OVOL guides the epithelial-hybrid-mesenchymal transition

Oncotarget

Volumn 6, Issue 17, 2015, Pages 15436-15448

  Jia, Dongya ^a   Jolly, Mohit Kumar ^a,b   Boareto, Marcelo ^a,d   Parsana, Princy ^e   Mooney, Steven M ^f   Pienta, Kenneth J ^f   Levine, Herbert ^a,b   Ben Jacob, Eshel ^a,c  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e Johns Hopkins University   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer systems biology; EMT; Metastasis; OVOL; Partial EMT

Indexed keywords

DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; MICRORNA; MIRN200 MICRORNA, HUMAN; OVOL1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; ZEB1 PROTEIN, HUMAN;

EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; HUMAN; MALE; METABOLISM; METASTASIS; PATHOLOGY; PHYSIOLOGY; PROCEDURES; PROSTATE TUMOR; SYSTEMS BIOLOGY; THEORETICAL MODEL;

DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICRORNAS; MODELS, THEORETICAL; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; SYSTEMS BIOLOGY; TRANSCRIPTION FACTORS; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 84934311597     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3623     Document Type: Article

References (57)

1. Gupta GP, Massagué J. Cancer metastasis: building a framework. Cell. 2006; 127:679-95.
2. Nieto MA. Epithelial plasticity: a common theme in embryonic and cancer cells. Science. 2013; 342:1234850.
3. Revenu C, Gilmour D. EMT 2.0: shaping epithelia through collective migration. Curr Opin Genet Dev. 2009; 19:338-42.
4. Micalizzi DS, Farabaugh SM, Ford HL. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. J Mammary Gland Biol Neoplasia. 2010; 15:117-34.
5. Arnoux V, Côme C, Kusewitt DF, Hudson LG, Savagner P. Cutaneous Wound Reepithelialization. Rise and Fall of Epithelial Phenotype. Springer US. 2005; :111-34.
6. Huang RY-J, Wong MK, Tan TZ, Kuay KT, Ng a HC, Chung VY, et al. 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. 2013; 4:e915.
7. Sampson VB, David JM, Puig I, Patil PU, de Herreros AG, Thomas G V, Rajasekaran AK. Wilms' tumor protein induces an epithelial-mesenchymal hybrid differentiation state in clear cell renal cell carcinoma. PLoS One. 2014; 9:e102041.
8. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol. 2006; 172:973-81.
9. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009; 139:871-90.
10. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013; 339:580-4.
11. Lecharpentier A, Vielh P, Perez-Moreno P, Planchard D, Soria JC, Farace F. Detection of circulating tumour cells with a hybrid (epithelial/mesenchymal) phenotype in patients with metastatic non-small cell lung cancer. Br J Cancer. 2011; 105:1338-41.
12. Hou J-M, Krebs M, Ward T, Sloane R, Priest L, Hughes A, Clack G, Ranson M, Blackhall F, Dive C. Circulating Tumor Cells as a Window on Metastasis Biology in Lung Cancer. Am J Pathol. 2011; 178:989-96.
13. Armstrong AJ, Marengo MS, Oltean S, Kemeny G, Bitting RL, Turnbull JD, Herold CI, Marcom PK, George DJ, Garcia-Blanco MA. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol cancer Res MCR. 2011; 9:997-1007.
14. Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS, Spencer JA, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell. 2014; 158:1110-22.
15. Ben-Jacob E, Coffey DS, Levine H. Bacterial survival strategies suggest rethinking cancer cooperativity. Trends Microbiol. 2012; 20:403-10.
16. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008; 9:582-9.
17. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, Goodall GJ. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 2008; 68:7846-54.
18. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008; May 10:593-601.
