Skip to main content
Top
Published in: Tumor Biology 2/2016

01-02-2016 | Review

Perspective: Cooperation of Nanog, NF-κΒ, and CXCR4 in a regulatory network for directed migration of cancer stem cells

Authors: Masoumeh Es-haghi, Sara Soltanian, Hesam Dehghani

Published in: Tumor Biology | Issue 2/2016

Login to get access

Abstract

Directed cell migration is a crucial mobility phase of cancer stem cells having stemness and tumorigenic characteristics. It is known that CXCR4 plays key roles in the perception of chemotactic gradients throughout the directed migration of CSCs. There are a number of complex signaling pathways and transcription factors that coordinate with CXCR4/CXCL12 axis during directed migration. In this review, we focus on some transcription factors such as Nanog, NF-κB, and Bmi-1 that cooperate with CXCR4/CXCL12 for the maintenance of stemness and induction of metastasis behavior in cancer stem cells.
Literature
1.
go back to reference Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV, et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer. 2012;12(11):767–75.CrossRefPubMed Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV, et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer. 2012;12(11):767–75.CrossRefPubMed
3.
go back to reference Flemming A. Cancer stem cells: targeting the root of cancer relapse. Nat Rev Drug Discov. 2015;14(3):165.CrossRefPubMed Flemming A. Cancer stem cells: targeting the root of cancer relapse. Nat Rev Drug Discov. 2015;14(3):165.CrossRefPubMed
4.
go back to reference Soltanian S, Matin MM. Cancer stem cells and cancer therapy. Tumour Biol: J Int Soc Oncodevelopmental Biol Med. 2011;32(3):425–40.CrossRef Soltanian S, Matin MM. Cancer stem cells and cancer therapy. Tumour Biol: J Int Soc Oncodevelopmental Biol Med. 2011;32(3):425–40.CrossRef
5.
go back to reference Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell. 2008;2(4):333–44.CrossRefPubMedPubMedCentral Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell. 2008;2(4):333–44.CrossRefPubMedPubMedCentral
6.
go back to reference Li Y, Rogoff HA, Keates S, Gao Y, Murikipudi S, Mikule K, et al. Suppression of cancer relapse and metastasis by inhibiting cancer stemness. Proc Natl Acad Sci. 2015;112(6):1839–44.CrossRefPubMedPubMedCentral Li Y, Rogoff HA, Keates S, Gao Y, Murikipudi S, Mikule K, et al. Suppression of cancer relapse and metastasis by inhibiting cancer stemness. Proc Natl Acad Sci. 2015;112(6):1839–44.CrossRefPubMedPubMedCentral
7.
8.
go back to reference Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744–9.CrossRefPubMed Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005;5(9):744–9.CrossRefPubMed
9.
go back to reference Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481(7379):85–9.CrossRef Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481(7379):85–9.CrossRef
10.
go back to reference Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009;28(1–2):15–33.CrossRefPubMed Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009;28(1–2):15–33.CrossRefPubMed
12.
go back to reference Schulenburg A, Blatt K, Cerny-Reiterer S, Sadovnik I, Herrmann H, Marian B, et al. Cancer stem cells in basic science and in translational oncology: can we translate into clinical application? J Hematol Oncol. 2015;8(1):16.CrossRefPubMedPubMedCentral Schulenburg A, Blatt K, Cerny-Reiterer S, Sadovnik I, Herrmann H, Marian B, et al. Cancer stem cells in basic science and in translational oncology: can we translate into clinical application? J Hematol Oncol. 2015;8(1):16.CrossRefPubMedPubMedCentral
13.
go back to reference Lopez-Lazaro M. The migration ability of stem cells can explain the existence of cancer of unknown primary site. Rethinking metastasis. Oncoscience. 2015;2(5):467–75.CrossRefPubMedPubMedCentral Lopez-Lazaro M. The migration ability of stem cells can explain the existence of cancer of unknown primary site. Rethinking metastasis. Oncoscience. 2015;2(5):467–75.CrossRefPubMedPubMedCentral
14.
go back to reference Case LB, Waterman CM. Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch. Nat Cell Biol. 2015;17(8):955–63. Case LB, Waterman CM. Integration of actin dynamics and cell adhesion by a three-dimensional, mechanosensitive molecular clutch. Nat Cell Biol. 2015;17(8):955–63.
