Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance

Ebrahim H. Maleki; Ahmad Reza Bahrami; Maryam M. Matin

doi:10.1016/j.gendis.2022.11.025

您当前的位置：

首页 >

文章列表页 >

Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance

Review article | 更新时间：2024-02-04

- Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance
- Genes & Diseases Vol. 1, Issue 1, Pages: 189-204(2024)
- 作者机构：
  
  1. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, 917794 Mashhad,Iran,8974
  2. Jagiellonian Centre for Experimental Therapeutics (JCET), Jagiellonian University,Krakow,Poland,31-007
  3. Doctoral School of Exact and Natural Sciences, Jagiellonian University,Krakow,Poland,30-348
  4. Industrial Biotechnology Research Group, Institute of Biotechnology, Ferdowsi University of Mashhad, 917794 Mashhad,Iran,8974
  5. Novel Diagnostics and Therapeutics Research Group, Institute of Biotechnology, Ferdowsi University of Mashhad, 917794 Mashhad,Iran,8974
  6. Stem Cell and Regenerative Medicine Research Group, Iranian Academic Center for Education, Culture and Research (ACECR), Khorasan Razavi Branch, 917751 Mashhad,Iran,376
- 作者简介：
- 基金信息：
- DOI：10.1016/j.gendis.2022.11.025
  CLC：
- Published：2024，
  
  Published Online：1 January 2024，
扫描看全文
Ebrahim H. Maleki, Ahmad Reza Bahrami, Maryam M. Matin. Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance. [J]. Genes & Diseases 1(1):189-204(2024)
DOI：

Ebrahim H. Maleki, Ahmad Reza Bahrami, Maryam M. Matin. Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance. [J]. Genes & Diseases 1(1):189-204(2024) DOI： 10.1016/j.gendis.2022.11.025.

摘要

Abstract

Intra-tumor heterogeneity is now arguably one of the most-studied topics in tumor biology

as it represents a major obstacle to effective cancer treatment. Since tumor cells are highly diverse at genetic

epigenetic

and phenotypic levels

intra-tumor heterogeneity can be assumed as an important contributing factor to the nullification of chemotherapeutic effects

and recurrence of the tumor. Based on the role of heterogeneous subpopulations of cancer cells with varying cell-cycle dynamics and behavior during cancer progression and treatment; herein

we aim to establish a comprehensive definition for adaptation of neoplastic cells against therapy. We discuss two parallel and yet distinct subpopulations of tumor cells that play pivotal roles in reducing the effects of chemotherapy: “resistant” and “tolerant” populations. Furthermore

this review also highlights the impact of the quiescent phase of the cell cycle as a survival mechanism for cancer cells. Beyond understanding the mechanisms underlying the quiescence

it provides an insightful perspective on cancer stem cells (CSCs) and their dual and intertwined functions based on their cell cycle state in response to treatment. Moreover

CSCs

epithelial–mesenchymal transformed cells

circulating tumor cells (CTCs)

and disseminated tumor cells (DTCs)

which are mostly in a quiescent state of the cell cycle are proved to have multiple biological links and can be implicated in our viewpoint of cell cycle heterogeneity in tumors. Overall

increasing our knowledge of cell cycle heterogeneity is a key to identifying new therapeutic solutions

and this emerging concept may provide us with new opportunities to prevent the dreadful cancer recurrence.

关键词

Keywords

Cancer stem cells (CSCs)CarcinomaCell cycle heterogeneityQuiescenceTherapy resistanceTherapy toleranceTumor dormancy

references

1 K. Santos-de-Frutos, N. DjouderWhen dormancy fuels tumour relapse Commun Biol, 4 (1) (2021), p. 747

2 Z. Momenimovahed, A. Tiznobaik, S. Taheri, et al.Ovarian cancer in the world: epidemiology and risk factors Int J Womens Health, 11 (2019), pp. 287-299

3 L. Yang, H.J. Xie, Y.Y. Li, et al.Molecular mechanisms of platinum-based chemotherapy resistance in ovarian cancer (Review) Oncol Rep, 47 (4) (2022), p. 82

4 R.D. Mahmood, R.D. Morgan, R.J. Edmondson, et al.First-line management of advanced high-grade serous ovarian cancer Curr Oncol Rep, 22 (6) (2020), p. 64

5 E.H. Maleki, A.R. Bahrami, H. Sadeghian, et al.Discovering the structure–activity relationships of different O-prenylated coumarin derivatives as effective anticancer agents in human cervical cancer cells Toxicol In Vitro, 63 (2020), Article 104745

6 H. Uramoto, F. TanakaRecurrence after surgery in patients with NSCLC Transl Lung Cancer Res, 3 (4) (2014), pp. 242-249

7 D. O'Connor, K. Sibson, M. Caswell, et al.Early UK experience in the use of clofarabine in the treatment of relapsed and refractory paediatric acute lymphoblastic leukaemia Br J Haematol, 154 (4) (2011), pp. 482-485

8 G. Housman, S. Byler, S. Heerboth, et al.Drug resistance in cancer: an overview Cancers (Basel), 6 (3) (2014), pp. 1769-1792

9 F. Lüönd, S. Tiede, G. ChristoforiBreast cancer as an example of tumour heterogeneity and tumour cell plasticity during malignant progression Br J Cancer, 125 (2) (2021), pp. 164-175

10 N. AsliMolecular dissection of intra-tumoral heterogeneity in human epithelial carcinoma J Stem Cell Res Med, 1 (2016)

11 S.J. Altschuler, L.F. WuCellular heterogeneity: do differences make a difference? Cell, 141 (4) (2010), pp. 559-563

12 W.M. ElsasserOutline of a theory of cellular heterogeneity Proc Natl Acad Sci U S A, 81 (16) (1984), pp. 5126-5129

13 P.C. NowellThe clonal evolution of tumor cell populations Science, 194 (4260) (1976), pp. 23-28

14 P.R. Prasetyanti, J.P. MedemaIntra-tumor heterogeneity from a cancer stem cell perspective Mol Cancer, 16 (1) (2017), p. 41

