The ubiquitin E3 ligase ITCH enhances breast tumor progression by inhibiting the Hippo tumor suppressor pathway

Oncotarget

Volumn 5, Issue 21, 2014, Pages 10886-10900

  Salah, Zaidoun ^a,b   Itzhaki, Ella ^a   Aqeilan, Rami I ^a,c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b AL QUDS UNIVERSITY   (Palestine)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Breast cancer; Hippo pathway; ITCH; Metastasis; YAP

Indexed keywords

PROTEIN HIPPO; PROTEIN ITCH; PROTEIN YAP; TUMOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; HIPPO PROTEIN, HUMAN; ITCH PROTEIN, HUMAN; LATS1 PROTEIN, HUMAN; MESSENGER RNA; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST METASTASIS; BREAST TUMOR; CANCER SURVIVAL; CARCINOGENICITY; ENZYME ACTIVE SITE; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; POINT MUTATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR INVASION; UPREGULATION; ANIMAL; APOPTOSIS; CELL ADHESION; CELL MOTION; CELL PROLIFERATION; CELL TRANSFORMATION; DISEASE COURSE; DRUG SCREENING; ENZYME IMMUNOASSAY; EXPERIMENTAL MAMMARY NEOPLASM; GENETICS; LUNG TUMOR; METABOLISM; MORTALITY; NONOBESE DIABETIC MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; SECONDARY; TUMOR CELL CULTURE; UBIQUITINATION; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED NOD; MICE, SCID; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; UBIQUITINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84916910418     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2540     Document Type: Article

References (55)

