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05.05.2022 | Review Article

Ribosomal proteins induce stem cell-like characteristics in glioma cells as an “extra-ribosomal function”

verfasst von: Takuichiro Hide, Ichiyo Shibahara, Madoka Inukai, Ryota Shigeeda, Yuki Shirakawa, Hirofumi Jono, Naoki Shinojima, Akitake Mukasa, Toshihiro Kumabe

Erschienen in: Brain Tumor Pathology | Ausgabe 2/2022

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Abstract

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.

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 10:459–466PubMedCrossRef

Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMed

Singh SK, Clarke ID, Hide T et al (2004) Cancer stem cells in nervous system tumors. Oncogene 23:7267–7273PubMedCrossRef

Singh SK, Hawkins C, Clarke ID et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRef

Andersen BM, Faust Akl C, Wheeler MA et al (2021) Glial and myeloid heterogeneity in the brain tumour microenvironment. Nat Rev Cancer 21:786–802PubMedCrossRef

Hernandez A, Domenech M, Munoz-Marmol AM et al (2021) Glioblastoma: relationship between metabolism and immunosuppressive microenvironment. Cells 10(12):3529PubMedPubMedCentralCrossRef

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 21:39PubMedPubMedCentralCrossRef

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 30:94–104PubMedPubMedCentralCrossRef

10.

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 36:63–73PubMedCrossRef

11.

Ito N, Katoh K, Kushige H et al (2018) Ribosome incorporation into somatic cells promotes lineage transdifferentiation towards multipotency. Sci Rep 8:1634PubMedPubMedCentralCrossRef

12.

Shirakawa Y, Hide T, Yamaoka M et al (2020) Ribosomal protein S6 promotes stem-like characters in glioma cells. Cancer Sci 111:2041–2051PubMedPubMedCentralCrossRef

13.

Domenech M, Hernandez A, Plaja A et al (2021) Hypoxia: the cornerstone of glioblastoma. Int J Mol Sci 22(22):12608PubMedPubMedCentralCrossRef

14.

Vartanian A, Singh SK, Agnihotri S et al (2014) GBM’s multifaceted landscape: highlighting regional and microenvironmental heterogeneity. Neuro Oncol 16:1167–1175PubMedPubMedCentralCrossRef

15.

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):4226CrossRef

16.

Simon T, Jackson E, Giamas G (2020) Breaking through the glioblastoma micro-environment via extracellular vesicles. Oncogene 39:4477–4490PubMedPubMedCentralCrossRef

17.

Mohiuddin E, Wakimoto H (2021) Extracellular matrix in glioblastoma: opportunities for emerging therapeutic approaches. Am J Cancer Res 11:3742–3754PubMedPubMedCentral

18.

Broekman ML, Maas SLN, Abels ER et al (2018) Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol 14:482–495PubMedPubMedCentralCrossRef

19.

Kressler D, Hurt E, Bassler J (2010) Driving ribosome assembly. Biochim Biophys Acta 1803:673–683PubMedCrossRef

20.

Zhou X, Liao WJ, Liao JM et al (2015) Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol 7:92–104PubMedPubMedCentralCrossRef

21.

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 117:1649–1657PubMedCrossRef

22.

Biever A, Valjent E, Puighermanal E (2015) Ribosomal protein S6 phosphorylation in the nervous system: from regulation to function. Front Mol Neurosci 8:75PubMedPubMedCentralCrossRef

23.

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 34:1183–1191PubMedCrossRef

24.

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 34:126PubMedPubMedCentralCrossRef

25.

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 73:1811–1820PubMedCrossRef

26.

Puchalski RB, Shah N, Miller J et al (2018) An anatomic transcriptional atlas of human glioblastoma. Science 360:660–663PubMedPubMedCentralCrossRef

27.

Shirakawa Y, Ohta K, Miyake S et al (2021) Glioma cells acquire stem-like characters by extrinsic ribosome stimuli. Cells 10(11):2970PubMedPubMedCentralCrossRef

28.

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 28:11024–11029PubMedPubMedCentralCrossRef

29.

Lopez-Leal R, Alvarez J, Court FA (2016) Origin of axonal proteins: Is the axon-schwann cell unit a functional syncytium? Cytoskeleton (Hoboken) 73:629–639CrossRef

30.

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 478:21–39PubMedCrossRef

31.

Yi YW, You KS, Park JS et al (2021) Ribosomal protein S6: a potential therapeutic target against cancer? Int J Mol Sci 23(1):48PubMedPubMedCentralCrossRef

32.

Pecoraro A, Pagano M, Russo G et al (2021) Ribosome biogenesis and cancer: overview on ribosomal proteins. Int J Mol Sci 22(11):5496PubMedPubMedCentralCrossRef

33.

