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Volume 48 Issue 7
Jul.  2021
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Article Contents

Characterization of tree shrew telomeres and telomerase

doi: 10.1016/j.jgg.2021.06.004
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This work was supported by the National Key Research and Development Program of China (2018YFC2000400 and 2020YFA0112300 to C. Chen), National Natural Science Foundation of China (81830087 and 31771516 to C. Chen), project of Innovative Research Team of Yunnan Province (2019HC005), and CAS “light of West China” Program (xbzg-zdsys-201909).

  • Received Date: 2021-03-13
  • Accepted Date: 2021-06-04
  • Rev Recd Date: 2021-05-27
  • Publish Date: 2021-07-20
  • The use of tree shrews as experimental animals for biomedical research is a new practice. Several recent studies suggest that tree shrews are suitable for studying cancers, including breast cancer, glioblastoma, lung cancer, and hepatocellular carcinoma. However, the telomeres and the telomerase of tree shrews have not been studied to date. Here, we characterize telomeres and telomerase in tree shrews. The telomere length of tree shrews is approximately 23 kb, which is longer than that of primates and shorter than that of mice, and it is extended in breast tumor tissues according to Southern blot and flow-fluorescence in situ hybridization (FISH) analyses. Tree shrew spleen, bone marrow, testis, ovary, and uterus show high telomerase activities, which are increased in breast tumor tissues by telomeric repeat amplification protocol assays. The telomere length becomes shorter, and telomerase activity decreases with age. The tree shrew TERT and TERC are more highly similar to primates than to rodents. These findings lay a solid foundation for using tree shrews to study aging and cancers.

  • These authors contributed equally to this work.
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  • Achi, M.V., Ravindranath, N., Dym, M., 2000. Telomere length in male germ cells is inversely correlated with telomerase activity. Biol. Reprod. 63, 591-598.
    Armanios, M., Blackburn, E.H., 2012. The telomere syndromes. Nat. Rev. Genet. 13, 693-704.
    Artandi, S.E., DePinho, R.A., 2000. Mice without telomerase:what can they teach us about human cancer? Nat. Med. 6, 852-855.
    Artandi, S.E., DePinho, R.A., 2010. Telomeres and telomerase in cancer. Carcinogenesis 31, 9-18.
    Balistreri, C.R., Colonna-Romano, G., Lio, D., Candore, G., Caruso, C., 2009. TLR4 polymorphisms and ageing:implications for the pathophysiology of age-related diseases. J. Clin. Immunol. 29, 406-415.
    Beier, F., Balabanov, S., Buckley, T., Dietz, K., Hartmann, U., Rojewski, M., Kanz, L., Schrezenmeier, H., Brümmendorf, T.H., 2005. Accelerated telomere shortening in glycosylphosphatidylinositol (GPI)-negative compared with GPI-positive granulocytes from patients with paroxysmal nocturnal hemoglobinuria (PNH) detected by proaerolysin flow-FISH. Blood 106, 531-533.
    Blasco, M.A., 2005. Telomeres and human disease:ageing, cancer and beyond. Nat. Rev. Genet. 6, 611-622.
    Calado, R.T., Dumitriu, B., 2013. Telomere dynamics in mice and humans. Semin. Hematol. 50, 165-174.
    Cesare, A.J., Reddel, R.R., 2010. Alternative lengthening of telomeres:models, mechanisms and implications. Nat. Rev. Genet. 11, 319-330.
    Chang, S., Khoo, C.M., Naylor, M.L., Maser, R.S., DePinho, R.A., 2003. Telomerebased crisis:functional differences between telomerase activation and ALT in tumor progression. Genes Dev. 17, 88-100.
    Davis, T., Kipling, D., 2005. Telomeres and telomerase biology in vertebrates:progress towards a non-human model for replicative senescence and ageing. Biogerontology 6, 371-385.
    de Magalhães, J.P., 2013. How ageing processes influence cancer. Nat. Rev. Cancer 13, 357-365.
    Dunham, M.A., Neumann, A.A., Fasching, C.L., Reddel, R.R., 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26, 447-450.
    Eisenberg, D.T., Tackney, J., Cawthon, R.M., Cloutier, C.T., Hawkes, K., 2017. Paternal and grandpaternal ages at conception and descendant telomere lengths in chimpanzees and humans. Am. J. Phys. Anthropol. 162, 201-207.