1. Harvey KF, Zhang X, Thomas DM. The Hippo pathway and human cancer. Nat Rev Cancer. 2013; 13:246-257.
2. Salah Z, Aqeilan RI. WW domain interactions regulate the Hippo tumor suppressor pathway. Cell Death Dis. 2011; 2:e172.
3. Nishio M, Otsubo K, Maehama T, Mimori K, Suzuki A. Capturing the mammalian Hippo: elucidating its role in cancer. Cancer Sci. 2013; 104:1271-1277.
4. Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem. 2008; 283:5496-5509.
5. Zhang J, Smolen GA, Haber DA. Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res. 2008; 68:2789-2794.
6. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 2007; 21:2747-2761.
7. Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH, Zhao S, Xiong Y, Guan KL. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol. 2008; 28:2426-2436.
8. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell. 2007; 130:1120-1133.
9. Zhao B, Kim J, Ye X, Lai ZC, Guan KL. Both TEAD-binding and WW domains are required for the growth stimulation and oncogenic transformation activity of yesassociated protein. Cancer Res. 2009; 69:1089-1098.
10. Grusche FA, Richardson HE, Harvey KF. Upstream regulation of the hippo size control pathway. Curr Biol. 2010; 20:R574-582.
11. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti AR, Poletti A, Daidone MG, Dupont S, Basso G, Bicciato S, Piccolo S. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell. 2011; 147:759-772.
12. Yu FX, Guan KL. The Hippo pathway: regulators and regulations. Genes Dev. 2013; 27:355-371.
13. Yu FX, Zhao B, Panupinthu N, Jewell JL, Lian I, Wang LH, Zhao J, Yuan H, Tumaneng K, Li H, Fu XD, Mills GB, Guan KL. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell. 2012; 150: 780-791.
14. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C, Hong W. Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J Biol Chem. 2011; 286: 7018-7026.
15. Wang W, Huang J, Chen J. Angiomotin-like proteins associate with and negatively regulate YAP1. J Biol Chem. 2011; 286:4364-4370.
16. Zhao B, Li L, Lu Q, Wang LH, Liu CY, Lei Q, Guan KL. Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev. 2011; 25:51-63.
17. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, Camargo FD. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell. 2011; 144:782-795.
18. Salah Z, Cohen S, Itzhaki E, Aqeilan RI. NEDD4 E3 ligase inhibits the activity of the Hippo pathway by targeting LATS1 for degradation. Cell Cycle. 2013; 12:3817-3823.
19. Yeung B, Ho KC, Yang X. WWP1 E3 ligase targets LATS1 for ubiquitin-mediated degradation in breast cancer cells. PLoS One. 2013; 8:e61027.
20. Wang C, An J, Zhang P, Xu C, Gao K, Wu D, Wang D, Yu H, Liu JO, Yu L. The Nedd4-like ubiquitin E3 ligases target angiomotin/p130 to ubiquitin-dependent degradation. Biochem J. 2012; 444:279-289.
21. Salah Z, Melino G, Aqeilan RI. Negative regulation of the Hippo pathway by E3 ubiquitin ligase ITCH is sufficient to promote tumorigenicity. Cancer Res. 2011; 71:2010-2020.
22. Bernassola F, Karin M, Ciechanover A, Melino G. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell. 2008; 14:10-21.
23. Perry WL, Hustad CM, Swing DA, O'Sullivan TN, Jenkins NA, Copeland NG. The itchy locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice. Nat Genet. 1998; 18:143-146.
24. Fang D, Elly C, Gao B, Fang N, Altman Y, Joazeiro C, Hunter T, Copeland N, Jenkins N, Liu YC. Dysregulation of T lymphocyte function in itchy mice: a role for Itch in TH2 differentiation. Nat Immunol. 2002; 3:281-287.
25. Fang D, Kerppola TK. Ubiquitin-mediated fluorescence complementation reveals that Jun ubiquitinated by Itch/AIP4 is localized to lysosomes. Proc Natl Acad Sci U S A. 2004; 101:14782-14787.
26. Gao M, Labuda T, Xia Y, Gallagher E, Fang D, Liu YC, Karin M. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science. 2004; 306:271-275.
27. Rossi M, De Laurenzi V, Munarriz E, Green DR, Liu YC, Vousden KH, Cesareni G, Melino G. The ubiquitinprotein ligase Itch regulates p73 stability. Embo J. 2005; 24: 836-848.
28. Rossi M, Aqeilan RI, Neale M, Candi E, Salomoni P, Knight RA, Croce CM, Melino G. The E3 ubiquitin ligase Itch controls the protein stability of p63. Proc Natl Acad Sci U S A. 2006; 103:12753-12758.
29. Sundvall M, Korhonen A, Paatero I, Gaudio E, Melino G, Croce CM, Aqeilan RI, Elenius K. Isoform-specific monoubiquitination, endocytosis, and degradation of alternatively spliced ErbB4 isoforms. Proc Natl Acad Sci U S A. 2008; 105:4162-4167.
30. Datta S, HoenerhoffMJ, Bommi P, Sainger R, Guo WJ, Dimri M, Band H, Band V, Green JE, Dimri GP. Bmi-1 cooperates with H-Ras to transform human mammary epithelial cells via dysregulation of multiple growthregulatory pathways. Cancer Res. 2007; 67:10286-10295.
