Cancer stem cells as key drivers of tumour progression

Journal of Biomedical Science - Tập 25 Số 1 - 2018
Ain Zubaidah Ayob1, Thamil Selvee Ramasamy1
1Stem Cell Biology Laboratory, Department of Molecular Medicine, Faculty of Medicine, University of Malaya, 50603, Wilayah Persekutuan Kuala Lumpur, Malaysia

Tóm tắt

Từ khóa


Tài liệu tham khảo

Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.

Beck B, Blanpain C. Unravelling cancer stem cell potential. Nat Rev Cancer. 2013;13:727–38.

Weiswald LB, Bellet D, Dangles-Marie V. Spherical cancer models in tumor biology. Neoplasia. 2015;17:1–15.

Sell S. On the stem cell origin of cancer. Am J Pathol. 2010;176:2584–94.

Pisco AO, Huang S. Non-genetic cancer cell plasticity and therapy-induced stemness in tumour relapse: ‘what does not kill me strengthens me’. Br J Cancer. 2015;112:1725–32.

Biddle A, Gammon L, Liang X, Costea DE, Mackenzie IC. Phenotypic plasticity determines cancer stem cell therapeutic resistance in oral squamous cell carcinoma. EBioMedicine. 2016;4:138–45.

Ye J, Wu D, Wu P, Chen Z, Huang J. The cancer stem cell niche: cross talk between cancer stem cells and their microenvironment. Tumour Biol. 2014;35:3945–51.

Moolgavkar SH, Luebeck EG. Multistage carcinogenesis and the incidence of human cancer. Genes Chromosom Cancer. 2003;38:302–6.

Hatina J. The dynamics of cancer stem cells. Neoplasma. 2012;59:700–7.

Tysnes BB, Bjerkvig R. Cancer initiation and progression: involvement of stem cells and the microenvironment. Biochimica et Biophysica Acta (BBA)-reviews on. Cancer. 2007;1775:283–97.

Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–8.

Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci. 2003;100:3983–8.

Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401.

Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov. 2009;8:806–23.

Boumahdi S, Driessens G, Lapouge G, Rorive S, Nassar D, Le Mercier M, Delatte B, Caauwe A, Lenglez S, Nkusi E. SOX2 controls tumour initiation and cancer stem-cell functions in squamous-cell carcinoma. Nature. 2014;511:246–50.

Demaria S, Pikarsky E, Karin M, Coussens LM, Chen Y-C, El-Omar EM, Trinchieri G, Dubinett SM, Mao JT, Szabo E. Cancer and inflammation: promise for biological therapy. J Immunother. 2010;33:335.

Lu H, Ouyang W, Huang C. Inflammation, a key event in cancer development. Mol Cancer Res. 2006;4:221–33.

Blaylock RL. Cancer microenvironment, inflammation and cancer stem cells: a hypothesis for a paradigm change and new targets in cancer control. Surg Neurol Int. 2015;6:92.

Morales-Sánchez A, Fuentes-Pananá EM. Human viruses and cancer. Viruses. 2014;6:4047–79.

Ohnishi S, Ma N, Thanan R, Pinlaor S, Hammam O, Murata M, Kawanishi S. DNA damage in inflammation-related carcinogenesis and cancer stem cells. Oxidative Med Cell Longev. 2013;2013:9.

Okada F. Inflammation and free radicals in tumor development and progression. Redox Rep. 2002;7:357–68.

Ma N, Thanan R, Kobayashi H, Hammam O, Wishahi M, El Leithy T, Hiraku Y, Amro E-K, Oikawa S, Ohnishi S. Nitrative DNA damage and Oct3/4 expression in urinary bladder cancer with Schistosomahaematobium infection. Biochem Biophys Res Commun. 2011;414:344–9.

Thanan R, Murata M, Ma N, Hammam O, Wishahi M, El Leithy T, Hiraku Y, Oikawa S, Kawanishi S. Nuclear localization of COX-2 in relation to the expression of stemness markers in urinary bladder cancer. Mediat Inflamm. 2012;2012:8.

Logan CM, Giordano A, Puca A, Cassone M. Prostaglandin E2: at the crossroads between stem cell development, inflammation and cancer. Cancer Biol Ther. 2007;6:1517–20.

Kawanishi S, Hiraku Y, Oikawa S. Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging. Mut Res. 2001;488:65–76.

Thanan R, Pairojkul C, Pinlaor S, Khuntikeo N, Wongkham C, Sripa B, Ma N, Vaeteewoottacharn K, Furukawa A, Kobayashi H. Inflammation-related DNA damage and expression of CD133 and Oct3/4 in cholangiocarcinoma patients with poor prognosis. Free Radic Biol Med. 2013;65:1464–72.

Lau EY-T, Ho NP-Y, Lee TK-W. Cancer Stem Cells and Their Microenvironment: Biology and Therapeutic Implications. Stem Cells Int. 2017;2017:11.