15.
go back to reference Liao WT, Ye YP, Deng YJ, Bian XW, Ding YQ. Metastatic cancer stem cells: from the concept to therapeutics. Am J Stem Cells. 2014;3(2):46–62.PubMedPubMedCentral Liao WT, Ye YP, Deng YJ, Bian XW, Ding YQ. Metastatic cancer stem cells: from the concept to therapeutics. Am J Stem Cells. 2014;3(2):46–62.PubMedPubMedCentral
16.
go back to reference Bravo-Cordero JJ, Hodgson L, Condeelis J. Directed cell invasion and migration during metastasis. Curr Opin Cell Biol. 2012;24(2):277–83.CrossRefPubMed Bravo-Cordero JJ, Hodgson L, Condeelis J. Directed cell invasion and migration during metastasis. Curr Opin Cell Biol. 2012;24(2):277–83.CrossRefPubMed
18.
go back to reference Smith HA, Kang Y. The metastasis-promoting roles of tumor-associated immune cells. J Mol Med (Berlin, Germany). 2013;91(4):411–29.CrossRef Smith HA, Kang Y. The metastasis-promoting roles of tumor-associated immune cells. J Mol Med (Berlin, Germany). 2013;91(4):411–29.CrossRef
19.
go back to reference Patel P, Chen EI. Cancer stem cells, tumor dormancy, and metastasis. Front Endocrinol. 2012;3:125.CrossRef Patel P, Chen EI. Cancer stem cells, tumor dormancy, and metastasis. Front Endocrinol. 2012;3:125.CrossRef
20.
go back to reference Albini A, Bruno A, Gallo C, Pajardi G, Noonan DM, Dallaglio K. Cancer stem cells and the tumor microenvironment: interplay in tumor heterogeneity. Connect Tissue Res. 2015;56(5):414–25.CrossRefPubMedPubMedCentral Albini A, Bruno A, Gallo C, Pajardi G, Noonan DM, Dallaglio K. Cancer stem cells and the tumor microenvironment: interplay in tumor heterogeneity. Connect Tissue Res. 2015;56(5):414–25.CrossRefPubMedPubMedCentral
21.
go back to reference Parent CA, Weiner OD. The symphony of cell movement: how cells orchestrate diverse signals and forces to control migration. Curr Opin Cell Biol. 2013;25(5):523–5.CrossRefPubMed Parent CA, Weiner OD. The symphony of cell movement: how cells orchestrate diverse signals and forces to control migration. Curr Opin Cell Biol. 2013;25(5):523–5.CrossRefPubMed
22.
go back to reference Swaney KF, Huang CH, Devreotes PN. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys. 2010;39:265–89.CrossRefPubMedPubMedCentral Swaney KF, Huang CH, Devreotes PN. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys. 2010;39:265–89.CrossRefPubMedPubMedCentral
25.
go back to reference Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol. 2004;14(3):171–9.CrossRefPubMed Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol. 2004;14(3):171–9.CrossRefPubMed
26.
go back to reference Zlotnik A. Chemokines and cancer. Int J Cancer J Int Cancer. 2006;119(9):2026–9.CrossRef Zlotnik A. Chemokines and cancer. Int J Cancer J Int Cancer. 2006;119(9):2026–9.CrossRef
27.
go back to reference Haviv YS, van Houdt WJ, Lu B, Curiel DT, Zhu ZB. Transcriptional targeting in renal cancer cell lines via the human CXCR4 promoter. Mol Cancer Ther. 2004;3(6):687–91.PubMed Haviv YS, van Houdt WJ, Lu B, Curiel DT, Zhu ZB. Transcriptional targeting in renal cancer cell lines via the human CXCR4 promoter. Mol Cancer Ther. 2004;3(6):687–91.PubMed
28.
go back to reference Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells (Dayton, Ohio). 2005;23(7):879–94.CrossRef Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, et al. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1-CXCR4 axis. Stem Cells (Dayton, Ohio). 2005;23(7):879–94.CrossRef
29.
go back to reference Jung MJ, Rho JK, Kim YM, Jung JE, Jin YB, Ko YG, et al. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene. 2013;32(2):209–21.CrossRefPubMed Jung MJ, Rho JK, Kim YM, Jung JE, Jin YB, Ko YG, et al. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene. 2013;32(2):209–21.CrossRefPubMed
30.
go back to reference Gao Y, Li C, Nie M, Lu Y, Lin S, Yuan P, et al. CXCR4 as a novel predictive biomarker for metastasis and poor prognosis in colorectal cancer. Tumor Biol. 2014;35(5):4171–5.CrossRef Gao Y, Li C, Nie M, Lu Y, Lin S, Yuan P, et al. CXCR4 as a novel predictive biomarker for metastasis and poor prognosis in colorectal cancer. Tumor Biol. 2014;35(5):4171–5.CrossRef
31.