15 N. El-Sayes, A. Vito, K. MossmanTumor Heterogeneity: a great barrier in the age of cancer Immunotherapy Cancers (Basel), 13 (4) (2021), p. 806

16 D.A. Lawson, K. Kessenbrock, R.T. Davis, et al.Tumour heterogeneity and metastasis at single-cell resolution Nat Cell Biol, 20 (12) (2018), pp. 1349-1360

17 Y.C.S. Ramón, M. Sesé, C. Capdevila, et al.Clinical implications of intratumor heterogeneity: challenges and opportunities J Mol Med (Berl)., 98 (2) (2020), pp. 161-177

18 C. Turnquist, R.A. Watson, A. Protheroe, et al.Tumor heterogeneity: does it matter? Expert Rev Anticancer Ther, 19 (10) (2019), pp. 857-867

19 G. Lenz, G.R. Onzi, L.S. Lenz, et al.The origins of phenotypic heterogeneity in cancer Cancer Res, 82 (1) (2022), pp. 3-11

20 H. GomezHow heterogeneity drives tumor growth: a computational study Philos Trans A Math Phys Eng Sci, 378 (2171) (2020), Article 20190244

21 R.J. Giedt, P.D. Koch, R. WeisslederSingle cell analysis of drug distribution by intravital imaging PLoS One, 8 (4) (2013), Article e60988

22 A. Kreso, J.E. DickEvolution of the cancer stem cell model Cell Stem Cell, 14 (3) (2014), pp. 275-291

23 K. Jiang, M. Dong, C. Li, et al.Unraveling heterogeneity of tumor cells and microenvironment and its clinical implications for triple negative breast cancer Front Oncol, 11 (2021), p. 557477

24 R.M. Douglas, G.G. HaddadInvited Review: effect of oxygen deprivation on cell cycle activity: a profile of delay and arrest J Appl Physiol, 94 (5) (2003), pp. 2068-2083

25 L.S. Lenz, J.L. Faccioni, P.A. Bracco, et al.Cancer cell fitness is dynamic Cancer Res, 81 (4) (2021), pp. 1040-1051

26 D.R. Chittajallu, S. Florian, R.H. Kohler, et al.In vivo cell-cycle profiling in xenograft tumors by quantitative intravital microscopy Nat Methods, 12 (6) (2015), pp. 577-585

27 S. Yano, Y. Zhang, S. Miwa, et al.Spatial-temporal FUCCI imaging of each cell in a tumor demonstrates locational dependence of cell cycle dynamics and chemoresponsiveness Cell Cycle, 13 (13) (2014), pp. 2110-2119

28 J.A. Aguirre-GhisoModels, mechanisms and clinical evidence for cancer dormancy Nat Rev Cancer, 7 (11) (2007), pp. 834-846

29 P.E. Goss, A.F. ChambersDoes tumour dormancy offer a therapeutic target? Nat Rev Cancer, 10 (12) (2010), pp. 871-877

30 A.H. Kyle, J.H. Baker, A.I. MinchintonTargeting quiescent tumor cells via oxygen and IGF-I supplementation Cancer Res, 72 (3) (2012), pp. 801-809

31 K.A. Beaumont, D.S. Hill, S.M. Daignault, et al.Cell cycle phase-specific drug resistance as an escape mechanism of melanoma cells J Invest Dermatol, 136 (7) (2016), pp. 1479-1489

32 A.E. Granada, A. Jiménez, J. Stewart-Ornstein, et al.The effects of proliferation status and cell cycle phase on the responses of single cells to chemotherapy Mol Biol Cell, 31 (8) (2020), pp. 845-857

33 S. Yano, K. Takehara, H. Tazawa, et al.Cell-cycle-dependent drug-resistant quiescent cancer cells induce tumor angiogenesis after chemotherapy as visualized by real-time FUCCI imaging Cell Cycle, 16 (5) (2017), pp. 406-414

34 K. Dökümcü, R.M. FarahaniEvolution of resistance in cancer: a cell cycle Perspective Front Oncol, 9 (2019), p. 376

35 V. Rodríguez-Fanjul, R. Guerrero-López, B. Fernández-Varas, et al.Comparison of colorectal cancer stem cells and oxaliplatin-resistant cells unveils functional similarities Cells, 11 (3) (2022), p. 511

36 Y. Zhang, L.H. Rohde, H. WuInvolvement of nucleotide excision and mismatch repair mechanisms in double strand break repair Curr Genomics, 10 (4) (2009), pp. 250-258

37 M.A. Shah, G.K. SchwartzCell cycle-mediated drug resistance: an emerging concept in cancer therapy Clin Cancer Res, 7 (8) (2001), pp. 2168-2181

38 Powathil G. Investigating the development of chemotherapeutic drug resistance in cancer: a multiscale computational study. arXiv preprint arXiv:1407.0865, 2014.