Zhao J. Cancer stem cells and Chemoresistance: the smartest survives the raid. Pharmacol Ther. 2016;160:145–58.

Chen X, Liao R, Li D, Sun J. Induced cancer stem cells generated by radiochemotherapy and their therapeutic implications. Oncotarget. 2017;8:17301–12.

Cabarcas SM, Mathews LA, Farrar WL. The cancer stem cell niche—there goes the neighborhood? Int J Cancer. 2011;129:2315–27.

Lee G, Hall III RR, Ahmed AU. Cancer Stem Cells: Cellular Plasticity, Niche, and its Clinical Relevance. J Stem Cell Res Ther. 2016;6:363.

Quante M, Tu SP, Tomita H, Gonda T, Wang SS, Takashi S, Baik GH, Shibata W, Diprete B, Betz KS, Friedman R, Varro A, Tycko B, Wang TC. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell. 2011;19:257–72.

Forsberg K, Valyi-Nagy I, Heldin C-H, Herlyn M, Westermark B. Platelet-derived growth factor (PDGF) in oncogenesis: development of a vascular connective tissue stroma in xenotransplanted human melanoma producing PDGF-BB. Proc Natl Acad Sci. 1993;90:393–7.

Giannoni E, Bianchini F, Masieri L, Serni S, Torre E, Calorini L, Chiarugi P. Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness. Cancer Res. 2010;70:6945–56.

Hawinkels L, Paauwe M, Verspaget H, Wiercinska E, Van Der Zon J, Van Der Ploeg K, Koelink P, Lindeman J, Mesker W, Ten Dijke P. Interaction with colon cancer cells hyperactivates TGF-β signaling in cancer-associated fibroblasts. Oncogene. 2014;33:97–107.

Strutz F, Zeisberg M, Hemmerlein B, Sattler B, Hummel K, Becker V, Müller GA. Basic fibroblast growth factor expression is increased in human renal fibrogenesis and may mediate autocrine fibroblast proliferation. Kidney Int. 2000;57:1521–38.

Kalluri R. The biology and function of fibroblasts in cancer. Nat Rev Cancer. 2016;16:582–98.

Valenti G, Quinn HM, Heynen G, Lan L, Holland JD, Vogel R, Wulf-Goldenberg A, Birchmeier W. Cancer stem cells regulate cancer-associated fibroblasts via activation of hedgehog signaling in mammary gland tumors. Cancer Res. 2017;77:2134–47.

Vermeulen L, Felipe De Sousa EM, Van Der Heijden M, Cameron K, De Jong JH, Borovski T, Tuynman JB, Todaro M, Merz C, Rodermond H. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol. 2010;12:468–76.

Lau Eunice Yuen T, Lo J, Cheng Bowie Yik L, Ma Mark Kin F, Lee Joyce Man F, Ng Johnson Kai Y, Chai S, Lin Chi H, Tsang Suk Y, Ma S, Ng Irene Oi L, Lee Terence Kin W. Cancer-associated fibroblasts regulate tumor-initiating cell plasticity in hepatocellular carcinoma through c-met/FRA1/HEY1 signaling. Cell Rep. 2016;15:1175–89.

Soon PSH, Kim E, Pon CK, Gill AJ, Moore K, Spillane AJ, Benn DE, Baxter RC. Breast cancer-associated fibroblasts induce epithelial-to-mesenchymal transition in breast cancer cells. Endocr Relat Cancer. 2013;20:1–12.

Yu Y, Xiao C, Tan L, Wang Q, Li X, Feng Y. Cancer-associated fibroblasts induce epithelial–mesenchymal transition of breast cancer cells through paracrine TGF-β signalling. Br J Cancer. 2014;110:724.

Nishimura K, Semba S, Aoyagi K, Sasaki H, Yokozaki H. Mesenchymal stem cells provide an advantageous tumor microenvironment for the restoration of cancer stem cells. Pathobiology. 2012;79:290–306.

Davis H, Irshad S, Bansal M, Rafferty H, Boitsova T, Bardella C, Jaeger E, Lewis A, Freeman-Mills L, Giner FC, Rodenas-Cuadrado P, Mallappa S, Clark S, Thomas H, Jeffery R, Poulsom R, Rodriguez-Justo M, Novelli M, Chetty R, Silver A, Sansom OJ, Greten FR, Wang LM, East JE, Tomlinson I, Leedham SJ. Aberrant epithelial GREM1 expression initiates colonic tumorigenesis from cells outside the stem cell niche. Nat Med. 2014;21:62–70.

Cuiffo BG, Campagne A, Bell GW, Lembo A, Orso F, Lien EC, Bhasin MK, Raimo M, Hanson SE, Marusyk A, El-Ashry D, Hematti P, Polyak K, Mechta-Grigoriou F, Mariani O, Volinia S, Vincent-Salomon A, Taverna D, Karnoub AE. MSC-regulated microRNAs converge on the transcription factor FOXP2 and promote breast cancer metastasis. Cell Stem Cell. 2014;15:762–74.