19. Lu M, Jolly MK, Levine H, Onuchic JN, Ben-Jacob E. MicroRNA-based regulation of epithelial-hybrid-mesenchymal fate determination. Proc Natl Acad Sci U S A. 2013; 110:18174-9.
20. Lu M, Jolly MK, Onuchic J, Ben-Jacob E. Toward Decoding the Principles of Cancer Metastasis Circuits. Cancer Res. 2014; 74:4574-87.
21. Roca H, Pande M, Huo JS, Hernandez J, Cavalcoli JD, Pienta KJ, McEachin RC. A bioinformatics approach reveals novel interactions of the OVOL transcription factors in the regulation of epithelial-mesenchymal cell reprogramming and cancer progression. BMC Syst Biol. 2014; 8:29.
22. Watanabe K, Villarreal-Ponce A, Sun P, Salmans ML, Fallahi M, Andersen B, Dai X. Mammary morphogenesis and regeneration require the inhibition of EMT at terminal end buds by Ovol2 transcriptional repressor. Dev Cell. 2014; 29:59-74.
23. Dai X, Schonbaum C, Degenstein L, Bai W, Mahowald A, Fuchs E. The ovo gene required for cuticle formation and oogenesis in flies is involved in hair formation and spermatogenesis in mice. Genes Dev. 1998; 12:3452-63.
24. Mackay DR, Hu M, Li B, Rheaume C, Dai X. The mouse Ovol2 gene is required for cranial neural tube development. Dev Biol. 2006; 291:38-52.
25. Payre F, Vincent A, Carreno S. ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature. 1999; 400:271-5.
26. Nair M, Teng A, Bilanchone V, Agrawal A, Li B, Dai X. Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J Cell Biol. 2006; Apr 173:253-64.
27. Kowanetz M, Valcourt U, Bergstrom R, Heldin C-H, Moustakas A. Id2 and Id3 Define the Potency of Cell Proliferation and Differentiation Responses to Transforming Growth Factor? and Bone Morphogenetic Protein. Mol Cell Biol. 2004; 24:4241-54.
28. Gomis RR, Alarcon C, He W, Wang Q, Seoane J, Lash A, Massague J. A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci U S A. 2006; 103:12747-52.
29. Roca H, Hernandez J, Weidner S, McEachin RC, Fuller D, Sud S, et al. Transcription Factors OVOL1 and OVOL2 Induce the Mesenchymal to Epithelial Transition in Human Cancer. PLoS One. 2013; 8:e76773.
30. Nair M, Bilanchone V, Ortt K, Sinha S, Dai X. Ovol1 represses its own transcription by competing with transcription activator c-Myb and by recruiting histone deacetylase activity. Nucleic Acids Res. 2007; 35:1687-97.
31. Guo L, Chen C, Shi M, Wang F, Chen X, Diao D, Hu M, Yu M, Qian L, Guo N. Stat3-coordinated Lin-28-let-7-HMGA2 and miR-200-ZEB1 circuits initiate and maintain oncostatin M-driven epithelial-mesenchymal transition. Oncogene. 2013; 32:5272-82.
32. Li S, Yang J. Ovol Proteins: Guardians against EMT during Epithelial Differentiation. Dev Cell. 2014; 29:1-2.
33. Lee B, Villarreal-Ponce A, Fallahi M, Ovadia J, Sun P, Yu Q-C, Ito S, Sinha S, Nie Q, Dai X. Transcriptional mechanisms link epithelial plasticity to adhesion and differentiation of epidermal progenitor cells. Dev Cell. 2014; 29:47-58.
34. Pinto CA, Widodo E, Waltham M, Thompson EW. Breast cancer stem cells and epithelial mesenchymal plasticity-Implications for chemoresistance. Cancer Lett. 2013; 341:56-62.
35. Futterman MA, García AJ, Zamir E a. Evidence for partial epithelial-to-mesenchymal transition (pEMT) and recruitment of motile blastoderm edge cells during avian epiboly. Dev Dyn. 2011; 240:1502-11.
36. Schliekelman MJ, Taguchi A, Zhu J, Dai X, Rodriguez J, Celiktas M, et al. Molecular portraits of epithelial, mesenchymal and hybrid states in lung adenocarcinoma and their relevance to survival. Cancer Res. 2015; canres-2535.
37. Leroy P, Mostov KE. Slug Is Required for Cell Survival during Partial Epithelial-Mesenchymal Transition of HGF-induced tubulogenesis. J Cell Sci. 2007; 18:1943-52.
38. Jordan NV, Johnson GL, Abell AN. Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell Cycle. 2011; 10:2865-73.
