Cancer stem cell plasticity drives therapeutic resistance

Cancers

Volumn 8, Issue 1, 2016, Pages

  Doherty, Mary R ^a   Smigiel, Jacob M ^a   Junk, Damian J ^a   Jackson, Mark W ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Cancer stem cells; Cellular plasticity; Cytokines; Epithelial mesenchymal; Therapeutic resistance; Tumor microenvironment

Indexed keywords

INTERLEUKIN 17; ONCOSTATIN M; ONCOSTATIN M RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

CANCER CELL LINE; CANCER STEM CELL; CANCER THERAPY; CELL DIFFERENTIATION; CELL INTERACTION; CELL KILLING; CELL PLASTICITY; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CIRCULATING TUMOR CELL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; METASTASIS; MOLECULARLY TARGETED THERAPY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; THERAPY RESISTANCE; TUMOR MICROENVIRONMENT; TUMOR RECURRENCE;

EID: 84954411415     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers8010008     Document Type: Review

References (106)

1. Weigelt, B.; Peterse, J.L.; van’t Veer, L.J. Breast cancer metastasis: Markers and models. Nat. Rev. Cancer 2005, 5, 591-602. [CrossRef] [PubMed]
2. Nguyen, D.X.; Bos, P.D.; Massague, J. Metastasis: From dissemination to organ-specific colonization. Nat. Rev. Cancer 2009, 9, 274-284. [CrossRef] [PubMed]
3. Guarneri, V.; Broglio, K.; Kau, S.W.; Cristofanilli, M.; Buzdar, A.U.; Valero, V.; Buchholz, T.; Meric, F.; Middleton, L.; Hortobagyi, G.N.; et al. Prognostic value of pathologic complete response after primary chemotherapy in relation to hormone receptor status and other factors. J. Clin. Oncol. 2006, 24, 1037-1044. [CrossRef] [PubMed]
4. Kuerer, H.M.; Newman, L.A.; Smith, T.L.; Ames, F.C.; Hunt, K.K.; Dhingra, K.; Theriault, R.L.; Singh, G.; Binkley, S.M.; Sneige, N.; et al. Clinical course of breast cancer patients with complete pathologic primary tumor and axillary lymph node response to doxorubicin-based neoadjuvant chemotherapy. J. Clin. Oncol. 1999, 17, 460-469. [PubMed]
5. Liedtke, C.; Mazouni, C.; Hess, K.R.; Andre, F.; Tordai, A.; Mejia, J.A.; Symmans, W.F.; Gonzalez-Angulo, A.M.; Hennessy, B.; Green, M.; et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J. Clin. Oncol. 2008, 26, 1275-1281. [CrossRef] [PubMed]
6. Egeblad, M.; Nakasone, E.S.; Werb, Z. Tumors as organs: Complex tissues that interface with the entire organism. Dev. Cell 2010, 18, 884-901. [CrossRef] [PubMed]
7. Visvader, J.E.; Lindeman, G.J. Cancer stem cells: Current status and evolving complexities. Cell Stem Cell 2012, 10, 717-728. [CrossRef] [PubMed]
8. Jordan, C.T.; Guzman, M.L.; Noble, M. Cancer stem cells. N. Engl. J. Med. 2006, 355, 1253-1261. [CrossRef] [PubMed]
9. Adorno-Cruz, V.; Kibria, G.; Liu, X.; Doherty, M.; Junk, D.J.; Guan, D.; Hubert, C.; Venere, M.; Mulkearns-Hubert, E.; Sinyuk, M.; et al. Cancer stem cells: Targeting the roots of cancer, seeds of metastasis, and sources of therapy resistance. Cancer Res. 2015, 75, 924-929. [CrossRef] [PubMed]
10. Lathia, J.D.; Venere, M.; Rao, M.S.; Rich, J.N. Seeing is believing: Are cancer stem cells the loch ness monster of tumor biology? Stem Cell Rev. 2011, 7, 227-237. [CrossRef] [PubMed]