go back to reference Gagliardi F, Narayanan A, Reni M, Franzin A, Mazza E, Boari N, et al. The role of CXCR4 in highly malignant human gliomas biology: current knowledge and future directions. Glia. 2014;62(7):1015–23.CrossRefPubMed Gagliardi F, Narayanan A, Reni M, Franzin A, Mazza E, Boari N, et al. The role of CXCR4 in highly malignant human gliomas biology: current knowledge and future directions. Glia. 2014;62(7):1015–23.CrossRefPubMed
32.
go back to reference Fareh M, Turchi L, Virolle V, Debruyne D, Almairac F. The miR 302–367 cluster drastically affects self-renewal and infiltration properties of glioma-initiating cells through CXCR4 repression and consequent disruption of the SHH-GLI-NANOG network. Cell Death Differ. 2012;19(2):232–44.CrossRefPubMed Fareh M, Turchi L, Virolle V, Debruyne D, Almairac F. The miR 302–367 cluster drastically affects self-renewal and infiltration properties of glioma-initiating cells through CXCR4 repression and consequent disruption of the SHH-GLI-NANOG network. Cell Death Differ. 2012;19(2):232–44.CrossRefPubMed
33.
go back to reference Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest. 2010;120(3):694–705.CrossRefPubMedPubMedCentral Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest. 2010;120(3):694–705.CrossRefPubMedPubMedCentral
34.
go back to reference Kim EK, Yun SJ, Ha JM, Kim YW, Jin IH, Woo DH, et al. Synergistic induction of cancer cell migration regulated by G[beta][gamma] and phosphatidylinositol 3-kinase. Exp Mol Med. 2012;44:483–91.CrossRefPubMedPubMedCentral Kim EK, Yun SJ, Ha JM, Kim YW, Jin IH, Woo DH, et al. Synergistic induction of cancer cell migration regulated by G[beta][gamma] and phosphatidylinositol 3-kinase. Exp Mol Med. 2012;44:483–91.CrossRefPubMedPubMedCentral
35.
go back to reference Kim BJ, Hannanta-anan P, Chau M, Kim YS, Swartz MA, Wu M. Cooperative roles of SDF-1alpha and EGF gradients on tumor cell migration revealed by a robust 3D microfluidic model. PLoS ONE. 2013;8(7), e68422.CrossRefPubMedPubMedCentral Kim BJ, Hannanta-anan P, Chau M, Kim YS, Swartz MA, Wu M. Cooperative roles of SDF-1alpha and EGF gradients on tumor cell migration revealed by a robust 3D microfluidic model. PLoS ONE. 2013;8(7), e68422.CrossRefPubMedPubMedCentral
36.
go back to reference Akekawatchai C, Holland JD, Kochetkova M, Wallace JC, McColl SR. Transactivation of CXCR4 by the insulin-like growth factor-1 receptor (IGF-1R) in human MDA-MB-231 breast cancer epithelial cells. J Biol Chem. 2005;280(48):39701–8.CrossRefPubMed Akekawatchai C, Holland JD, Kochetkova M, Wallace JC, McColl SR. Transactivation of CXCR4 by the insulin-like growth factor-1 receptor (IGF-1R) in human MDA-MB-231 breast cancer epithelial cells. J Biol Chem. 2005;280(48):39701–8.CrossRefPubMed
37.
go back to reference Mimeault M, Batra SK. Frequent deregulations in the hedgehog signaling network and cross-talks with the epidermal growth factor receptor pathway involved in cancer progression and targeted therapies. Pharmacol Rev. 2010;62(3):497–524.CrossRefPubMedPubMedCentral Mimeault M, Batra SK. Frequent deregulations in the hedgehog signaling network and cross-talks with the epidermal growth factor receptor pathway involved in cancer progression and targeted therapies. Pharmacol Rev. 2010;62(3):497–524.CrossRefPubMedPubMedCentral
38.
go back to reference Wu F, Yang LY, Li YF, Ou DP, Chen DP, Fan C. Novel role for epidermal growth factor-like domain 7 in metastasis of human hepatocellular carcinoma. Hepatol (Baltimore, Md). 2009;50(6):1839–50.CrossRef Wu F, Yang LY, Li YF, Ou DP, Chen DP, Fan C. Novel role for epidermal growth factor-like domain 7 in metastasis of human hepatocellular carcinoma. Hepatol (Baltimore, Md). 2009;50(6):1839–50.CrossRef
39.
