Ribosomal proteins induce stem cell-like characteristics in glioma cells as an "extra-ribosomal function".
Glioblastoma
Glioma stem cells
Plasticity
Ribosomal protein S6
Ribosome
Journal
Brain tumor pathology
ISSN: 1861-387X
Titre abrégé: Brain Tumor Pathol
Pays: Japan
ID NLM: 9716507
Informations de publication
Date de publication:
Apr 2022
Apr 2022
Historique:
received:
05
03
2022
accepted:
21
04
2022
pubmed:
5
5
2022
medline:
14
5
2022
entrez:
4
5
2022
Statut:
ppublish
Résumé
The characteristic features of plasticity and heterogeneity in glioblastoma (GB) cells cause therapeutic difficulties. GB cells are exposed to various stimuli from the tumor microenvironment and acquire the potential to resist chemoradiotherapy. To investigate how GB cells acquire stem cell-like phenotypes, we focused on ribosomal proteins, because ribosome incorporation has been reported to induce stem cell-like phenotypes in somatic cells. Furthermore, dysregulation of ribosome biogenesis has been reported in several types of cancer. We focused on ribosomal protein S6, which promotes sphere-forming ability and stem cell marker expression in GB cells. We expect that investigation of dysregulation of ribosome biogenesis and extra-ribosomal function in GB will provide new insights about the plasticity, heterogeneity, and therapeutic resistance of GB cells, which can potentially lead to revolutionary therapeutic strategies.
Identifiants
pubmed: 35508789
doi: 10.1007/s10014-022-00434-5
pii: 10.1007/s10014-022-00434-5
doi:
Substances chimiques
Ribosomal Proteins
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
51-56Subventions
Organisme : Grants-in-Aid for Scientific Research (C) from Ministry of Education, Culture, Sports, Science and Technology
ID : JP20K09374
Informations de copyright
© 2022. The Author(s), under exclusive licence to The Japan Society of Brain Tumor Pathology.
Références
Stupp R, Hegi ME, Mason WP et al (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459–466
pubmed: 19269895
Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996
pubmed: 15758009
Singh SK, Clarke ID, Hide T et al (2004) Cancer stem cells in nervous system tumors. Oncogene 23:7267–7273
pubmed: 15378086
Singh SK, Hawkins C, Clarke ID et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401
pubmed: 15549107
Andersen BM, Faust Akl C, Wheeler MA et al (2021) Glial and myeloid heterogeneity in the brain tumour microenvironment. Nat Rev Cancer 21:786–802
pubmed: 34584243
Hernandez A, Domenech M, Munoz-Marmol AM et al (2021) Glioblastoma: relationship between metabolism and immunosuppressive microenvironment. Cells 10(12):3529
pubmed: 34944036
pmcid: 8700075
Neftel C, Laffy J, Filbin MG et al (2019) An integrative model of cellular states, plasticity, and genetics for glioblastoma. Cell 178(835–849):e821
Yang K, Wu Z, Zhang H et al (2022) Glioma targeted therapy: insight into future of molecular approaches. Mol Cancer 21:39
pubmed: 35135556
pmcid: 8822752
Hide T, Komohara Y, Miyasato Y et al (2018) Oligodendrocyte progenitor cells and macrophages/microglia produce glioma stem cell niches at the tumor border. EBioMedicine 30:94–104
pubmed: 29559295
pmcid: 5952226
Hide T, Shibahara I, Kumabe T (2019) Novel concept of the border niche: glioblastoma cells use oligodendrocytes progenitor cells (GAOs) and microglia to acquire stem cell-like features. Brain Tumor Pathol 36:63–73