39 A.C. Yeh, S. RamaswamyMechanisms of cancer cell dormancy--another hallmark of cancer? Cancer Res, 75 (23) (2015), pp. 5014-5022

40 B.D. Larsen, J. Benada, P.Y.K. Yung, et al.Cancer cells use self-inflicted DNA breaks to evade growth limits imposed by genotoxic stress Science, 376 (6592) (2022), pp. 476-483

41 J. Zhang, J. Si, L. Gan, et al.Research progress on therapeutic targeting of quiescent cancer cells Artif Cells Nanomed Biotechnol, 47 (1) (2019), pp. 2810-2819

42 W.N. Nik Nabil, Z. Xi, Z. Song, et al.Towards a framework for better understanding of quiescent cancer cells Cells, 10 (3) (2021), p. 562

43 A. Mitra, L. Mishra, S. LiEMT, CTCs and CSCs in tumor relapse and drug-resistance Oncotarget, 6 (13) (2015), pp. 10697-10711

44 L. Zhao, K. Zhang, H. He, et al.The relationship between mesenchymal stem cells and tumor dormancy Front Cell Dev Biol (2021), p. 9

45 S. AldossaryReview on pharmacology of cisplatin: clinical use, toxicity and mechanism of resistance of cisplatin Biomed Pharmacol J, 11 (2019), pp. 7-15

46 S. Dasari, S. Njiki, A. Mbemi, et al.Pharmacological effects of cisplatin combination with natural products in cancer chemotherapy Int J Mol Sci, 23 (3) (2022)

47 Y. Luo, J.D. LeversonNew opportunities in chemosensitization and radiosensitization: modulating the DNA-damage response Expert Rev Anticancer Ther, 5 (2) (2005), pp. 333-342

48 E. Tzamali, G. Tzedakis, V. SakkalisModeling how heterogeneity in cell cycle length affects cancer cell growth dynamics in response to treatment Front Oncol, 10 (2020), p. 1552

49 J. ZhaoCancer stem cells and chemoresistance: the smartest survives the raid Pharmacol Ther, 160 (2016), pp. 145-158

50 F.U. Vaidya, A. Sufiyan Chhipa, V. Mishra, et al.Molecular and cellular paradigms of multidrug resistance in cancer Cancer Rep, 5 (12) (2022), Article e1291

51 X. Chen, W. Zhang, W. Yang, et al.Acquired resistance for immune checkpoint inhibitors in cancer immunotherapy: challenges and prospects Aging, 14 (2) (2022), pp. 1048-1064

52 X. Wang, H. Zhang, X. ChenDrug resistance and combating drug resistance in cancer Cancer Drug Resist, 2 (2) (2019), pp. 141-160

53 T. Akhtarkhavari, A.R. Bahrami, M.M. MatinDownregulation of miR-21 as a promising strategy to overcome drug resistance in cancer Eur J Pharmacol, 932 (2022), Article 175233

54 T. Haider, V. Pandey, N. Banjare, et al.Drug resistance in cancer: mechanisms and tackling strategies Pharmacol Rep, 72 (5) (2020), pp. 1125-1151

55 G.G. Powathil, K.E. Gordon, L.A. Hill, et al.Modelling the effects of cell-cycle heterogeneity on the response of a solid tumour to chemotherapy: biological insights from a hybrid multiscale cellular automaton model J Theor Biol, 308 (2012), pp. 1-19

56 A.A. Cohen, N. Geva-Zatorsky, E. Eden, et al.Dynamic proteomics of individual cancer cells in response to a drug Science, 322 (5907) (2008), pp. 1511-1516

57 K.E. Gascoigne, S.S. TaylorCancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs Cancer Cell, 14 (2) (2008), pp. 111-122

58 A. Kreso, C.A. O'Brien, P. van Galen, et al.Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer Science, 339 (6119) (2013), pp. 543-548

59 P. Valent, D. Bonnet, R. De Maria, et al.Cancer stem cell definitions and terminology: the devil is in the details Nat Rev Cancer, 12 (11) (2012), pp. 767-775

60 M.V. BlagosklonnyTarget for cancer therapy: proliferating cells or stem cells Leukemia, 20 (3) (2006), pp. 385-391

61 T. Ryl, E.E. Kuchen, E. Bell, et al.Cell-cycle position of single MYC-driven cancer cells dictates their susceptibility to a chemotherapeutic drug Cell Syst, 5 (3) (2017), pp. 237-250 e238

62 Y. Sun, Y. Liu, X. Ma, et al.The influence of cell cycle regulation on chemotherapy Int J Mol Sci, 22 (13) (2021), p. 6923

63 S. Sheikhi-Mohammareh, A. Shiri, E.H. Maleki, et al.Synthesis of various derivatives of [1,3]Selenazolo[4,5-d]pyrimidine and exploitation of these heterocyclic systems as antibacterial, antifungal, and anticancer agents ChemistrySelect, 5 (32) (2020), pp. 10060-10066

64 M. Mollaei, Z.M. Hassan, F. Khorshidi, et al.Chemotherapeutic drugs: cell death- and resistance-related signaling pathways. Are they really as smart as the tumor cells? Transl Oncol, 14 (5) (2021), Article 101056

65 P. Bavi, S. Uddin, M. Ahmed, et al.Bortezomib stabilizes mitotic cyclins and prevents cell cycle progression via inhibition of UBE2C in colorectal carcinoma Am J Pathol, 178 (5) (2011), pp. 2109-2120

66 M. Motwani, T.M. Delohery, G.K. SchwartzSequential dependent enhancement of caspase activation and apoptosis by flavopiridol on paclitaxel-treated human gastric and breast cancer cells Clin Cancer Res, 5 (7) (1999), pp. 1876-1883

67 M.P.F. Damen, J. van Rheenen, C.L.G.J. ScheeleTargeting dormant tumor cells to prevent cancer recurrence FEBS J, 288 (21) (2021), pp. 6286-6303

68 P.H. O'FarrellQuiescence: early evolutionary origins and universality do not imply uniformity Philos Trans R Soc Lond B Biol Sci, 366 (1584) (2011), pp. 3498-3507

69 N. Urbán, T.H. CheungStem cell quiescence: the challenging path to activation Development, 148 (3) (2021), p. dev165084

70 A. Fiore, V.A. Spencer, H. Mori, et al.laminin-111 and the level of nuclear actin regulate epithelial quiescence via exportin-6 Cell Rep, 19 (10) (2017), pp. 2102-2115

71 S.L. Spencer, S.D. Cappell, F.C. Tsai, et al.The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit Cell, 155 (2) (2013), pp. 369-383