11. Al-Hajj, M.; Wicha, M.S.; ito-Hernandez, A.; Morrison, S.J.; Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100, 3983-3988. [CrossRef] [PubMed]
12. Rycaj, K.; Tang, D.G. Cell-of-origin of cancer versus cancer stem cells: Assays and interpretations. Cancer Res. 2015, 75, 4003-4011. [CrossRef] [PubMed]
13. Korkaya, H.; Liu, S.; Wicha, M.S. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J. Clin. Investig. 2011, 121, 3804-3809. [CrossRef] [PubMed]
14. Korkaya, H.; Liu, S.; Wicha, M.S. Regulation of cancer stem cells by cytokine networks: Attacking cancer’s inflammatory roots. Clin. Cancer Res. 2011, 17, 6125-6129. [CrossRef] [PubMed]
15. Charafe-Jauffret, E.; Ginestier, C.; Bertucci, F.; Cabaud, O.; Wicinski, J.; Finetti, P.; Josselin, E.; Adelaide, J.;Nguyen, T.T.; Monville, F.; et al. ALDH1-positive cancer stem cells predict engraftment of primary breast tumors and are governed by a common stem cell program. Cancer Res. 2013, 73, 7290-7300. [CrossRef] [PubMed]
16. Ginestier, C.; Hur, M.H.; Charafe-Jauffret, E.; Monville, F.; Dutcher, J.; Brown, M.; Jacquemier, J.; Viens, P.; Kleer, C.G.; Liu, S.; et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1, 555-567. [CrossRef] [PubMed]
17. Junk, D.J.; Cipriano, R.; Bryson, B.L.; Gilmore, H.L.; Jackson, M.W. Tumor microenvironmental signaling elicits epithelial-mesenchymal plasticity through cooperation with transforming genetic events. Neoplasia 2013, 15, 1100-1109. [CrossRef] [PubMed]
18. Blick, T.; Hugo, H.; Widodo, E.; Waltham, M.; Pinto, C.; Mani, S.A.; Weinberg, R.A.; Neve, R.M.; Lenburg, M.E.; Thompson, E.W. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the cd44hi/cd24lo/- stem cell phenotype in human breast cancer. J. Mammary Gland Biol. Neoplasia 2010, 15, 235-252. [CrossRef] [PubMed]
19. Mani, S.A.; Guo, W.; Liao, M.J.; Eaton, E.N.; Ayyanan, A.; Zhou, A.Y.; Brooks, M.; Reinhard, F.; Zhang, C.C.; Shipitsin, M.; et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133, 704-715. [CrossRef] [PubMed]
20. Mitra, A.; Mishra, L.; Li, S. EMT, CTCs and CSC in tumor relapse and drug-resistance. Oncotarget 2015, 6, 10697-10711. [CrossRef] [PubMed]
21. Liu, S.; Cong, Y.; Wang, D.; Sun, Y.; Deng, L.; Liu, Y.; Martin-Trevino, R.; Shang, L.; McDermott, S.P.; Landis, M.D.; et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Rep. 2014, 2, 78-91. [CrossRef] [PubMed]
22. Hollier, B.G.; Tinnirello, A.A.; Werden, S.J.; Evans, K.W.; Taube, J.H.; Sarkar, T.R.; Sphyris, N.; Shariati, M.; Kumar, S.V.; Battula, V.L.; et al. FOXC2 expression links epithelial-mesenchymal transition and stem cell properties in breast cancer. Cancer Res. 2013, 73, 1981-1992. [CrossRef] [PubMed]
23. Chaffer, C.L.; Marjanovic, N.D.; Lee, T.; Bell, G.; Kleer, C.G.; Reinhardt, F.; D’Alessio, A.C.; Young, R.A.; Weinberg, R.A. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell 2013, 154, 61-74. [CrossRef] [PubMed]
24. Badea, L.; Herlea, V.; Dima, S.O.; Dumitrascu, T.; Popescu, I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepato-gastroenterology 2008, 55, 2016-2027. [PubMed]