    Eisenhauer, K.M., Gerstein, R.M., Chiu, C.P., Conti, M., Hsueh, A.J., 1997. Telomerase activity in female and male rat germ cells undergoing meiosis and in early embryos. Biol. Reprod. 56, 1120-1125.
    Fan, Y., Huang, Z.Y., Cao, C.C., Chen, C.-S., Chen, Y.-X., Fan, D.-D., He, J., Hou, H.-L., Hu, L., Hu, X.-T., Jiang, X.-T., Lai, R., Lang, Y.-S., et al., 2013. Genome of the Chinese tree shrew. Nat. Commun. 4, 1426.
    Fedriga, R., Gunelli, R., Nanni, O., Amadori, D., Calistri, D., 2001. Telomerase activity detected by quantitative assay in bladder carcinoma and exfoliated cells in urine. Neoplasia 3, 446-450.
    Flores, I., Blasco, M.A., 2010. The role of telomeres and telomerase in stem cell aging. FEBS Lett. 584, 3826-3830.
    Fradiani, P.A., Ascenzioni, F., Lavitrano, M., Donini, P., 2004. Telomeres and telomerase activity in pig tissues. Biochimie 86, 7-12.
    Galati, A., Micheli, E., Cacchione, S., 2013. Chromatin structure in telomere dynamics. Front. Oncol. 3, 46.
    Gallardo, F., Laterreur, N., Cusanelli, E., Ouenzar, F., Querido, E., Wellinger, R.J., Chartrand, P., 2011. Live cell imaging of telomerase RNA dynamics reveals cell cycle-dependent clustering of telomerase at elongating telomeres. Mol. Cell. 44, 819-827.
    Gardner, J.P., Kimura, M., Chai, W., Durrani, J.F., Tchakmakjian, L., Cao, X., Lu, X., Li, G., Peppas, A.P., Skurnick, J., et al., 2007. Telomere dynamics in macaques and humans. J. Gerontol. A. Biol. Sci. Med. Sci. 62, 367-374.
    Ge, G.Z., Xia, H.J., He, B.L., Zhang, H.-L., Liu, W.-J., Shao, M., Wang, C.-Y., Xiao, J., Ge, F., Li, F.-B., et al., 2016. Generation and characterization of a breast carcinoma model by PyMT overexpression in mammary epithelial cells of tree shrew, an animal close to primates in evolution. Int. J. Cancer 138, 642-651.
    Ghareghomi, S., Ahmadian, S., Zarghami, N., Kahroba, H., 2021. Fundamental insights into the interaction between telomerase/TERT and intracellular signaling pathways. Biochimie 181, 12-24.
    Gomes, N.M., Ryder, O.A., Houck, M.L., Charter, S.J., Walker, W., Forsyth, N.R., Austad, S.N., Venditti, C., Pagel, M., Shay, J.W., et al., 2011. Comparative biology of mammalian telomeres:hypotheses on ancestral states and the roles of telomeres in longevity determination. Aging Cell 10, 761-768.
    Gomez, D.E., Armando, R.G., Farina, H.G., Menna, P.L., Cerrudo, C.S., Ghiringhelli, P.D., Alonso, D.F., 2012. Telomere structure and telomerase in health and disease (review). Int. J. Oncol. 41, 1561-1569.
    Henson, J.D., Neumann, A.A., Yeager, T.R., Reddel, R.R., 2002. Alternative lengthening of telomeres in mammalian cells. Oncogene 21, 598-610.
    Jobling, A.I., Wan, R., Gentle, A., Bui, B.V., McBrien, N.A., 2009. Retinal and choroidal TGF-b in the tree shrew model of myopia:isoform expression, activation and effects on function. Exp. Eye Res. 88, 458-466.
    Kakuo, S., Asaoka, K., Ide, T., 1999. Human is a unique species among primates in terms of telomere length. Biochem. Biophys. Res. Commun. 263, 308-314.
    Kazemi Noureini, S., Fatemi, L., Wink, M., 2018. Telomere shortening in breast cancer cells (MCF7) under treatment with low doses of the benzylisoquinoline alkaloid chelidonine. PLoS One 13, e0204901.
