Telomere length and Wnt/β-catenin pathway in adamantinomatous craniopharyngiomas

in European Journal of Endocrinology
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  • 1 Department of Internal Medicine of Ribeirao Preto Medical School, University of Sao Paulo, Ribeirao Preto, Sao Paulo, Brazil
  • | 2 Department of Pediatrics of Ribeirao Preto Medical School, University of Sao Paulo, Ribeirao Preto, Sao Paulo, Brazil
  • | 3 Neuroendocrinology Research Center/Endocrinology Section, Medical School and Hospital Universitário Clementino Fraga Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
  • | 4 Institute of Neuroscience of Castilla y León, University of Salamanca, Salamanca, Spain
  • | 5 Department of Surgery and Anatomy of Ribeirao Preto Medical School, Hematology and Oncology of Ribeirao Preto Medical School, University of Sao Paulo, Ribeirao Preto, Sao Paulo, Brazil
  • | 6 Department of Medical Imaging, Hematology and Oncology of Ribeirao Preto Medical School, University of Sao Paulo, Ribeirao Preto, Sao Paulo, Brazil

Correspondence should be addressed to M de Castro; Email: castrom@fmrp.usp.br

*(J I S Mota and R M P Silva-Júnior contributed equally to this work)

(R M P Silva-Júnior is now at Institute of Neuroscience of Castilla y León, University of Salamanca, Salamanca, Spain)

(C S Martins is now at Faculty of Medicine, Federal University of Mato Grosso do Sul, Campo Grande, Brazil)

§(J G O Ozaki is now at Sonimed Medicina Diagnóstica, Campo Grande, Brazil)

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Objectives

To evaluate how telomere length behaves in adamantinomtous craniopharyngioma (aCP) and if it contributes to the pathogenesis of aCPs with and without CTNNB1 mutations.

Design

Retrospective cross-sectional study enrolling 42 aCP patients from 2 tertiary institutions.

Methods

Clinicopathological features were retrieved from the patient’s charts. Fresh frozen tumors were used for RNA and DNA analyses. Telomere length was evaluated by qPCR (T/S ratio). Somatic mutations in TERT promoter (TERTp) and CTNNB1 were detected by Sanger and/or whole-exome sequencing. We performed RNA-Seq to identify differentially expressed genes in aCPs presenting with shorter or longer telomere lengths.

Results

Mutations in CTNNB1 were detected in 29 (69%) tumors. There was higher frequency of CTNNB1 mutations in aCPs from patients diagnosed under the age of 15 years (85% vs 15%; P = 0.04) and a trend to recurrent disease (76% vs 24%; P = 0.1). No mutation was detected in the TERTp region. The telomeres were shorter in CTNNB1-mutated aCPs (0.441, IQR: 0.297–0.597vs 0.607, IQR: 0.445–0.778; P = 0.04), but it was neither associated with clinicopathological features nor with recurrence. RNAseq identified a total of 387 differentially expressed genes, generating two clusters, being one enriched for short telomeres and CTNNB1-mutated aCPs.

Conclusions: CTNNB1

mutations are more frequent in children and adolescents and appear to associate with progressive disease. CTNNB1-mutated aCPs have shorter telomeres, demonstrating a relationship between the Wnt/β-catenin pathway and telomere biology in the pathogenesis of aCPs.

 

     European Society of Endocrinology

Sept 2018 onwards Past Year Past 30 Days
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Full Text Views 12 12 12
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  • 1

    Bunin GR, Surawicz TS, Witman PA, Preston-Martin S, Davis F, Bruner JM. The descriptive epidemiology of craniopharyngioma. Journal of Neurosurgery 1998 89 547551. (https://doi.org/10.3171/jns.1998.89.4.0547)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Karavitaki N, Cudlip S, Adams CB, Wass JA. Craniopharyngiomas. Endocrine Reviews 2006 27 371397. (https://doi.org/10.1210/er.2006-0002)

  • 3

    Karavitaki N, Wass JA. Non-adenomatous pituitary tumours. Best Practice and Research: Clinical Endocrinology and Metabolism 2009 23 651665. (https://doi.org/10.1016/j.beem.2009.05.007)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Prabhu VC, Brown HG. The pathogenesis of craniopharyngiomas. Child’s Nervous System 2005 21 622627. (https://doi.org/10.1007/s00381-005-1190-9)