25. Kalluri, R.; Weinberg, R.A. The basics of epithelial-mesenchymal transition. J. Clin. Investig. 2009, 119, 1420-1428. [CrossRef] [PubMed]
26. Lamouille, S.; Xu, J.; Derynck, R. Molecular mechanisms of epithelial-mesenchymal transition. Nature Rev.Mol. cell Biol. 2014, 15, 178-196. [CrossRef] [PubMed]
27. Tsai, J.H.; Yang, J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev. 2013, 27, 2192-2206. [CrossRef] [PubMed]
28. Doyle, S.; Evans, A.J.; Rakha, E.A.; Green, A.R.; Ellis, I.O. Influence of E-cadherin expression on themammographic appearance of invasive nonlobular breast carcinoma detected at screening. Radiology 2009, 253, 51-55. [CrossRef] [PubMed]
29. Rakha, E.A.; Abd El Rehim, D.; Pinder, S.E.; Lewis, S.A.; Ellis, I.O. E-cadherin expression in invasive non-lobular carcinoma of the breast and its prognostic significance. Histopathology 2005, 46, 685-693. [CrossRef] [PubMed]
30. Rakha, E.A.; Patel, A.; Powe, D.G.; Benhasouna, A.; Green, A.R.; Lambros, M.B.; Reis-Filho, J.S.; Ellis, I.O. Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast. Am. J. Surg. Pathol. 2010, 34, 1472-1479. [CrossRef] [PubMed]
31. Liu, T.; Zhang, X.; Shang, M.; Zhang, Y.; Xia, B.; Niu, M.; Liu, Y.; Pang, D. Dysregulated expression of slug, vimentin, and E-cadherin correlates with poor clinical outcome in patients with basal-like breast cancer. J. Surg. Oncol. 2013, 107, 188-194. [CrossRef] [PubMed]
32. Markiewicz, A.; Welnicka-Jaskiewicz, M.; Seroczynska, B.; Skokowski, J.; Majewska, H.; Szade, J.; Zaczek, A.J. Epithelial-mesenchymal transition markers in lymph node metastases and primary breast tumors-relation to dissemination and proliferation. Am. J. Transl. Res. 2014, 6, 793-808. [PubMed]
33. Wu, S.; Liu, S.; Liu, Z.; Huang, J.; Pu, X.; Li, J.; Yang, D.; Deng, H.; Yang, N.; Xu, J. Classification of circulating tumor cells by epithelial-mesenchymal transition markers. PLoS NOE 2015, 10, e0123976. [CrossRef] [PubMed]
34. Yu, M.; Bardia, A.; Wittner, B.S.; Stott, S.L.; Smas, M.E.; Ting, D.T.; Isakoff, S.J.; Ciciliano, J.C.; Wells, M.N.; Shah, A.M.; et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013, 339, 580-584. [CrossRef] [PubMed]
35. Satelli, A.; Mitra, A.; Brownlee, Z.; Xia, X.; Bellister, S.; Overman, M.J.; Kopetz, S.; Ellis, L.M.; Meng, Q.H.; Li, S. Epithelial-mesenchymal transitioned circulating tumor cells capture for detecting tumor progression. Clin. Cancer Res. 2015, 21, 899-906. [CrossRef] [PubMed]
36. Baccelli, I.; Schneeweiss, A.; Riethdorf, S.; Stenzinger, A.; Schillert, A.; Vogel, V.; Klein, C.; Saini, M.; Bauerle, T.; Wallwiener, M.; et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat. Biotechnol. 2013, 31, 539-544. [CrossRef] [PubMed]
37. Hiraga, T.; Ito, S.; Nakamura, H. Cancer stem-like cell marker CD44 promotes bone metastases by enhancing tumorigenicity, cell motility, and hyaluronan production. Cancer Res. 2013, 73, 4112-4122. [CrossRef] [PubMed]
38. Van den Hoogen, C.; van der Horst, G.; Cheung, H.; Buijs, J.T.; Lippitt, J.M.; Guzman-Ramirez, N.; Hamdy, F.C.; Eaton, C.L.; Thalmann, G.N.; Cecchini, M.G.; et al. High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res. 2010, 70, 5163-5173. [CrossRef] [PubMed]