39. Garcãa de Herreros A. Epithelial to mesenchymal transition in tumor cells as consequence of phenotypic instability. Front Cell Dev Biol. 2014; 2 (December) :1-5.
40. Zhang T, Zhu Q, Xie Z, Chen Y, Qiao Y, Li L, Jing N. The zinc finger transcription factor Ovol2 acts downstream of the bone morphogenetic protein pathway to regulate the cell fate decision between neuroectoderm and mesendoderm. J Biol Chem. 2013; 288:6166-77.
41. Chng Z, Teo A, Pedersen RA, Vallier L. SIP1 Mediates Cell-Fate Decisions between Neuroectoderm and Mesendoderm in Human Pluripotent Stem Cells. Cell Stem Cell. 2010; 6:59-70.
42. Jolly MK, Huang B, Lu M, Mani SA, Levine H, Ben-jacob E. Towards elucidating the connection between epithelial-mesenchymal transitions and stemness. J R Soc Interface. 2014; 11:20140962.
43. Chao Y, Wu Q, Acquafondata M, Dhir R, Wells A. Partial Mesenchymal to Epithelial Reverting Transition in Breast and Prostate Cancer Metastases. Cancer Microenviron. 2011; 5:19-28.
44. Ocaña OH, Córcoles R, Fabra A, Moreno-Bueno G, Acloque H, Vega S, Barrallo-Gimeno A, Cano A, Nieto MA. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell. 2012; 22:709-24.
45. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell. 2012; 22:725-36.
46. Johansson J, Berg T, Kurzejamska E, Pang M-F, Tabor V, Jansson M, Roswall P, Pietras K, Sund M, Religa P, Fuxe J. MiR-155-mediated loss of C/EBPβ shifts the TGF-β response from growth inhibition to epithelial-mesenchymal transition, invasion and metastasis in breast cancer. Oncogene. 2013; 32:5614-24.
47. Xie P, Sun L, Nayak B, Haruna Y, Liu F, Kashihara N, Kanwar YS. C/EBP-β Modulates Transcription of Tubulointerstitial Nephritis Antigen in Obstructive Uropathy. J Am Soc Nephrol. 2009; 20:807-19.
48. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med. 2003; 9:964-8.
49. Oliveras-Ferraros C, Corominas-Faja B, Vazquez-Martin SA, Martin-Castillo B, Iglesias JM, López-Bonet E, Martin áG, Menendez JA. Epithelial-to-mesenchymal transition (EMT) confers primary resistance to trastuzumab (Herceptin). Cell Cycle. 2012; 11:4020-32.
50. Smit MA, Peeper DS. Epithelial-mesenchymal transition and senescence: Two cancer-related processes are crossing paths. Aging (Albany NY). 2010; 2:735-41.
51. Balázsi G, van Oudenaarden A, Collins JJ. Cellular decision making and biological noise: from microbes to mammals. Cell. 2011; 144:910-25.
52. Steinway SN, Gomez Tejeda Zañudo J, Ding W, Rountree CB, Feith DJ, Loughran TP, Albert R. Network modeling of TGFβ signaling in hepatocellular carcinoma epithelial-to-mesenchymal transition reveals joint Sonic hedgehog and Wnt pathway activation. Cancer Res. 2014; 74:5963-77.
53. Huang B, Lu M, Jolly MK, Tsarfaty I, Onuchic J, Ben-Jacob E. The three-way switch operation of Rac1/RhoA GTPase-based circuit controlling amoeboid-hybrid-mesenchymal transition. Sci Rep. 2014; 4:6449.
54. Chung S, Cooper CR, Farach-Carsron MC, Ogunnaike BA. A control engineering approach to understanding the TGF-b paradox in cancer. J R Soc Interface. 2012; 9:1389-97.
55. Boareto M, Jolly MK, Lu M, Onuchic JN, Clementi C, Ben-Jacob E. Jagged-Delta asymmetry in Notch signaling can give rise to a Sender/Receiver hybrid phenotype. Proc Natl Acad Sci. 2015; 112:E402-9.
56. Lin K, Baritaki S, Militello L, Malaponte G, Bevelacqua Y, Bonavida B. The Role of B-RAF Mutations in Melanoma and the Induction of EMT via Dysregulation of the NF-kB/Snail/RKIP/PTEN Circuit. Genes Cancer. 2010; 1:409-20.
57. Lu M, Jolly MK, Gomoto R, Huang B, Onuchic J, Ben-Jacob E. Tristability in Cancer-Associated MicroRNA-TF Chimera Toggle Switch. J Phys Chem B. 2013; 117:13164-74.