pubmed: 30968276
Ito N, Katoh K, Kushige H et al (2018) Ribosome incorporation into somatic cells promotes lineage transdifferentiation towards multipotency. Sci Rep 8:1634
pubmed: 29374279
pmcid: 5786109
Shirakawa Y, Hide T, Yamaoka M et al (2020) Ribosomal protein S6 promotes stem-like characters in glioma cells. Cancer Sci 111:2041–2051
pubmed: 32246865
pmcid: 7293102
Domenech M, Hernandez A, Plaja A et al (2021) Hypoxia: the cornerstone of glioblastoma. Int J Mol Sci 22(22):12608
pubmed: 34830491
pmcid: 8620858
Vartanian A, Singh SK, Agnihotri S et al (2014) GBM’s multifaceted landscape: highlighting regional and microenvironmental heterogeneity. Neuro Oncol 16:1167–1175
pubmed: 24642524
pmcid: 4136895
Basheer AS, Abas F, Othman I et al (2021) Role of inflammatory mediators, macrophages, and neutrophils in glioma maintenance and progression: mechanistic understanding and potential therapeutic applications. Cancers (Basel) 13(16):4226
Simon T, Jackson E, Giamas G (2020) Breaking through the glioblastoma micro-environment via extracellular vesicles. Oncogene 39:4477–4490
pubmed: 32366909
pmcid: 7269906
Mohiuddin E, Wakimoto H (2021) Extracellular matrix in glioblastoma: opportunities for emerging therapeutic approaches. Am J Cancer Res 11:3742–3754
pubmed: 34522446
pmcid: 8414390
Broekman ML, Maas SLN, Abels ER et al (2018) Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol 14:482–495
pubmed: 29985475
pmcid: 6425928
Kressler D, Hurt E, Bassler J (2010) Driving ribosome assembly. Biochim Biophys Acta 1803:673–683
pubmed: 19879902
Zhou X, Liao WJ, Liao JM et al (2015) Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol 7:92–104
pubmed: 25735597
pmcid: 4481666
Zhang D, Chen HP, Duan HF et al (2016) Aggregation of ribosomal protein S6 at nucleolus is cell cycle-controlled and its function in Pre-rRNA processing is phosphorylation dependent. J Cell Biochem 117:1649–1657
pubmed: 26639987
Biever A, Valjent E, Puighermanal E (2015) Ribosomal protein S6 phosphorylation in the nervous system: from regulation to function. Front Mol Neurosci 8:75
pubmed: 26733799
pmcid: 4679984
Chow S, Minden MD, Hedley DW (2006) Constitutive phosphorylation of the S6 ribosomal protein via mTOR and ERK signaling in the peripheral blasts of acute leukemia patients. Exp Hematol 34:1183–1191
pubmed: 16939811
Chen B, Tan Z, Gao J et al (2015) Hyperphosphorylation of ribosomal protein S6 predicts unfavorable clinical survival in non-small cell lung cancer. J Exp Clin Cancer Res 34:126
pubmed: 26490682
pmcid: 4618148
Khalaileh A, Dreazen A, Khatib A et al (2013) Phosphorylation of ribosomal protein S6 attenuates DNA damage and tumor suppression during development of pancreatic cancer. Cancer Res 73:1811–1820
pubmed: 23361300
Puchalski RB, Shah N, Miller J et al (2018) An anatomic transcriptional atlas of human glioblastoma. Science 360:660–663
pubmed: 29748285
pmcid: 6414061
Shirakawa Y, Ohta K, Miyake S et al (2021) Glioma cells acquire stem-like characters by extrinsic ribosome stimuli. Cells 10(11):2970
pubmed: 34831193
pmcid: 8616507
Court FA, Hendriks WT, MacGillavry HD et al (2008) Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J Neurosci 28:11024–11029
pubmed: 18945910
pmcid: 6671360
Lopez-Leal R, Alvarez J, Court FA (2016) Origin of axonal proteins: Is the axon-schwann cell unit a functional syncytium? Cytoskeleton (Hoboken) 73:629–639