72 V.A. Spencer, S. Costes, J.L. Inman, et al.Depletion of nuclear actin is a key mediator of quiescence in epithelial cells J Cell Sci, 124 (Pt 1) (2011), pp. 123-132

73 J.R. Valcourt, J.M. Lemons, E.M. Haley, et al.Staying alive: metabolic adaptations to quiescence Cell Cycle, 11 (9) (2012), pp. 1680-1696

74 R. Kumari, P. JatMechanisms of Cellular Senescence: cell cycle arrest and senescence associated secretory phenotype Front Cell Dev Biol, 9 (2021)

75 A. Sebestyén, T. Dankó, D. Sztankovics, et al.The role of metabolic ecosystem in cancer progression — metabolic plasticity and mTOR hyperactivity in tumor tissues Cancer Metastasis Rev, 40 (4) (2021), pp. 989-1033

76 M.J. Considine, J.A. ConsidineOn the language and physiology of dormancy and quiescence in plants J Exp Bot, 67 (11) (2016), pp. 3189-3203

77 J. Campisi, F. d'Adda di FagagnaCellular senescence: when bad things happen to good cells Nat Rev Mol Cell Biol, 8 (9) (2007), pp. 729-740

78 F. Rodier, J. CampisiFour faces of cellular senescence J Cell Biol, 192 (4) (2011), pp. 547-556

79 Z. Mao, Z. Ke, V. Gorbunova, et al.Replicatively senescent cells are arrested in G1 and G2 phases Aging (Albany NY), 4 (6) (2012), pp. 431-435

80 C. Ye, X. Zhang, J. Wan, et al.Radiation-induced cellular senescence results from a slippage of long-term G2 arrested cells into G1 phase Cell Cycle (Georgetown, Tex), 12 (9) (2013), pp. 1424-1432

81 S. Sun, D. GreshamCellular quiescence in budding yeast Yeast (Chichester, England), 38 (1) (2021), pp. 12-29

82 L. Li, H. CleversCoexistence of quiescent and active adult stem cells in mammals Science, 327 (5965) (2010), pp. 542-545

83 K. Mohammad, P. Dakik, Y. Medkour, et al.Quiescence entry, maintenance, and exit in adult stem cells Int J Mol Sci, 20 (9) (2019), p. 2158

84 N.Y. Fu, A.C. Rios, B. Pal, et al.Identification of quiescent and spatially restricted mammary stem cells that are hormone responsive Nat Cell Biol, 19 (3) (2017), pp. 164-176

85 D. Walter, A. Lier, A. Geiselhart, et al.Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells Nature, 520 (7548) (2015), pp. 549-552

86 B.R. Pennycook, A.R. BarrRestriction point regulation at the crossroads between quiescence and cell proliferation FEBS Lett, 594 (13) (2020), pp. 2046-2060

87 E. ParrThe default state of the cell: quiescence or proliferation? Bioessays, 34 (1) (2012), pp. 36-37

88 M. Malumbres, M. BarbacidTo cycle or not to cycle: a critical decision in cancer Nat Rev Cancer, 1 (3) (2001), pp. 222-231

89 S.H. Lee, T. Reed-Newman, S. Anant, et al.Regulatory role of quiescence in the biological function of cancer stem cells Stem Cell Rev Rep, 16 (6) (2020), pp. 1185-1207

90 A.P.Z.P. Fiore, PdF. Ribeiro, A. Bruni-CardosoSleeping beauty and the microenvironment enchantment: microenvironmental regulation of the proliferation-quiescence decision in normal tissues and in cancer development Front Cell Dev Biol, 6 (2018), p. 59

91 K. Chen, C. Zhang, S. Ling, et al.The metabolic flexibility of quiescent CSC: implications for chemotherapy resistance Cell Death Dis, 12 (9) (2021), p. 835

92 J. DittmerMechanisms governing metastatic dormancy in breast cancer Semin Cancer Biol, 44 (2017), pp. 72-82

93 M.H. ManjiliTumor dormancy and relapse: from a natural byproduct of evolution to a disease state Cancer Res, 77 (10) (2017), pp. 2564-2569

94 X.-L. Gao, M. Zhang, Y.-L. Tang, et al.Cancer cell dormancy: mechanisms and implications of cancer recurrence and metastasis Onco Targets Ther, 10 (2017), pp. 5219-5228

95 D. Lu, S. Chen, X. Tan, et al.Fra-1 promotes breast cancer chemosensitivity by driving cancer stem cells from dormancy Cancer Res, 72 (2012), pp. 3451-3456

96 D.A. Nathanson, B. Gini, J. Mottahedeh, et al.Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA Science, 343 (6166) (2014), pp. 72-76

97 T. Shimizu, E. Sugihara, S. Yamaguchi-Iwai, et al.IGF2 preserves osteosarcoma cell survival by creating an autophagic state of dormancy that protects cells against chemotherapeutic stress Cancer Res, 74 (22) (2014), pp. 6531-6541

98 N. Almog, L. Ma, C. Schwager, et al.Consensus micro RNAs governing the switch of dormant tumors to the fast-growing angiogenic phenotype PLoS One, 7 (8) (2012), Article e44001

99 K. Ameri, E. MaltepeHIGD1A-mediated dormancy and tumor survival Mol Cell Oncol, 2 (4) (2015), Article e1030537

100 T. Lyu, N. Jia, J. Wang, et al.Expression and epigenetic regulation of angiogenesis-related factors during dormancy and recurrent growth of ovarian carcinoma Epigenetics, 8 (12) (2013), pp. 1330-1346

101 G. Fluegen, A. Avivar-Valderas, Y. Wang, et al.Phenotypic heterogeneity of disseminated tumour cells is preset by primary tumour hypoxic microenvironments Nat Cell Biol, 19 (2) (2017), pp. 120-132