39. Lawson, D.A.; Bhakta, N.R.; Kessenbrock, K.; Prummel, K.D.; Yu, Y.; Takai, K.; Zhou, A.; Eyob, H.; Balakrishnan, S.; Wang, C.Y.; et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature 2015, 526, 131-135. [CrossRef] [PubMed]
40. Singh, A.; Settleman, J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 2010, 29, 4741-4751. [CrossRef] [PubMed]
41. Creighton, C.J.; Li, X.; Landis, M.; Dixon, J.M.; Neumeister, V.M.; Sjolund, A.; Rimm, D.L.; Wong, H.; Rodriguez, A.; Herschkowitz, J.I.; et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl. Acad. Sci. USA 2009, 106, 13820-13825. [CrossRef] [PubMed]
42. Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444, 756-760. [CrossRef] [PubMed]
43. Signore, M.; Ricci-Vitiani, L.; De Maria, R. Targeting apoptosis pathways in cancer stem cells. Cancer Lett. 2013, 332, 374-382. [CrossRef] [PubMed]
44. Moitra, K.; Lou, H.; Dean, M. Multidrug efflux pumps and cancer stem cells: Insights into multidrug resistance and therapeutic development. Clin. Pharmacol. Ther. 2011, 89, 491-502. [CrossRef] [PubMed]
45. Gottesman, M.M. Mechanisms of cancer drug resistance. Annu Rev. Med. 2002, 53, 615-627. [CrossRef] [PubMed]
46. Holohan, C.; van Schaeybroeck, S.; Longley, D.B.; Johnston, P.G. Cancer drug resistance: An evolving paradigm. Nat. Rev. Cancer 2013, 13, 714-726. [CrossRef] [PubMed]
47. Goldman, A.; Majumder, B.; Dhawan, A.; Ravi, S.; Goldman, D.; Kohandel, M.; Majumder, P.K.; Sengupta, S. Temporally sequenced anticancer drugs overcome adaptive resistance by targeting a vulnerable chemotherapy-induced phenotypic transition. Nat. Commun. 2015, 6, 6139. [CrossRef] [PubMed]
48. Biddle, A.; Liang, X.; Gammon, L.; Fazil, B.; Harper, L.J.; Emich, H.; Costea, D.E.; Mackenzie, I.C. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res. 2011, 71, 5317-5326. [CrossRef] [PubMed]
49. Li, Q.Q.; Xu, J.D.; Wang, W.J.; Cao, X.X.; Chen, Q.; Tang, F.; Chen, Z.Q.; Liu, X.P.; Xu, Z.D. Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clin. Cancer Res. 2009, 15, 2657-2665. [CrossRef] [PubMed]
50. Sun, L.; Yao, Y.; Liu, B.; Lin, Z.; Lin, L.; Yang, M.; Zhang, W.; Chen, W.; Pan, C.; Liu, Q.; et al. MiR-200b and miR-15b regulate chemotherapy-induced epithelial-mesenchymal transition in human tongue cancer cells by targeting BMI1. Oncogene 2012, 31, 432-445. [CrossRef] [PubMed]
51. Sharma, S.V.; Lee, D.Y.; Li, B.; Quinlan, M.P.; Takahashi, F.; Maheswaran, S.; McDermott, U.; Azizian, N.; Zou, L.; Fischbach, M.A.; et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141, 69-80. [CrossRef] [PubMed]
52. Pisco, A.O.; 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, 1725-1732. [CrossRef] [PubMed]
53. Hu, X.; Ghisolfi, L.; Keates, A.C.; Zhang, J.; Xiang, S.; Lee, D.K.; Li, C.J. Induction of cancer cell stemness by chemotherapy. Cell Cycle 2012, 11, 2691-2698. [CrossRef] [PubMed]
54. Ghisolfi, L.; Keates, A.C.; Hu, X.; Lee, D.K.; Li, C.J. Ionizing radiation induces stemness in cancer cells. PLoS ONE 2012, 7, e43628. [CrossRef] [PubMed]
55. Liu, S.; Ginestier, C.; Ou, S.J.; Clouthier, S.G.; Patel, S.H.; Monville, F.; Korkaya, H.; Heath, A.; Dutcher, J.; Kleer, C.G.; et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res. 2011, 71, 614-624. [CrossRef] [PubMed]
