Notch-Jagged signalling can give rise to clusters of cells exhibiting a hybrid epithelial/mesenchymal phenotype

Journal of the Royal Society Interface

Volumn 13, Issue 118, 2016, Pages

  Boareto, Marcelo ^a,d,j   Jolly, Mohit Kumar ^a,b   Goldman, Aaron ^f,g,h   Pietilä, Mika ^e,k   Mani, Sendurai A ^e   Sengupta, Shiladitya ^f,g,h,i   Ben Jacob, Eshel ^a,c,j   Levine, Herbert ^a,b   Onuchic, José N ^a  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^h BRIGHAM AND WOMEN S HOSPITAL   (United States)

ⁱ DANA FARBER CANCER INSTITUTE   (United States)

^j ETH ZURICH   (Switzerland)

^k UNIVERSITY OF TURKU   (Finland)

more..

Author keywords

Cell; Cell communication; Circulating tumour cells; Epithelial; Hybrid epithelial mesenchymal phenotype; Mesenchymal transition; Multistability; Notch signalling

Indexed keywords

CELL DEATH; CELLS; CYTOLOGY; PATHOLOGY; TUMORS;

CELL COMMUNICATION; CIRCULATING TUMOUR CELLS; EPITHELIAL; HYBRID EPITHELIAL/MESENCHYMAL PHENOTYPE; MESENCHYMAL TRANSITION; MULTI STABILITIES;

CELL SIGNALING;

JAGGED1; NOTCH RECEPTOR; JAG1 PROTEIN, HUMAN; PROTEIN JAGGED 1; TUMOR PROTEIN;

APOPTOSIS; ARTICLE; CELL COMMUNICATION; CIRCULATING TUMOR CELL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; METASTASIS; PHENOTYPE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; THEORETICAL MODEL; TUMOR GROWTH; BIOLOGICAL MODEL; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; JAGGED-1 PROTEIN; MODELS, BIOLOGICAL; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASMS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84973402922     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2015.1106     Document Type: Article

References (71)

