Skip to main content

Advertisement

SpringerLink
Log in

Biological effects of cancer stem cells irradiated by charged particle: a systematic review of in vitro studies

  • Review
  • Published:
Journal of Cancer Research and Clinical Oncology Aims and scope Submit manuscript

Abstract

Purpose

The existence of cancer stem cells (CSCs) is closely related to tumor recurrence, metastasis, and resistance to chemoradiotherapy. In addition, given the unique physical and biological advantages of charged particle, we hypothesized that charged particle irradiation would produce strong killing effects on CSCs. The purpose of our systematic review is to evaluate the biological effects of CSCs irradiated by charged particle, including proliferation, invasion, migration, and changes in the molecular level.

Methods

We searched PubMed, EMBASE, and Web of Science until 17 march 2022 according to the key words. Included studies have to be vitro studies of CSCs irradiated by charged particle. Outcomes included one or more of radiation sensitivity, proliferation, metastasis, invasion, and molecular level changes, like DNA damage after been irradiated.

Results

Eighteen studies were included in the final analysis. The 18 articles include 12-carbon ion irradiation, 4-proton irradiation, 1 α-particle irradiation, 1-carbon ion combine proton irradiation.

Conclusion

Through the extraction and analysis of data, we came to this conclusion: CSCs have obvious radio-resistance compared with non-CSCs, and charged particle irradiation or in combination with drugs could overcome this resistance, specifically manifested in inhibiting CSCs’ proliferation, invasion, migration, and causing more and harder to repair DNA double-stranded breaks (DSB) of CSCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available in the PubMed: https://pubmed.ncbi.nlm.nih.gov/, Web of Science: https://www.webofscience.com/wos/alldb/basic-search, and EMBASE: https://www.embase.com/.

Abbreviations

CSCs:

Cancer stem cells

SCID:

Severe combined immune deficiency

RT:

Radiotherapy

LET:

Linear energy transfer

RBE:

Relative biological effects

CIRT:

Carbon ion radiotherapy

DNA:

Deoxyribonucleic acid

DSB:

Double-strand breaks

OER:

Oxygen enhancement ratio

SOBP:

Spread-out Bragg peak

HNSCC:

Head and neck squamous cell carcinoma

PRISMA:

Preferred Reporting Items for Systematic Review and Meta-Analysis

ATG:

Autophagy-related genes

ALDH:

Aldehyde dehydrogenase

FACS:

Fluorescence-activated cell sorter

MACS:

Magnetic-activated cell sorting

MBM:

Mixed beam model

NIRS:

National Institute of Radiological Sciences

MKM:

Microdosimetric-kinetic model

LEM:

Local effect model

NHEJ:

Non-homologous end joining

HR:

Homologous recombination

DNA-PK:

DNA-dependent protein kinase

ROS:

Reactive oxygen species

References

  • Al-Hajj M, Wicha M, Benito-Hernandez A, Morrison S, Clarke M (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7):3983–3988

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bao S, Wu Q, Mclendon R, Hao Y, Shi Q, Hjelmeland A, Dewhirst M, Bigner D, Rich J (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120):756–760

    CAS  PubMed  Google Scholar 

  • Beerman I, Seita J, Inlay M, Weissman I, Rossi D (2014) Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell 15(1):37–50

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bird RP, Burki HJ (1975) Survival of synchronized Chinese hamster cells exposed to radiation of different linear-energy transfer. Int J Radiat Biol Relat Stud Phys Chem Med 27(2):105–120

    CAS  PubMed  Google Scholar 

  • Bonnet D, Dick J (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3(7):730–737

    CAS  PubMed  Google Scholar 

  • Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI, Lu KH, Chen DT, Tai LK, Yung MC, Chang SC (2009) Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophy Res Comm. 11:231

    Google Scholar 

  • Chiblak S, Tang Z, Campos B, Gal Z, Unterberg A, Debus J, Herold-Mende C, Abdollahi A (2016) Radiosensitivity of Patient-Derived Glioma Stem Cell 3-Dimensional Cultures to Photon, Proton, and Carbon Irradiation. Int J Radiat Oncol Biol Phys 95(1):112–119

    PubMed  Google Scholar 

  • Cho IC, Niu H, Liu YC, Lee TF, Chen FH (2019) Application of a vertical charged-particle irradiation platform in glioblastoma multiforme cancer stem cell research. Nucl Instr Method Phy Res 441:102–107