Houthuijzen J, Daenen L, Roodhart J, Voest E. The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression. Br J Cancer. 2012;106:1901–6.

Lopatina T, Gai C, Deregibus MC, Kholia S, Camussi G. Cross talk between cancer and mesenchymal stem cells through extracellular vesicles carrying nucleic acids. Front Oncol. 2016;6:125.

Bliss SA, Sinha G, Sandiford OA, Williams LM, Engelberth DJ, Guiro K, Isenalumhe LL, Greco SJ, Ayer S, Bryan M, Kumar R, Ponzio NM, Rameshwar P. Mesenchymal stem cell-derived exosomes stimulate cycling quiescence and early breast cancer dormancy in bone marrow. Cancer Res. 2016;76:5832–44.

Vallabhaneni KC, Penfornis P, Dhule S, Guillonneau F, Adams KV, Mo YY, Xu R, Liu Y, Watabe K, Vemuri MC, Pochampally R. Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites. Oncotarget. 2015;6:4953–67.

Bruno S, Collino F, Deregibus MC, Grange C, Tetta C, Camussi G. Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev. 2012;22:758–71.

Zhang X, Tu H, Yang Y, Fang L, Wu Q, Li J. Mesenchymal stem cell-derived extracellular vesicles: roles in tumor growth, progression, and drug resistance. Stem Cells Int. 2017;2017:12.

Du T, Ju G, Wu S, Cheng Z, Cheng J, Zou X, Zhang G, Miao S, Liu G, Zhu Y. Microvesicles derived from human Wharton’s jelly mesenchymal stem cells promote human renal cancer cell growth and aggressiveness through induction of hepatocyte growth factor. PLoS One. 2014;9:e96836.

Li T, Zhang C, Ding Y, Zhai W, Liu K, Bu F, Tu T, Sun L, Zhu W, Zhou F. Umbilical cord-derived mesenchymal stem cells promote proliferation and migration in MCF-7 and MDA-MB-231 breast cancer cells through activation of the ERK pathway. Oncol Rep. 2015;34:1469–77.

Wang W, Zhong W, Yuan J, Yan C, Hu S, Tong Y, Mao Y, Hu T, Zhang B, Song G. Involvement of Wnt/β-catenin signaling in the mesenchymal stem cells promote metastatic growth and chemoresistance of cholangiocarcinoma. Oncotarget. 2015;6:42276.

Kitamura T, Qian BZ, Pollard JW. Immune cell promotion of metastasis. Nat Rev Immunol. 2015;15:73–86.

Raggi C, Correnti M, Sica A, Andersen JB, Cardinale V, Alvaro D, Chiorino G, Forti E, Glaser S, Alpini G. Cholangiocarcinoma stem-like subset shapes tumor-initiating niche by educating associated macrophages. J Hepatol. 2017;66:102–15.

Zhou W, Susan QK, Zhi H, William F, Xiaoguang F, Jeremy P, Ling W, Andrew ES, Roger EM, Xiaoxia L, Jeremy NR, Shideng. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol. 2015;17:170–82.

Ostuni R, Kratochvill F, Murray PJ, Natoli G. Macrophages and cancer: from mechanisms to therapeutic implications. Trends Immunol. 2015;36:229–39.

Williams CB, Yeh ES, Soloff AC. Tumor-associated macrophages: unwitting accomplices in breast cancer malignancy. NPJ Breast Cancer. 2016;2:15025.

Su MJ, Aldawsari H, Amiji M. Pancreatic cancer cell exosome-mediated macrophage reprogramming and the role of MicroRNAs 155 and 125b2 transfection using nanoparticle delivery systems. Sci Rep. 2016;6:30110.

Braicu C, Tomuleasa C, Monroig P, Cucuianu A, Berindan-Neagoe I, Calin GA. Exosomes as divine messengers: are they the Hermes of modern molecular oncology? Cell Death Differ. 2014;22:34.

Zheng P, Chen L, Yuan X, Luo Q, Liu Y, Xie G, Ma Y, Shen L. Exosomal transfer of tumor-associated macrophage-derived miR-21 confers cisplatin resistance in gastric cancer cells. J Exp Clin Cancer Res. 2017;36:53.

Semenza GL. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Ann Rev Pathol. 2014;9:47–71.

Semenza GL. The hypoxic tumor microenvironment: a driving force for breast cancer progression. Biochimica et Biophysica Acta (BBA)-molecular. Cell Res. 2016;1863:382–91.

Höckel M, Vorndran B, Schlenger K, Baußmann E, Knapstein PG. Tumor oxygenation: a new predictive parameter in locally advanced cancer of the uterine cervix. Gynecol Oncol. 1993;51:141–9.

Brizel DM, Scully SP, Harrelson JM, Layfield LJ, Bean JM, Prosnitz LR, Dewhirst MW. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res. 1996;56:941–3.