1. Gupta GP, Massagué J. 2006 Cancer metastasis: building a framework. Cell 127, 679-695. (doi:10. 1016/j.cell.2006.11.001)
2. Tsai JH, Yang J. 2013 Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev. 27, 2192-2206. (doi:10.1101/gad.225334.113)
3. Yang J et al. 2004 Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939. (doi:10.1016/j.cell. 2004.06.006)
4. Yu M et al. 2013 Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580-584. (doi:10.1126/science.1228522)
5. Aceto N et al. 2014 Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158, 1110-1122. (doi:10.1016/j. cell.2014.07.013)
6. De Craene B, Berx G. 2013 Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer 13, 97-110. (doi:10. 1038/nrc3447)
7. Jolly MK, Boareto M, Huang B, Jia D, Lu M, Ben-Jacob E, Onuchic JN, Levine H. 2015 Implications of the hybrid epitheliakl/mesenchymal phenotype in metastasis. Front. Oncol. 5, 155. (doi:10.3389/fonc. 2015.00155)
8. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T. 2008 A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582- 589. (doi:10.1038/embor. 2008.74)
9. Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U, Hermeking H. 2011 miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10, 4256-4271. (doi:10.4161/cc.10.24. 18552)
10. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ. 2008 A doublenegative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelialmesenchymal transition. Cancer Res. 68, 7846-7854. (doi:10.1158/0008-5472.CAN-08-1942)
11. Guaita S et al. 2002 Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J. Biol. Chem. 277, 39 209-39 216. (doi:10.1074/jbc.M206400200)
12. Ahn Y-H et al. 2012 ZEB1 drives prometastatic actin cytoskeletal remodeling by downregulating miR-34a expression. J. Clin. Invest. 122, 3170-3183. (doi:10. 1172/JCI63608)
13. Lu M, Jolly MK, Levine H, Onuchic JN, Ben-Jacob E. 2013 MicroRNA-based regulation of epithelialhybrid-mesenchymal fate determination. Proc. Natl Acad. Sci. USA 110, 18 174-18 179. (doi:10.1073/ pnas.1318192110)
14. Kumar S, Das A, Sen S. 2014 Extracellular matrix density promotes EMT by weakening cell-cell adhesions. Mol. Biosyst. 10, 838-850. (doi:10. 1039/c3mb70431a)
15. Espinoza I, Miele L. 2013 Deadly crosstalk: Notch signaling at the intersection of EMT and cancer stem cells. Cancer Lett. 341, 41-45. (doi:10.1016/j. canlet.2013.08.027)
16. Wei SC et al. 2015 Matrix stiffness drives epithelial- mesenchymal transition and tumour metastasis through a TWIST1- G3BP2 mechanotransduction pathway. Nat. Cell Biol. 17, 678-688. (doi:10.1038/ncb3157)
17. Plaks V, Kong N, Werb Z. 2015 The cancer stem cell niche: how essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 16, 225-238. (doi:10.1016/j.stem.2015.02.015)
18. Andersson ER, Sandberg R, Lendahl U. 2011 Notch signaling: simplicity in design, versatility in function. Development 138, 3593- 3612. (doi:10. 1242/dev.063610)
19. Shimojo H, Ohtsuka T, Kageyama R. 2011 Dynamic expression of notch signaling genes in neural stem/ progenitor cells. Front. Neurosci. 5, 78. (doi:10.3389/ fnins.2011.00078)
20. Manderfield LJ, High FA, Engleka KA, Liu F, Li L, Rentschler S, Epstein JA. 2012 Notch activation of Jagged1 contributes to the assembly of the arterial wall. Circulation 125, 314-323. (doi:10.1161/ CIRCULATIONAHA.111.047159)
21. Boareto M, Jolly MK, Lu M, Onuchic JN, Clementi C, Ben-Jacob E. 2015 Jagged- Delta asymmetry in Notch signaling can give rise to a sender/receiver hybrid phenotype. Proc. Natl Acad. Sci. USA 112, E402- E409. (doi:10.1073/pnas.1416287112)
22. Jolly MK, Boareto M, Lu M, Onuchic JN, Clementi C, Ben-Jacob E. 2015 Operating principles of Notch-Delta-Jagged module of cell-cell communication. New J. Phys. 17, 055021. (doi:10.1088/1367-2630/ 17/5/055021)
23. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. 2008 Notch signaling mediates hypoxiainduced tumor cell migration and invasion. Proc. Natl Acad. Sci. USA 105, 6392-6397. (doi:10.1073/ pnas.0802047105)
24. Niessen K, Fu Y, Chang L, Hoodless PA, McFadden D, Karsan A. 2008 Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J. Cell Biol. 182, 315- 325. (doi:10. 1083/jcb.200710067)
25. Brabletz S et al. 2011 The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J. 30, 770-782. (doi:10.1038/emboj.2010.349)