  • 5

    Sekine S, Takata T, Shibata T, Mori M, Morishita Y, Noguchi M, Uchida T, Kanai Y, Hirohashi S. Expression of enamel proteins and LEF1 in adamantinomatous craniopharyngioma: evidence for its odontogenic epithelial differentiation. Histopathology 2004 45 573579. (https://doi.org/10.1111/j.1365-2559.2004.02029.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Gaston-Massuet C, Andoniadou CL, Signore M, Jayakody SA, Charolidi N, Kyeyune R, Vernay B, Jacques TS, Taketo MM & Le Tissier P et al.Increased wingless (Wnt) signaling in pituitary progenitor/stem cells gives rise to pituitary tumors in mice and humans. PNAS 2011 108 1148211487. (https://doi.org/10.1073/pnas.1101553108)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Zhan T, Rindtorff N, Boutros M. Wnt signaling in cancer. Oncogene 2017 36 14611473. (https://doi.org/10.1038/onc.2016.304)

  • 8

    Sekine S, Shibata T, Kokubu A, Morishita Y, Noguchi M, Nakanishi Y, Sakamoto M, Hirohashi S. Craniopharyngiomas of adamantinomatous type harbor-catenin gene mutations. American Journal of Pathology 2002 161 19972001. (https://doi.org/10.1016/s0002-9440(1064477-x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Buslei R, Nolde M, Hofmann B, Meissner S, Eyupoglu IY, Siebzehnrübl F, Hahnen E, Kreutzer J, Fahlbusch R. Common mutations of beta-catenin in adamantinomatous craniopharyngiomas but not in other tumours originating from the sellar region. Acta Neuropathologica 2005 109 589597. (https://doi.org/10.1007/s00401-005-1004-x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Campanini ML, Colli LM, Paixao BM, Cabral TP, Amaral FC, Machado HR, Neder LS, Saggioro F, Moreira AC & Antonini SR et al.CTNNB1 gene mutations, pituitary transcription factors, and microRNA expression involvement in the pathogenesis of adamantinomatous craniopharyngiomas. Hormones and Cancer 2010 1 187196. (https://doi.org/10.1007/s12672-010-0041-7)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Hölsken A, Sill M, Merkle J, Schweizer L, Buchfelder M, Flitsch J, Fahlbusch R, Metzler M, Kool M & Pfister SM et al.Adamantinomatous and papillary craniopharyngiomas are characterized by distinct epigenomic as well as mutational and transcriptomic profiles. Acta Neuropathologica Communications 2016 29 420. (https://doi.org/10.1186/s40478-016-0287-6)

    • Search Google Scholar
    • Export Citation
  • 12

    Brastianos PK, Taylor-Weiner A, Manley PE, Jones RT, Dias-Santagata D, Thorner AR, Lawrence MS, Rodriguez FJ, Bernardo LA & Schubert L et al.Exome sequencing identifies BRAF mutations in papillary craniopharyngiomas. Nature Genetics 2014 46 161165. (https://doi.org/10.1038/ng.2868)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Colli LM, Saggioro F, Serafini LN, Camargo RC, Machado HR, Moreira AC, Antonini SR, de Castro M. Components of the canonical and non-canonical Wnt pathways are not mis-expressed in pituitary tumors. PLoS ONE 2013 26 e62424. (https://doi.org/10.1371/journal.pone.0062424)