    Kido, A., Tsujiuchi, T., Morishita, T., Tsutsumi, M., Takahama, M., Miyauchi, Y., Mii, Y., Tamai, S., Konishi, Y., 1998. Telomerase activity correlates with growth of transplantable osteosarcomas in rats treated with cis-diammine dichloroplatinum or the angiogenesis inhibitor AGM-1470. Jpn. J. Cancer Res. 89, 1074-1081.
    Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
    Le Gall, J.Y., Ardaillou, R., 2009. The biology of aging. Bull Acad. Natl. Med. 193, 365-402.
    Lee, W.W., Nam, K.H., Terao, K., Yoshikawa, Y., 2002. Age-related telomere length dynamics in peripheral blood mononuclear cells of healthy cynomolgus monkeys measured by Flow FISH. Immunology 105, 458-465.
    Lewinska, A., Adamczyk-Grochala, J., Kwasniewicz, E., Wnuk, M., 2017. Downregulation of methyltransferase Dnmt2 results in condition-dependent telomere shortening and senescence or apoptosis in mouse fibroblasts. J. Cell. Physiol. 232, 3714-3726.
    Li, Y., Su, J.J., Qin, L.L., Yang, C., Luo, D., Ban, K.-C., Kensler, T.W., Roebuck, B.D., 2000. Chemopreventive effect of oltipraz on AFB(1)-induced hepatocarcinogenesis in tree shrew model. World J. Gastroenterol. 6, 647-650.
    Lingner, J., Hughes, T.R., Shevchenko, A., Mann, M., Lundblad, V., Cech, T.R., 1997. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561-567.
    Londoño-Vallejo, J.A., Der-Sarkissian, H., Cazes, L., Bacchetti, S., Reddel, R.R., 2004. Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res. 64, 2324-2327.
    Mender, I., Shay, J.W., 2015. Telomere restriction fragment (TRF) analysis. Bio. Protoc. 5, e1658.
    Moyzis, Robert, K., 1991. The human telomere. Sci. Am. 265, 48-55.
    Murnane, J.P., 2012. Telomere dysfunction and chromosome instability. Mutat. Res. 730, 28-36.
    Pai, R.B., Pai, S.B., Yang, L., Joshi, H.C., 2010. Abundance of a distinct cluster of telomere t-stumps in advanced breast cancer cell line. Oncol. Lett. 1, 339-343.
    Peek, G.W., Tollefsbol, T.O., 2016. Down-regulation of hTERT and Cyclin D1 transcription via PI3K/Akt and TGF-β pathways in MCF-7 cancer cells with PX-866 and raloxifene. Exp. Cell Res. 344, 95-102.
    Pickett, H.A., Henson, J.D., Au, A.Y., Neumann, A.A., Reddel, R.R., 2011. Normal mammalian cells negatively regulate telomere length by telomere trimming. Hum. Mol. Genet. 20, 4684-4692.
    Pinto, T.N.C., Fernandes, J.R., Arruda, L.B., Duarte, A.J.,S., Benard, G., 2021. Costeffective trap qPCR approach to evaluate telomerase activity:an important tool for aging, cancer, and chronic disease research. Clinics (Sao Paulo) 76, e2432.
    Prowse, K.R., Greider, C.W., 1995. Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proc. Natl. Acad. Sci. U. S. A. 92, 4818-4822.
    Ravindranath, N., Dalal, R., Solomon, B., Djakiew, D., Dym, M., 1997. Loss of telomerase activity during male germ cell differentiation. Endocrinology 138, 4026-4029.
    Sanchini, M.A., Bravaccini, S., Medri, L., Gunelli, R., Nanni, O., Monti, F., Baccarani, P.C., Ravaioli, A., Bercovich, E., Amadori, et al., 2004. Urine telomerase:an important marker in the diagnosis of bladder cancer. Neoplasia 6, 234-239.
    Schmelting, B., Corbach-Söhle, S., Kohlhause, S., Schlumbohm, C., Flügge, G., Fuchs, E., 2014. Agomelatine in the tree shrew model of depression:effects on stress-induced nocturnal hyperthermia and hormonal status. Eur. Neuropsychopharmacol 24, 437-447.