56. Celis, J.E.; Gromov, P.; Cabezon, T.; Moreira, J.M.; Ambartsumian, N.; Sandelin, K.; Rank, F.; Gromova, I. Proteomic characterization of the interstitial fluid perfusing the breast tumor microenvironment: A novel resource for biomarker and therapeutic target discovery. Mol. Cell. Proteom. 2004, 3, 327-344. [CrossRef] [PubMed]
57. Gonzalez-Moreno, O.; Lecanda, J.; Green, J.E.; Segura, V.; Catena, R.; Serrano, D.; Calvo, A. Vegf elicits epithelial-mesenchymal transition (EMT) in prostate intraepithelial neoplasia (pin)-like cells via an autocrine loop. Exp. Cell Res. 2010, 316, 554-567. [CrossRef] [PubMed]
58. Sullivan, N.J.; Sasser, A.K.; Axel, A.E.; Vesuna, F.; Raman, V.; Ramirez, N.; Oberyszyn, T.M.; Hall, B.M. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009, 28, 2940-2947. [CrossRef] [PubMed]
59. Liu, X. Inflammatory cytokines augments TGF-β1-induced epithelial-mesenchymal transition in A549 cells by up-regulating TβR-I. Cell Motil. Cytoskelet. 2008, 65, 935-944. [CrossRef] [PubMed]
60. Waerner, T.; Alacakaptan, M.; Tamir, I.; Oberauer, R.; Gal, A.; Brabletz, T.; Schreiber, M.; Jechlinger, M. Beug, H. ILEI: A cytokine essential for emt, tumor formation, and late events in metastasis in epithelial cells. Cancer Cell 2006, 10, 227-239. [CrossRef] [PubMed]
61. West, N.R.; Murray, J.I.; Watson, P.H. Oncostatin-m promotes phenotypic changes associated with mesenchymal and stem cell-like differentiation in breast cancer. Oncogene 2014, 33, 1485-1494. [CrossRef] [PubMed]
62. Techasen, A.; Loilome, W.; Namwat, N.; Dokduang, H.; Jongthawin, J.; Yongvanit, P. Cytokines released from activated human macrophages induce epithelial mesenchymal transition markers of cholangiocarcinoma cells. Asian Pac. J. Cancer Prev. 2012, 13, 115-118. [PubMed]
63. Kan, C.E.; Cipriano, R.; Jackson, M.W. C-myc functions as a molecular switch to alter the response of human mammary epithelial cells to oncostatin M. Cancer Res. 2011. [CrossRef] [PubMed]
64. Ng, G.; Winder, D.; Muralidhar, B.; Gooding, E.; Roberts, I.; Pett, M.; Mukherjee, G.; Huang, J.; Coleman, N. Gain and overexpression of the oncostatin M receptor occur frequently in cervical squamous cell carcinoma and are associated with adverse clinical outcome. J. Pathol. 2007, 212, 325-334. [CrossRef] [PubMed]
65. Smith, D.A.; Kiba, A.; Zong, Y.; Witte, O.N. Interleukin-6 and oncostatin-M synergize with the PI3K/AKT pathway to promote aggressive prostate malignancy in mouse and human tissues. Mol. Cancer Res. 2013, 11, 1159-1165. [CrossRef] [PubMed]
66. Tripathi, C.; Tewari, B.N.; Kanchan, R.K.; Baghel, K.S.; Nautiyal, N.; Shrivastava, R.; Kaur, H.; Bhatt, M.L.; Bhadauria, S. Macrophages are recruited to hypoxic tumor areas and acquire a Pro-Angiogenic M2-Polarized phenotype via hypoxic cancer cell derived cytokines oncostatin m and eotaxin. Oncotarget 2014, 5, 5350-5368. [CrossRef] [PubMed]
67. Lauber, S.; Wong, S.; Cutz, J.C.; Tanaka, M.; Barra, N.; Lhotak, S.; Ashkar, A.; Richards, C.D. Novel function of oncostatin m as a potent tumour-promoting agent in lung. Int. J. Cancer 2015, 136, 831-843. [CrossRef] [PubMed]