Pinto G, Saenz-de-Santa-Maria I, Chastagner P et al (2021) Patient-derived glioblastoma stem cells transfer mitochondria through tunneling nanotubes in tumor organoids. Biochem J 478:21–39
pubmed: 33245115
Yi YW, You KS, Park JS et al (2021) Ribosomal protein S6: a potential therapeutic target against cancer? Int J Mol Sci 23(1):48
pubmed: 35008473
pmcid: 8744729
Pecoraro A, Pagano M, Russo G et al (2021) Ribosome biogenesis and cancer: overview on ribosomal proteins. Int J Mol Sci 22(11):5496
pubmed: 34071057
pmcid: 8197113
Orgebin E, Lamoureux F, Isidor B et al (2020) Ribosomopathies: new therapeutic perspectives. Cells 9(9):2080
pmcid: 7564184
Norris K, Hopes T, Aspden JL (2021) Ribosome heterogeneity and specialization in development. Wiley Interdiscip Rev RNA 12:e1644
pubmed: 33565275
pmcid: 8647923
Warner JR, McIntosh KB (2009) How common are extraribosomal functions of ribosomal proteins? Mol Cell 34:3–11
pubmed: 19362532
pmcid: 2679180
Narla A, Ebert BL (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115:3196–3205
pubmed: 20194897
pmcid: 2858486
Barna M, Pusic A, Zollo O et al (2008) Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature 456:971–975
pubmed: 19011615
pmcid: 2880952
Bursac S, Prodan Y, Pullen N et al (2021) Dysregulated ribosome biogenesis reveals therapeutic liabilities in cancer. Trends Cancer 7:57–76
pubmed: 32948502
El Khoury W, Nasr Z (2021) Deregulation of ribosomal proteins in human cancers. Biosci Rep. https://doi.org/10.1042/BSR20211577
doi: 10.1042/BSR20211577
pubmed: 34873618
pmcid: 8685657
Jeon YJ, Kim IK, Hong SH et al (2008) Ribosomal protein S6 is a selective mediator of TRAIL-apoptotic signaling. Oncogene 27:4344–4352
pubmed: 18362888
Yanai A, Inoue N, Yagi T et al (2015) Activation of mTOR/S6K but not MAPK pathways might be associated with high Ki-67, ER(+), and HER2(-) breast cancer. Clin Breast Cancer 15:197–203
pubmed: 25600244
Grundy M, Jones T, Elmi L et al (2018) Early changes in rpS6 phosphorylation and BH3 profiling predict response to chemotherapy in AML cells. PLoS ONE 13:e0196805
pubmed: 29723246
pmcid: 5933738
Hagner PR, Mazan-Mamczarz K, Dai B et al (2011) Ribosomal protein S6 is highly expressed in non-Hodgkin lymphoma and associates with mRNA containing a 5’ terminal oligopyrimidine tract. Oncogene 30:1531–1541
pubmed: 21102526
Liu Z, Yun R, Yu X et al (2016) Overexpression of Notch3 and pS6 is associated with poor prognosis in human ovarian epithelial cancer. Mediators Inflamm 2016:5953498
pubmed: 27445438
pmcid: 4944072
Pinto AP, Degen M, Barron P et al (2013) Phosphorylated S6 as an immunohistochemical biomarker of vulvar intraepithelial neoplasia. Mod Pathol 26:1498–1507
pubmed: 23765247
Molinolo AA, Hewitt SM, Amornphimoltham P et al (2007) Dissecting the Akt/mammalian target of rapamycin signaling network: emerging results from the head and neck cancer tissue array initiative. Clin Cancer Res 13:4964–4973
pubmed: 17785546
Zheng Z, Zheng Y, Zhang M et al (2016) Reciprocal expression of p-AMPKa and p-S6 is strongly associated with the prognosis of gastric cancer. Tumour Biol 37:4803–4811
pubmed: 26520441
Knoll M, Macher-Goeppinger S, Kopitz J et al (2016) The ribosomal protein S6 in renal cell carcinoma: functional relevance and potential as biomarker. Oncotarget 7:418–432
pubmed: 26506236
Corcoran RB, Rothenberg SM, Hata AN et al (2013) TORC1 suppression predicts responsiveness to RAF and MEK inhibition in BRAF-mutant melanoma. Sci Transl Med 5:196ra198
Li YJ, Wang Y, Wang YY (2019) MicroRNA-99b suppresses human cervical cancer cell activity by inhibiting the PI3K/AKT/mTOR signaling pathway. J Cell Physiol 234:9577–9591
pubmed: 30480801
Ganger DR, Hamilton PD, Fletcher JW et al (1997) Metallopanstimulin is overexpressed in a patient with colonic carcinoma. Anticancer Res 17:1993–1999
pubmed: 9216656
Fernandez-Pol JA, Fletcher JW, Hamilton PD et al (1997) Expression of metallopanstimulin and oncogenesis in human prostatic carcinoma. Anticancer Res 17:1519–1530
pubmed: 9179190
Atsuta Y, Aoki N, Sato K et al (2002) Identification of metallopanstimulin-1 as a member of a tumor associated antigen in patients with breast cancer. Cancer Lett 182:101–107
pubmed: 12175529
Wang YW, Qu Y, Li JF et al (2006) In vitro and in vivo evidence of metallopanstimulin-1 in gastric cancer progression and tumorigenicity. Clin Cancer Res 12:4965–4973
pubmed: 16914586
Fernandez-Pol JA (2012) Increased serum level of RPMPS-1/S27 protein in patients with various types of cancer is useful for the early detection, prevention and therapy. Cancer Genomics Proteomics 9:203–256
pubmed: 22798506
Xiong X, Zhao Y, He H et al (2011) Ribosomal protein S27-like and S27 interplay with p53-MDM2 axis as a target, a substrate and a regulator. Oncogene 30:1798–1811
pubmed: 21170087
Liu Y, Ma J, Zhang L et al (2021) Overexpressed MPS-1 contributes to endometrioma development through the NF-kappaB signaling pathway. Reprod Biol Endocrinol 19:111
pubmed: 34266426
pmcid: 8281640
Feldheim J, Kessler AF, Schmitt D et al (2020) Ribosomal protein S27/Metallopanstimulin-1 (RPS27) in Glioma-a new disease biomarker? Cancers (Basel) 12(5):1085
Anam MB, Istiaq A, Kariya R et al (2021) Ribosome induces transdifferentiation of A549 and H-111-TC cancer cell lines. Biochem Biophys Rep 26:100946
pubmed: 33644423
pmcid: 7887644
Kudo M, Anam MB, Istiaq A et al (2021) Ribosome incorporation induces EMT-like phenomenon with cell cycle arrest in human breast cancer cell. Cells Tissues Organs. https://doi.org/10.1159/000513908:1-10
doi: 10.1159/000513908:1-10
pubmed: 33640894
Setayesh-Mehr Z, Poorsargol M (2021) Toxic proteins application in cancer therapy. Mol Biol Rep 48:3827–3840
pubmed: 33895972
Rotondo R, Ragucci S, Castaldo S et al (2021) Cytotoxicity effect of quinoin, type 1 ribosome-inactivating protein from quinoa seeds, on glioblastoma cells. Toxins (Basel) 13(10):684
Lapik YR, Fernandes CJ, Lau LF et al (2004) Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol Cell 15:17–29
pubmed: 15225545
Holzel M, Rohrmoser M, Schlee M et al (2005) Mammalian WDR12 is a novel member of the Pes1-Bop1 complex and is required for ribosome biogenesis and cell proliferation. J Cell Biol 170:367–378
pubmed: 16043514
pmcid: 2171466
Li YZ, Zhang C, Pei JP et al (2022) The functional role of Pescadillo ribosomal biogenesis factor 1 in cancer. J Cancer 13:268–277
pubmed: 34976188
pmcid: 8692700
Mi L, Qi Q, Ran H et al (2021) Suppression of ribosome biogenesis by targeting WD repeat domain 12 (WDR12) inhibits glioma stem-like cell growth. Front Oncol 11:751792
pubmed: 34868955
pmcid: 8633585
Li JL, Chen C, Chen W et al (2020) Integrative genomic analyses identify WDR12 as a novel oncogene involved in glioblastoma. J Cell Physiol 235:7344–7355
pubmed: 32180229