    • Search Google Scholar
    • Export Citation
  • 14

    Li Z, Xu J, Huang S, You C. Aberrant membranous expression of β-catenin predicts poor prognosis in patients with craniopharyngioma. Annals of Diagnostic Pathology 2015 19 403408. (https://doi.org/10.1016/j.anndiagpath.2015.10.002)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Jucá CEB, Colli LM, Martins CS, Campanini ML, Paixão B, Jucá RV, Saggioro FP, de Oliveira RS, Moreira AC & Machado HR et al.Impact of the canonical Wnt pathway activation on the pathogenesis and prognosis of adamantinomatous craniopharyngiomas. Hormone and Metabolic Research 2018 50 575581. (https://doi.org/10.1055/a-0593-5956)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Andoniadou CL, Gaston-Massuet C, Reddy R, Schneider RP, Blasco MA, Le Tissier P, Jacques TS, Pevny LH, Dattani MT, Martinez-Barbera JP. Identification of novel pathways involved in the pathogenesis of human adamantinomatous craniopharyngioma. Acta Neuropathologica 2012 124 259271. (https://doi.org/10.1007/s00401-012-0957-9)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Martinez-Barbera JP 60 Years of Neuroendocrinology: Biology of human craniopharyngioma: lessons from mouse models. Journal of Endocrinology 2015 226 T161T172. (https://doi.org/10.1530/JOE-15-0145)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Gomes DC, Jamra SA, Leal LF, Colli LM, Campanini ML, Oliveira RS, Martinelli Jr CE, Elias PC, Moreira AC & Machado HR et al.Sonic Hedgehog pathway is upregulated in adamantinomatous craniopharyngiomas. European Journal of Endocrinology 2015 172 603608. (https://doi.org/10.1530/EJE-14-0934)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Apps JR, Carreno G, Gonzalez-Meljem JM, Haston S, Guiho R, Cooper JE, Manshaei S, Jani N, Hölsken A & Pettorini B et al.Tumour compartment transcriptomics demonstrates the activation of inflammatory and odontogenic programmes in human adamantinomatous craniopharyngioma and identifies the MAPK/ERK pathway as a novel therapeutic target. Acta Neuropathologica 2018 135 757777. (https://doi.org/10.1007/s00401-018-1830-2)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Carreno G, Boult JKR, Apps J, Gonzalez-Meljem JM, Haston S, Guiho R, Stache C, Danielson LS, Koers A & Smith LM et al.SHH pathway inhibition is protumourigenic in adamantinomatous craniopharyngioma. Endocrine-Related Cancer 2019 26 355366. (https://doi.org/10.1530/ERC-18-0538)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, Allshire RC. Telomere reduction in human colorectal carcinoma and with ageing. Nature 1990 346 866868. (https://doi.org/10.1038/346866a0)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Wyatt HD, West SC, Beattie TL. InTERTpreting telomerase structure and function. Nucleic Acids Research 2010 38 56095622. (https://doi.org/10.1093/nar/gkq370)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Fu D, Collins K. Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation. Molecular Cell 2007 28 773785. (https://doi.org/10.1016/j.molcel.2007.09.023)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Vinagre J, Almeida A, Pópulo H, Batista R, Lyra J, Pinto V, Coelho R, Celestino R, Prazeres H & Lima L et al.Frequency of tert promoter mutations in human cancers. Nature Communications 2013 4 2185. (https://doi.org/10.1038/ncomms3185)