68. Wong, S.; Botelho, F.M.; Rodrigues, R.M.; Richards, C.D. Oncostatin M overexpression induces matrix deposition, STAT3 activation, and SMAD1 dysregulation in lungs of fibrosis-resistant BALB/c mice. Lab. Investig. 2014, 94, 1003-1016. [CrossRef] [PubMed]
69. Atkinson, R.L.; Yang, W.T.; Rosen, D.G.; Landis, M.D.; Wong, H.; Lewis, M.T.; Creighton, C.J.; Sexton, K.R.; Hilsenbeck, S.G.; Sahin, A.A.; et al. Cancer stem cell markers are enriched in normal tissue adjacent to triple negative breast cancer and inversely correlated with DNA repair deficiency. Breast cancer Res. 2013, 15, R77. [CrossRef] [PubMed]
70. Li, Q.; Zhu, J.; Sun, F.; Liu, L.; Liu, X.; Yue, Y. Oncostatin m promotes proliferation of ovarian cancer cells through signal transducer and activator of transcription 3. Int. J. Mol. Med. 2011, 28, 101-108. [PubMed]
71. Zhu, M.; Che, Q.; Liao, Y.; Wang, H.; Wang, J.; Chen, Z.; Wang, F.; Dai, C.; Wan, X. Oncostatin m activates STAT3 to promote endometrial cancer invasion and angiogenesis. Oncol. Rep. 2015, 34, 129-138. [CrossRef] [PubMed]
72. Bolin, C.; Tawara, K.; Sutherland, C.; Redshaw, J.; Aranda, P.; Moselhy, J.; Anderson, R.; Jorcyk, C.L. Oncostatin m promotes mammary tumor metastasis to bone and osteolytic bone degradation. Genes Cancer 2012, 3, 117-130. [CrossRef] [PubMed]
73. Holzer, R.G.; Ryan, R.E.; Tommack, M.; Schlekeway, E.; Jorcyk, C.L. Oncostatin M stimulates the detachment of a reservoir of invasive mammary carcinoma cells: Role of cyclooxygenase-2. Clin. Exp. Metastasis 2004, 21, 167-176. [CrossRef] [PubMed]
74. Jorcyk, C.L.; Holzer, R.G.; Ryan, R.E. Oncostatin m induces cell detachment and enhances the metastatic capacity of T-47D human breast carcinoma cells. Cytokine 2006, 33, 323-336. [CrossRef] [PubMed]
75. Queen, M.M.; Ryan, R.E.; Holzer, R.G.; Keller-Peck, C.R.; Jorcyk, C.L. Breast cancer cells stimulate neutrophils to produce oncostatin m: Potential implications for tumor progression. Cancer Res. 2005, 65, 8896-8904. [CrossRef] [PubMed]
76. Ryan, R.E.; Martin, B.; Mellor, L.; Jacob, R.B.; Tawara, K.; McDougal, O.M.; Oxford, J.T.; Jorcyk, C.L. Oncostatin M binds to extracellular matrix in a bioactive conformation: Implications for inflammation and metastasis. Cytokine 2015, 72, 71-85. [CrossRef] [PubMed]
77. Caffarel, M.M.; Coleman, N. Oncostatin m receptor is a novel therapeutic target in cervical squamous cell carcinoma. J. Pathol. 2014, 232, 386-390. [CrossRef] [PubMed]
78. Winder, D.M.; Chattopadhyay, A.; Muralidhar, B.; Bauer, J.; English, W.R.; Zhang, X.; Karagavriilidou, K.; Roberts, I.; Pett, M.R.; Murphy, G.; et al. Overexpression of the oncostatin m receptor in cervical squamous cell carcinoma cells is associated with a pro-angiogenic phenotype and increased cell motility and invasiveness. J. Pathol. 2011, 225, 448-462. [CrossRef] [PubMed]
79. West, N.R.; Murphy, L.C.; Watson, P.H. Oncostatin m suppresses oestrogen receptor-alpha expression and is associated with poor outcome in human breast cancer. Endocr.-Relat. Cancer 2012, 19, 181-195. [CrossRef] [PubMed]