    Schneper, L.M., Brooks-Gunn, J., Notterman, D.A., Suomi, S.J., 2016. Early-life experiences and telomere length in adult rhesus monkeys:an exploratory study. Psychosom. Med. 78, 1066-1071.
    Schrader, A., Crispatzu, G., Oberbeck, S., Mayer, P., Pützer, S., von Jan, J., Vasyutina, E., Warner, K., Weit, N., Pflug, N., et al., 2018. Actionable perturbations of damage responses by TCL1/ATM and epigenetic lesions form the basis of T-PLL. Nat. Commun. 9, 697.
    Shay, J.W., Bacchetti, S., 1997. A survey of telomerase activity in human cancer. Eur. J. Cancer. 33, 787-791.
    Smith, E.M., Pendlebury, D.F., Nandakumar, J., 2020. Structural biology of telomeres and telomerase. Cell. Mol. Life Sci. 77, 61-79.
    Steinert, S., White, D.M., Zou, Y., Shay, J.W., Wright, W.E., 2002. Telomere biology and cellular aging in nonhuman primate cells. Exp. Cell Res. 272, 146-152.
    Takubo, K., Izumiyama-Shimomura, N., Honma, N., Sawabe, M., Arai, T., Kato, M., Oshimura, M., Nakamura, K.-I., 2002. Telomere lengths are characteristic in each human individual. Exp. Gerontol. 37, 523-531.
    Tsujiuchi, T., Tsutsumi, M., Kido, A., Kobitsu, K., Takahama, M., Majima, T., Denda, A., Nakae, D., Konishi, Y., 1996. Increased telomerase activity in hyperplastic nodules and hepatocellular carcinomas induced by a choline-deficient Lamino acid-defined diet in rats. Jpn. J. Cancer Res. 87, 1111-1115.
    Vinagre, J., Almeida, A., Pópulo, H., Batista, R., Lyra, J., Pinto, V., Coelho, R., Celestino, R., Prazeres, H., Lima, L., et al., 2013. Frequency of TERT promoter mutations in human cancers. Nat. Commun. 4, 2185.
    Wang, Y., 1987. Taxonomic research on Burma-Chinese tree shrew, Tupaia belangeri(Wagner), from Southern China. Zool. Res. 8, 213-230.
    Werner, B., Beier, F., Hummel, S., Balabanov, S., Lassay, L., Orlikowsky, T., Dingli, D., Brümmendorf, T.H., Traulsen, A., 2015. Reconstructing the in vivo dynamics of hematopoietic stem cells from telomere length distributions. Elife 4, e08687.
    Wright, W.E., Shay, J.W., Piatyszek, M.A., 1995. Modifications of a telomeric repeat amplification protocol (TRAP) result in increased reliability, linearity and sensitivity. Nucleic Acids Res. 23, 3794-3795.
    Xia, H.J., He, B.L., Wang, C.Y., Zhang, H.-L., Ge, G.-Z., Zhang, Y.-X., Lv, L.-B., Jiao, J.-L., Chen, C., 2014. PTEN/PIK3CA genes are frequently mutated in spontaneous and medroxyprogesterone acetate-accelerated 7,12-dimethylbenz(a)anthracene-induced mammary tumours of tree shrews. Eur. J. Cancer 50, 3230-3242.
    Xia, H.J., Wang, C.Y., Zhang, H.L., Zhang, H.-L., Jiang, D., Luo, Y., Liu, R., Chen, C., 2012. Characterization of spontaneous breast tumor in tree shrews (Tupaia belangeri chinenesis). Zool. Res. 33, 55-59.
    Xiao, J., Liu, R., Chen, C.S., 2017. Tree shrew (Tupaia belangeri) as a novel laboratory disease animal model. Zool. Res. 38, 127-137.
    Yang, C., Ruan, P., Ou, C., Su, J., Cao, J., Luo, C., Tang, Y., Wang, Q., Qin, H., Sun, W., et al., 2015. Chronic hepatitis B virus infection and occurrence of hepatocellular carcinoma in tree shrews (Tupaia belangeri chinensis). Virol. J. 12, 26.
    Zhang, J., Yang, B., Wen, X., Sun, G., 2018. Genetic variation and relationships in the mitochondrial DNA D-loop region of Qinghai indigenous and commercial pig breeds. Cell. Mol. Biol. Lett. 23, 31.
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