    • Search Google Scholar
    • Export Citation
  • 25

    Lee SE, Chang SH, Kim WY, Lim SD, Kim WS, Hwang TS, Han HS. Frequent somatic tert promoter mutations and CTNNB1 mutations in hepatocellular carcinoma. Oncotarget 2016 7 6926769275. (https://doi.org/10.18632/oncotarget.12121)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Juratli TA, Thiede C, Koerner MVA, Tummala SS, Daubner D, Shankar GM, Williams EA, Martinez-Lage M, Soucek S & Robel K et al.Intratumoral heterogeneity and tert promoter mutations in progressive/higher-grade meningiomas. Oncotarget 2017 8 109228109237. (https://doi.org/10.18632/oncotarget.22650)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Macerola E, Loggini B, Giannini R, Garavello G, Giordano M, Proietti A, Niccoli C, Basolo F, Fontanini G. Coexistence of tert promoter and BRAF mutations in cutaneous melanoma is associated with more clinicopathological features of aggressiveness. Virchows Archiv 2015 467 177184. (https://doi.org/10.1007/s00428-015-1784-x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Melo M, da Rocha AG, Vinagre J, Batista R, Peixoto J, Tavares C, Celestino R, Almeida A, Salgado C & Eloy C et al.Tert promoter mutations are a major indicator of poor outcome in differentiated thyroid carcinomas. Journal of Clinical Endocrinology and Metabolism 2014 99 E754E765. (https://doi.org/10.1210/jc.2013-3734)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Rusinek D, Pfeifer A, Krajewska J, Oczko-Wojciechowska M, Handkiewicz-Junak D, Pawlaczek A, Zebracka-Gala J, Kowalska M, Cyplinska R & Zembala-Nozynska E et al.Coexistence of tert promoter mutations and the BRAF V600E alteration and its impact on histopathological features of papillary thyroid carcinoma in a selected series of polish patients. International Journal of Molecular Sciences 2018 19 2647. (https://doi.org/10.3390/ijms19092647)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Shi X, Liu R, Qu S, Zhu G, Bishop J, Liu X, Sun H, Shan Z, Wang E & Luo Y et al.Association of tert promoter mutation 1,295,228 C>T with BRAF V600E mutation, older patient age, and distant metastasis in anaplastic thyroid cancer. Journal of Clinical Endocrinology and Metabolism 2015 100 E632E637. (https://doi.org/10.1210/jc.2014-3606)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Martins CS, de Castro M, Calado RT. Absence of tert promoter mutations in pituitary adenomas. Journal of Endocrinological Investigation 2016 39 933934. (https://doi.org/10.1007/s40618-016-0479-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Barthel FP, Wei W, Tang M, Martinez-Ledesma E, Hu X, Amin SB, Akdemir KC, Seth S, Song X & Wang Q et al.Systematic analysis of telomere length and somatic alterations in 31 cancer types. Nature Genetics 2017 49 349357. (https://doi.org/10.1038/ng.3781)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Castelo-Branco P, Choufani S, Mack S, Gallagher D, Zhang C, Lipman T, Zhukova N, Walker EJ, Martin D & Merino D et al.Methylation of the tert promoter and risk stratification of childhood brain tumours: an integrative genomic and molecular study. Lancet: Oncology 2013 14 534542. (https://doi.org/10.1016/S1470-2045(1370110-4)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34

    Miyake Y, Adachi JI, Suzuki T, Mishima K, Araki R, Mizuno R, Nishikawa R. Tert promoter methylation is significantly associated with tert upregulation and disease progression in pituitary adenomas. Journal of Neuro-Oncology 2019 141 131138. (https://doi.org/10.1007/s11060-018-03016-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35

    Higham CE, Johannsson G, Shalet SM. Hypopituitarism. Lancet 2016 12 24032415. (https://doi.org/10.1016/S0140-6736(1630053-8)

  • 36

    Conde WL, Monteiro CA. Body mass index cutoff points for evaluation of nutritional status in Brazilian children and adolescents. Jornal de Pediatria 2006 82 266272. (https://doi.org/10.2223/JPED.1502)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37

    Øystese KAB, Hisanawi S, Zucknick M, Bollerslev J, Ringstad G. Are volume measurements of non-functioning pituitary adenomas reliable? Endocrine 2019 63 171176. (https://doi.org/10.1007/s12020-018-1752-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38

    Puget S, Garnett M, Wray A, Grill J, Habrand JL, Bodaert N, Zerah M, Bezerra M, Renier D & Pierre-Kahn A et al.Pediatric craniopharyngiomas: classification and treatment according to the degree of hypothalamic involvement. Journal of Neurosurgery 2007 106 (1Supplement) 312. (https://doi.org/10.3171/ped.2007.106.1.3)

    • Search Google Scholar
    • Export Citation
  • 39

    Gutierrez-Rodrigues F, Santana-Lemos BA, Scheucher PS, Alves-Paiva RM, Calado RT. Direct comparison of flow-FISH and qPCR as diagnostic tests for telomere length measurement in humans. PLoS ONE 2014 19 e113747. (https://doi.org/10.1371/journal.pone.0113747)

    • Search Google Scholar
    • Export Citation
  • 40

    Martins CS, Santana-Lemos BA, Saggioro FP, Neder L, Machado HR, Moreira AC, Calado RT, de Castro M. Telomere length and telomerase expression in pituitary tumors. Journal of Endocrinological Investigation 2015 38 12431246. (https://doi.org/10.1007/s40618-015-0298-3)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41

    Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 2014 15 550. (https://doi.org/10.1186/s13059-014-0550-8)