80. Gurluler, E.; Tumay, L.V.; Guner, O.S.; Kucukmetin, N.T.; Hizli, B.; Zorluoglu, A. Oncostatin-M as a novel biomarker in colon cancer patients and its association with clinicopathologic variables. Eur. Rev. Med. Pharmacol. Sci. 2014, 18, 2042-2047. [PubMed]
81. Garcia-Tunon, I.; Ricote, M.; Ruiz, A.; Fraile, B.; Paniagua, R.; Royuela, M. Osm, lif, its receptors, and its relationship with the malignance in human breast carcinoma (in situ and in infiltrative). Cancer Investig. 2008, 26, 222-229. [CrossRef] [PubMed]
82. Royuela, M.; Ricote, M.; Parsons, M.S.; Garcia-Tunon, I.; Paniagua, R.; de Miguel, M.P. Immunohistochemical analysis of the IL-6 family of cytokines and their receptors in benign, hyperplasic, and malignant human prostate. J. Pathol. 2004, 202, 41-49. [CrossRef] [PubMed]
83. Torres, C.; Perales, S.; Alejandre, M.J.; Iglesias, J.; Palomino, R.J.; Martin, M.; Caba, O.; Prados, J.C.; Aranega, A.; Delgado, J.R.; et al. Serum cytokine profile in patients with pancreatic cancer. Pancreas 2014, 43, 1042-1049. [CrossRef] [PubMed]
84. Vlaicu, P.; Mertins, P.; Mayr, T.; Widschwendter, P.; Ataseven, B.; Hogel, B.; Eiermann, W.; Knyazev, P.; Ullrich, A. Monocytes/macrophages support mammary tumor invasivity by co-secreting lineage-specific EGFR ligands and a STAT3 activator. BMC Cancer 2013, 13, 197. [CrossRef] [PubMed]
85. Grenier, A.; Combaux, D.; Chastre, J.; Gougerot-Pocidalo, M.A.; Gibert, C.; Dehoux, M.; Chollet-Martin, S. Oncostatin m production by blood and alveolar neutrophils during acute lung injury. Lab. Investig. 2001, 81, 133-141. [CrossRef] [PubMed]
86. Grenier, A.; Dehoux, M.; Boutten, A.; Arce-Vicioso, M.; Durand, G.; Gougerot-Pocidalo, M.A.; Chollet-Martin, S. Oncostatin M production and regulation by human polymorphonuclear neutrophils. Blood 1999, 93, 1413-1421. [PubMed]
87. Zhu, Q.; Zhang, X.; Zhang, L.; Li, W.; Wu, H.; Yuan, X.; Mao, F.; Wang, M.; Zhu, W.; Qian, H.; et al. The IL-6-STAT3 axis mediates a reciprocal crosstalk between cancer-derived mesenchymal stem cells and neutrophils to synergistically prompt gastric cancer progression. Cell. Death Dis. 2014, 5, e1295. [CrossRef] [PubMed]
88. Guo, S.; Li, Z.Z.; Gong, J.; Xiang, M.; Zhang, P.; Zhao, G.N.; Li, M.; Zheng, A.; Zhu, X.; Lei, H.; et al. Oncostatin m confers neuroprotection against ischemic stroke. J. Neurosci. 2015, 35, 12047-12062. [CrossRef] [PubMed]
89. Levano, K.S.; Jung, E.H.; Kenny, P.A. Breast cancer subtypes express distinct receptor repertoires for tumor-associated macrophage derived cytokines. Biochem. Biophys. Res. Commun. 2011, 411, 107-110. [CrossRef] [PubMed]
90. Singh, R.A.; Sodhi, A. Cisplatin-treated macrophages produce oncostatin m: Regulation by serine/threonine and protein tyrosine kinases/phosphatases and Ca2+/calmodulin. Immunol. Lett. 1998, 62, 159-164. [CrossRef]
91. Sodhi, A.; Shishodia, S.; Shrivastava, A. Cisplatin-stimulated murine bone marrow-derived macrophages secrete oncostatin m. Immunol. Cell. Biol. 1997, 75, 492-496. [CrossRef] [PubMed]
92. Richards, C.D. The enigmatic cytokine oncostatin m and roles in disease. ISRN Inflamm. 2013, 2013, 512103. [CrossRef] [PubMed]