26. de Antonellis P et al. 2011 MiR-34a targeting of Notch ligand delta-like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS ONE 6, e24584. (doi:10.1371/journal.pone.0024584)
27. Bu P et al. 2013 A microRNA miR-34a-regulated bimodal switch targets notch in colon cancer stem cells. Cell Stem Cell 12, 602-615. (doi:10.1016/j. stem.2013.03.002)
28. Tian X-J, Zhang H, Xing J. 2013 Coupled reversible and irreversible bistable switches underlying TGFbinduced epithelial to mesenchymal transition. Biophys. J. 105, 1079- 1089. (doi:10.1016/j.bpj. 2013.07.011)
29. Steinway SN, Gomez Tejeda Zañudo J, Ding W, Rountree CB, Feith DJ, Loughran TP, Albert R. 2014 Network modeling of TGFb signaling in hepatocellular carcinoma epithelial-to-mesenchymal transition reveals joint Sonic hedgehog and Wnt pathway activation. Cancer Res. 74, 5963- 5977. (doi:10.1158/0008-5472.CAN-14-0225)
30. Park S-MM, Gaur AB, Lengyel E, Peter ME. 2008 The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22, 894-907. (doi:10.1101/gad.1640608)
31. Schliekelman MJ et al. 2015 Molecular portraits of epithelial, mesenchymal and hybrid states in lung adenocarcinoma and their relevance to survival. Cancer Res. 75, 1789-1800. (doi:10.1158/0008-5472.CAN-14-2535)
32. Huang RY-J et al. 2013 An EMT spectrum defines an anoikis-resistant and spheroidogenic intermediate mesenchymal state that is sensitive to e-cadherin restoration by a src-kinase inhibitor, saracatinib (AZD0530). Cell Death Dis. 4, e915. (doi:10.1038/ cddis.2013.442)
33. Jia D, Jolly MK, Boareto M, Parsana P, Mooney SM, Pienta KJ, Levine H, Ben-Jacob E. 2015 OVOL guides the epithelial-hybrid-mesenchymal transition. Oncotarget 6, 15 436-15 448. (doi:10.18632/ oncotarget.3623)
34. Petrovic J, Formosa-Jordan P, Luna-Escalante JC, Abelló G, Ibañes M, Neves J, Giraldez F. 2014 Ligand-dependent Notch signaling strength orchestrates lateral induction and lateral inhibition in the developing inner ear. Development 141, 2313-2324. (doi:10.1242/dev.108100)
35. Lu J et al. 2013 Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 23, 171-185. (doi:10.1016/j.ccr.2012.12.021)
36. Yaswen P. 2015 Reinforcing targeted therapeutics with phenotypic stability factors. Cell Cycle 13, 3818-3822. (doi:10.4161/15384101.2014.985071)
37. Jolly MK, Jia D, Boareto M, Mani SA, Pienta KJ, Ben-Jacob E, Levine H. 2015 Coupling the modules of EMT and stemness: a tunable 'stemness window' model. Oncotarget 6, 25 161- 25 174. (doi:10. 18632/oncotarget.4629)
38. Jolly MK, Huang B, Lu M, Mani SA, Levine H, Ben-Jacob E. 2014 Towards elucidating the connection between epithelial2mesenchymal transitions and stemness. J. R. Soc. Interface 11, 20140962. (doi:10. 1098/rsif.2014.0962)
39. Grosse-Wilde A, Fouquier d' Herouei A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, del Sol A, Walters K-A, Huang S. 2015 Stemness of the hybrid epithelial/mesenchymal state in breast cancer and its association with poor survival. PLoS ONE 10, e0126522. (doi:10.1371/journal.pone. 0126522)
40. Goldman A, Majumder B, Dhawan A, Ravi S, Goldman D, Kohandel M, Majumder PK, Sengupta S. 2015 Temporally sequenced anticancer drugs overcome adaptive resistance by targeting a vulnerable chemotherapy-induced phenotypic transition. Nat. Commun. 6, 6139. (doi:10.1038/ ncomms7139)
41. Pattabiraman DR, Weinberg RA. 2014 Tackling the cancer stem cells-what challenges do they pose? Nat. Rev. Drug Discov. 13, 497-512. (doi:10.1038/ nrd4253)
42. Benedito R, Roca C, Sörensen I, Adams S, Gossler A, Fruttiger M, Adams RH. 2009 The Notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137, 1124-1135. (doi:10.1016/j. cell.2009.03.025)
43. Saravanamuthu SS, Gao CY, Zelenska PS. 2009 Notch signaling is required for lateral induction of Jagged1 during FGF-induced lens fiber differentiation. Dev. Biol. 332, 166- 176. (doi:10. 1016/j.ydbio.2009.05.566)
44. Hartman BH, Reh TA, Bermingham-McDonogh O. 2010 Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc. Natl Acad. Sci. USA 107, 15 792-15 797. (doi:10.1073/pnas.1002827107)
45. Lecharpentier A, Vielh P, Perez-Moreno P, Planchard D, Soria JC, Farace F. 2011 Detection of circulating tumour cells with a hybrid (epithelial/ mesenchymal) phenotype in patients with metastatic non-small cell lung cancer. Br. J. Cancer 105, 1338-1341. (doi:10.1038/bjc.2011.405)