    • Search Google Scholar
    • Export Citation
  • 42

    Anders S, Pyl PT, Huber W. Seq – a Python framework to work with high-throughput sequencing data. Bioinformatics 2015 31 166169. (https://doi.org/10.1093/bioinformatics/btu638)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43

    Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Research 2005 33 W741W748. (https://doi.org/10.1093/nar/gki475)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44

    Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR, Ma’ayan A. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 2013 14 128. (https://doi.org/10.1186/1471-2105-14-128)

    • Search Google Scholar
    • Export Citation
  • 45

    Karavitaki N, Brufani C, Warner JT, Adams CB, Richards P, Ansorge O, Shine B, Turner HE, Wass JA. Craniopharyngiomas in children and adults: systematic analysis of 121 cases with long-term follow-up. Clinical Endocrinology 2005 62 397409. (https://doi.org/10.1111/j.1365-2265.2005.02231.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46

    Müller HL Craniopharyngioma. Endocrine Reviews 2014 35 513543. (https://doi.org/10.1210/er.2013-1115)

  • 47

    Müller HL, Merchant TE, Puget S, Martinez-Barbera JP. New outlook on the diagnosis, treatment and follow-up of childhood-onset craniopharyngioma. Nature Reviews: Endocrinology 2017 13 299312. (https://doi.org/10.1038/nrendo.2016.217)

    • Search Google Scholar
    • Export Citation
  • 48

    Momin AA, Recinos MA, Cioffi G, Patil N, Soni P, Almeida JP, Kruchko C, Barnholtz-Sloan JS, Recinos PF, Kshettry VR. Descriptive epidemiology of craniopharyngiomas in the United States. Pituitary 2021 24 517522. (https://doi.org/10.1007/s11102-021-01127-6)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49

    Barbosa AP, Varela A, Carvalho D, Cerejo A, Pereira J, Castro L, Vinha E, Monteiro M, Cruz J & Vaz R et al.Craniopharyngiomas. Clinicopathological aspects in different age groups. Acta Médica Portuguesa 2002 15 123129.

    • Search Google Scholar
    • Export Citation
  • 50

    Nogueira MC, Berbel Júnior AS, Koenigkam-Santos M, Moreira AC, Nonino CB, de Castro M. Nutritional and endocrinologic evaluation of patients with craniopharyngioma. Clinical Nutrition ESPEN 2015 10 e213e218. (https://doi.org/10.1016/j.clnesp.2015.06.001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 51

    Wijnen M, Olsson DS, van den Heuvel-Eibrink MM, Hammarstrand C, Janssen JAMJL, van der Lely AJ, Johannsson G, Neggers SJCMM. Excess morbidity and mortality in patients with craniopharyngioma: a hospital-based retrospective cohort study. European Journal of Endocrinology 2018 178 93102. (https://doi.org/10.1530/EJE-17-0707)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 52

    Sterkenburg AS, Hoffmann A, Gebhardt U, Warmuth-Metz M, Daubenbüchel AM, Müller HL. Survival, hypothalamic obesity, and neuropsychological/psychosocial status after childhood-onset craniopharyngioma: newly reported long-term outcomes. Neuro-Oncology 2015 17 10291038. (https://doi.org/10.1093/neuonc/nov044)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 53

    Müller HL The diagnosis and treatment of craniopharyngioma. Neuroendocrinology 2020 110 753766. (https://doi.org/10.1159/000504512)

  • 54

    Otte A, Müller HL. Childhood-onset craniopharyngioma. Journal of Clinical Endocrinology and Metabolism 2021 106 e3820–e3836. (https://doi.org/10.1210/clinem/dgab397)

    • Search Google Scholar
    • Export Citation
  • 55

    Brastianos PK, Santagata S. ENDOCRINE TUMORS: BRAF V600E mutations in papillary craniopharyngioma. European Journal of Endocrinology 2016 174 R139R144. (https://doi.org/10.1530/EJE-15-0957)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 56

    Kato K, Nakatani Y, Kanno H, Inayama Y, Ijiri R, Nagahara N, Miyake T, Tanaka M, Ito Y & Aida N et al.Possible linkage between specific histological structures and aberrant reactivation of the Wnt pathway in adamantinomatous craniopharyngioma. Journal of Pathology 2004 203 814821. (https://doi.org/10.1002/path.1562)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 57

