. W. Shay, and Y. Matsuura (1999)
Clin. Cancer Res. 5, 601-609
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Telomere Length Dynamics and Chromosomal Instability in Cells Derived from Telomerase Null Mice.
M. P. Hande, E. Samper, P. Lansdorp, and M. A. Blasco (1999)
J. Cell Biol. 144, 589-601
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Cloning of Human Telomerase Catalytic Subunit (hTERT) Gene Promoter and Identification of Proximal Core Promoter Sequences Essential for Transcriptional Activation in Immortalized and Cancer Cells.
M. Takakura, S. Kyo, T. Kanaya, H. Hirano, J. Takeda, M. Yutsudo, and M. Inoue (1999)
Cancer Res. 59, 551-557
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