    CAS  Google Scholar 

  • Clarke M, Dick J, Dirks P, Eaves C, Jamieson C, Jones D, Visvader J, Weissman I, Wahl G (2006) Cancer stem cells–perspectives on current status and future directions: AACR Workshop on cancer stem cells. Can Res 66(19):9339–9344

    CAS  Google Scholar 

  • Collins A, Berry P, Hyde C, Stower M, Maitland N (2005) Prospective identification of tumorigenic prostate cancer stem cells. Can Res 65(23):10946–10951

    CAS  Google Scholar 

  • Cui X, Oonishi K, Tsujii H, Yasuda T, Matsumoto Y, Furusawa Y, Akashi M, Kamada T, Okayasu R (2011) Effects of Carbon Ion Beam on Putative Colon Cancer Stem Cells and Its Comparison with X-rays. Can Res 71(10):3676–3687

    CAS  Google Scholar 

  • Diehn M, Cho RW, Lobo NA, Kalisky T, Clarke MF (2009) Association of Reactive Oxygen Species Levels and Radioresistance in Cancer Stem Cells. Nature 458(7239):780–783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fulawka L, Donizy P, Halon A (2014) Cancer stem cells–the current status of an old concept: literature review and clinical approaches. Biol Res 47:66

    PubMed  PubMed Central  Google Scholar 

  • Gao MQ, Choi YP, Kang S, Youn JH, Cho NH (2010) CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 29(18):2672–2680

    CAS  PubMed  Google Scholar 

  • Greve B, Beller C, Cassens U, Sibrowski W (2010) The Impact of Erythrocyte Lysing Procedures on the Recovery of Hematopoietic Progenitor Cells in Flow Cytometric Analysis. Stem Cells 24(3):793–799

    Google Scholar 

  • Hamada N (2009) Recent Insights into the Biological Action of Heavy-Ion Radiation. J Radiat Res 1:1–9

    Google Scholar 

  • Hawkins R (1998) A microdosimetric-kinetic theory of the dependence of the RBE for cell death on LET. Med Phys 25:1157–1170

    CAS  PubMed  Google Scholar 

  • Higgins JPT, Green S (2011) Cochrane handbook for systematic reviews of interventions version 5.1.0. http://handbook.cochrane.org/

  • Inaniwa T, Furukawa T, Kase Y, Matsufuji N, Toshito T, Matsumoto Y, Furusawa Y, Noda K (2010) Treatment planning for a scanned carbon beam with a modified microdosimetric kinetic model. Phys Med Biol 55(22):6721–6737

    PubMed  Google Scholar 

  • Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, Kai K, Takahashi E, Imamura Y, Baba Y, Ohmura M, Suematsu M, Baba H, Saya H (2011) CD44 Variant Regulates Redox Status in Cancer Cells by Stabilizing the xCT Subunit of System xc− and Thereby Promotes Tumor Growth. Cancel Cell. 19:387

    CAS  Google Scholar 

  • Jung MH, Park JC (2015) ERK/p38 MAPK inhibition reduces radio-resistance to a pulsed proton beam in breast cancer stem cells. J Korean Phys Soc 67(8):1444–1447

    Google Scholar 

  • Kakeji Y, Kurita K, Minami Y, Takiguchi G, Nishita M (2016) Wnt5a-Ror2 signaling in mesenchymal stem cells promotes proliferation of gastric cancer cells by activating CXCL16-CXCR6 axis. Cancer Sci 21:321

    Google Scholar 

  • Kanai T, Endo M, Minohara S, Miyahara N, Koyama-ito H, Tomura H, Matsufuji N, Futami Y, Fukumura A, Hiraoka T, Furusawa Y, Ando K, Suzuki M, Soga F, Kawachi K (1999) Biophysical characteristics of HIMAC clinical irradiation system for heavy-ion radiation therapy. Int J Radiat Oncol Biol Phys 44(1):201–210

    CAS  PubMed  Google Scholar 

  • Karger C, Peschke P (2017) RBE and related modeling in carbon-ion therapy. Phys Med Biol 63(1):102

    Google Scholar 

  • Karger C, Peschke P, Sanchez-Brandelik R, Scholz M, Debus J (2006) Radiation tolerance of the rat spinal cord after 6 and 18 fractions of photons and carbon ions: experimental results and clinical implications. Int J Radiat Oncol Biol Phys 66(5):1488–1497