go back to reference Delfortrie S, Pinte S, Mattot V, Samson C, Villain G, Caetano B, et al. Egfl7 promotes tumor escape from immunity by repressing endothelial cell activation. Cancer Res. 2011;71(23):7176–86.CrossRefPubMed Delfortrie S, Pinte S, Mattot V, Samson C, Villain G, Caetano B, et al. Egfl7 promotes tumor escape from immunity by repressing endothelial cell activation. Cancer Res. 2011;71(23):7176–86.CrossRefPubMed
40.
go back to reference Bai R, Zhao H, Zhang X, Du S. Characterization of sonic hedgehog inhibition in gastric carcinoma cells. Oncol Lett. 2014;7(5):1381–4.PubMedPubMedCentral Bai R, Zhao H, Zhang X, Du S. Characterization of sonic hedgehog inhibition in gastric carcinoma cells. Oncol Lett. 2014;7(5):1381–4.PubMedPubMedCentral
41.
go back to reference McLennan R, Dyson L, Prather KW, Morrison JA, Baker RE, Maini PK, et al. Multiscale mechanisms of cell migration during development: theory and experiment. Dev (Cambridge, England). 2012;139(16):2935–44.CrossRef McLennan R, Dyson L, Prather KW, Morrison JA, Baker RE, Maini PK, et al. Multiscale mechanisms of cell migration during development: theory and experiment. Dev (Cambridge, England). 2012;139(16):2935–44.CrossRef
42.
43.
go back to reference Schlueter PJ, Sang X, Duan C, Wood AW. Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev Biol. 2007;305(1):377–87.CrossRefPubMedPubMedCentral Schlueter PJ, Sang X, Duan C, Wood AW. Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev Biol. 2007;305(1):377–87.CrossRefPubMedPubMedCentral
44.
go back to reference Haider H, Jiang S, Idris NM, Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ Res. 2008;103(11):1300–8.CrossRefPubMed Haider H, Jiang S, Idris NM, Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ Res. 2008;103(11):1300–8.CrossRefPubMed
45.
go back to reference Huang CE, Yu CC, Hu FW, Chou MY, Tsai LL. Enhanced chemosensitivity by targeting Nanog in head and neck squamous cell carcinomas. Int J Mol Sci. 2014;15(9):14935–48.CrossRefPubMedPubMedCentral Huang CE, Yu CC, Hu FW, Chou MY, Tsai LL. Enhanced chemosensitivity by targeting Nanog in head and neck squamous cell carcinomas. Int J Mol Sci. 2014;15(9):14935–48.CrossRefPubMedPubMedCentral
46.
go back to reference Ji W, Jiang Z. Effect of shRNA-mediated inhibition of Nanog gene expression on the behavior of human gastric cancer cells. Oncol Letters. 2013;6(2):367–74. Ji W, Jiang Z. Effect of shRNA-mediated inhibition of Nanog gene expression on the behavior of human gastric cancer cells. Oncol Letters. 2013;6(2):367–74.
47.
go back to reference Borrull A, Ghislin S, Deshayes F, Lauriol J, Alcaide-Loridan C, Middendorp S. Nanog and Oct4 overexpression increases motility and transmigration of melanoma cells. J Cancer Res Clin Oncol. 2012;138(7):1145–54.CrossRefPubMed Borrull A, Ghislin S, Deshayes F, Lauriol J, Alcaide-Loridan C, Middendorp S. Nanog and Oct4 overexpression increases motility and transmigration of melanoma cells. J Cancer Res Clin Oncol. 2012;138(7):1145–54.CrossRefPubMed
48.
go back to reference Siu MK, Wong ES, Kong DS, Chan HY, Jiang L, Wong OG, et al. Stem cell transcription factor NANOG controls cell migration and invasion via dysregulation of E-cadherin and FoxJ1 and contributes to adverse clinical outcome in ovarian cancers. Oncogene. 2013;32(30):3500–9.CrossRefPubMed Siu MK, Wong ES, Kong DS, Chan HY, Jiang L, Wong OG, et al. Stem cell transcription factor NANOG controls cell migration and invasion via dysregulation of E-cadherin and FoxJ1 and contributes to adverse clinical outcome in ovarian cancers. Oncogene. 2013;32(30):3500–9.CrossRefPubMed
49.
go back to reference Dang H, Ding W, Emerson D, Rountree CB. Snail1 induces epithelial-to-mesenchymal transition and tumor initiating stem cell characteristics. BMC Cancer. 2011;11:396.CrossRefPubMedPubMedCentral Dang H, Ding W, Emerson D, Rountree CB. Snail1 induces epithelial-to-mesenchymal transition and tumor initiating stem cell characteristics. BMC Cancer. 2011;11:396.CrossRefPubMedPubMedCentral
50.