102 S.V. Sharma, D.Y. Lee, B. Li, et al.A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations Cell, 141 (1) (2010), pp. 69-80

103 A. Der Vartanian, M. Quétin, S. Michineau, et al.PAX3 confers functional heterogeneity in skeletal muscle stem cell responses to environmental stress Cell Stem Cell, 24 (6) (2019), pp. 958-973 e959

104 A. Scaramozza, D. Park, S. Kollu, et al.Lineage tracing reveals a subset of reserve muscle stem cells capable of clonal expansion under stress Cell Stem Cell, 24 (6) (2019), pp. 944-957 e945

105 Z. Yu, T.G. Pestell, M.P. Lisanti, R.G. PestellCancer stem cells Int J Biochem Cell Biol, 44 (12) (2012), pp. 2144-2151

106 E. Batlle, H. CleversCancer stem cells revisited Nat Med, 23 (10) (2017), pp. 1124-1134

107 B. Aramini, V. Masciale, G. Grisendi, et al.Dissecting tumor growth: the role of cancer stem cells in drug resistance and recurrence Cancers (Basel), 14 (4) (2022), p. 976

108 N.A. Dallas, L. Xia, F. Fan, et al.Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition Cancer Res, 69 (5) (2009), pp. 1951-1957

109 V. Levina, A.M. Marrangoni, R. DeMarco, et al.Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties PLoS One, 3 (8) (2008), Article e3077

110 M.F. Clarke, J.E. Dick, P.B. Dirks, et al.Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells Cancer Res, 66 (19) (2006), pp. 9339-9344

111 S. Shigdar, Y. Li, S. Bhattacharya, et al.Inflammation and cancer stem cells Cancer Lett, 345 (2) (2014), pp. 271-278

112 S. Beyes, N.G. Bediaga, A. ZippoAn Epigenetic Perspective on intra-tumour heterogeneity: novel insights and new challenges from multiple fields Cancers (Basel), 13 (19) (2021), p. 4969

113 P. Dalerba, R.W. Cho, M.F. ClarkeCancer stem cells: models and concepts Annu Rev Med, 58 (2007), pp. 267-284

114 J.E. TroskoThe concept of “cancer stem cells” in the context of classic carcinogenesis hypotheses and experimental findings Life (Basel), 11 (12) (2021), p. 1308

115 D. Bonnet, J.E. DickHuman acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat Med, 3 (7) (1997), pp. 730-737

116 M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, et al.Prospective identification of tumorigenic breast cancer cells Proc Natl Acad Sci U S A, 100 (7) (2003), pp. 3983-3988

117 A.T. Collins, P.A. Berry, C. Hyde, et al.Prospective identification of tumorigenic prostate cancer stem cells Cancer Res, 65 (23) (2005), pp. 10946-10951

118 A. Eramo, F. Lotti, G. Sette, et al.Identification and expansion of the tumorigenic lung cancer stem cell population Cell Death Differ, 15 (3) (2008), pp. 504-514

119 P.C. Hermann, S.L. Huber, T. Herrler, et al.Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer Cell Stem Cell, 1 (3) (2007), pp. 313-323

120 S. Ma, K.W. Chan, T.K. Lee, et al.Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations Mol Cancer Res, 6 (7) (2008), pp. 1146-1153

121 C.A. O’Brien, A. Pollett, S. Gallinger, et al.A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature, 445 (7123) (2007), pp. 106-110

122 M.E. Prince, R. Sivanandan, A. Kaczorowski, et al.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) (2007), pp. 973-978

123 S.K. Singh, C. Hawkins, I.D. Clarke, et al.Identification of human brain tumor initiating cells Nature, 432 (7015) (2004), pp. 396-401

124 S. Takaishi, T. Okumura, S. Tu, et al.Identification of gastric cancer stem cells using the cell surface marker CD44 Stem Cells, 27 (5) (2009), pp. 1006-1020

125 S. Zhang, C. Balch, M.W. Chan, et al.Identification and characterization of ovarian cancer-initiating cells from primary human tumors Cancer Res, 68 (11) (2008), pp. 4311-4320

126 N. Cirillo, C. Wu, S.S. PrimeHeterogeneity of cancer stem cells in tumorigenesis, metastasis, and resistance to antineoplastic treatment of head and neck tumours Cells, 10 (11) (2021), p. 3068

127 S. FuldaTargeting apoptosis for anticancer therapy Semin Cancer Biol, 31 (2015), pp. 84-88

128 J.L. Koff, S. Ramachandiran, L. Bernal-MizrachiA time to kill: targeting apoptosis in cancer Int J Mol Sci, 16 (2) (2015), pp. 2942-2955

129 A.R. Safa, K.E. PollokTargeting the anti-apoptotic protein c-FLIP for cancer therapy Cancers (Basel), 3 (2) (2011), pp. 1639-1671

130 K.D. Tang, M.T. LingTargeting drug-resistant prostate cancer with dual PI3K/mTOR inhibition Curr Med Chem, 21 (26) (2014), pp. 3048-3056

131 F. Zang, X. Wei, X. Leng, et al.C-FLIP(L) contributes to TRAIL resistance in HER2-positive breast cancer Biochem Biophys Res Commun, 450 (1) (2014), pp. 267-273

132 J.L. Dembinski, S. KraussCharacterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma Clin Exp Metastasis, 26 (7) (2009), pp. 611-623

133 W.C. Lin, N. Rajbhandari, C. Liu, et al.Dormant cancer cells contribute to residual disease in a model of reversible pancreatic cancer Cancer Res, 73 (6) (2013), pp. 1821-1830

134 M.Q. Gao, Y.P. Choi, S. Kang, et al.CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells Oncogene, 29 (18) (2010), pp. 2672-2680

135 A. Roesch, M. Fukunaga-Kalabis, E.C. Schmidt, et al.A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth Cell, 141 (4) (2010), pp. 583-594