    CAS  PubMed  Google Scholar 

  • Keysar S, Jimeno A (2010) More than markers: biological significance of cancer stem cell-defining molecules. Mol Cancer Ther 9(9):2450–2457

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koom WS, Sai S, Suzuki M, Fujimori A, Yamada S, Tsujii H (2020) Superior Effect of the Combination of Carbon-Ion Beam Irradiation and 5-Fluorouracil on Colorectal Cancer Stem Cells in vitro and in vivo. Onco Targets Ther 13:12625–12635

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lapidot T, Sirard, and Christian. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367(6464):645–645

    CAS  PubMed  Google Scholar 

  • Li C (2007) Identification of pancreatic cancer stem cells. Cancer Res 67:333

    Google Scholar 

  • Lianidou E, Markou A (2011) Circulating Tumor Cells in Breast Cancer: Detection Systems, Molecular Characterization, and Future Challenges. Clin Chem 57(9):1242–1255

    CAS  PubMed  Google Scholar 

  • Mavragani I, Nikitaki Z, Souli M, Aziz A, Nowsheen S, Aziz K, Rogakou E, Georgakilas A (2017) Complex DNA Damage: A Route to Radiation-Induced Genomic Instability and Carcinogenesis. Cancers 11:333

    Google Scholar 

  • Mihatsch J, Toulany M, Bareiss PM, Grimm S, Lengerke C, Kehlbach R, Rodemann HP (2011) Selection of radioresistant tumor cells and presence of ALDH1 activity in vitro. Radiother Oncol 99(3):300–306

    CAS  PubMed  Google Scholar 

  • Miyasaka Y, Komatsu S, Abe T, Kubo N, Okano N, Shibuya K, Shirai K, Kawamura H, Saitoh JI, Ebara T (2021) Comparison of Oncologic Outcomes between Carbon Ion Radiotherapy and Stereotactic Body Radiotherapy for Early-Stage Non-Small Cell Lung Cancer. Cancers 13(2):176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moertel H, Georgi J, Distel L, Eyrich W, Fritsch M, Grabenbauer G, Sauer R (2004) Effects of low energy protons on clonogenic survival, DSB repair and cell cycle in human glioblastoma cells and B14 fibroblasts. Radiother Oncol 73:S115-118

    CAS  PubMed  Google Scholar 

  • Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 4(1):1–9

    PubMed  PubMed Central  Google Scholar 

  • Narang H, Kumar A, Bhat N, Pandey BN, Ghosh A (2015) Effect of proton and gamma irradiation on human lung carcinoma cells: Gene expression, cell cycle, cell death, epithelial-mesenchymal transition and cancer-stem cell trait as biological end points. Mutat Res 780:35–46

    CAS  PubMed  Google Scholar 

  • Nikolova T, Ensminger M, Brich ML, Kaina B (2010) Homologous recombination protects mammalian cells from replication-associated DNA double-strand breaks arising in response to methyl methanesulfonate. DNA Repair 9(10):1050–1063

    CAS  PubMed  Google Scholar 

  • O’Brien C, Pollett A, Gallinger S, Dick J (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445(7123):106–110

    CAS  PubMed  Google Scholar 

  • Odoux C, Fohrer H, Hoppo T, Guzik L, Stolz DB, Lewis DW, Gollin SM, Gamblin TC, Geller DA, Lagasse E (2008) A Stochastic Model for Cancer Stem Cell Origin in Metastatic Colon Cancer. Can Res 68(17):6932

    CAS  Google Scholar 

  • Oonishi K, Cui X, Hirakawa H, Fujimori A, Kamijo T, Yamada S, Yokosuka O, Kamada T (2012) Different effects of carbon ion beams and X-rays on clonogenic survival and DNA repair in human pancreatic cancer stem-like cells. Radiother Oncol 105(2):258–265

    CAS  PubMed  Google Scholar 

  • Paganetti H (2014) Relative biological effectiveness (RBE) values for proton beam therapy. Variations as a function of biological endpoint, dose, and linear energy transfer. Phys Med Biol 59:419–472

    Google Scholar 

  • Paganetti H, Niemierko A, Ancukiewicz M, Gerweck EL, Goitein M (2002) Relative biological effectiveness (RBE) values for proton beam therapy. Inter J Rad Oncol 53:407–421