go back to reference Palla AR, Piazzolla D, Alcazar N, Canamero M, Grana O, Gomez-Lopez G, et al. The pluripotency factor NANOG promotes the formation of squamous cell carcinomas. Scientific Rep. 2015;5:10205.CrossRef Palla AR, Piazzolla D, Alcazar N, Canamero M, Grana O, Gomez-Lopez G, et al. The pluripotency factor NANOG promotes the formation of squamous cell carcinomas. Scientific Rep. 2015;5:10205.CrossRef
51.
go back to reference Wang ML, Chiou SH, Wu CW. Targeting cancer stem cells: emerging role of Nanog transcription factor. OncoTargets Ther. 2013;6:1207–20. Wang ML, Chiou SH, Wu CW. Targeting cancer stem cells: emerging role of Nanog transcription factor. OncoTargets Ther. 2013;6:1207–20.
52.
go back to reference Zbinden M, Duquet A, Lorente-Trigos A, Ngwabyt SN, Borges I, Ruiz i Altaba A. NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 2010;29(15):2659–74.CrossRefPubMedPubMedCentral Zbinden M, Duquet A, Lorente-Trigos A, Ngwabyt SN, Borges I, Ruiz i Altaba A. NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 2010;29(15):2659–74.CrossRefPubMedPubMedCentral
54.
go back to reference Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, et al. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of hedgehog pathway. Cancer Lett. 2012;322(2):169–76.CrossRefPubMedPubMedCentral Li X, Ma Q, Xu Q, Liu H, Lei J, Duan W, et al. SDF-1/CXCR4 signaling induces pancreatic cancer cell invasion and epithelial-mesenchymal transition in vitro through non-canonical activation of hedgehog pathway. Cancer Lett. 2012;322(2):169–76.CrossRefPubMedPubMedCentral
56.
go back to reference Feldmann G, Dhara S, Fendrich V, Bedja D, Beaty R, Mullendore M, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res. 2007;67(5):2187–96.CrossRefPubMedPubMedCentral Feldmann G, Dhara S, Fendrich V, Bedja D, Beaty R, Mullendore M, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res. 2007;67(5):2187–96.CrossRefPubMedPubMedCentral
57.
go back to reference Sanchez-Sanchez AV, Camp E, Leal-Tassias A, Atkinson SP, Armstrong L, Diaz-Llopis M, et al. Nanog regulates primordial germ cell migration through Cxcr4b. Stem Cells (Dayton, Ohio). 2010;28(9):1457–64.CrossRef Sanchez-Sanchez AV, Camp E, Leal-Tassias A, Atkinson SP, Armstrong L, Diaz-Llopis M, et al. Nanog regulates primordial germ cell migration through Cxcr4b. Stem Cells (Dayton, Ohio). 2010;28(9):1457–64.CrossRef
58.
go back to reference Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, et al. Nanog safeguards pluripotency and mediates germline development. Nature. 2007;450(7173):1230–4.CrossRefPubMed Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, et al. Nanog safeguards pluripotency and mediates germline development. Nature. 2007;450(7173):1230–4.CrossRefPubMed
59.
go back to reference Blaser H, Eisenbeiss S, Neumann M, Reichman-Fried M, Thisse B, Thisse C, et al. Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J Cell Sci. 2005;118(Pt 17):4027–38.CrossRefPubMed Blaser H, Eisenbeiss S, Neumann M, Reichman-Fried M, Thisse B, Thisse C, et al. Transition from non-motile behaviour to directed migration during early PGC development in zebrafish. J Cell Sci. 2005;118(Pt 17):4027–38.CrossRefPubMed
60.
go back to reference Lee CC, Lai JH, Hueng DY, Ma HI, Chung Y, Sun YY, et al. Disrupting the CXCL12/CXCR4 axis disturbs the characteristics of glioblastoma stem-like cells of rat RG2 glioblastoma. Cancer Cell Int. 2013;13(1):85.CrossRefPubMedPubMedCentral Lee CC, Lai JH, Hueng DY, Ma HI, Chung Y, Sun YY, et al. Disrupting the CXCL12/CXCR4 axis disturbs the characteristics of glioblastoma stem-like cells of rat RG2 glioblastoma. Cancer Cell Int. 2013;13(1):85.CrossRefPubMedPubMedCentral
61.
