Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Review Article

Chaperones and Their Role in Telomerase Ribonucleoprotein Biogenesis and Telomere Maintenance

Author(s): Maria Alejandra Viviescas, Maria Isabel Nogueira Cano* and Marcela Segatto

Volume 16, Issue 1, 2019

Page: [31 - 43] Pages: 13

DOI: 10.2174/1570164615666180713103133

Price: $65

Abstract

Telomere length maintenance is important for genome stability and cell division. In most eukaryotes, telomeres are maintained by the telomerase ribonucleoprotein (RNP) complex, minimally composed of the Telomerase Reverse Transcriptase (TERT) and the telomerase RNA (TER) components. In addition to TERT and TER, other protein subunits are part of the complex and are involved in telomerase regulation, assembly, disassembly, and degradation. Among them are some molecular chaperones such as Hsp90 and its co-chaperone p23 which are found associated with the telomerase RNP complex in humans, yeast and probably in protozoa. Hsp90 and p23 are necessary for the telomerase RNP assembly and enzyme activity. In budding yeast, the Hsp90 homolog (Hsp82) is also responsible for the association and dissociation of telomerase from the telomeric DNA by its direct interaction with a telomere end-binding protein (Cdc13), responsible for regulating telomerase access to telomeres. In addition, AAA+ ATPases, such as Pontin and Reptin, which are also considered chaperone- like proteins, associate with the human telomerase complex by the direct interaction of Pontin with TERT and dyskerin. They are probably responsible for telomerase RNP assembly since their depletion impairs the accumulation of the complex. Moreover, various RNA chaperones, are also pivotal in the assembly and migration of the mature telomerase complex and complex intermediates. In this review, we will focus on the importance of molecular chaperones for telomerase RNP biogenesis and how they impact telomere length maintenance and cellular homeostasis.

Keywords: Chaperones, telomerase, telomeres, ribonucleoprotein complex, biogenesis, quadruplex structure.

Graphical Abstract
[1]
Muller, H.J. The remaking of chromosomes. Collect. Net. (Woods Hole), 1938, 13, 181-198.
[2]
McClintock, B. The stability of broken ends of chromosomes in Zea Mays. Genetics, 1941, 26(2), 234-282.
[3]
Blackburn, E.H.; Gall, J.G. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J. Mol. Biol., 1978, 120(1), 33-53.
[4]
Greider, C.W.; Blackburn, E.H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell, 1985, 43(2 Pt 1), 405-413.
[5]
Meyne, J.; Ratliff, R.L.; Moyzis, R.K. Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc. Natl. Acad. Sci. USA, 1989, 86(18), 7049-7053.
[6]
Cano, M.I. Telomere biology of trypanosomatids: More questions than answers. Trends Parasitol., 2001, 17(9), 425-429.
[7]
Weinrich, S.L.; Pruzan, R.; Ma, L.; Ouellette, M.; Tesmer, V.M.; Holt, S.E.; Bodnar, A.G.; Lichtsteiner, S.; Kim, N.W.; Trager, J.B.; Taylor, R.D.; Carlos, R.; Andrews, W.H.; Wright, W.E.; Shay, J.W.; Harley, C.B.; Morin, G.B. Reconstitution of human telomerase with the template RNA component HTR and the catalytic protein subunit HTRT. Nat. Genet., 1997, 17(4), 498-502.
[8]
Giardini, M.A.; Segatto, M.; da Silva, M.S.; Nunes, V.S.; Cano, M.I.N. Telomere and telomerase biology. Prog. Mol. Biol. Transl. Sci., 2014, 125, 1-40.
[9]
de Lange, T. Opinion: T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biol., 2004, 5(4), 323-329.
[10]
Griffith, J.D.; Comeau, L.; Rosenfield, S.; Stansel, R.M.; Bianchi, A.; Moss, H.; de Lange, T. Mammalian telomeres end in a large duplex loop. Cell, 1999, 97(4), 503-514.
[11]
Blackburn, E.H.; Greider, C.W.; Henderson, E.; Lee, M.S.; Shampay, J.; Shippen-Lentz, D. Recognition and elongation of telomeres by telomerase. Genome, 1989, 31(2), 553-560.
[12]
Greider, C.W.; Blackburn, E.H. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature, 1989, 337(6205), 331-337.
[13]
Lingner, J.; Cech, T.R. Purification of telomerase from Euplotes Aediculatus: Requirement of a primer 3′ overhang. Proc. Natl. Acad. Sci. USA, 1996, 93(20), 10712-10717.
[14]
Nakamura, T.M.; Morin, G.B.; Chapman, K.B.; Weinrich, S.L.; Andrews, W.H.; Lingner, J.; Harley, C.B.; Cech, T.R. Telomerase catalytic subunit homologs from fission yeast and human. Science, 1997, 277(5328), 955-959.
[15]
Lundblad, V.; Blackburn, E.H. An alternative pathway for yeast telomere maintenance rescues Est1- senescence. Cell, 1993, 73(2), 347-360.
[16]
Chen, Q.; Ijpma, A.; Greider, C.W. Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol. Cell. Biol., 2001, 21(5), 1819-1827.