Carnero A, Lleonart M. The hypoxic microenvironment: a determinant of cancer stem cell evolution. Inside Cell. 2016;1:96–105.

Bennewith KL, Durand RE. Quantifying transient hypoxia in human tumor xenografts by flow cytometry. Cancer Res. 2004;64:6183–9.

Brurberg KG, Thuen M, Ruud E-BM, Rofstad EK. Fluctuations in p O2 in irradiated human melanoma xenografts. Radiat Res. 2006;165:16–25.

Azuma T, Yao S, Zhu G, Flies AS, Flies SJ, Chen L. B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells. Blood. 2008;111:3635–43.

Li Z, Rich JN, Hypoxia and hypoxia inducible factors in cancer stem cell maintenance, in Diverse Effects of Hypoxia on Tumor Progression. Berlin, Heidelberg: Springer; 2010. p. 21-30.

Anido J, Sáez-Borderías A, Gonzàlez-Juncà A, Rodón L, Folch G, Carmona MA, Prieto-Sánchez RM, Barba I, Martínez-Sáez E, Prudkin L. TGF-β receptor inhibitors target the CD44 high/Id1 high glioma-initiating cell population in human glioblastoma. Cancer Cell. 2010;18:655–68.

Scheel C, Eaton EN, Li SH-J, Chaffer CL, Reinhardt F, Kah K-J, Bell G, Guo W, Rubin J, Richardson AL. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell. 2011;145:926–40.

Scheel C, Weinberg RA. Phenotypic plasticity and epithelial-mesenchymal transitions in cancer and normal stem cells? Int J Cancer. 2011;129:2310–4.

Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, Baek JH, Semenza GL. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor–null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res. 2006;66:2725–31.

Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene. 2008;27:6958–69.

Liu X, He L, Stensaas L, Dinger B, Fidone S. Adaptation to chronic hypoxia involves immune cell invasion and increased expression of inflammatory cytokines in rat carotid body. Am J Phys Lung Cell Mol Phys. 2009;296:L158–L66.

Liu F, Liu Y, Lui VC, Lamb JR, Tam PK, Chen Y. Hypoxia modulates lipopolysaccharide induced TNF-α expression in murine macrophages. Exp Cell Res. 2008;314:1327–36.

Pavlides S, Tsirigos A, Vera I, Flomenberg N, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG. Loss of stromal caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the “reverse Warburg effect”: a transcriptional informatics analysis with validation. Cell Cycle. 2010;9:2201–19.

Kitamura T, Qian B-Z, Soong D, Cassetta L, Noy R, Sugano G, et al. CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J Exp Med. 2015;212:1043.

Butler JM, Kobayashi H, Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer. 2010;10:138–46.

Campos MS, Neiva KG, Meyers KA, Krishnamurthy S, Nor JE. Endothelial derived factors inhibit anoikis of head and neck cancer stem cells. Oral Oncol. 2011;48:26–32.

Liang Z, Brooks J, Willard M, Liang K, Yoon Y, Kang S, Shim H. CXCR4/CXCL12 axis promotes VEGF-mediated tumor angiogenesis through Akt signaling pathway. Biochem Biophys Res Commun. 2007;359:716–22.

Galan-Moya EM, Le Guelte A, Lima Fernandes E, Thirant C, Dwyer J, Bidere N, Couraud PO, Scott MG, Junier MP, Chneiweiss H, Gavard J. Secreted factors from brain endothelial cells maintain glioblastoma stem-like cell expansion through the mTOR pathway. EMBO Rep. 2011;12:470–6.

Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, Tozzi F, Sceusi E, Zhou Y, Tachibana I, Maru DM, Hawke DH, Rak J, Mani SA, Zweidler-McKay P, Ellis LM. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell. 2013;23:171–85.

Yan GN, Yang L, Lv YF, Shi Y, Shen LL, Yao XH, Guo QN, Zhang P, Cui YH, Zhang X. Endothelial cells promote stem-like phenotype of glioma cells through activating the hedgehog pathway. J Pathol. 2014;234:11–22.

Sun L, Pan J, Yu L, Liu H, Shu X, Sun L, Lou J, Yang Z, Ran Y. Tumor endothelial cells promote metastasis and cancer stem cell-like phenotype through elevated Epiregulin in esophageal cancer. Am J Cancer Res. 2016;6:2277–88.

Krishnamurthy S, Warner KA, Dong Z, Imai A, Nor C, Ward BB, Helman JI, Taichman RS, Bellile EL, McCauley LK, Polverini PJ, Prince ME, Wicha MS, Nor JE. Endothelial interleukin-6 defines the tumorigenic potential of primary human cancer stem cells. Stem Cells. 2014;32:2845–57.

Xu J, Zhang C, He Y, Wu H, Wang Z, Song W, Li W, He W, Cai S, Zhan W. Lymphatic endothelial cell-secreted CXCL1 stimulates lymphangiogenesis and metastasis of gastric cancer. Int J Cancer. 2012;130:787–97.

Johnson LA, Jackson DG. Inflammation-induced secretion of CCL21 in lymphatic endothelium is a key regulator of integrin-mediated dendritic cell transmigration. Int Immunol. 2010;22:839–49.

Heusschen R, van Gink M, Griffioen AW, Thijssen VL. MicroRNAs in the tumor endothelium: novel controls on the angioregulatory switchboard. Biochim Biophys Acta. 2010;1805:87–96.

Sigurdsson V, Hilmarsdottir B, Sigmundsdottir H, Fridriksdottir AJ, Ringner M, Villadsen R, Borg A, Agnarsson BA, Petersen OW, Magnusson MK, Gudjonsson T. Endothelial induced EMT in breast epithelial cells with stem cell properties. PLoS One. 2011;6:e23833.

Guo J, Liu C, Zhou X, Xu X, Deng L, Li X, et al. Conditioned Medium from Malignant Breast Cancer Cells Induces an EMT-Like Phenotype and an Altered N-Glycan Profile in Normal Epithelial MCF10A Cells. Int J Mol Sci. 2017;18:1528.

Folkins C, Shaked Y, Man S, Tang T, Lee CR, Zhu Z, Hoffman RM, Kerbel RS. Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1. Cancer Res. 2009;69:7243–51.

Bussolati B, Grange C, Sapino A, Camussi G. Endothelial cell differentiation of human breast tumour stem/progenitor cells. J Cell Mol Med. 2009;13:309–19.

Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 2010;468:824–8.

Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010;468:829–33.

Soda Y, Marumoto T, Friedmann-Morvinski D, Soda M, Liu F, Michiue H, Pastorino S, Yang M, Hoffman RM, Kesari S. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci. 2011;108:4274–80.

Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol. 2012;196:395–406.

Novak K. Measuring the matrix. Nat Rev Cancer. 2003;3:394–5.

Rupp T, Langlois B, Koczorowska MM, Radwanska A, Sun Z, Hussenet T, Lefebvre O, Murdamoothoo D, Arnold C, Klein A. Tenascin-C orchestrates glioblastoma angiogenesis by modulation of pro-and anti-angiogenic signaling. Cell Rep. 2016;17:2607–19.

Xia S, Lal B, Tung B, Wang S, Goodwin CR, Laterra J. Tumor microenvironment tenascin-C promotes glioblastoma invasion and negatively regulates tumor proliferation. Neuro-Oncology. 2015;18:507–17.

Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massague J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17:867–74.

Chiquet-Ehrismann R, Orend G, Chiquet M, Tucker RP, Midwood KS. Tenascins in stem cell niches. Matrix Biol. 2014;37:112–23.

Nie S, Gurrea M, Zhu J, Thakolwiboon S, Heth JA, Muraszko KM, Fan X, Lubman DM. Tenascin-C: a novel candidate marker for cancer stem cells in glioblastoma identified by tissue microarrays. J Proteome Res. 2015;14:814–22.

Fukunaga-Kalabis M, Martinez G, Nguyen T-TK, Kim D, Santiago-Walker A, Roesch A, Herlyn M. Tenascin-C promotes melanoma progression by maintaining the ABCB5-positive side population. Oncogene. 2010;29:6115.

Jachetti E, Caputo S, Mazzoleni S, Brambillasca CS, Parigi SM, Grioni M, Piras IS, Restuccia U, Calcinotto A, Freschi M, Bachi A, Galli R, Bellone M. Tenascin-C protects cancer stem-like cells from immune surveillance by arresting T-cell activation. Cancer Res. 2015;75:2095–108.

Farace C, Oliver JA, Melguizo C, Alvarez P, Bandiera P, Rama AR, Malaguarnera G, Ortiz R, Madeddu R, Prados J. Microenvironmental modulation of Decorin and Lumican in Temozolomide-resistant glioblastoma and neuroblastoma cancer stem-like cells. PLoS One. 2015;10:e0134111.

Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature. 2004;432:332–7.

Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121:335–48.

Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W, Yamauchi M, Gasser DL, Weaver VM. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 2009;139:891–906.

Lopez JI, Kang I, You WK, McDonald DM, Weaver VM. In situ force mapping of mammary gland transformation. Integr Biol (Camb). 2011;3:910–21.

Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer. 2005;5:275–84.

Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, Pickell K, Aguilar J, Lazetic S, Smith-Berdan S, Clarke MF, Hoey T, Lewicki J, Gurney AL. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One. 2008;3:e2428.

Abubaker K, Latifi A, Luwor R, Nazaretian S, Zhu H, Quinn MA, Thompson EW, Findlay JK, Ahmed N. Short-term single treatment of chemotherapy results in the enrichment of ovarian cancer stem cell-like cells leading to an increased tumor burden. Mol Cancer. 2013;12:24.

Taylor ST, Hickman JA, Dive C. Epigenetic determinants of resistance to etoposide regulation of Bcl-XL and Bax by tumor microenvironmental factors. J Natl Cancer Inst. 2000;92:18–23.

Maier S, Dahlstroem C, Haefliger C, Plum A, Piepenbrock C. Identifying DNA methylation biomarkers of cancer drug response. Am J Pharmacogenomics. 2005;5:223–32.

Dean M. ABC transporters, drug resistance, and cancer stem cells. J Mammary Gland Biol Neoplasia. 2009;14:3–9.

An Y, Ongkeko WM. ABCG2: the key to chemoresistance in cancer stem cells? Expert Opin Drug Metab Toxicol. 2009;5:1529–42.

Xu F, Wang F, Yang T, Sheng Y, Zhong T, Chen Y. Differential drug resistance acquisition to doxorubicin and paclitaxel in breast cancer cells. Cancer Cell Int. 2014;14:538.

Xu X, Chai S, Wang P, Zhang C, Yang Y, Yang Y, Wang K. Aldehyde dehydrogenases and cancer stem cells. Cancer Lett. 2015;369:50–7.

Wang YH, Scadden DT. Harnessing the apoptotic programs in cancer stem-like cells. EMBO Rep. 2015;16:1084–98.

Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.

Ramasamy TS, Ayob AZ, Myint HHL, Thiagarajah S, Amini F. Targeting colorectal cancer stem cells using curcumin and curcumin analogues: insights into the mechanism of the therapeutic efficacy. Cancer Cell Int. 2015;15:96.

Todaro M, Francipane MG, Medema JP, Stassi G. Colon cancer stem cells: promise of targeted therapy. Gastroenterology. 2010;138:2151–62.

Cheung TH, Rando TA. Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol. 2013;14:329–40.

Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010;140:62–73.

Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, Akita H, Takiuchi D, Hatano H, Nagano H. CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest. 2010;120:3326.

Deleyrolle LP, Harding A, Cato K, Siebzehnrubl FA, Rahman M, Azari H, Olson S, Gabrielli B, Osborne G, Vescovi A. Evidence for label-retaining tumour-initiating cells in human glioblastoma. Brain. 2011;134:1331–43.

Ishii A, Kimura T, Sadahiro H, Kawano H, Takubo K, Suzuki M, Ikeda E. Histological characterization of the tumorigenic “Peri-necrotic niche” harboring quiescent stem-like tumor cells in glioblastoma. PLoS One. 2016;11:e0147366.

Zeuner A. The secret life of quiescent cancer stem cells. Mol Cell Oncol. 2015;2:e968067.

Gao M, Choi Y, Kang S, Youn J, Cho N. CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene. 2010;29:2672–80.

Wu M, Fernandez N, Celebre A, Srikanth M, Kessler J, Karamchandani J, Das S. SC-35BMP signaling regulates a quiescent cancer stem cell phenotype responsible for treatment resistance in glioblastoma. Neuro Oncol. 2014;16:v204.

Wang H, Zhang G, Zhang H, Zhang F, Zhou B, Ning F, Wang HS, Cai SH, Du J. Acquisition of epithelial-mesenchymal transition phenotype and cancer stem cell-like properties in cisplatin-resistant lung cancer cells through AKT/beta-catenin/snail signaling pathway. Eur J Pharmacol. 2013;723:156–66.

Maseki S, Ijichi K, Tanaka H, Fujii M, Hasegawa Y, Ogawa T, Murakami S, Kondo E, Nakanishi H. Acquisition of EMT phenotype in the gefitinib-resistant cells of a head and neck squamous cell carcinoma cell line through Akt/GSK-3beta/snail signalling pathway. Br J Cancer. 2012;106:1196–204.

Gomez-Casal R, Bhattacharya C, Ganesh N, Bailey L, Basse P, Gibson M, Epperly M, Levina V. Non-small cell lung cancer cells survived ionizing radiation treatment display cancer stem cell and epithelial-mesenchymal transition phenotypes. Mol Cancer. 2013;12:94.

Tu C-C, Cheng L-H, Hsu H-H, Chen L-M, Lin Y-M, Chen M-C, Lee N-H, Tsai F-J, Huang C-Y, Wu W-J. Activation of snail and EMT-like signaling via the IKKαβ/NF-κB pathway in Apicidin-resistant HA22T hepatocellular carcinoma cells. Chin J Physiol. 2013;56:326–33.

Li J, Liu H, Yu J, Yu H. Chemoresistance to doxorubicin induces epithelial-mesenchymal transition via upregulation of transforming growth factor β signaling in HCT116 colon cancer cells. Mol Med Rep. 2015;12:192–8.

Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS, Ali S, Abbruzzese JL, Gallick GE, Sarkar FH. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res. 2009;69:2400–7.

Lee HH, Bellat V, Law B. Chemotherapy induces adaptive drug resistance and metastatic potentials via phenotypic CXCR4-expressing cell state transition in ovarian cancer. PLoS One. 2017;12:e0171044.