    Apps JR, Martinez-Barbera JP. Molecular pathology of adamantinomatous craniopharyngioma: review and opportunities for practice. Neurosurgical Focus 2016 41 E4. (https://doi.org/10.3171/2016.8.FOCUS16307)

    • Search Google Scholar
    • Export Citation
  • 58

    Hara T, Akutsu H, Takano S, Kino H, Ishikawa E, Tanaka S, Miyamoto H, Sakamoto N, Hattori K & Sakata-Yanagimoto M et al.Clinical and biological significance of adamantinomatous craniopharyngioma with CTNNB1 mutation. Journal of Neurosurgery 2018 131 217226. (https://doi.org/10.3171/2018.3.JNS172528)

    • Search Google Scholar
    • Export Citation
  • 59

    Fujio S, Juratli TA, Takajo T, Arita K, Nagano Y, Yoshimoto K, Nayyar N, Curry Jr WT, Martinez-Lage M & Cahill DP et al.Craniopharyngiomas, including recurrent cases, lack tert promoter hotspot mutations. Neurologia Medico-Chirurgica 2021 61 385391. (https://doi.org/10.2176/nmc.rc.2020-0339)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 60

    Gardner M, Bann D, Wiley L, Cooper R, Hardy R, Nitsch D, Martin-Ruiz C, Shiels P, Sayer AA & Barbieri M et al.Gender and telomere length: systematic review and meta-analysis. Experimental Gerontology 2014 51 1527. (https://doi.org/10.1016/j.exger.2013.12.004)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 61

    Lex K, Maia Gil M, Lopes-Bastos B, Figueira M, Marzullo M, Giannetti K, Carvalho T, Ferreira MG. Telomere shortening produces an inflammatory environment that increases tumor incidence in zebrafish. PNAS 2020 117 1506615074. (https://doi.org/10.1073/pnas.1920049117)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 62

    Gonzalez-Meljem JM, Haston S, Carreno G, Apps JR, Pozzi S, Stache C, Kaushal G, Virasami A, Panousopoulos L & Mousavy-Gharavy SN et al.Stem cell senescence drives age-attenuated induction of pituitary tumours in mouse models of paediatric craniopharyngioma. Nature Communications 2017 8 1819. (https://doi.org/10.1038/s41467-017-01992-5)

    • Search Google Scholar
    • Export Citation
  • 63

    Zhang Y, Toh L, Lau P, Wang X. Human telomerase reverse transcriptase (hTERT) is a novel target of the Wnt/β-catenin pathway in human cancer. Journal of Biological Chemistry 2012 287 3249432511. (https://doi.org/10.1074/jbc.M112.368282)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 64

    Behrooz AB, Syahir A. Could we address the interplay between CD133, Wnt/β-catenin, and tert signaling pathways as a potential target for glioblastoma therapy? Frontiers in Oncology 2021 11 642719. (https://doi.org/10.3389/fonc.2021.642719)

    • Search Google Scholar
    • Export Citation
  • 65

    Tefferi A, Lasho TL, Begna KH, Patnaik MM, Zblewski DL, Finke CM, Laborde RR, Wassie E, Schimek L & Hanson CA et al.A pilot study of the telomerase inhibitor imetelstat for myelofibrosis. New England Journal of Medicine 2015 373 908919. (https://doi.org/10.1056/NEJMoa1310523)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 66

    Sugarman ET, Zhang G, Shay JW. In perspective: an update on telomere targeting in cancer. Molecular Carcinogenesis 2019 58 15811588. (https://doi.org/10.1002/mc.23035)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 67

    Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, Charlat O, Wiellette E, Zhang Y & Wiessner S et al.Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009 461 614620. (https://doi.org/10.1038/nature08356)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 68

    Mashima T, Taneda Y, Jang MK, Mizutani A, Muramatsu Y, Yoshida H, Sato A, Tanaka N, Sugimoto Y, Seimiya H. MTOR signaling mediates resistance to tankyrase inhibitors in Wnt-driven colorectal cancer. Oncotarget 2017 8 4790247915. (https://doi.org/10.18632/oncotarget.18146)

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