46. Hou J-M et al. 2011 Circulating tumor cells as a window on metastasis biology in lung cancer. Am. J. Pathol. 178, 989-996. (doi:10.1016/j.ajpath. 2010.12.003)
47. Armstrong AJ et al. 2011 Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol. Cancer Res. 9, 997-1007. (doi:10. 1158/1541-7786.MCR-10-0490)
48. Joosse SA, Gorges TM, Pantel K. 2015 Biology, detection, and clinical implications of circulating tumor cells. EMBO Mol. Med. 7, 1-11. (doi:10. 15252/emmm.201303698)
49. Liotta LA, Klelnerman J, Saldel GM. 1976 The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res. 36, 889-894.
50. Nieto MA. 2013 Epithelial plasticity: a common theme in embryonic and cancer cells. Science 342, 1234850. (doi:10.1126/science.1234850)
51. Voulgari A, Pintzas A. 2009 Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim. Biophys. Acta Rev. Cancer 1796, 75-90. (doi:10.1016/j.bbcan.2009.03. 002)
52. Arnoux V, Côme C, Kusewitt DF, Hudson LG, Savagner P. 2005 Cutaneous wound reepithelialization. In Rise and fall of epithelial phenotype, pp. 111- 134. New York, NY: Springer US.
53. Tam WL, Weinberg RA. 2013 The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat. Med. 19, 1438-1449. (doi:10.1038/nm.3336)
54. Ombrato L, Malanchi I. 2014 The EMT universe: space between cancer cell dissemination and metastasis initiation. Crit. Rev. Oncog. 19, 349-361. (doi:10.1615/CritRevOncog.2014011802)
55. Andriani F et al. 2015 Conversion to stem-cell state in response to microenvironmental cues is regulated by balance between epithelial and mesenchymal features in lung cancer cells. Mol. Oncol. 10, 253-271. (doi:10.1016/j.molonc.2015.10.002)
56. Sansone P et al. 2007 IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J. Clin. Invest. 117, 3988-4002. (doi:10.1172/ JCI32533)
57. Johnston DA, Dong B, Hughes CCW. 2009 TNF induction of jagged-1 in endothelial cells is NFkBdependent. Gene 435, 36-44. (doi:10.1016/j.gene.2009.01.003)
58. Li D, Masiero M, Banham AH, Harris AL. 2014 The notch ligand JAGGED1 as a target for anti-tumor therapy. Front. Oncol. 4, 254. (doi:10.3389/fonc. 2014.00254)
59. Kangsamaksin T, Murtomaki A, Kofler NM, Cuervo H, Chaudhri RA, Tattersall IW, Rosenstiel PE, Shawber CJ, Kitajewski J. 2014 Notch decoys that selectively block Dll/Notch or Jag/Notch disrupt angiogenesis by unique mechanisms to inhibit tumor growth. Cancer Discov. 5, 182-197. (doi:10.1158/2159-8290.CD-14-0650)
60. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B, Miele L. 2008 Rational targeting of Notch signaling in cancer. Oncogene 27, 5124-5131. (doi:10.1158/ AACR.EDB-08-8135)
61. De Back W, Zhou JX, Brusch L. 2013 On the role of lateral stabilization during early patterning in the on the role of lateral stabilization during early patterning in the pancreas. J. R. Soc. Interface 10, 20120766. (doi:10.1098/rsif.2012.0766)
62. Savill NJ, Sherratt JA. 2003 Control of epidermal stem cell clusters by Notch-mediated lateral induction. Dev. Biol. 258, 141-153. (doi:10.1016/S0012-1606(03)00107-6)
63. Liu S et al. 2014 Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Rep. 2, 78-91. (doi:10.1016/j.stemcr.2013.11.009)
64. Enderling H. 2015 Cancer stem cells: small subpopulation or evolving fraction? Integr. Biol. (Camb). 7, 14-23. (doi:10.1039/c4ib00191e)
65. Poleszczuk J, Hahnfeldt P, Enderling H. 2015 Evolution and phenotypic selection of cancer stem cells. PLoS Comput. Biol. 11, e1004025. (doi:10. 1371/journal.pcbi.1004025)
66. Dhawan A, Kohandel M, Hill R, Sivaloganathan S. 2014 Tumour control probability in cancer stem cells hypothesis. PLoS ONE 9, 5-10. (doi:10.1371/ journal.pone.0096093)
67. Sehl ME, Shimada M, Landeros A, Lange K, Wicha MS. 2015 Modeling of cancer stem cell state transitions predicts therapeutic response. PLoS ONE 10, e0135797. (doi:10.1371/journal.pone. 0135797)
68. Yang KR, Mooney SM, Zarif JC, Coffey DS, Taichman RS, Pienta KJ. 2014 Niche inheritance: a cooperative pathway to enhance cancer cell fitness though ecosystem engineering. J. Cell. Biochem. 115, 1478-1485. (doi:10.1002/jcb. 24813)
69. Ben-Jacob E, Coffey DS, Levine H. 2012 Bacterial survival strategies suggest rethinking cancer cooperativity. Trends Microbiol. 20, 403-410. (doi:10.1016/j.tim.2012.06.001)
70. Clewley R. 2012 Hybrid models and biological model reduction with PyDSTool. PLoS Comput. Biol. 8, e1002628. (doi:10.1371/journal.pcbi. 1002628)
71. MB, 0000-0002-9915-6376