Hu X, Ghisolfi L, Keates AC, Zhang J, Xiang S, Lee DK, Li CJ. Induction of cancer cell stemness by chemotherapy. Cell Cycle. 2012;11:2691–8.

He K, Xu T, Xu Y, Ring A, Kahn M, Goldkorn A. Cancer cells acquire a drug resistant, highly tumorigenic, cancer stem-like phenotype through modulation of the PI3K/Akt/beta-catenin/CBP pathway. Int J Cancer. 2013;134:43–54.

Goldman A, Majumder B, Dhawan A, Ravi S, Goldman D, Kohandel M, Majumder PK, Sengupta S. Temporally sequenced anticancer drugs overcome adaptive resistance by targeting a vulnerable chemotherapy-induced phenotypic transition. Nat Commun. 2015;11:6139.

Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, Wong KK, Brandstetter K, Wittner B, Ramaswamy S, Classon M, Settleman J. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell. 2010;141:69–80.

Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.

Aguilar E, Marin de Mas I, Zodda E, Marin S, Morrish F, Selivanov V, Meca-Cortés Ó, Delowar H, Pons M, Izquierdo I. Metabolic reprogramming and dependencies associated with epithelial cancer stem cells independent of the epithelial-mesenchymal transition program. Stem Cells. 2016;34:1163–76.

Palorini R, Votta G, Balestrieri C, Monestiroli A, Olivieri S, Vento R, Chiaradonna F. Energy metabolism characterization of a novel cancer stem cell-like line 3AB-OS. J Cell Biochem. 2014;115:368–79.

Liu P, Liao J, Tang Z, Wu W, Yang J, Zeng Z, Hu Y, Wang P, Ju H, Xu R. Metabolic regulation of cancer cell side population by glucose through activation of the Akt pathway. Cell Death Differ. 2014;21:124–35.

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.

Li F, Tiede B, Massague J, Kang Y. Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res. 2006;17:3–14.

Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK, Ng L, Cheung LW, Lan XR, Lan HY, Tan VP, Yau TC, Poon RT, Wong BC. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell. 2010;6:603–15.

Dieter SM, Ball CR, Hoffmann CM, Nowrouzi A, Herbst F, Zavidij O, Abel U, Arens A, Weichert W, Brand K, Koch M, Weitz J, Schmidt M, von Kalle C, Glimm H. Distinct types of tumor-initiating cells form human colon cancer tumors and metastases. Cell Stem Cell. 2011;9:357–65.

Fidler IJ, Poste G. The “seed and soil” hypothesis revisited. Lancet Oncol. 2008;9:808.

Li S, Li Q. Cancer stem cells and tumor metastasis. Int J Oncol. 2014;44:1806–12.

Bernards R, Weinberg RA. A progression puzzle. Nature. 2002;418:823.

Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet. 2002;33:49–54.

Hunter K, Welch DR, Liu ET. Genetic background is an important determinant of metastatic potential. Nat Genet. 2003;34:23.

Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436:518–24.

Hanniford D, Zhong J, Koetz L, Gaziel-Sovran A, Lackaye DJ, Shang S, Pavlick A, Shapiro R, Berman R, Darvishian F, Shao Y, Osman I, Hernando E. A miRNA-based signature detected in primary melanoma tissue predicts development of brain metastasis. Clin Cancer Res. 2015;21:4903–12.

Riester M, Wu H-J, Zehir A, Gönen M, Moreira AL, Downey RJ, Michor F. Distance in cancer gene expression from stem cells predicts patient survival. PLoS One. 2017;12:e0173589.

Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2008;1:313–23.

Hermann PC, Heeschen C. Metastatic cancer stem cells--quo vadis? Clin Chem. 2013;59:1268–9.

Lawson DA, Bhakta NR, Kessenbrock K, Prummel KD, Yu Y, Takai K, Zhou A, Eyob H, Balakrishnan S, Wang C-Y. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature. 2015;526:131.

Smith BA, Sokolov A, Uzunangelov V, Baertsch R, Newton Y, Graim K, Mathis C, Cheng D, Stuart JM, Witte ON. A basal stem cell signature identifies aggressive prostate cancer phenotypes. Proc Natl Acad Sci. 2015;112:E6544–E52.

Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer. 2009;9:285–93.

Sceneay J, Smyth MJ, Möller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32:449–64.

Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.

Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol. 2006;8:1369–75.

Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol. 2008;10:1349–55.

Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–79.

Lobb RJ, Lima LG, Moller A. Exosomes: Key mediators of metastasis and pre-metastatic niche formation. Semin Cell Dev Biol. 2017;67:3-10.

Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, Yu Y, Chow A, O’Connor STF, Chin AR, Yen Y, Wang Y, Marcusson EG, Chu P, Wu J, Wu X, Li AX, Li Z, Gao H, Ren X, Boldin MP, Lin PC, Wang SE. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 2014;25:501–15.

Schillaci O, Fontana S, Monteleone F, Taverna S, Di Bella MA, Di Vizio D, Alessandro R. Exosomes from metastatic cancer cells transfer amoeboid phenotype to non-metastatic cells and increase endothelial permeability: their emerging role in tumor heterogeneity. Sci Rep. 2017;7:4711.

Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011;71:5346–56.

Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, García-Santos G, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012;18:883–91.

Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur Basant K, Becker A, Hoshino A, Mark MT, Molina H, Xiang J, Zhang T, Theilen T-M, García-Santos G, Williams C, Ararso Y, Huang Y, Rodrigues G, Shen T-L, Labori KJ, IMB L, Kure EH, Hernandez J, Doussot A, Ebbesen SH, Grandgenett Paul M, Hollingsworth Michael A, Jain M, Mallya K, Batra SK, Jarnagin William R, Schwartz Robert E, Matei I, Peinado H, Stanger BZ, Bromberg J, Lyden D. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17:816.

Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331:1559–64.

Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med. 2013;19:1438–49.

Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 2009;11:R46.

Theodoropoulos PA, Polioudaki H, Agelaki S, Kallergi G, Saridaki Z, Mavroudis D, Georgoulias V. Circulating tumor cells with a putative stem cell phenotype in peripheral blood of patients with breast cancer. Cancer Lett. 2010;288:99–106.

Kasimir-Bauer S, Hoffmann O, Wallwiener D, Kimmig R, Fehm T. Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res. 2012;14:R15.

Yang M-H, Imrali A, Heeschen C. Circulating cancer stem cells: the importance to select. Chin J Cancer Res. 2015;27:437.

Grillet F, Bayet E, Villeronce O, Zappia L, Lagerqvist EL, Lunke S, et al. Circulating tumour cells from patients with colorectal cancer have cancer stem cell hallmarks in ex vivo culture. Gut. 2016;66:1802-10.

Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res. 2010;70:5649–69.

Joosse SA, Gorges TM, Pantel K. Biology, detection, and clinical implications of circulating tumor cells. EMBO Mol Med. 2015;7:1–11.

Giancotti FG. Mechanisms governing metastatic dormancy and reactivation. Cell. 2013;155:750–64.

Eyles J, Puaux A-L, Wang X, Toh B, Prakash C, Hong M, Tan TG, Zheng L, Ong LC, Jin Y. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest. 2010;120:2030–9.

Naumov GN, Akslen LA, Folkman J. Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle. 2006;5:1779–87.

Gao XL, Zhang M, Tang YL, Liang XH. Cancer cell dormancy: mechanisms and implications of cancer recurrence and metastasis. OncoTargets Ther. 2017;10:5219.

Kleffel S, Schatton T.Tumour dormancy and cancer stem cells: two sides of the same coin?, in Systems Biology of Tumor Dormancy. New York: Springer; 2013. p. 145-79.

Sosa MS, Avivar-Valderas A, Bragado P, Wen H-C, Aguirre-Ghiso JA. ERK1/2 and p38α/β signaling in tumor cell quiescence: opportunities to control dormant residual disease. Clin Cancer Res. 2011;17:5850–7.

Gohongi T, Fukumura D, Boucher Y, Yun C-O, Soff GA, Compton C, et al. Tumor-host interactions in the gallbladder suppress distal angiogenesis and tumor growth: Involvement of transforming growth factor β1. Nat Med. 1999;5:1203-8.

Schober M, Fuchs E. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-β and integrin/focal adhesion kinase (FAK) signaling. Proc Natl Acad Sci. 2011;108:10544–9.

Kobayashi A, Okuda H, Xing F, Pandey PR, Watabe M, Hirota S, Pai SK, Liu W, Fukuda K, Chambers C, Wilber A, Watabe K. Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med. 2011;208:2641.

Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423:255–60.

Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P, Wicha MS. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66:6063–71.

Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science. 2008;319:195–8.

Lyden D, Young AZ, Zagzag D, Yan W. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature. 1999;401:670.

Stankic M, Pavlovic S, Chin Y, Brogi E, Padua D, Norton L, Massague J, Benezra R. TGF-β-Id1 signaling opposes Twist1 and promotes metastatic colonization via a mesenchymal-to-epithelial transition. Cell Rep. 2013;5:1228–42.

Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4:71.

Zhang XH-F, Wang Q, Gerald W, Hudis CA, Norton L, Smid M, Foekens JA, Massagué J. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell. 2009;16:67–78.

Chou J, Lin JH, Brenot A, Kim JW, Provot S, Werb Z. GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol. 2013;15:201.

Png KJ, Halberg N, Yoshida M, Tavazoie SF. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature. 2012;481:190.

Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 2003;3:537–49.

Weber GF, Ashkar S, Cantor H. Interaction between CD44 and osteopontin as a potential basis for metastasis formation. Proc Assoc Am Physicians. 1997;109:1–9.

Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr H-A, Delaloye J-F, Huelsken J. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2011;481:85.

Agliano A, Calvo A, Box C. The challenge of targeting cancer stem cells to halt metastasis. Semin Cancer Biol. 2017;44:25–42.