[17]
Laroche, T.; Martin, S.G.; Tsai-Pflugfelder, M.; Gasser, S.M. The dynamics of yeast telomeres and silencing proteins through the cell cycle. J. Struct. Biol., 2000, 129(2-3), 159-174.
[18]
Stewart, S.A.; Weinberg, R.A. Senescence: Does it all happen at the ends? Oncogene, 2002, 21(4), 627-630.
[19]
Smogorzewska, A.; de Lange, T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem., 2004, 73(1), 177-208.
[20]
Cohen, P.; Blackburn, E.H. Two types of telomeric chromatin in Tetrahymena Thermophila. J. Mol. Biol., 1998, 280(3), 327-344.
[21]
De Lange, T. Telomere-related genome instability in cancer. Cold Spring Harb. Symp. Quant. Biol., 2005, 70, 197-204.
[22]
He, H.; Multani, A.S.; Cosme-Blanco, W.; Tahara, H.; Ma, J.; Pathak, S.; Deng, Y.; Chang, S. POT1b protects telomeres from end-to-end chromosomal fusions and aberrant homologous recombination. EMBO J., 2006, 25(21), 5180-5190.
[23]
Hockemeyer, D.; Daniels, J-P.; Takai, H.; de Lange, T. Recent expansion of the telomeric complex in rodents: Two distinct POT1 proteins protect mouse telomeres. Cell, 2006, 126(1), 63-77.
[24]
Wu, L.; Multani, A.S.; He, H.; Cosme-Blanco, W.; Deng, Y.; Deng, J.M.; Bachilo, O.; Pathak, S.; Tahara, H.; Bailey, S.M.; Deng, Y.; Behringer, R.R.; Chang, S. Pot1 deficiency initiates dna damage checkpoint activation and aberrant homologous recombination at telomeres. Cell, 2006, 126(1), 49-62.
[25]
Zhong, Z.; Shiue, L.; Kaplan, S.; de Lange, T. A mammalian factor that binds telomeric TTAGGG repeats in vitro. Mol. Cell. Biol., 1992, 12(11), 4834-4843.
[26]
Smogorzewska, A. van Steensel, B.; Bianchi, A.; Oelmann, S.; Schaefer, M.R.; Schnapp, G.; de Lange, T. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol., 2000, 20(5), 1659-1668.
[27]
van Steensel, B.; de Lange, T. Control of telomere length by the human telomeric protein TRF1. Nature, 1997, 385(6618), 740-743.
[28]
Li, B.; Oestreich, S.; de Lange, T. Identification of human Rap1: implications for telomere evolution. Cell, 2000, 101(5), 471-483.
[29]
Palm, W.; de Lange, T. How shelterin protects mammalian telomeres. Annu. Rev. Genet., 2008, 42(1), 301-334.
[30]
Svendsen, J.M.; Smogorzewska, A.; Sowa, M.E.; O’Connell, B.C.; Gygi, S.P.; Elledge, S.J.; Harper, J.W. Mammalian BTBD12/SLX4 assembles a holliday junction resolvase and is required for DNA repair. Cell, 2009, 138(1), 63-77.
[31]
Wang, F.; Podell, E.R.; Zaug, A.J.; Yang, Y.; Baciu, P.; Cech, T.R.; Lei, M. The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature, 2007, 445(7127), 506-510.
[32]
Xin, H.; Liu, D.; Songyang, Z. The telosome/shelterin complex and its functions. Genome Biol., 2008, 9(9), 232.
[33]
Takai, K.K.; Kibe, T.; Donigian, J.R.; Frescas, D.; de Lange, T. Telomere protection by TPP1/POT1 requires tethering to TIN2. Mol. Cell, 2011, 44(4), 647-659.
[34]
Martínez, P.; Blasco, M.A. Telomeric and extra-telomeric roles for telomerase and the telomere-binding proteins. Nat. Rev. Cancer, 2011, 11(3), 161-176.
[35]
Schramke, V.; Luciano, P.; Brevet, V.; Guillot, S.; Corda, Y.; Longhese, M.P.; Gilson, E.; Géli, V. RPA regulates telomerase action by providing Est1p access to chromosome ends. Nat. Genet., 2004, 36(1), 46-54.
[36]
Gao, H.; Cervantes, R.B.; Mandell, E.K.; Otero, J.H.; Lundblad, V. RPA-like proteins mediate yeast telomere function. Nat. Struct. Mol. Biol., 2007, 14(3), 208-214.
[37]
Wellinger, R.J. The CST complex and telomere maintenance: The exception becomes the rule. Mol. Cell, 2009, 36(2), 168-169.
[38]
Longhese, M.P. DNA damage response at functional and dysfunctional telomeres. Genes Dev., 2008, 22(2), 125-140.
[39]
Giraud-Panis, M-J.; Teixeira, M.T.; Géli, V.; Gilson, E. CST meets shelterin to keep telomeres in check. Mol. Cell, 2010, 39(5), 665-676.
[40]
Chen, L-Y.; Redon, S.; Lingner, J. The human CST complex is a terminator of telomerase activity. Nature, 2012, 488(7412), 540-544.
[41]
Miyake, Y.; Nakamura, M.; Nabetani, A.; Shimamura, S.; Tamura, M.; Yonehara, S.; Saito, M.; Ishikawa, F. RPA-like mammalian Ctc1-Stn1-Ten1 complex binds to single-stranded DNA and protects telomeres independently of the Pot1 pathway. Mol. Cell, 2009, 36(2), 193-206.
[42]
Surovtseva, Y.V.; Churikov, D.; Boltz, K.A.; Song, X.; Lamb, J.C.; Warrington, R.; Leehy, K.; Heacock, M.; Price, C.M.; Shippen, D.E. Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell, 2009, 36(2), 207-218.
[43]
Gu, P.; Min, J-N.; Wang, Y.; Huang, C.; Peng, T.; Chai, W.; Chang, S. CTC1 deletion results in defective telomere replication, leading to catastrophic telomere loss and stem cell exhaustion. EMBO J., 2012, 31(10), 2309-2321.
[44]
Blackburn, E.H. Telomeres: No end in sight. Cell, 1994, 77(5), 621-623.
[45]
Olovnikov, A.M. Principle of marginotomy in template synthesis of polynucleotides. Dokl. Akad. Nauk SSSR, 1971, 201(6), 1496-1499.
[46]
Watson, J.D. Origin of concatemeric T7 DNA. Nat. New Biol., 1972, 239(94), 197-201.
[47]
de Lange, T. How telomeres solve the end-protection problem. Science, 2009, 326(5955), 948-952.
[48]
Blasco, M.A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet., 2007, 8(4), 299-309.
[49]
Artandi, S.E.; DePinho, R.A. Telomeres and telomerase in cancer. Carcinogenesis, 2010, 31(1), 9-18.
[50]
Martínez, P.; Blasco, M.A. Role of shelterin in cancer and aging. Aging Cell, 2010, 9(5), 653-666.
[51]
Calado, R.T.; Young, N.S. Telomere maintenance and human bone marrow failure. Blood, 2008, 111(9), 4446-4455.
[52]
Calado, R.T.; Young, N.S. Telomere diseases. Natl. Engl. J. Med., 2009, 361(24), 2353-2365.
[53]
Mason, P.J.; Bessler, M. The genetics of dyskeratosis congenita. Cancer Genet., 2011, 204(12), 635-645.
[54]
Blasco, M.A. Telomeres and human disease: Ageing, cancer and beyond. Nat. Rev. Genet., 2005, 6(8), 611-622.
[55]
Blasco, M.A.; Rizen, M.; Greider, C.W.; Hanahan, D. Differential Regulation of telomerase activity and telomerase RNA during multi-stage tumorigenesis. Nat. Genet., 1996, 12(2), 200-204.
[56]
Nishio, N.; Kojima, S. Recent progress in dyskeratosis congenita. Int. J. Hematol., 2010, 92(3), 419-424.
[57]
Islam, A.; Rafiq, S.; Kirwan, M.; Walne, A.; Cavenagh, J.; Vulliamy, T.; Dokal, I. Haematological recovery in dyskeratosis congenita patients treated with danazol. Br. J. Haematol., 2013, 162(6), 854-856.
[58]
Bohn, O.L.; Whitten, J.; Spitzer, B.; Kobos, R.; Prockop, S.; Boulad, F.; Arcila, M.; Wang, L.; Teruya-Feldstein, J. Posttransplant lymphoproliferative disorder complicating hematopoietic stem cell transplantation in a patient with dyskeratosis congenita. Int. J. Surg. Pathol., 2013, 21(5), 520-525.
[59]
Alder, J.K.; Parry, E.M.; Yegnasubramanian, S.; Wagner, C.L.; Lieblich, L.M.; Auerbach, R.; Auerbach, A.D.; Wheelan, S.J.; Armanios, M. Telomere phenotypes in females with heterozygous mutations in the dyskeratosis congenita 1 (DKC1) gene. Hum. Mutat., 2013, 34(11), 1481-1485.
[60]
Sherr, C.J.; McCormick, F. The RB and P53 pathways in cancer. Cancer Cell, 2002, 2(2), 103-112.
[61]
Kurz, D.J.; Decary, S.; Hong, Y.; Trivier, E.; Akhmedov, A.; Erusalimsky, J.D. Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J. Cell Sci., 2004, 117(11), 2417-2426.
[62]
Oeseburg, H.; de Boer, R.A.; van Gilst, W.H.; van der Harst, P. Telomere biology in healthy aging and disease. Pflugers Arch. - Eur. J. Physiol., 2010, 459(2), 259-268.
[63]
Shay, J.W.; Wright, W.E. Telomerase: A target for cancer therapeutics. Cancer Cell, 2002, 2(4), 257-265.
[64]
Fagagna, F. d’Adda di; Reaper, P.M.; Clay-Farrace, L.; Fiegler, H.; Carr, P.; von Zglinicki, T.; Saretzki, G.; Carter, N.P.; Jackson, S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature, 2003, 426(6963), 194-198.
[65]
Mondello, C.; Scovassi, A.I. Telomeres, telomerase, and apoptosis. Biochem. Cell Biol., 2004, 82(4), 498-507.
[66]
Saretzki, G.; Ludwig, A.; von Zglinicki, T.; Runnebaum, I.B. Ribozyme-mediated telomerase inhibition induces immediate cell loss but not telomere shortening in ovarian cancer cells. Cancer Gene Ther., 2001, 8(10), 827-834.
[67]
Cao, Y.; Li, H.; Deb, S.; Liu, J-P. TERT regulates cell survival independent of telomerase enzymatic activity. Oncogene, 2002, 21(20), 3130-3138.
[68]
Jiang, Y-A.; Luo, H-S.; Zhang, Y-Y.; Fan, L-F.; Jiang, C-Q.; Chen, W-J. Telomerase activity and cell apoptosis in colon cancer cell by human telomerase reverse transcriptase gene antisense oligodeoxynucleotide. World J. Gastroenterol., 2003, 9(9), 1981-1984.
[69]
Smith, L.L.; Coller, H.A.; Roberts, J.M. Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nat. Cell Biol., 2003, 5(5), 474-479.
[70]
Hackett, J.A.; Greider, C.W. Balancing instability: Dual roles for telomerase and telomere dysfunction in tumorigenesis. Oncogene, 2002, 21(4), 619-626.
[71]
Wu, X.; Amos, C.I.; Zhu, Y.; Zhao, H.; Grossman, B.H.; Shay, J.W.; Luo, S.; Hong, W.K.; Spitz, M.R. Telomere dysfunction: A potential cancer predisposition factor. J. Natl. Cancer Inst., 2003, 95(16), 1211-1218.
[72]
Deng, Y.; Chan, S.S.; Chang, S. Telomere dysfunction and tumour suppression: The senescence connection. Nat. Rev. Cancer, 2008, 8(6), 450-458.
[73]
Shay, J.W.; Wright, W.E. Telomeres and telomerase in normal and cancer stem cells. FEBS Lett., 2010, 584(17), 3819-3825.
[74]
Gonzalez-Suarez, E.; Samper, E.; Ramírez, A.; Flores, J.M.; Martín-Caballero, J.; Jorcano, J.L.; Blasco, M.A. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, MTERT, in basal keratinocytes. EMBO J., 2001, 20(11), 2619-2630.
[75]
Artandi, S.E.; Alson, S.; Tietze, M.K.; Sharpless, N.E.; Ye, S.; Greenberg, R.A.; Castrillon, D.H.; Horner, J.W.; Weiler, S.R.; Carrasco, R.D.; DePinho, R.A. Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc. Natl. Acad. Sci., 2002, 99(12), 8191-8196.
[76]
Shammas, M.A.; Simmons, C.G.; Corey, D.R.; Shmookler Reis, R.J. Telomerase inhibition by peptide nucleic acids reverses ‘immortality’ of transformed human cells. Oncogene, 1999, 18(46), 6191-6200.
[77]
Forsyth, N.R.; Wright, W.E.; Shay, J.W. Telomerase and differentiation in multicellular organisms: Turn it off, turn it on, and turn it off again. Differentiation, 2002, 69(4-5), 188-197.
[78]
Holt, S.E.; Aisner, D.L.; Baur, J.; Tesmer, V.M.; Dy, M.; Ouellette, M.; Trager, J.B.; Morin, G.B.; Toft, D.O.; Shay, J.W.; Wright, W.E.; White, M.A. Functional requirement of P23 and Hsp90 in telomerase complexes. Genes Dev., 1999, 13(7), 817-826.
[79]
Collins, K. The biogenesis and regulation of telomerase holoenzymes. Nat. Rev. Mol. Cell Biol., 2006, 7(7), 484-494.
[80]
Wojtyla, A.; Gladych, M.; Rubis, B. Human telomerase activity regulation. Mol. Biol. Rep., 2011, 38(5), 3339-3349.
[81]
Wright, W.E.; Piatyszek, M.A.; Rainey, W.E.; Byrd, W.; Shay, J.W. Telomerase activity in human germline and embryonic tissues and cells. Dev. Genet., 1996, 18(2), 173-179.
[82]
Cong, Y-S.; Wright, W.E.; Shay, J.W. Human telomerase and its regulation. Microbiol. Mol. Biol. Rev., 2002, 66(3), 407-425.
[83]
Grandori, C.; Cowley, S.M.; James, L.P.; Eisenman, R.N. The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol., 2000, 16(1), 653-699.
[84]
Wang, J.; Xie, L.Y.; Allan, S.; Beach, D.; Hannon, G.J. Myc activates telomerase. Genes Dev., 1998, 12(12), 1769-1774.
[85]
Greenberg, R.; O’Hagan, R.C.; Deng, H.; Xiao, Q.; Hann, S.R.; Adams, R.R.; Lichtsteiner, S.; Chin, L.; Morin, G.B.; DePinho, R. Telomerase reverse transcriptase gene is a direct target of c-myc but is not functionally equivalent in cellular transformation. Oncogene, 1999, 18(5), 1219-1226.
[86]
Ulaner, G.A.; Hu, J.; Vu, T.H.; Giudice, L.C.; Hoffman, A.R. 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(31), 4168-4172.
[87]
Yi, X.; Tesmer, V.M.; Savre-Train, I.; Shay, J.W.; Wright, W.E. Both transcriptional and posttranscriptional mechanisms regulate human telomerase template RNA levels. Mol. Cell. Biol., 1999, 19(6), 3989-3997.
[88]
Feng, J.; Funk, W.D.; Wang, S.S.; Weinrich, S.L.; Avilion, A.A.; Chiu, C.P.; Adams, R.R.; Chang, E.; Allsopp, R.C.; Yu, J. The RNA component of human telomerase. Science, 1995, 269(5228), 1236-1241.
[89]
Aigner, S.; Postberg, J.; Lipps, H.J.; Cech, T.R. The Euplotes La motif protein P43 has properties of a telomerase-specific subunit. Biochemistry, 2003, 42(19), 5736-5747.
[90]
O’Connor, C.M.; Collins, K.L. A novel RNA binding domain in tetrahymena telomerase P65 initiates hierarchical assembly of telomerase holoenzyme. Mol. Cell. Biol., 2006, 26(6), 2029-2036.
[91]
Collins, K.; Witkin, K.L.; Prathapam, R. Positive and negative regulation of tetrahymena telomerase holoenzyme. Mol. Cell. Biol., 2007, 27(6), 2074-2083.
[92]
Rubtsova, M.P.; Vasilkova, D.P.; Naraykina, Y.V.; Dontsova, O.A. Peculiarities of yeasts and human telomerase RNAs processing. Acta Naturae, 2016, 8(4), 14-22.
[93]
Cech, T.R.; Seto, A.G.; Zaug, A.J.; Sobel, S.G.; Wolin, S.L. Saccharomyces Cerevisiae telomerase is an sm small nuclear ribonucleoprotein particle. Nature, 1999, 401(6749), 177-180.
[94]
Mitchell, J.R.; Cheng, J.; Collins, K. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol. Cell. Biol., 1999, 19(1), 567-576.
[95]
Mitchell, J.R.; Collins, K. Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol. Cell, 2000, 6(2), 361-371.
[96]
Pogacić, V.; Dragon, F.; Filipowicz, W. Human H/ACA small nucleolar RNPs and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol. Cell. Biol., 2000, 20(23), 9028-9040.
[97]
Darzacq, X.; Kittur, N.; Roy, S.; Shav-Tal, Y.; Singer, R.H.; Meier, U.T. Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J. Cell Biol., 2006, 173(2), 207-218.
[98]
Seimiya, H.; Sawada, H.; Muramatsu, Y.; Shimizu, M.; Ohko, K.; Yamane, K.; Tsuruo, T. Involvement of 14-3-3 proteins in nuclear localization of telomerase. EMBO J., 2000, 19(11), 2652-2661.
[99]
Akiyama, M.; Hideshima, T.; Hayashi, T.; Tai, Y-T.; Mitsiades, C.S.; Mitsiades, N.; Chauhan, D.; Richardson, P.; Munshi, N.C.; Anderson, K.C. Nuclear factor-kappaB P65 mediates tumor necrosis factor alpha-induced nuclear translocation of telomerase reverse transcriptase protein. Cancer Res., 2003, 63(1), 18-21.
[100]
Jakob, S.; Schroeder, P.; Lukosz, M.; Büchner, N.; Spyridopoulos, I.; Altschmied, J.; Haendeler, J. Nuclear protein tyrosine phosphatase Shp-2 is one important negative regulator of nuclear export of telomerase reverse transcriptase. J. Biol. Chem., 2008, 283(48), 33155-33161.
[101]
Khurts, S.; Masutomi, K.; Delgermaa, L.; Arai, K.; Oishi, N.; Mizuno, H.; Hayashi, N.; Hahn, W.C.; Murakami, S. Nucleolin interacts with telomerase. J. Biol. Chem., 2004, 279(49), 51508-51515.
[102]
Wong, J.M.Y.; Kusdra, L.; Collins, K. Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat. Cell Biol., 2002, 4(9), 731-736.
[103]
Lee, J.H.; Lee, Y.S.; Jeong, S.A.; Khadka, P.; Roth, J.; Chung, I.K. Catalytically active telomerase holoenzyme is assembled in the dense fibrillar component of the nucleolus during S phase. Histochem. Cell Biol., 2014, 141(2), 137-152.
[104]
Tomlinson, R.L.; Ziegler, T.D.; Supakorndej, T.; Terns, R.M.; Terns, M.P. Cell cycle-regulated trafficking of human telomerase to telomeres. Mol. Biol. Cell, 2006, 17(2), 955-965.
[105]
Fiset, S.; Chabot, B. HnRNP A1 may interact simultaneously with telomeric dna and the human telomerase RNA in vitro. Nucleic Acids Res., 2001, 29(11), 2268-2275.
[106]
Alves, D.; Li, H.; Codrington, R.; Orte, A.; Ren, X.; Klenerman, D.; Balasubramanian, S. Single-molecule analysis of human telomerase monomer. Nat. Chem. Biol., 2008, 4(5), 287-289.
[107]
Jiang, J.; Chan, H.; Cash, D.D.; Miracco, E.J.; Ogorzalek Loo, R.R.; Upton, H.E.; Cascio, D.; O’Brien Johnson, R.; Collins, K.; Loo, J.A.; Zhou, Z.H.; Feigon, J. Structure of Tetrahymena telomerase reveals previously unknown subunits, functions, and interactions. Science, 2015, 350(6260), aab4070-aab4070.
[108]
Malyavko, A.N.; Parfenova, Y.Y.; Zvereva, M.I.; Dontsova, O.A. Telomere length regulation in budding yeasts. FEBS Lett., 2014, 588(15), 2530-2536.