go back to reference Singh AP, Arora S, Bhardwaj A, Srivastava SK, Kadakia MP, Wang B, et al. CXCL12/CXCR4 protein signaling axis induces sonic hedgehog expression in pancreatic cancer cells via extracellular regulated kinase- and Akt kinase-mediated activation of nuclear factor kappaB: implications for bidirectional tumor-stromal interactions. J Biol Chem. 2012;287(46):39115–24.CrossRefPubMedPubMedCentral Singh AP, Arora S, Bhardwaj A, Srivastava SK, Kadakia MP, Wang B, et al. CXCL12/CXCR4 protein signaling axis induces sonic hedgehog expression in pancreatic cancer cells via extracellular regulated kinase- and Akt kinase-mediated activation of nuclear factor kappaB: implications for bidirectional tumor-stromal interactions. J Biol Chem. 2012;287(46):39115–24.CrossRefPubMedPubMedCentral
62.
go back to reference Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, et al. The canonical NF-kappaB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res. 2010;70(24):10464–73.CrossRefPubMedPubMedCentral Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, et al. The canonical NF-kappaB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res. 2010;70(24):10464–73.CrossRefPubMedPubMedCentral
63.
go back to reference Helbig G, Christopherson 2nd KW, Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, et al. NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem. 2003;278(24):21631–8.CrossRefPubMed Helbig G, Christopherson 2nd KW, Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, et al. NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem. 2003;278(24):21631–8.CrossRefPubMed
64.
go back to reference Zhi Y, Lu H, Duan Y, Sun W, Guan G, Dong Q, et al. Involvement of the nuclear factor-kappaB signaling pathway in the regulation of CXC chemokine receptor-4 expression in neuroblastoma cells induced by tumor necrosis factor-alpha. Int J Mol Med. 2015;35(2):349–57.PubMed Zhi Y, Lu H, Duan Y, Sun W, Guan G, Dong Q, et al. Involvement of the nuclear factor-kappaB signaling pathway in the regulation of CXC chemokine receptor-4 expression in neuroblastoma cells induced by tumor necrosis factor-alpha. Int J Mol Med. 2015;35(2):349–57.PubMed
65.
go back to reference Zhi Y, Duan Y, Zhou X, Yin X, Guan G, Zhang H, et al. NF-kappaB signaling pathway confers neuroblastoma cells migration and invasion ability via the regulation of CXCR4. Med Sci Monit : Int Med J Exp Clin Res. 2014;20:2746–52.CrossRef Zhi Y, Duan Y, Zhou X, Yin X, Guan G, Zhang H, et al. NF-kappaB signaling pathway confers neuroblastoma cells migration and invasion ability via the regulation of CXCR4. Med Sci Monit : Int Med J Exp Clin Res. 2014;20:2746–52.CrossRef
66.
go back to reference Po A, Ferretti E, Miele E, De Smaele E, Paganelli A, Canettieri G, et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J. 2010;29(15):2646–58.CrossRefPubMedPubMedCentral Po A, Ferretti E, Miele E, De Smaele E, Paganelli A, Canettieri G, et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J. 2010;29(15):2646–58.CrossRefPubMedPubMedCentral
68.
go back to reference Xia P, Xu XY. PI3K/Akt/mTOR signaling pathway in cancer stem cells: from basic research to clinical application. Am J Cancer Res. 2015;5(5):1602–9.PubMedPubMedCentral Xia P, Xu XY. PI3K/Akt/mTOR signaling pathway in cancer stem cells: from basic research to clinical application. Am J Cancer Res. 2015;5(5):1602–9.PubMedPubMedCentral
69.
go back to reference Martelli AM, Evangelisti C, Follo MY, Ramazzotti G, Fini M, Giardino R, et al. Targeting the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling network in cancer stem cells. Curr Med Chem. 2011;18(18):2715–26.CrossRefPubMed Martelli AM, Evangelisti C, Follo MY, Ramazzotti G, Fini M, Giardino R, et al. Targeting the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling network in cancer stem cells. Curr Med Chem. 2011;18(18):2715–26.CrossRefPubMed
70.
go back to reference Weng W, Zhang X, Xu K, Zheng T, Goel A. Long non-coding RNA Hotair, enhances Sdf1a-CXCR4-induced migration and invasion in esophageal squamous cell carcinoma. Gastroenterology. 2015;148(4):S-560-S-1.CrossRef Weng W, Zhang X, Xu K, Zheng T, Goel A. Long non-coding RNA Hotair, enhances Sdf1a-CXCR4-induced migration and invasion in esophageal squamous cell carcinoma. Gastroenterology. 2015;148(4):S-560-S-1.CrossRef
71.