    Google Scholar 

  • Park SJ, Heo K, Choi C, Yang K, Adachi A, Okada H, Yoshida Y, Ohno T, Nakano T, Takahashi A (2017) Carbon ion irradiation abrogates Lin28B-induced X-ray resistance in melanoma cells. J Radiat Res 58(6):765–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci P, Fiore PD (2010) Biological and Molecular Heterogeneity of Breast Cancers Correlates with Their Cancer Stem Cell Content. Cell 1:140

    Google Scholar 

  • Pedroni E, Bacher R, Blattmann H, Böhringer T, Coray A, Lomax A, Lin S, Munkel G, Scheib S, Schneider U (1995) The 200-MeV proton therapy project at the Paul Scherrer Institute: conceptual design and practical realization. Med Phys 22(1):37–53

    CAS  PubMed  Google Scholar 

  • Phillips TM, Mcbride WH, Pajonk F (2006) The Response of CD24-/low/CD44+ Breast Cancer-Initiating Cells to Radiation. J Natl Cancer Inst 98:1777–1785

    PubMed  Google Scholar 

  • Plaks V, Kong N, Werb Z (2015) The Cancer Stem Cell Niche: How Essential Is the Niche in Regulating Stemness of Tumor Cells? Cell Stem Cell 16(3):225–238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Podberezin M, Wen J, Chang CCJ (2012) Cancer Stem Cells A Review of Potential Clinical Applications. Arch Pathol Lab Med 137(8):1111

    PubMed  Google Scholar 

  • Prince M, Sivanandan R, Kaczorowski A, Wolf G, Kaplan M, Dalerba P, Weissman I, Clarke M, Ailles L (2007) Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 104(3):973–978

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu S, Liu J, Xing F (2017) “Hints” in the killer protein gasdermin D: unveiling the secrets of gasdermins driving cell death. Cell Death Differ 24(4):588–596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, Maria RD (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445(7123):111

    CAS  PubMed  Google Scholar 

  • S., Chakraborty, J., M., Stark, C.-L., Sun, H., Modi, and W. 2012. Chronic myelogenous leukemia stem and progenitor cells demonstrate chromosomal instability related to repeated breakage-fusion-bridge cycles mediated by increased nonhomologous end joining. Blood.

  • Sai S, Vares G, Kim EH, Karasawa K, Wang B, Nenoi M, Horimoto Y, Hayashi M (2015a) Carbon ion beam combined with cisplatin effectively disrupts triple negative breast cancer stem-like cells in vitro. Mol Cancer 14:1–13

    Google Scholar 

  • Sai S, Wakai T, Vares G, Yamada S, Kamijo T, Kamada T, Shirai T (2015b) Combination of carbon ion beam and gemcitabine causes irreparable DNA damage and death of radioresistant pancreatic cancer stem-like cells in vitro and in vivo. Oncotarget 6(8):5517–5535

    PubMed  PubMed Central  Google Scholar 

  • Sai S, Kim EH, Vares G, Suzuki M, Hayashi M (2020) Combination of carbon-ion beam and dual tyrosine kinase inhibitor, lapatinib, effectively destroys HER2 positive breast cancer stem-like cells. Am J Cancer Res 10(8):2371–2386

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sai S, Kim EH, Koom WS, Vares G, Suzuki M, Yamada S, Hayashi M (2021) Carbon-Ion Beam Irradiation and the miR-200c Mimic Effectively Eradicate Pancreatic Cancer Stem Cells Under in vitro and in vivo Conditions. Onco Targets Ther 14:4749–4760

    PubMed  PubMed Central  Google Scholar 

  • Schieber M, Chandel N (2013) ROS links glucose metabolism to breast cancer stem cell and EMT phenotype. Cancer Cell 23(3):265–267

    CAS  PubMed  Google Scholar 

  • Schniewind I, Hadiwikarta WW, Grajek J, Poleszczuk J, Richter S, Peitzsch M, Muller J, Klusa D, Beyreuther E, Lock S, Luhr A, Frosch S, Groeben C, Sommer U, Krause M, Dubrovska A, von Neubeck C, Kurth I, Peitzsch C (2022) Cellular plasticity upon proton irradiation determines tumor cell radiosensitivity. Cell Rep 38(8):1104

    Google Scholar 

  • Scholz M, Kellerer A, Kraft-Weyrather W, Kraft G (1997) Computation of cell survival in heavy ion beams for therapy The model and its approximation. Radiat Environ Biophys 36(1):59–66