31. Chambers AF. MDA-MB-435 and M14 cell lines: identical but not M14 melanoma? Cancer Res. 2009; 69:5292-5293.
32. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010; 123:725-731.
33. Tome Y, Uehara F, Mii S, Yano S, Zhang L, Sugimoto N, Maehara H, Bouvet M, Tsuchiya H, Kanaya F, Hoffman RM. 3-dimensional tissue is formed from cancer cells in vitro on Gelfoam(R), but not on Matrigel. Journal of cellular biochemistry. 2014; 115:1362-1367.
34. Hoffman RM. The multiple uses of fluorescent proteins to visualize cancer in vivo. Nat Rev Cancer. 2005; 5:796-806.
35. Hoffman RM, Yang M. Whole-body imaging with fluorescent proteins. Nat Protoc. 2006; 1:1429-1438.
36. Hoffman RM, Yang M. Subcellular imaging in the live mouse. Nat Protoc. 2006; 1:775-782.
37. Yamamoto N, Jiang P, Yang M, Xu M, Yamauchi K, Tsuchiya H, Tomita K, Wahl GM, Moossa AR, Hoffman RM. Cellular dynamics visualized in live cells in vitro and in vivo by differential dual-color nuclearcytoplasmic fluorescent-protein expression. Cancer Res. 2004; 64:4251-4256.
38. Wang C, An J, Zhang P, Xu C, Gao K, Wu D, Wang D, Yu H, Liu JO, Yu L. The Nedd4-like ubiquitin E3 ligases target angiomotin/p130 to ubiquitin-dependent degradation. Biochem J. 2012; 444:279-289.
39. Oka T, Schmitt AP, Sudol M. Opposing roles of angiomotin-like-1 and zona occludens-2 on pro-apoptotic function of YAP. Oncogene. 2012; 31:128-134.
40. Adler JJ, Heller BL, Bringman LR, Ranahan WP, Cocklin RR, Goebl MG, Oh M, Lim HS, Ingham RJ, Wells CD. Amot130 adapts atrophin-1 interacting protein 4 to inhibit yes-associated protein signaling and cell growth. J Biol Chem. 2013; 288:15181-15193.
41. Adler JJ, Heller BL, Bringman LR, Ranahan WP, Cocklin RR, Goebl MG, Oh M, Lim HS, Ingham RJ, Wells CD. Amot130 adapts atrophin-1 interacting protein 4 to inhibit yes-associated protein signaling and cell growth. J Biol Chem. 2013; 288:15181-15193.
42. Oberst A, Malatesta M, Aqeilan RI, Rossi M, Salomoni P, Murillas R, Sharma P, Kuehn MR, Oren M, Croce CM, Bernassola F, Melino G. The Nedd4-binding partner 1 (N4BP1) protein is an inhibitor of the E3 ligase Itch. Proc Natl Acad Sci U S A. 2007; 104:11280-11285.
43. Abu-Odeh M, Bar-Mag T, Huang H, Kim T, Salah Z, Abdeen SK, Sudol M, Reichmann D, Sidhu S, Kim PM, Aqeilan RI. Characterizing WW Domain Interactions of Tumor Suppressor WWOX Reveals Its Association with Multiprotein Networks. J Biol Chem. 2014; 289: 8865-8880.
44. Chen ZJ, Sun LJ. Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell. 2009; 33:275-286.
45. Abu-Odeh M, Salah S, Herbel C, Hofmann TG, Aqeilan RI. WWOX, the common fragile site FRA16D gene product, regulates ATM activation and the DNA damage response. Proc Natl Acad Sci U S A. 2014; In press.
46. Harvey KF, Zhang X, Thomas DM. The Hippo pathway and human cancer. Nat Rev Cancer. 2013; 13:246-257.
47. Inda MC, Defelipe J, Munoz A. The distribution of chandelier cell axon terminals that express the GABA plasma membrane transporter GAT-1 in the human neocortex. Cereb Cortex. 2007; 17:2060-2071.
48. Overholtzer M, Zhang J, Smolen GA, Muir B, Li W, Sgroi DC, Deng CX, Brugge JS, Haber DA. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci U S A. 2006; 103:12405-12410.
49. Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 2012; 26:54-68.
50. Zhang X, George J, Deb S, Degoutin JL, Takano EA, Fox SB, Bowtell DD, Harvey KF. The Hippo pathway transcriptional co-activator, YAP, is an ovarian cancer oncogene. Oncogene. 2011; 30:2810-2822.
51. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science. 2002; 298:597-600.
52. Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, Brummelkamp TR. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol. 2007; 17:2054-2060.
53. Chen D, Sun Y, Wei Y, Zhang P, Rezaeian AH, Teruya- Feldstein J, Gupta S, Liang H, Lin HK, Hung MC, Ma L. LIFR is a breast cancer metastasis suppressor upstream of the Hippo-YAP pathway and a prognostic marker. Nat Med. 2012; 18:1511-1517.
54. Ishihara T, Tsuda H, Hotta A, Kozaki K, Yoshida A, Noh JY, Ito K, Imoto I, Inazawa J. ITCH is a putative target for a novel 20q11.22 amplification detected in anaplastic thyroid carcinoma cells by array-based comparative genomic hybridization. Cancer Sci. 2008; 99:1940-1949.
55. Lorenzetto E, Brenca M, Boeri M, Verri C, Piccinin E, Gasparini P, Facchinetti F, Rossi S, Salvatore G, Massimino M, Sozzi G, Maestro R, Modena P. YAP1 acts as oncogenic target of 11q22 amplification in multiple cancer subtypes. Oncotarget. 2014; 5:2608-2621.