[109]
Taggart, A.K.P.; Teng, S-C.; Zakian, V.A. Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science, 2002, 297(5583), 1023-1026.
[110]
Gallardo, F.; Olivier, C.; Dandjinou, A.T.; Wellinger, R.J.; Chartrand, P. TLC1 RNA nucleo-cytoplasmic trafficking links telomerase biogenesis to its recruitment to telomeres. EMBO J., 2008, 2721, 748-757.
[111]
Fisher, T.S.; Taggart, A.K.P.; Zakian, V.A. Cell cycle-dependent regulation of yeast telomerase by Ku. Nat. Struct. Mol. Biol., 2004, 11(12), 1198-1205.
[112]
Chan, A.; Boulé, J-B.; Zakian, V.A.; McElver, J.; Weber, S. Two pathways recruit telomerase to Saccharomyces Cerevisiae telomeres. PLoS Genet., 2008, 4(10), e1000236.
[113]
Jády, B.E.; Richard, P.; Bertrand, E.; Kiss, T. Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol. Biol. Cell, 2006, 17(2), 944-954.
[114]
Stern, J.L.; Zyner, K.G.; Pickett, H.A.; Cohen, S.B.; Bryan, T.M. Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol. Cell. Biol., 2012, 32(13), 2384-2395.
[115]
Sexton, A.N.; Regalado, S.G.; Lai, C.S.; Cost, G.J.; O’Neil, C.M.; Urnov, F.D.; Gregory, P.D.; Jaenisch, R.; Collins, K.; Hockemeyer, D. Genetic and molecular identification of three human TPP1 functions in telomerase action: Recruitment, activation, and homeostasis set point regulation. Genes Dev., 2014, 28(17), 1885-1899.
[116]
Vogan, J.M.; Collins, K. Dynamics of human telomerase holoenzyme assembly and subunit exchange across the cell cycle. J. Biol. Chem., 2015, 290(35), 21320-21335.
[117]
Schmidt, J.C.; Cech, T.R. Human telomerase: Biogenesis, trafficking, recruitment, and activation. Genes Dev., 2015, 29(11), 1095-1105.
[118]
Zhou, X.Z.; Lu, K.P. The Pin2/TRF1-interacting protein PinX1 is a potent telomerase inhibitor. Cell, 2001, 107(3), 347-359.
[119]
Lin, J.; Blackburn, E.H. Nucleolar protein PinX1p regulates telomerase by sequestering its protein catalytic subunit in an inactive complex lacking telomerase RNA. Genes Dev., 2004, 18(4), 387-396.
[120]
Banik, S.S.R.; Counter, C.M. Characterization of interactions between PinX1 and human telomerase subunits HTERT and HTR. J. Biol. Chem., 2004, 279(50), 51745-51748.
[121]
Soohoo, C.Y.; Shi, R.; Lee, T.H.; Huang, P.; Lu, K.P.; Zhou, X.Z. Telomerase inhibitor PinX1 provides a link between TRF1 and telomerase to prevent telomere elongation. J. Biol. Chem., 2011, 286(5), 3894-3906.
[122]
Yonekawa, T.; Yang, S.; Counter, C.M. PinX1 localizes to telomeres and stabilizes TRF1 at mitosis. Mol. Cell. Biol., 2012, 32(8), 1387-1395.
[123]
Yoo, J.E.; Park, Y.N.; Oh, B-K. PinX1, a Telomere Repeat-Binding Factor 1 (TRF1)-interacting protein, maintains telomere integrity by modulating TRF1 homeostasis, the process in which Human Telomerase Reverse Transcriptase (HTERT) plays dual roles. J. Biol. Chem., 2014, 289(10), 6886-6898.
[124]
Redon, S.; Reichenbach, P.; Lingner, J. The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res., 2010, 38(17), 948-952.
[125]
Zappulla, D.C.; Cech, T.R. RNA as a flexible scaffold for proteins: Yeast telomerase and beyond. Cold Spring Harb. Symp. Quant. Biol., 2006, 71, 217-224.
[126]
MacNeil, D.; Bensoussan, H.; Autexier, C. telomerase regulation from beginning to the end. Genes., 2016, 7(9), 64.
[127]
Grozdanov, P.N.; Roy, S.; Kittur, N.; Meier, U.T. SHQ1 Is required prior to NAF1 for assembly of H/ACA small nucleolar and telomerase RNPs. RNA, 2009, 15(6), 1188-1197.
[128]
Nano, N.; Houry, W.A. Chaperone-like activity of the AAA+ proteins Rvb1 and Rvb2 in the assembly of various complexes. Philos. Trans. R. Soc. B. Biol. Sci., 2013, 368(1617), 20110399-20110399.
[129]
Forsythe, H.L.; Jarvis, J.L.; Turner, J.W.; Elmore, L.W.; Holt, S.E. Stable association of Hsp90 and P23, but Not Hsp70, with active human telomerase. J. Biol. Chem., 2001, 276(19), 15571-15574.
[130]
Keppler, B.R.; Grady, A.T.; Jarstfer, M.B. The biochemical role of the heat shock protein 90 chaperone complex in establishing human telomerase activity. J. Biol. Chem., 2006, 281(29), 19840-19848.