go back to reference Song LB, Li J, Liao WT, Feng Y, Yu CP, Hu LJ, et al. The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest. 2009;119(12):3626–36.CrossRefPubMedPubMedCentral Song LB, Li J, Liao WT, Feng Y, Yu CP, Hu LJ, et al. The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest. 2009;119(12):3626–36.CrossRefPubMedPubMedCentral
72.
go back to reference Paranjape AN, Balaji SA, Mandal T, Krushik EV, Nagaraj P, Mukherjee G, et al. Bmi1 regulates self-renewal and epithelial to mesenchymal transition in breast cancer cells through Nanog. BMC Cancer. 2014;14:785.CrossRefPubMedPubMedCentral Paranjape AN, Balaji SA, Mandal T, Krushik EV, Nagaraj P, Mukherjee G, et al. Bmi1 regulates self-renewal and epithelial to mesenchymal transition in breast cancer cells through Nanog. BMC Cancer. 2014;14:785.CrossRefPubMedPubMedCentral
73.
go back to reference Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66(12):6063–71.CrossRefPubMedPubMedCentral Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66(12):6063–71.CrossRefPubMedPubMedCentral
74.
go back to reference Liang J, Wang P, Xie S, Wang W, Zhou X, Hu J, et al. Bmi-1 regulates the migration and invasion of glioma cells through p16. Cell Biol Int. 2015;39(3):283–90. Liang J, Wang P, Xie S, Wang W, Zhou X, Hu J, et al. Bmi-1 regulates the migration and invasion of glioma cells through p16. Cell Biol Int. 2015;39(3):283–90.
75.
go back to reference Jiang L, Wu J, Yang Y, Liu L, Song L, Li J, et al. Bmi-1 promotes the aggressiveness of glioma via activating the NF-kappaB/MMP-9 signaling pathway. BMC Cancer. 2012;12:406.CrossRefPubMedPubMedCentral Jiang L, Wu J, Yang Y, Liu L, Song L, Li J, et al. Bmi-1 promotes the aggressiveness of glioma via activating the NF-kappaB/MMP-9 signaling pathway. BMC Cancer. 2012;12:406.CrossRefPubMedPubMedCentral
76.
go back to reference Li D, Feng J, Wu T, Wang Y, Sun Y, Ren J, et al. Long intergenic noncoding RNA HOTAIR is overexpressed and regulates PTEN methylation in laryngeal squamous cell carcinoma. Am J Pathol. 2013;182(1):64–70.CrossRefPubMed Li D, Feng J, Wu T, Wang Y, Sun Y, Ren J, et al. Long intergenic noncoding RNA HOTAIR is overexpressed and regulates PTEN methylation in laryngeal squamous cell carcinoma. Am J Pathol. 2013;182(1):64–70.CrossRefPubMed
77.
go back to reference Zhou X, Chen J, Tang W. The molecular mechanism of HOTAIR in tumorigenesis, metastasis, and drug resistance. Acta Biochim Biophys Sin. 2014;46(12):1011–5.CrossRefPubMed Zhou X, Chen J, Tang W. The molecular mechanism of HOTAIR in tumorigenesis, metastasis, and drug resistance. Acta Biochim Biophys Sin. 2014;46(12):1011–5.CrossRefPubMed
78.
go back to reference Zhu M, Guo J, Xia H, Li W, Lu Y, Dong X, et al. Alpha-fetoprotein activates AKT/mTOR signaling to promote CXCR4 expression and migration of hepatoma cells. Oncoscience. 2015;2(1):59–70.CrossRefPubMedPubMedCentral Zhu M, Guo J, Xia H, Li W, Lu Y, Dong X, et al. Alpha-fetoprotein activates AKT/mTOR signaling to promote CXCR4 expression and migration of hepatoma cells. Oncoscience. 2015;2(1):59–70.CrossRefPubMedPubMedCentral
79.
go back to reference Yi T, Zhai B, Yu Y, Kiyotsugu Y, Raschle T, Etzkorn M, et al. Quantitative phosphoproteomic analysis reveals system-wide signaling pathways downstream of SDF-1/CXCR4 in breast cancer stem cells. Proc Natl Acad Sci. 2014;111(21):E2182–90.CrossRefPubMedPubMedCentral Yi T, Zhai B, Yu Y, Kiyotsugu Y, Raschle T, Etzkorn M, et al. Quantitative phosphoproteomic analysis reveals system-wide signaling pathways downstream of SDF-1/CXCR4 in breast cancer stem cells. Proc Natl Acad Sci. 2014;111(21):E2182–90.CrossRefPubMedPubMedCentral
80.