136 A. Zeuner, F. Francescangeli, P. Contavalli, et al.Elimination of quiescent/slow-proliferating cancer stem cells by Bcl-XL inhibition in non-small cell lung cancer Cell Death Differ, 21 (12) (2014), pp. 1877-1888

137 M.S. Holtz, S.J. Forman, R. BhatiaNonproliferating CML CD34+ progenitors are resistant to apoptosis induced by a wide range of proapoptotic stimuli Leukemia, 19 (6) (2005), pp. 1034-1041

138 S. Ebinger, E.Z. Ozdemir, C. Ziegenhain, et al.Characterization of rare, dormant, and therapy-resistant cells in acute lymphoblastic leukemia Cancer Cell, 30 (6) (2016), pp. 849-862

139 J. Chen, Y. Li, T.S. Yu, et al.A restricted cell population propagates glioblastoma growth after chemotherapy Nature, 488 (7412) (2012), pp. 522-526

140 X. Lan, D.J. Jorg, F.M.G. Cavalli, et al.Fate mapping of human glioblastoma reveals an invariant stem cell hierarchy Nature, 549 (7671) (2017), pp. 227-232

141 D.H. Liang, D.S. Choi, J.E. Ensor, et al.The autophagy inhibitor chloroquine targets cancer stem cells in triple negative breast cancer by inducing mitochondrial damage and impairing DNA break repair Cancer Lett, 376 (2) (2016), pp. 249-258

142 S. Kabraji, X. Sole, Y. Huang, et al.AKT1(low) quiescent cancer cells persist after neoadjuvant chemotherapy in triple negative breast cancer Breast Cancer Res, 19 (1) (2017), p. 88

143 M.L. De Angelis, F. Francescangeli, F. La Torre, et al.Stem cell plasticity and dormancy in the development of cancer therapy resistance Front Oncol, 9 (2019), p. 626

144 I. Puig, S.P. Tenbaum, I. Chicote, et al.TET2 controls chemoresistant slow-cycling cancer cell survival and tumor recurrence J Clin Invest, 128 (9) (2018), pp. 3887-3905

145 S.M. Tu, M.R. Estecio, S.H. Lin, et al.Stem cell theory of cancer: rude awakening or bad dream from cancer dormancy? Cancers (Basel), 14 (3) (2022), p. 655

146 J. Bajaj, E. Diaz, T. ReyaStem cells in cancer initiation and progression J Cell Biol, 219 (1) (2020), Article e201911053

147 N. Hirata, S. Yamada, T. Shoda, et al.Sphingosine-1-phosphate promotes expansion of cancer stem cells via S1PR3 by a ligand-independent Notch activation Nat Commun, 5 (2014), p. 4806

148 A.R. SafaDrug and apoptosis resistance in cancer stem cells: a puzzle with many pieces Cancer Drug Resist, 5 (4) (2022), pp. 850-872

149 G. Manic, A. Sistigu, F. Corradi, et al.Replication stress response in cancer stem cells as a target for chemotherapy Semin Cancer Biol, 53 (2018), pp. 31-41

150 M. Maugeri-Sacca, M. Bartucci, R. De MariaDNA damage repair pathways in cancer stem cells Mol Cancer Ther, 11 (8) (2012), pp. 1627-1636

151 H. Moreira, A. Szyjka, J. Grzesik, et al.Celastrol and resveratrol modulate SIRT genes expression and exert anticancer activity in colon cancer cells and cancer stem-like cells Cancers (Basel), 14 (6) (2022), p. 1372

152 P.K. Mandal, C. Blanpain, D.J. RossiDNA damage response in adult stem cells: pathways and consequences Nat Rev Mol Cell Biol, 12 (3) (2011), pp. 198-202

153 I. Vitale, G. Manic, R. De Maria, et al.DNA damage in stem cells Mol Cell, 66 (3) (2017), pp. 306-319

154 S. Bao, Q. Wu, R.E. McLendon, et al.Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature, 444 (7120) (2006), pp. 756-760

155 S. Facchino, M. Abdouh, W. Chatoo, et al.BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery J Neurosci, 30 (30) (2010), pp. 10096-10111

156 W. Chen, J. Dong, J. Haiech, et al.Cancer stem cell quiescence and plasticity as major challenges in cancer therapy Stem Cells Int, 2016 (2016), Article 1740936

157 S. Banerjee, A. Nomura, V. Sangwan, et al.CD133+ tumor initiating cells in a syngenic murine model of pancreatic cancer respond to Minnelide Clin Cancer Res, 20 (9) (2014), pp. 2388-2399

158 Y.C. Lim, T.L. Roberts, B.W. Day, et al.A role for homologous recombination and abnormal cell-cycle progression in radioresistance of glioma-initiating cells Mol Cancer Ther, 11 (9) (2012), p. 1863

159 M. Yuan, C.G. Eberhart, M. KaiRNA binding protein RBM14 promotes radio-resistance in glioblastoma by regulating DNA repair and cell differentiation Oncotarget, 5 (9) (2014), pp. 2820-2826

160 A. Desai, B. Webb, S.L. GersonCD133+ cells contribute to radioresistance via altered regulation of DNA repair genes in human lung cancer cells Radiother Oncol, 110 (3) (2014), pp. 538-545

161 D.M. Janzen, E. Tiourin, J.A. Salehi, et al.An apoptosis-enhancing drug overcomes platinum resistance in a tumour-initiating subpopulation of ovarian cancer Nat Commun, 6 (2015), p. 7956

162 F. Karimi-Busheri, A. Rasouli-Nia, J.R. Mackey, et al.Senescence evasion by MCF-7 human breast tumor-initiating cells Breast Cancer Res, 12 (3) (2010), p. R31

163 M. Venere, P. Hamerlik, Q. Wu, et al.Therapeutic targeting of constitutive PARP activation compromises stem cell phenotype and survival of glioblastoma-initiating cells Cell Death Differ, 21 (2) (2014), pp. 258-269

164 B. Ffrench, C. Gasch, K. Hokamp, et al.CD10(-)/ALDH(-) cells are the sole cisplatin-resistant component of a novel ovarian cancer stem cell hierarchy Cell Death Dis, 8 (10) (2017), p. e3128

165 W.K. Yu, Z. Wang, C.C. Fong, et al.Chemoresistant lung cancer stem cells display high DNA repair capability to remove cisplatin-induced DNA damage Br J Pharmacol, 174 (4) (2017), pp. 302-313

166 T.H. Cheung, T.A. RandoMolecular regulation of stem cell quiescence Nat Rev Mol Cell Biol, 14 (6) (2013), pp. 329-340

167 C.G. Ferreira, C. Tolis, G. Giacconep53 and chemosensitivity Ann Oncol, 10 (9) (1999), pp. 1011-1021

168 M.S. Sosa, P. Bragado, J.A. Aguirre-GhisoMechanisms of disseminated cancer cell dormancy: an awakening field Nat Rev Cancer, 14 (9) (2014), pp. 611-622

169 F. Crea, N.R. Nur Saidy, C.C. Collins, et al.The epigenetic/noncoding origin of tumor dormancy Trends Mol Med, 21 (4) (2015), pp. 206-211

170 C. Lagadec, S. Meignan, E. Adriaenssens, et al.TrkA overexpression enhances growth and metastasis of breast cancer cells Oncogene, 28 (18) (2009), pp. 1960-1970

171 X. Huang, G. Gan, X. Wang, et al.The HGF-MET axis coordinates liver cancer metabolism and autophagy for chemotherapeutic resistance Autophagy, 15 (7) (2019), pp. 1258-1279

172 S. Moeckel, K. LaFrance, J. Wetsch, et al.ATF4 contributes to autophagy and survival in sunitinib treated brain tumor initiating cells (BTICs) Oncotarget, 10 (3) (2019), pp. 368-382

173 R. Ojha, N.M. Leli, A. Onorati, et al.ER translocation of the MAPK pathway drives therapy resistance in BRAF-mutant melanoma Cancer Discov, 9 (3) (2019), pp. 396-415

174 J. Ou, Y. Peng, W. Yang, et al.ABHD5 blunts the sensitivity of colorectal cancer to fluorouracil via promoting autophagic uracil yield Nat Commun, 10 (1) (2019), p. 1078

175 J.D. Rabinowitz, E. WhiteAutophagy and metabolism Science, 330 (6009) (2010), pp. 1344-1348

176 S. GhaffariLysosomal regulation of metabolism in quiescent hematopoietic stem cells: more than just autophagy Cell Stem Cell, 28 (3) (2021), pp. 374-377

177 F. Nazio, M. Bordi, V. Cianfanelli, et al.Autophagy and cancer stem cells: molecular mechanisms and therapeutic applications Cell Death Differ, 26 (4) (2019), pp. 690-702

178 K. Rothe, V. Porter, X. JiangCurrent outlook on autophagy in human leukemia: foe in cancer stem cells and drug resistance, friend in new therapeutic interventions Int J Mol Sci, 20 (3) (2019), p. 461

179 A.G. Smith, K.F. MacleodAutophagy, cancer stem cells and drug resistance J Pathol, 247 (5) (2019), pp. 708-718

180 H. Jo, Y. Jia, K.K. Subramanian, et al.Cancer cell-derived clusterin modulates the phosphatidylinositol 3’-kinase-Akt pathway through attenuation of insulin-like growth factor 1 during serum deprivation Mol Cell Biol, 28 (13) (2008), pp. 4285-4299

181 X. Wang, J. Lee, C. XieAutophagy regulation on cancer stem cell maintenance, metastasis, and therapy resistance Cancers (Basel), 14 (2) (2022), p. 381

182 K.L. Harper, M.S. Sosa, D. Entenberg, et al.Mechanism of early dissemination and metastasis in Her2(+) mammary cancer Nature, 540 (7634) (2016), pp. 588-592

183 H. Hosseini, M.M.S. Obradovic, M. Hoffmann, et al.Early dissemination seeds metastasis in breast cancer Nature, 540 (7634) (2016), pp. 552-558

184 D.A. Lawson, N.R. Bhakta, K. Kessenbrock, et al.Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells Nature, 526 (7571) (2015), pp. 131-135

185 M. Werner-Klein, S. Scheitler, M. Hoffmann, et al.Genetic alterations driving metastatic colony formation are acquired outside of the primary tumour in melanoma Nat Commun, 9 (1) (2018), p. 595

186 K.D. Seely, A.D. Morgan, L.D. Hagenstein, et al.Bacterial involvement in progression and metastasis of colorectal neoplasia Cancers (Basel)., 14 (4) (2022), p. 1019

187 K. Weidenfeld, D. BarkanEMT and stemness in tumor dormancy and outgrowth: are they intertwined processes? Front Oncol, 8 (2018), p. 381

188 A.F. Chambers, A.C. Groom, I.C. MacDonaldDissemination and growth of cancer cells in metastatic sites Nat Rev Cancer, 2 (8) (2002), pp. 563-572

189 K. Pantel, R.H. BrakenhoffDissecting the metastatic cascade Nat Rev Cancer, 4 (6) (2004), pp. 448-456

190 A. Dasgupta, A.R. Lim, C.M. GhajarCirculating and disseminated tumor cells: harbingers or initiators of metastasis? Mol Oncol, 11 (1) (2017), pp. 40-61

191 O. Hen, D. BarkanDormant disseminated tumor cells and cancer stem/progenitor-like cells: similarities and opportunities Semin Cancer Biol, 60 (2020), pp. 157-165

192 M.A. Nieto, R.Y. Huang, R.A. Jackson, J.P. ThieryEMT: 2016 Cell, 166 (1) (2016), pp. 21-45

193 T. BrabletzTo differentiate or not--routes towards metastasis Nat Rev Cancer, 12 (6) (2012), pp. 425-436

194 S. Ohashi, M. Natsuizaka, S. Naganuma, et al.A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors Cancer Res, 71 (21) (2011), pp. 6836-6847

195 H. Uramoto, T. Iwata, T. Onitsuka, et al.Epithelial-mesenchymal transition in EGFR-TKI acquired resistant lung adenocarcinoma Anticancer Res, 30 (7) (2010), pp. 2513-2517

196 M. Xie, L. Zhang, C.S. He, et al.Activation of Notch-1 enhances epithelial-mesenchymal transition in gefitinib-acquired resistant lung cancer cells J Cell Biochem, 113 (5) (2012), pp. 1501-1513

197 K. Polyak, R.A. WeinbergTransitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits Nat Rev Cancer, 9 (4) (2009), pp. 265-273

198 H. Zhang, A. Steed, M. Co, et al.Cancer stem cells, epithelial-mesenchymal transition, ATP and their roles in drug resistance in cancer Cancer Drug Resist, 4 (2021), pp. 684-709

199 P.W. Derksen, X. Liu, F. Saridin, et al.Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis Cancer Cell, 10 (5) (2006), pp. 437-449

200 F.G. GiancottiMechanisms governing metastatic dormancy and reactivation Cell, 155 (4) (2013), pp. 750-764

201 G. Kallergi, M.A. Papadaki, E. Politaki, et al.Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients Breast Cancer Res, 13 (3) (2011), p. R59

202 M. Mego, S.A. Mani, B.N. Lee, et al.Expression of epithelial-mesenchymal transition-inducing transcription factors in primary breast cancer: the effect of neoadjuvant therapy Int J Cancer, 130 (4) (2012), pp. 808-816

203 S. Lamouille, J. Xu, R. DerynckMolecular mechanisms of epithelial-mesenchymal transition Nat Rev Mol Cell Biol, 15 (3) (2014), pp. 178-196

204 J.M. Lee, S. Dedhar, R. Kalluri, et al.The epithelial-mesenchymal transition: new insights in signaling, development, and disease J Cell Biol, 172 (7) (2006), pp. 973-981

205 B. Aktas, M. Tewes, T. Fehm, et al.Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients Breast Cancer Res, 11 (4) (2009), p. R46

206 V.S. LeBleu, J.T. O’Connell, K.N. Gonzalez Herrera, et al.PGC-1alpha mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis Nat Cell Biol, 16 (10) (2014), pp. 992-1003

207 L.A. Byers, L. Diao, J. Wang, et al.An epithelial-mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance Clin Cancer Res, 19 (1) (2013), pp. 279-290

208 M. Yu, A. Bardia, B.S. Wittner, et al.Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition Science, 339 (6119) (2013), pp. 580-584

209 P. Carlson, A. Dasgupta, C.A. Grzelak, et al.Targeting the perivascular niche sensitizes disseminated tumour cells to chemotherapy Nat Cell Biol, 21 (2) (2019), pp. 238-250

210 N. Ogba, N.G. Manning, B.S. Bliesner, et al.Luminal breast cancer metastases and tumor arousal from dormancy are promoted by direct actions of estradiol and progesterone on the malignant cells Breast Cancer Res, 16 (6) (2014), p. 489

211 J.A. Aguirre-Ghiso, M.S. SosaEmerging topics on disseminated cancer cell dormancy and the paradigm of metastasis Annu Rev Cancer Biol, 2 (1) (2018), pp. 377-393

212 B. Polzer, C.A. KleinMetastasis awakening: the challenges of targeting minimal residual cancer Nat Med, 19 (3) (2013), pp. 274-275

213 C.M. GhajarMetastasis prevention by targeting the dormant niche Nat Rev Cancer, 15 (4) (2015), pp. 238-247

214 C. Holohan, S. Van Schaeybroeck, D.B. Longley, et al.Cancer drug resistance: an evolving paradigm Nat Rev Cancer, 13 (10) (2013), pp. 714-726

215 B. Abderrahman, V.C. JordanRethinking extended adjuvant antiestrogen therapy to increase survivorship in breast cancer JAMA Oncol, 4 (1) (2018), pp. 15-16

216 A. Recasens, L. MunozTargeting cancer cell dormancy Trends Pharmacol Sci, 40 (2) (2019), pp. 128-141

217 L. García-Prat, M. Martínez-Vicente, E. Perdiguero, et al.Autophagy maintains stemness by preventing senescence Nature, 529 (7584) (2016), pp. 37-42

218 N. Kudlova, J.B. De Sanctis, M. HajduchCellular senescence: molecular targets, biomarkers, and senolytic drugs Int J Mol Sci, 23 (8) (2022), p. 4168

219 E.C. Filippi-Chiela, MmBe Silva, M.P. Thomé, et al.Single-cell analysis challenges the connection between autophagy and senescence induced by DNA damage Autophagy, 11 (7) (2015), pp. 1099-1113

220 M.A. Essers, A. TrumppTargeting leukemic stem cells by breaking their dormancy Mol Oncol, 4 (5) (2010), pp. 443-450

221 Y. Saito, N. Uchida, S. Tanaka, et al.Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML Nat Biotechnol, 28 (3) (2010), pp. 275-280

222 R.J. Vanner, M. Remke, M. Gallo, et al.Quiescent sox2(+) cells drive hierarchical growth and relapse in sonic hedgehog subgroup medulloblastoma Cancer Cell, 26 (1) (2014), pp. 33-47

查看原文

Views

下载量

CSCD

Alert me when the article has been cited

提交

Tools