Orgebin E, Lamoureux F, Isidor B et al (2020) Ribosomopathies: new therapeutic perspectives. Cells 9(9):2080PubMedCentralCrossRef

34.

Norris K, Hopes T, Aspden JL (2021) Ribosome heterogeneity and specialization in development. Wiley Interdiscip Rev RNA 12:e1644PubMedPubMedCentralCrossRef

35.

Warner JR, McIntosh KB (2009) How common are extraribosomal functions of ribosomal proteins? Mol Cell 34:3–11PubMedPubMedCentralCrossRef

36.

Narla A, Ebert BL (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115:3196–3205PubMedPubMedCentralCrossRef

37.

Barna M, Pusic A, Zollo O et al (2008) Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature 456:971–975PubMedPubMedCentralCrossRef

38.

Bursac S, Prodan Y, Pullen N et al (2021) Dysregulated ribosome biogenesis reveals therapeutic liabilities in cancer. Trends Cancer 7:57–76PubMedCrossRef

39.

El Khoury W, Nasr Z (2021) Deregulation of ribosomal proteins in human cancers. Biosci Rep. https://doi.org/10.1042/BSR20211577CrossRefPubMedPubMedCentral

40.

Jeon YJ, Kim IK, Hong SH et al (2008) Ribosomal protein S6 is a selective mediator of TRAIL-apoptotic signaling. Oncogene 27:4344–4352PubMedCrossRef

41.

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 15:197–203PubMedCrossRef

42.

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:e0196805PubMedPubMedCentralCrossRef

43.

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 30:1531–1541PubMedCrossRef

44.

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 2016:5953498PubMedPubMedCentral

45.

Pinto AP, Degen M, Barron P et al (2013) Phosphorylated S6 as an immunohistochemical biomarker of vulvar intraepithelial neoplasia. Mod Pathol 26:1498–1507PubMedCrossRef

46.

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 13:4964–4973PubMedCrossRef

47.

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 37:4803–4811PubMedCrossRef

48.

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 7:418–432PubMedCrossRef

49.

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 5:196ra198CrossRef

50.

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 234:9577–9591PubMedCrossRef

51.

Ganger DR, Hamilton PD, Fletcher JW et al (1997) Metallopanstimulin is overexpressed in a patient with colonic carcinoma. Anticancer Res 17:1993–1999PubMed

52.

Fernandez-Pol JA, Fletcher JW, Hamilton PD et al (1997) Expression of metallopanstimulin and oncogenesis in human prostatic carcinoma. Anticancer Res 17:1519–1530PubMed

53.

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 182:101–107PubMedCrossRef

54.

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 12:4965–4973PubMedCrossRef

55.

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 9:203–256PubMed

56.

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 30:1798–1811PubMedCrossRef

57.

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 19:111PubMedPubMedCentralCrossRef

58.

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):1085CrossRef

59.

Anam MB, Istiaq A, Kariya R et al (2021) Ribosome induces transdifferentiation of A549 and H-111-TC cancer cell lines. Biochem Biophys Rep 26:100946PubMedPubMedCentral

60.

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/10.1159/000513908:1-10CrossRefPubMed

61.

Setayesh-Mehr Z, Poorsargol M (2021) Toxic proteins application in cancer therapy. Mol Biol Rep 48:3827–3840PubMedCrossRef

62.

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):684CrossRef

63.

Lapik YR, Fernandes CJ, Lau LF et al (2004) Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol Cell 15:17–29PubMedCrossRef

64.

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 170:367–378PubMedPubMedCentralCrossRef

65.

Li YZ, Zhang C, Pei JP et al (2022) The functional role of Pescadillo ribosomal biogenesis factor 1 in cancer. J Cancer 13:268–277PubMedPubMedCentralCrossRef

66.

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 11:751792PubMedPubMedCentralCrossRef

67.

Li JL, Chen C, Chen W et al (2020) Integrative genomic analyses identify WDR12 as a novel oncogene involved in glioblastoma. J Cell Physiol 235:7344–7355PubMedCrossRef

Titel: Ribosomal proteins induce stem cell-like characteristics in glioma cells as an “extra-ribosomal function”
verfasst von: Takuichiro Hide
Ichiyo Shibahara
Madoka Inukai
Ryota Shigeeda
Yuki Shirakawa
Hirofumi Jono
Naoki Shinojima
Akitake Mukasa
Toshihiro Kumabe
Publikationsdatum: 05.05.2022
Verlag: Springer Nature Singapore
Erschienen in: Brain Tumor Pathology / Ausgabe 2/2022
Print ISSN: 1433-7398
Elektronische ISSN: 1861-387X
DOI: https://doi.org/10.1007/s10014-022-00434-5

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