go back to reference Aziz MH, Hafeez BB, Sand JM, Pierce DB, Aziz SW, Dreckschmidt NE, et al. Protein kinase Cvarepsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene. 2010;29(21):3100–9.CrossRefPubMedPubMedCentral Aziz MH, Hafeez BB, Sand JM, Pierce DB, Aziz SW, Dreckschmidt NE, et al. Protein kinase Cvarepsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene. 2010;29(21):3100–9.CrossRefPubMedPubMedCentral
81.
go back to reference Cho KH, Jeong KJ, Shin SC, Kang J, Park CG, Lee HY. STAT3 mediates TGF-beta1-induced TWIST1 expression and prostate cancer invasion. Cancer Lett. 2013;336(1):167–73.CrossRefPubMed Cho KH, Jeong KJ, Shin SC, Kang J, Park CG, Lee HY. STAT3 mediates TGF-beta1-induced TWIST1 expression and prostate cancer invasion. Cancer Lett. 2013;336(1):167–73.CrossRefPubMed
82.
go back to reference Jain K, Basu A. Protein kinase C-epsilon promotes EMT in breast cancer. Breast Cancer: Basic Clin Res. 2014;8:61–7. Jain K, Basu A. Protein kinase C-epsilon promotes EMT in breast cancer. Breast Cancer: Basic Clin Res. 2014;8:61–7.
84.
go back to reference Ivaska J, Kermorgant S, Whelan R, Parsons M, Ng T, Parker PJ. Integrin-protein kinase C relationships. Biochem Soc Trans. 2003;31(Pt 1):90–3.CrossRefPubMed Ivaska J, Kermorgant S, Whelan R, Parsons M, Ng T, Parker PJ. Integrin-protein kinase C relationships. Biochem Soc Trans. 2003;31(Pt 1):90–3.CrossRefPubMed
86.
go back to reference He H, Zhao ZH, Han FS, Wang XF, Zeng YJ. Activation of protein kinase C epsilon enhanced movement ability and paracrine function of rat bone marrow mesenchymal stem cells partly at least independent of SDF-1/CXCR4 axis and PI3K/AKT pathway. Int J Clin Exp Med. 2015;8(1):188–202.PubMedPubMedCentral He H, Zhao ZH, Han FS, Wang XF, Zeng YJ. Activation of protein kinase C epsilon enhanced movement ability and paracrine function of rat bone marrow mesenchymal stem cells partly at least independent of SDF-1/CXCR4 axis and PI3K/AKT pathway. Int J Clin Exp Med. 2015;8(1):188–202.PubMedPubMedCentral
87.
go back to reference Xie X, Piao L, Cavey GS, Old M, Teknos TN, Mapp AK, et al. Phosphorylation of Nanog is essential to regulate Bmi1 and promote tumorigenesis. Oncogene. 2014;33(16):2040–52.CrossRefPubMed Xie X, Piao L, Cavey GS, Old M, Teknos TN, Mapp AK, et al. Phosphorylation of Nanog is essential to regulate Bmi1 and promote tumorigenesis. Oncogene. 2014;33(16):2040–52.CrossRefPubMed
88.
go back to reference Ho B, Olson G, Figel S, Gelman I, Cance WG, Golubovskaya VM. Nanog increases focal adhesion kinase (FAK) promoter activity and expression and directly binds to FAK protein to be phosphorylated. J Biol Chem. 2012;287(22):18656–73.CrossRefPubMedPubMedCentral Ho B, Olson G, Figel S, Gelman I, Cance WG, Golubovskaya VM. Nanog increases focal adhesion kinase (FAK) promoter activity and expression and directly binds to FAK protein to be phosphorylated. J Biol Chem. 2012;287(22):18656–73.CrossRefPubMedPubMedCentral
89.
go back to reference Golubovskaya VM. FAK and Nanog cross talk with p53 in cancer stem cells. Anti Cancer Agents Med Chem. 2013;13(4):576–80.CrossRef Golubovskaya VM. FAK and Nanog cross talk with p53 in cancer stem cells. Anti Cancer Agents Med Chem. 2013;13(4):576–80.CrossRef
Metadata
Title
Perspective: Cooperation of Nanog, NF-κΒ, and CXCR4 in a regulatory network for directed migration of cancer stem cells
Authors
Masoumeh Es-haghi
Sara Soltanian
Hesam Dehghani
Publication date
01-02-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 2/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-4690-6

Other articles of this Issue 2/2016

Tumor Biology 2/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine