The role of autophagy in the cross-talk between epithelial-mesenchymal transitioned tumor cells and cancer stem-like cells

Molecular Cancer

Volumn 16, Issue 1, 2017, Pages

  Marcucci, Fabrizio ^a   Ghezzi, Pietro ^b   Rumio, Cristiano ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Autophagic; Cycling; Metastasis; Resistance; Tumor microenvironment; Tumor propagation

Indexed keywords

AUTOPHAGY; CANCER STEM CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SELF-RENEWAL; CELL SUBPOPULATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NONHUMAN; REVIEW; CELL COMMUNICATION; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY;

AUTOPHAGY; CELL COMMUNICATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASTIC STEM CELLS;

EID: 85011025989     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-016-0573-8     Document Type: Review

References (84)

1. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871-90.
2. Kalluri R. EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Invest. 2009;119:1417-9.
3. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9:265-73.
4. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010;29:4741-51.
5. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-11.
6. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313-23.
7. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells - what challenges do they pose? Nat Rev Drug Discov. 2014;13:497-512.
8. Avgustinova A, Benitah SA. The epigenetics of tumour initiation: cancer stem cells and their chromatin. Curr Opin Genet Dev. 2016;36:8-15.
9. Shukla S, Meeran SM. Epigenetics of cancer stem cells: Pathways and therapeutics. Biochim Biophys Acta. 2014;1840:3494-502.
10. Greaves M, Maley CC. Clonal evolution in cancer. Nature. 2012;481:306-13.
11. Wallin JJ, Guan J, Edgar KA, Zhou W, Francis R, Torres AC, et al. Active PI3K pathway causes an invasive phenotype which can be reversed or promoted by blocking the pathway at divergent nodes. PLoS One. 2012;7:e36402.
12. Lin Y, Dong C, Zhou BP. Epigenetic regulation of EMT: the Snail story. Curr Pharm Des. 2014;20:1698-705.
13. Korkaya H, Liu S, Wicha MS. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J Clin Invest. 2011;121:3804-9.
14. Marcucci F, Bellone M, Caserta CA, Corti A. Pushing tumor cells towards a malignant phenotype. Stimuli from the microenvironment, intercellular communications and alternative roads. Int J Cancer. 2014;135:1265-76.
15. Marcucci F, Stassi G, De Maria R. Epithelial-mesenchymal transition: a new target in anticancer drug discovery. Nat Rev Drug Discov. 2016;15:311-25.
16. Asiedu MK, Beauchamp-Perez FD, Ingle JN, Behrens MD, Radisky DC, Knutson KL. AXL induces epithelial to mesenchymal transition and regulates the function of breast cancer stem cells. Oncogene. 2014;33:1316-24.
17. Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, et al. Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update. Nat Rev Clin Oncol. 2015;12:445-64.
18. Lim YC, Kang HJ, Moon JH. C-Met pathway promotes self-renewal and tumorigenecity of head and neck squamous cell carcinoma stem-like cell. Oral Oncol. 2014;50:633-9.
19. Sette G, Salvati V, Memeo L, Fecchi K, Colarossi C, Di Matteo P, et al. EGFR inhibition abrogates leiomyosarcoma cell chemoresistance through inactivation of survival pathways and impairment of CSC potential. PLoS One. 2012;7:e46891.
20. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES, et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc Natl Acad Sci U S A. 2010;107:21737-42.
21. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704-15.
22. Keysar SB, Le PN, Miller B, Jackson BC, Eagles JR, Nieto C, et al. Regulation of head and neck squamous cancer stem cells by PI3K and SOX2. J Natl Cancer Inst. 2016. doi: 10.1093/jnci/djw189.
23. Lu H, Clauser KR, Tam WL, Fröse J, Ye X, Eaton EN, et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol. 2014;16:1105-17.
24. Thakur R, Trivedi R, Rastogi N, Singh M, Mishra DP. Inhibition of STAT3, FAK and Src mediated signaling reduces cancer stem cell load, tumorigenic potential and metastasis in breast cancer. Sci Rep. 2015;5:10194.
25. Zhang L, Zhang L, Li H, Ge C, Zhao F, Tian H, et al. CXCL3 contributes to CD133(+) CSCs maintenance and forms a positive feedback regulation loop with CD133 in HCC via Erk1/2 phosphorylation. Sci Rep. 2016;6:27426.
26. Zhang Z, Duan Q, Zhao H, Liu T, Wu H, Shen Q, et al. Gemcitabine treatment promotes pancreatic cancer stemness through the Nox/ROS/NF-ΚB/STAT3 signaling cascade. Cancer Lett. 2016;382:53-63.
27. Marcucci F, Rumio C, Lefoulon F. Anti-cancer stem-like cell compounds in clinical development - an overview and critical appraisal. Front Oncol. 2016;6:115.
28. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645-59.
29. Kuo SZ, Blair KJ, Rahimy E, Kiang A, Abhold E, Fan JB, et al. Salinomycin induces cell death and differentiation in head and neck squamous cell carcinoma stem cells despite activation of epithelial-mesenchymal transition and Akt. BMC Cancer. 2012;12:556.
30. Ocaña OH, Córcoles R, Fabra A, Moreno-Bueno G, Acloque H, Vega S, et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell. 2012;22:709-24.
31. Celià-Terrassa T, Meca-Cortés O, Mateo F, De Paz Martínez A, Rubio N, Arnal-Estapé A, et al. Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J Clin Invest. 2010;122:1849-68.
32. Gammon L, Biddle A, Heywood HK, Johannessen AC, Mackenzie IC. Sub-sets of cancer stem cells differ intrinsically in their patterns of oxygen metabolism. PLoS One. 2013;8:e62493.
33. Biddle A, Liang X, Gammon L, Fazil B, Harper LJ, Emich H, et al. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res. 2011;71:5317-26.
34. Pomp V, Leo C, Mauracher A, Korol D, Guo W, Varga Z. Differential expression of epithelial-mesenchymal transition and stem cell markers in intrinsic subtypes of breast cancer. Breast Cancer Res Treat. 2015;154:45-55.
35. Tan TZ, Miow QH, Miki Y, Noda T, Mori S, Huang RY, et al. Epithelial-mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer patients. EMBO Mol Med. 2014;6:1279-93.
36. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132:27-42.
37. Ojha R, Bhattacharyya S, Singh SK. Autophagy in cancer stem cells: A potential link between chemoresistance, recurrence, and metastasis. Biores Open Access. 2015;4:97-108.
38. Altman JK, Szilard A, Goussetis DJ, Sassano A, Colamonici M, Gounaris E, et al. Autophagy is a survival mechanism of acute myeloid leukemia precursors during dual mTORC2/mTORC1 targeting. Clin Cancer Res. 2014;20:2400-9.
39. Rausch V, Liu L, Apel A, Rettig T, Gladkich J, Labsch S, et al. Autophagy mediates survival of pancreatic tumour-initiating cells in a hypoxic microenvironment. J Pathol. 2012;227:325-35.
40. Yang MC, Wang HC, Hou YC, Tung HL, Chiu TJ, Shan YS. Blockade of autophagy reduces pancreatic cancer stem cell activity and potentiates the tumoricidal effect of gemcitabine. Mol Cancer. 2015;14:179.
41. Rothe K, Lin H, Lin KB, Leung A, Wang HM, Malekesmaeili M, et al. The core autophagy protein ATG4B is a potential biomarker and therapeutic target in CML stem/progenitor cells. Blood. 2014;123:3622-34.
42. Chen H, Luo Z, Dong L, Tan Y, Yang J, Feng G, et al. Wang, CD133/prominin-1-mediated autophagy and glucose uptake beneficial for hepatoma cell survival. PLoS One. 2013;8:e56878.
43. Catalano M, D'Alessandro G, Lepore F, Corazzari M, Caldarola S, Valacca C, et al. Autophagy induction impairs migration and invasion by reversing EMT in glioblastoma cells. Mol Oncol. 2015;9:1612-25.
44. Wang F, Li H, Yan XG, Zhou ZW, Yi ZG, He ZX, et al. Alisertib induces cell cycle arrest and autophagy and suppresses epithelial-to-mesenchymal transition involving PI3K/Akt/mTOR and sirtuin 1-mediated signaling pathways in human pancreatic cancer cells. Drug Des Devel Ther. 2015;9:575-601.
45. Xu LZ, Long ZJ, Peng F, Liu Y, Xu J, Wang C, et al. Aurora kinase a suppresses metabolic stress-induced autophagic cell death by activating mTOR signaling in breast cancer cells. Oncotarget. 2014;5:7498-511.
46. Qin W, Li C, Zheng W, Guo Q, Zhang Y, Kang M, et al. Inhibition of autophagy promotes metastasis and glycolysis by inducing ROS in gastric cancer cells. Oncotarget. 2015;6:39839-54.
47. Qiang L, Zhao B, Ming M, Wang N, He T-C, Hwang S, et al. Regulation of cell proliferation and migration by p62 through stabilization of Twist1. Proc Natl Acad Sci U S A. 2014;111:9241-6.
48. Grassi G, Di Caprio G, Santangelo L, Fimia GM, Cozzolino AM, Komatsu M, et al. Autophagy regulates hepatocyte identity and epithelial-to-mesenchymal and mesenchymal-to-epithelial transitions promoting Snail degradation. Cell Death Dis. 2015;6:e1880.
49. Lv Q, Wang W, Xue J, Hua F, Mu R, Lin H, et al. DEDD interacts with PI3KC3 to activate autophagy and attenuate epithelial-mesenchymal transition in human breast cancer. Cancer Res. 2012;72:3238-50.
50. Lock R, Kenific CM, Leidal AM, Salas E, Debnath J. Autophagy-dependent production of secreted factors facilitates oncogenic RAS-driven invasion. Cancer Discov. 2014;4:466-79.
51. + pancreatic cancer stem-like cells during intermittent hypoxia. Oncol Rep. 2014;32:935-42.
52. Poleszczuk J, Hahnfeldt P, Enderling H. Evolution and phenotypic selection of cancer stem cells. PLoS Comput Biol. 2015;11:e1004025.
53. Yang T, Rycaj K, Liu ZM, Tang DG. Cancer stem cells: constantly evolving and functionally heterogeneous therapeutic targets. Cancer Res. 2014;74:2922-7.
54. Roth S, Fodde R. Quiescent stem cells in intestinal homeostasis and cancer. Cell Commun Adhes. 2011;18:33-44.
55. Tang DG. Understanding cancer stem cell heterogeneity and plasticity. Cell Res. 2012;22:457-72.
56. Leth-Larsen R, Terp MG, Christensen AG, Elias D, Kühlwein T, Jensen ON, et al. Functional heterogeneity within the CD44 high human breast cancer stem cell-like compartment reveals a gene signature predictive of distant metastasis. Mol Med. 2012;18:1109-21.
57. high prostate cancer stem cells. Oncol Lett. 2014;7:2103-9.
58. Mukhopadhyay P, Farrell T, Sharma G, McGuire TR, O'Kane B, Sharp JG. Heterogeneity of functional properties of clone 66 murine breast cancer cells expressing various stem cell phenotypes. PLoS One. 2013;8:e78725.
59. Zhang B, Li L, Ho Y, Li M, Marcucci G, Tong W, et al. Heterogeneity of leukemia-initiating capacity of chronic myelogenous leukemia stem cells. J Clin Invest. 2016;126:975-91.
60. Liu S, Cong Y, Wang D, Sun Y, Deng L, Liu Y, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports. 2013;2:78-91.
61. Levina V, Marrangoni AM, DeMarco R, Gorelik E, Lokshin AE. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS One. 2008;3:e3077.
62. da Silva-Diz V, Simón-Extremera P, Bernat-Peguera A, de Sostoa J, Urpí M, Penín RM, et al. Cancer stem-like cells act via distinct signaling pathways in promoting late stages of malignant progression. Cancer Res. 2016;76:1245-59.
63. Tam WL, Lu H, Buikhuisen J, Soh BS, Lim E, Reinhardt F, et al. Protein kinase C α is a central signaling node and therapeutic target for breast cancer stem cells. Cancer Cell. 2013;24:347-64.
64. Wilkinson S, O'Prey J, Fricker M, Ryan KM. Hypoxia-selective macroautophagy and cell survival signaled by autocrine PDGFR activity. Genes Dev. 2009;23:1283-8.
65. Oshimori N, Oristain D, Fuchs E. TGF-β promotes heterogeneity and drug resistance in squamous cell carcinoma. Cell. 2015;160:963-76.
66. Ruscetti M, Quach B, Dadashian EL, Mulholland DJ, Wu H. Tracking and functional characterization of epithelial-mesenchymal transition and mesenchymal tumor cells during prostate cancer metastasis. Cancer Res. 2015;75:2749-59.
67. Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sánchez N, Marchesini M, et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature. 2014;514:628-32.
68. Ciavardelli D, Rossi C, Barcaroli D, Volpe S, Consalvo A, Zucchelli M, et al. Breast cancer stem cells rely on fermentative glycolysis and are sensitive to 2-deoxyglucose treatment. Cell Death Dis. 2014;5:e1336.
69. Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, et al. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015;527:525-30.
70. Fischer KR, Durrans A, Lee S, Sheng J, Li F, Wong STC, Choi H, et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature. 2015;527:472-6.
71. Klevebring D, Rosin G, Ma R, Lindberg J, Czene K, Kere J, et al. Sequencing of breast cancer stem cell populations indicates a dynamic conversion between differentiation states in vivo. Breast Cancer Res. 2014;16:R72.
72. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial - mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 2012;22:725-36.
73. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med. 2009;15:1010-2.
74. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell. 2011;146:633-44.
75. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med. 2013;19:1438-49.
76. Gurney A, Axelrod F, Bond CJ, Cain J, Chartier C, Donigan L, et al. Wnt pathway inhibition via the targeting of Frizzled receptors results in decreased growth and tumorigenicity of human tumors. Proc Natl Acad Sci U S A. 2012;109:11717-22.
77. Smith DC, Eisenberg PD, Manikhas G, Chugh R, Gubens MA, Stagg RJ, et al. A phase I dose escalation and expansion study of the anticancer stem cell agent demcizumab (anti-DLL4) in patients with previously treated solid tumors. Clin Cancer Res. 2014;20:6295-303.
78. Storm EE, Durinck S, de Sousa e Melo F, Tremayne J, Kljavin N, Tan C, et al. Targeting PTPRK-RSPO3 colon tumours promotes differentiation and loss of stem-cell function. Nature. 2016;529:97-100.
79. Kantara C, O'Connell M, Sarkar S, Moya S, Ullrich R, Singh P. Curcumin promotes autophagic survival of a subset of colon cancer stem cells, which are ablated by DCLK1-siRNA. Cancer Res. 2014;74:2487-98.
80. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012;488:522-6.
81. Yuan S, Wang F, Chen G, Zhang H, Feng L, Wang L, et al. Effective elimination of cancer stem cells by a novel drug combination strategy. Stem Cells. 2013;31:23-34.
82. Balic A, Sørensen MD, Trabulo SM, Sainz Jr B, Cioffi M, Vieira CR, et al. Chloroquine targets pancreatic cancer stem cells via inhibition of CXCR4 and hedgehog signaling. Mol Cancer Ther. 2014;13:1758-71.
83. Firat E, Weyerbrock A, Gaedicke S, Grosu AL, Niedermann G. Chloroquine or chloroquine-PI3K/Akt pathway inhibitor combinations strongly promote gamma-irradiation-induced cell death in primary stem-like glioma cells. PLoS One. 2012;7:e47357.
84. Vakifahmetoglu-Norberg H, Xia H-g, Yuan J. Pharmacologic agents targeting autophagy. J Clin Invest. 2015;125:5-13.