[131]
Toogun, O.A.; DeZwaan, D.C.; Freeman, B.C. The Hsp90 molecular chaperone modulates multiple telomerase activities. Mol. Cell. Biol., 2008, 28(1), 457-467.
[132]
Lee, H.; Sengupta, N.; Villagra, A.; Rezai-Zadeh, N.; Seto, E. Histone deacetylase 8 safeguards the Human Ever-Shorter Telomeres 1B (HEST1B) protein from ubiquitin-mediated degradation. Mol. Cell. Biol., 2006, 26(14), 5259-5269.
[133]
Richter, K.; Buchner, J. Hsp90: Chaperoning signal transduction. J. Cell. Physiol., 2001, 188(3), 281-290.
[134]
Hutchinson, D.; Ho, V.; Dodd, M.; Dawson, H.N.; Zumwalt, A.C.; Colton, C.A. NIH public access., 2008, 148(4), 825-832.
[135]
Pratt, W.B.; Toft, D.O. Regulation of signaling protein function and trafficking by the Hsp90/Hsp70-based chaperone machinery. Exp. Biol. Med., 2003, 228(2), 111-133.
[136]
Prodromou, C.; Roe, S.M.; O’Brien, R.; Ladbury, J.E.; Piper, P.W.; Pearl, L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell, 1997, 90(1), 65-75.
[137]
Grenert, J.P.; Sullivan, W.P.; Fadden, P.; Haystead, T.A.J.; Clark, J.; Mimnaugh, E.; Krutzsch, H.; Ochel, H-J.; Schulte, T.W.; Sausville, E.; Neckers, L.M.; Toft, D.O. The amino-terminal domain of heat shock protein 90 (Hsp90) that binds geldanamycin is an ATP/ADP switch domain that regulates Hsp90 conformation. J. Biol. Chem., 1997, 272(38), 23843-23850.
[138]
Marcu, M.G.; Schulte, T.W.; Neckers, L. Novobiocin and related coumarins and depletion of heat shock protein 90-dependent signaling proteins. J. Natl. Cancer Inst., 2000, 92(3), 242-248.
[139]
Marcu, M.G.; Chadli, A.; Bouhouche, I.; Catelli, M.; Neckers, L.M. The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the carboxyl terminus of the chaperone. J. Biol. Chem., 2000, 275(47), 37181-37186.
[140]
Johnson, J.L.; Toft, D.O. A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and P23. J. Biol. Chem., 1994, 269(40), 24989-24993.
[141]
Fang, Y.; Fliss, A.E.; Rao, J.; Caplan, A.J. SBA1 encodes a yeast Hsp90 cochaperone that is homologous to vertebrate P23 proteins. Mol. Cell. Biol., 1998, 18(7), 3727-3734.
[142]
Bohen, S.P. Genetic and biochemical analysis of P23 and ansamycin antibiotics in the function of Hsp90-dependent signaling proteins. Mol. Cell. Biol., 1998, 18(6), 3330-3339.
[143]
Sullivan, W.; Stensgard, B.; Caucutt, G.; Bartha, B.; McMahon, N.; Alnemri, E.S.; Litwack, G.; Toft, D. Nucleotides and two functional states of Hsp90. J. Biol. Chem., 1997, 272(12), 8007-8012.
[144]
Akalin, A.; Elmore, L.W.; Forsythe, H.L.; Amaker, B.A.; Mccollum, E.D.; Nelson, P.S.; Ware, J.L.; Holt, S.E. A novel mechanism for chaperone-mediated telomerase regulation during prostate cancer progression. Cancer Res., 2001, 61(12), 4791-4796.
[145]
Haendeler, J.; Hoffmann, J.; Rahman, S.; Zeiher, A.M.; Dimmeler, S. Regulation of telomerase activity and anti-apoptotic function by protein-protein interaction and phosphorylation. FEBS Lett., 2003, 536(1-3), 180-186.
[146]
Dezwaan, D.C.; Toogun, O.A.; Echtenkamp, F.J.; Freeman, B.C. The Hsp82 molecular chaperone promotes a switch between unextendable and extendable telomere states. Nat. Publ. Gr., 2009, 16(7), 711-716.
[147]
Lee, J.H.; Chung, I.K. Curcumin inhibits nuclear localization of telomerase by dissociating the Hsp90 co-chaperone P23 from HTERT. Cancer Lett., 2010, 290(1), 76-86.
[148]
Venteicher, A.S.; Meng, Z.; Mason, P.J.; Veenstra, T.D.; Artandi, S.E. Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly. Cell, 2008, 132(6), 945-957.
[149]
Gorynia, S.; Bandeiras, T.M.; Pinho, F.G.; McVey, C.E.; Vonrhein, C.; Round, A.; Svergun, D.I.; Donner, P.; Matias, P.M.; Carrondo, M.A. Structural and functional insights into a dodecameric molecular machine - the RuvBL1/RuvBL2 complex. J. Struct. Biol., 2011, 176(3), 279-291.
[150]
Torreira, E.; Jha, S.; López-Blanco, J.R.; Arias-Palomo, E.; Chacón, P.; Cañas, C.; Ayora, S.; Dutta, A.; Llorca, O. Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes. Structure, 2008, 16(10), 1511-1520.