93. Lotti, F.; Jarrar, A.M.; Pai, R.K.; Hitomi, M.; Lathia, J.; Mace, A.; Gantt, G.A., Jr.; Sukhdeo, K.; DeVecchio, J.; Vasanji, A.; et al. Chemotherapy activates cancer-associated fibroblasts to maintain colorectal cancer-initiating cells by IL-17A. J. Exp. Med. 2013, 210, 2851-2872. [CrossRef] [PubMed]
94. Bhola, N.E.; Balko, J.M.; Dugger, T.C.; Kuba, M.G.; Sanchez, V.; Sanders, M.; Stanford, J.; Cook, R.S.; Arteaga, C.L. TGF-β inhibition enhances chemotherapy action against triple-negative breast cancer. J. Clin. Investig. 2013, 123, 1348-1358. [CrossRef] [PubMed]
95. Liu, W.-H.; Chen, M.-T.; Wang, M.-L.; Lee, Y.-Y.; Chiou, G.-Y.; Chien, C.-S.; Huang, P.-I.; Chen, Y.-W.; Huang, M.-C.; Chiou, S.-H.; et al. Cisplatin-selected resistance is associated with increased motility and stem-like properties via activation of STAT3/snail axis in atypical teratoid/rhabdoid tumor cells. Oncotarget 2015, 6, 1750-1768. [CrossRef] [PubMed]
96. Repovic, P.; Fears, C.Y.; Gladson, C.L.; Benveniste, E.N. Oncostatin-M induction of vascular endothelial expression in astroglioma cells. Oncogene 2003, 22, 8117-8124. [CrossRef] [PubMed]
97. Li, Y.; Rogoff, H.A.; Keates, S.; Gao, Y.; Murikipudi, S.; Mikule, K.; Leggett, D.; Li, W.; Pardee, A.B.; Li, C.J. Suppression of cancer relapse and metastasis by inhibiting cancer stemness. Proc. Natl. Acad. Sci. USA 2015, 112, 1839-1844. [CrossRef] [PubMed]
98. Miller, E.; Lee, H.J.; Lulla, A.; Hernandez, L.; Gokare, P.; Lim, B. Current treatment of early breast cancer: Adjuvant and neoadjuvant therapy. F1000Research 2014, 3, 198. [CrossRef] [PubMed]
99. Pan, Q.; Li, Q.; Liu, S.; Ning, N.; Zhang, X.; Xu, Y.; Chang, A.E.; Wicha, M.S. Concise review: Targeting cancer stem cells using immunologic approaches. Stem Cells 2015, 33, 2085-2092. [CrossRef] [PubMed]
100. Gangopadhyay, S.; Nandy, A.; Hor, P.; Mukhopadhyay, A. Breast cancer stem cells: A novel therapeutic target. Clin. Breast Cancer 2013, 13, 7-15. [CrossRef] [PubMed]
101. Frank, N.Y.; Schatton, T.; Frank, M.H. The therapeutic promise of the cancer stem cell concept. J. Clin. Investig. 2010, 120, 41-50. [CrossRef] [PubMed]
102. Kolev, V.N.; Wright, Q.G.; Vidal, C.M.; Ring, J.E.; Shapiro, I.M.; Ricono, J.; Weaver, D.T.; Padval, M.V.; Pachter, J.A.; Xu, Q. PI3K/mTOR dual inhibitor VS-5584 preferentially targets cancer stem cells. Cancer Res. 2015, 75, 446-455. [CrossRef] [PubMed]
103. Kemper, K.; Prasetyanti, P.R.; de Lau, W.; Rodermond, H.; Clevers, H.; Medema, J.P. Monoclonal antibodies against LGR5 identify human colorectal cancer stem cells. Stem Cells 2012, 30, 2378-2386. [CrossRef] [PubMed]
104. Sachlos, E.; Risueno, R.M.; Laronde, S.; Shapovalova, Z.; Lee, J.H.; Russell, J.; Malig, M.; McNicol, J.D.; Fiebig-Comyn, A.; Graham, M.; et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 2012, 149, 1284-1297. [CrossRef] [PubMed]
105. Gupta, P.B.; Onder, T.T.; Jiang, G.; Tao, K.; Kuperwasser, C.; Weinberg, R.A.; Lander, E.S. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138, 645-659. [CrossRef] [PubMed]
106. Takebe, N.; Harris, P.J.; Warren, R.Q.; Ivy, S.P. Targeting cancer stem cells by inhibiting wnt, notch, and hedgehog pathways. Nat. Rev. Clin. Oncol. 2011, 8, 97-106. [CrossRef] [PubMed]