    CAS  PubMed  Google Scholar 

  • Shiba S, Okamoto M, Kiyohara H, Okazaki S, Kaminuma T, Shibuya K, Kohama I, Saito K, Yanagawa T, Chikuda H (2021) Impact of Carbon Ion Radiotherapy on Inoperable Bone Sarcoma. Cancers 13:1099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh S, Clarke I, Terasaki M, Bonn V, Hawkins C, Squire J, Dirks P (2003) Identification of a cancer stem cell in human brain tumors. Can Res 63(18):5821–5828

    CAS  Google Scholar 

  • Suetsugi A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H (2006) Characterization of CD133(+) hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 4:351

    Google Scholar 

  • Suit H, DeLaney T, Goldberg S, Paganetti H, Clasie B, Gerweck L, Niemierko A, Hall E, Flanz J, Hallman J, Trofimov A (2010) Proton vs carbon ion beams in the definitive radiation treatment of cancer patients. Radiother Oncol 95(1):3–22

    CAS  PubMed  Google Scholar 

  • Takahashi A, Kubo M, Ma H, Nakagawa A, Yoshida Y, Isono M, Kanai T, Ohno T, Furusawa Y, Funayama T (2014a) Nonhomologous end-joining repair plays a more important role than homologous recombination repair in defining radiosensitivity after exposure to high-LET radiation. Radiat Res 182(3):338

    PubMed  Google Scholar 

  • Takahashi M, Hirakawa H, Yajima H, Izumi-Nakajima N, Okayasu R, Fujimori A (2014b) Carbon ion beam is more effective to induce cell death in sphere-type A172 human glioblastoma cells compared with X-rays. Int J Radiat Biol 90(12):1125–1132

    CAS  PubMed  Google Scholar 

  • Tang DG, Patrawala L, Calhoun T, Bhatia B, Choy G, Schneider-Broussard R, Jeter C (2010) Prostate cancer stem/progenitor cells: Identification, characterization, and implications. Mol Carcinog 46(1):1–14

    Google Scholar 

  • Todaro M, Alea MP, Stefano A, Cammareri P, Vermeulen L, Iovino F, Tripodo C, Russo A, Gulotta G, Medema JP (2007) Colon Cancer Stem Cells Dictate Tumor Growth and Resist Cell Death by Production of Interleukin-4. Cell Stem Cell 1(4):389–402

    CAS  PubMed  Google Scholar 

  • Vares G, Ahire V, Sunada S, Kim EH, Sai S, Chevalier F, Romeo PH, Yamamoto T, Nakajima T, Saintigny Y (2020) A multimodal treatment of carbon ions irradiation, miRNA-34 and mTOR inhibitor specifically control high-grade chondrosarcoma cancer stem cells. Radiother Oncol 150:253–261

    CAS  PubMed  Google Scholar 

  • Vermeulen L, De Sousa F, Melo E, van der Heijden M, Cameron K, de Jong J, Borovski T, Tuynman J, Todaro M, Merz C, Rodermond H, Sprick M, Kemper K, Richel D, Stassi G, Medema J (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12(5):468–476

    CAS  PubMed  Google Scholar 

  • Vermeulen L, de Sousa e Melo F, Richel, DJ, Medema JP (2012) The developing cancer stem-cell model: clinical challenges and opportunities. The Lancet. Oncology 13(2):e83–e89. https://doi.org/10.1016/S1470-2045(11)70257-1

  • Wang H (2009) S-phase cells are more sensitive to high-linear energy transfer radiation. Int J Radiat Oncol Biol Phys 74(4):1236–1241

    CAS  PubMed  Google Scholar 

  • Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA (2010) Notch Promotes Radioresistance of Glioma Stem Cells. STEM CELLS 28(1):17–28

    CAS  PubMed  Google Scholar 

  • Wang WJ, Wu SP, Liu JB, Shi YS, Huang X, Zhang QB, Yao KT (2013) MYC Regulation of CHK1 and CHK2 Promotes Radioresistance in a Stem Cell-like Population of Nasopharyngeal Carcinoma Cells. Can Res 73(3):1219–1231

    CAS  Google Scholar 

  • Weyrather W, Ritter S, Scholz M, Kraft G (1999) RBE for carbon track-segment irradiation in cell lines of differing repair capacity. Int J Radiat Biol 75(11):1357–1364

    CAS  PubMed  Google Scholar 

  • Wozny AS, Vares G, Alphonse G, Lauret A, Monini C, Magne N, Cuerq C, Fujimori A, Monboisse JC, Beuve M, Nakajima T, Rodriguez-Lafrasse C (2019) ROS Production and Distribution: A New Paradigm to Explain the Differential Effects of X-ray and Carbon Ion Irradiation on Cancer Stem Cell Migration and Invasion. Cancers 11(4):468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wozny AS, Alphonse G, Cassard A, Malesys C, Louati S, Beuve M, Lalle P, Ardail D, Nakajima T, Rodriguez-Lafrasse C (2020) Impact of hypoxia on the double-strand break repair after photon and carbon ion irradiation of radioresistant HNSCC cells. Sci Rep 10(1):1–18

    Google Scholar 

  • Wu C, Alman BA (2008) Side population cells in human cancers. Cancer Lett 268(1):1–9

    CAS  PubMed  Google Scholar 

  • Yang G, Lu CY, Mei ZS, Sun XY, Han JT, Qian J, Liang YL, Pan Z, Kong DF, Xu SR, Liu ZP, Gao Y, Qi GJ, Shou YR, Chen SY, Cao ZX, Zhao Y, Lin C, Zhao YY, Geng YX, Ma WJ, Yan XQ (2021) Association of Cancer Stem Cell Radio-Resistance Under Ultra-High Dose Rate FLASH Irradiation With Lysosome-Mediated Autophagy. Frontiers Cell Develop Biol. 9:1388–1414

    Google Scholar 

  • Zhang M, Atkinson L, Rachel M, Jeffrey R (2010) Selective targeting of radiation-resistant tumor-initiating cells. Proc Natl Acad Sci USA 107:3522–3527

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, Poppleton H, Zakharenko S, Ellison DW, Gilbertson RJ (2009) Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457(7229):603–607

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

This research was funded by Science and Technology Plan Project of Chengguan District of Lanzhou, No.2020–2-2–5, National Key Research and Development Program of China, No. 2022YFC2401505, Talent innovation and venture project of Lanzhou city, No. 2021-RC-125 and Key R&D Program of Science and Technology Department of Gansu Province, No. 20YF8FA116.

Author information

Author notes

  1. Qian Wang and Ruifeng Liu have contributed equally to this work.

Authors and Affiliations

  1. Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou, 730030, China

    Qian Wang, Ruifeng Liu, Qiuning Zhang, Hongtao Luo, Xun Wu, Tianqi Du, Yanliang Chen, Mingyu Tan, Zhiqiang Liu, Shilong Sun & Xiaohu Wang

  2. The First School of Clinical Medicine, Lanzhou University, Lanzhou, 730030, China

    Qian Wang, Xun Wu, Tianqi Du, Yanliang Chen & Mingyu Tan

  3. Department of Postgraduate, University of Chinese Academy of Sciences, Beijing, 730030, China

    Ruifeng Liu, Qiuning Zhang, Hongtao Luo, Zhiqiang Liu, Shilong Sun & Xiaohu Wang

  4. Heavy Ion Therapy Center, Lanzhou Heavy Ions Hospital, Lanzhou, 730030, China

    Ruifeng Liu, Qiuning Zhang, Hongtao Luo, Zhiqiang Liu, Shilong Sun & Xiaohu Wang

  5. Evidence-Based Medicine Center, School of Basic Medical Sciences, Lanzhou University, Lanzhou, 730030, China

    Kehu Yang & Jinhui Tian

Authors
  1. Qian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruifeng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiuning Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongtao Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tianqi Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yanliang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mingyu Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhiqiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shilong Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kehu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jinhui Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Xiaohu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QW and RL contributed equally to this study. Conceptualization, QZ and XW; methodology, KY and JT; literature screening, XW, TD and YC; formal analysis, MT; data extraction, HL, ZL and SS; writing—original draft preparation, QW; writing—review and editing, RL; supervision, QZ and XW; funding acquisition, XW. All the authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Xiaohu Wang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of interest

All the authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.

Ethics approval

This is a systematic review. The Research Ethics Committee has confirmed that no ethical approval is required.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Q., Liu, R., Zhang, Q. et al. Biological effects of cancer stem cells irradiated by charged particle: a systematic review of in vitro studies. J Cancer Res Clin Oncol 149, 6625–6638 (2023). https://doi.org/10.1007/s00432-022-04561-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00432-022-04561-6

Keywords

Search

Navigation