[151]
Majerská, J.; Schrumpfová, P.P.; Dokládal, L.; Schořová, Š.; Stejskal, K.; Obořil, M.; Honys, D.; Kozáková, L.; Polanská, P.S.; Sýkorová, E. Tandem affinity purification of AtTERT reveals putative interaction partners of plant telomerase in vivo. Protoplasma, 2016.
[http://dx.doi.org/10.1007/s00709-016-1042-3]
[152]
Li, W.; Zeng, J.; Li, Q.; Zhao, L.; Liu, T.; Björkholm, M.; Jia, J.; Xu, D. Reptin is required for the transcription of telomerase reverse transcriptase and over-expressed in gastric cancer. Mol. Cancer, 2010, 9
[http://dx.doi.org/10.1186/1476-4598-9-132]
[153]
Darzacq, X.; Kittur, N.; Roy, S.; Shav-Tal, Y.; Singer, R.H.; Meier, U.T. Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J. Cell Biol., 2006, 173(2), 207-218.
[154]
Walbott, H.; Machado-Pinilla, R.; Liger, D.; Blaud, M.; Réty, S.; Grozdanov, P.N.; Godin, K.; van Tilbeurgh, H.; Varani, G.; Meier, U.T.; Leulliot, N. The H/ACA RNP assembly factor SHQ1 functions as an RNA mimic. Genes Dev., 2011, 25(22), 2398-2408.
[155]
Dez, C.; Noaillac-Depeyre, J.; Caizergues-Ferrer, M.; Henry, Y. Naf1p, an essential nucleoplasmic factor specifically required for accumulation of box H/ACA small nucleolar RNPs. Mol. Cell. Biol., 2002, 22(20), 7053-7065.
[156]
Hoareau-Aveilla, C.; Bonoli, M.; Caizergues-Ferrer, M.; Henry, Y. HNaf1 is required for accumulation of human box H/ACA SnoRNPs, ScaRNPs, and telomerase. RNA, 2006, 12(5), 832-840.
[157]
Li, S.; Duan, J.; Li, D.; Ma, S.; Ye, K. Structure of the Shq1-Cbf5-Nop10-Gar1 complex and implications for H/ACA RNP biogenesis and dyskeratosis congenita. EMBO J., 2011, 30, 5010-5020.
[158]
Machado-Pinilla, R.; Liger, D.; Leulliot, N.; Meier, U.T. Mechanism of the AAA+ ATPases pontin and reptin in the biogenesis of H/ACA RNPs. RNA, 2012, 18(10), 1833-1845.
[159]
Ballarino, M.; Morlando, M.; Pagano, F.; Fatica, A.; Bozzoni, I. The cotranscriptional assembly of SnoRNPs controls the biosynthesis of H/ACA SnoRNAs in Saccharomyces Cerevisiae. Mol. Cell. Biol., 2005, 25(13), 5396-5403.
[160]
Stanley, S.E.; Gable, D.L.; Wagner, C.L.; Carlile, T.M.; Hanumanthu, V.S.; Podlevsky, J.D.; Khalil, S.E.; DeZern, A.E.; Rojas-Duran, M.F.; Applegate, C.D.; Alder, J.K.; Parry, E.M.; Gilbert, W.V.; Armanios, M. Loss-of-function mutations in the RNA biogenesis factor NAF1 predispose to pulmonary fibrosis-emphysema. Sci. Transl. Med., 2016, 8(351), 351ra107.
[161]
Tajrishi, M.M.; Tuteja, R.; Tuteja, N. Nucleolin: The most abundant multifunctional phosphoprotein of nucleolus. Commun. Integr. Biol., 2011, 4(3), 267-275.
[162]
Raimer, A.C.; Gray, K.M.; Matera, A.G. SMN - a chaperone for nuclear RNP social occasions? RNA Biol., 2016, 14(6), 701-711.
[163]
Bachand, F.; Boisvert, F-M.; Côté, J.; Richard, S.; Autexier, C. The product of the survival of motor neuron (SMN) gene is a human telomerase-associated protein. Mol. Biol. Cell, 2002, 13(9), 3192-3202.
[164]
Pellizzoni, L.; Baccon, J.; Charroux, B.; Dreyfuss, G. The Survival Of Motor Neurons (SMN) protein interacts with the SnoRNP proteins fibrillarin and GAR1. Curr. Biol., 2001, 11(14), 1079-1088.
[165]
Poole, A.R.; Hebert, M.D. SMN and coilin negatively regulate dyskerin association with telomerase RNA. Biol. Open, 2016, 5(6), 726-735.
[166]
Cheung, D.H-C.; Ho, S-T.; Lau, K-F.; Jin, R.; Wang, Y-N.; Kung, H-F.; Huang, J-J.; Shaw, P-C. Nucleophosmin interacts with PIN2/TERF1-interacting telomerase inhibitor 1 (PinX1) and attenuates the PinX1 inhibition on telomerase activity. Sci. Rep., 2017, 7, 43650.
[167]
Fu, D.; Collins, K.; Hall, B. Distinct biogenesis pathways for human telomerase RNA and H/ACA small nucleolar RNAs. Mol. Cell, 2003, 11(2003), 1361-1372.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy