Multifaceted roles of ASB proteins and its pathological significance

doi:10.1007/s11515-018-1506-2

Front. Biol.

2018, Vol. 13

Issue (5) : 376-388 https://doi.org/10.1007/s11515-018-1506-2

RESEARCH ARTICLE

Multifaceted roles of ASB proteins and its pathological significance

Vivek Vishnu Anasa, Palaniyandi Ravanan, Priti Talwar(

)

Apoptosis and Cell Survival Research Lab, Department of Biosciences, School of Biosciences and Technology, VIT University, Vellore, Tamil Nadu, 632014 India

Download: PDF(1269 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

BACKGROUND: Post-translational (PT) modification in cells regulates many intracellular events like signal transduction, transcription, cell cycle, protein quality control, apoptosis and cellular development. Ubiquitination is one of the PT modifications which functions as a marker for degradation of target proteins by the proteasome and as a regulatory mechanism for several signalling pathways. The ubiquitination mechanism requires multiple enzymes, including E1, E2, and E3 ligases. Among them, E3 ligases play a major role in recognizing target proteins and an essential feature of protein homeostatic mechanisms within the cell. Most of the ASB (ankyrin repeat SOCS box) proteins function as RING family of E3 ubiquitin ligases characterized by the presence of two conserved domains N-terminal ankyrin repeat and C-terminal SOCS box domain

METHODS and RESULTS: Current studies have shown that some ASBs function as important regulators of several signalling pathways. This review gives an overview of ASB proteins on numerous cellular processes such as insulin signalling, spermatogenesis, myogenesis and in cellular development. Including various pathological situations, such as cancer, primary open-angle glaucoma, and inflammation, indicating that ASBs has important functions in both normal and pathological development

CONCLUSIONS: This article provides a precise comprehensive focus on ASBs protein structure, its biological functions, and their pathological significance.

Keywords ankyrin repeat SOCS box E3 ligase cancer spermatogenesis cellular development

Corresponding Author(s): Priti Talwar

Online First Date: 07 September 2018 Issue Date: 25 October 2018

Cite this article:

Vivek Vishnu Anasa,Palaniyandi Ravanan,Priti Talwar. Multifaceted roles of ASB proteins and its pathological significance[J]. Front. Biol., 2018, 13(5): 376-388.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-018-1506-2
https://academic.hep.com.cn/fib/EN/Y2018/V13/I5/376

Tab.1 Tabular column of chromosomal location and properties of human ASB genes with their respective substrates identified, cancers involved from NCBI (https://www.ncbi.nlm.nih.gov/pubmed/) and Entrez (www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=gene) databases.

Fig.1 Ubiquitination process and types of E3s. Ubiquitination is an ATP dependent cellular process. Ubiquitin is activated by E1, transferred via transthiolation from E1 to E2. Further, E2∼Ub interacts with an E3.E3s then facilitate ubiquitination of the substrate protein by proteasome formation or activation of other signaling Pathways. Multiple ubiquitination of substrate is required for recognition by the 26S proteasome. This may require the involvement of additional E2s and E3. There are 3 types of E3s HECT, RING and U-box. HECT E3s interacts with E2∼Ub and transfers ubiquitin directly to the Substrate. In case of RING E3s do not directly catalyse the ubiquitination of the target protein and require the presence of the E2 and often additional components (e.g. in the case of SCF Complexes) for ubiquitination to proceed. U-box E3s have a similar mode of action to RING E3s.

Fig.2 Modular protein structure of ASB and it family members.

Tab.2 ?Expression?pattern?and?subcellular?localization?of?ASB?genes?from?human?protein?atlas?database?(https://www.proteinatlas.org/)?and?NCBI?(https://www.ncbi.nlm.nih.gov/)

Fig.3 Physiological and pathological significance of ASB proteins.

1	Albertson D G, Collins C, McCormick F, Gray J W (2003). Chromosome aberrations in solid tumors. Nat Genet, 34(4): 369–376 https://doi.org/10.1038/ng1215 pmid: 12923544
2	Andresen C A, Smedegaard S, Sylvestersen K B, Svensson C, Iglesias-Gato D, Cazzamali G, Nielsen T K, Nielsen M L, Flores-Morales A (2014). Protein interaction screening for the ankyrin repeats and suppressor of cytokine signaling (SOCS) box (ASB) family identify Asb11 as a novel endoplasmic reticulum resident ubiquitin ligase. J Biol Chem, 289(4): 2043–2054 https://doi.org/10.1074/jbc.M113.534602 pmid: 24337577
3	Au V, Tsang F H, Man K, Fan S T, Poon R T, Lee N P (2014). Expression of ankyrin repeat and SOCS box containing 4 (ASB4) confers migration and invasion properties of hepatocellular carcinoma cells. Biosci Trends, 8(2): 101–110 https://doi.org/10.5582/bst.8.101 pmid: 24815387
4	Baer C, Claus R, Plass C (2013). Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res, 73(2): 473–477 https://doi.org/10.1158/0008-5472.CAN-12-3731 pmid: 23316035
5	Bello N F, Lamsoul I, Heuzé M L, Métais A, Moreaux G, Calderwood D A, Duprez D, Moog-Lutz C, Lutz P G (2009). The E3 ubiquitin ligase specificity subunit ASB2b is a novel regulator of muscle differentiation that targets filamin B to proteasomal degradation. Cell Death Differ, 16(6): 921–932 https://doi.org/10.1038/cdd.2009.27 pmid: 19300455
6	Ben-Baruch A (2006). Inflammation-associated immune suppression in cancer: the roles played by cytokines, chemokines and additional mediators. Seminars in cancer biology, Elsevier.
7	Blenk S, Engelmann J, Weniger M, Schultz J, Dittrich M, Rosenwald A, Müller-Hermelink H K, Müller T, Dandekar T (2007). Germinal center B cell-like (GCB) and activated B cell-like (ABC) type of diffuse large B cell lymphoma (DLBCL): analysis of molecular predictors, signatures, cell cycle state and patient survival. Cancer Inform, 3: 399–420 https://doi.org/10.1177/117693510700300004 pmid: 19455257
8	Bode M, Wu Y, Pi X, Lockyer P, Dechyapirom W, Portbury A L, Patterson C (2011). Regulation of ASB4 expression in the immortalized murine endothelial cell lines MS1 and SVR: a role for TNF-a and oxygen. Cell Biochem Funct, 29(4): 334 https://doi.org/10.1002/cbf.1755 pmid: 21506136
9	Boengler K, Pipp F, Fernandez B, Richter A, Schaper W, Deindl E (2003). The ankyrin repeat containing SOCS box protein 5: a novel protein associated with arteriogenesis. Biochem Biophys Res Commun, 302(1): 17–22 https://doi.org/10.1016/S0006-291X(03)00095-0 pmid: 12593841
10	Bork P (1993). Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins, 17(4): 363–374 https://doi.org/10.1002/prot.340170405 pmid: 8108379
11	Chung A S, Guan Y J, Yuan Z L, Albina J E, Chin Y E (2005). Ankyrin repeat and SOCS box 3 (ASB3) mediates ubiquitination and degradation of tumor necrosis factor receptor II. Mol Cell Biol, 25(11): 4716–4726 https://doi.org/10.1128/MCB.25.11.4716-4726.2005 pmid: 15899873
12	Clermont Y (1972). Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev, 52(1): 198–236 https://doi.org/10.1152/physrev.1972.52.1.198 pmid: 4621362
13	Costa M L, Escaleira R, Cataldo A, Oliveira F, Mermelstein C S (2004). Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Braz J Med Biol Res, 37(12): 1819–1830 https://doi.org/10.1590/S0100-879X2004001200007 pmid: 15558188
14	Coussens L M, Werb Z (2002). Inflammation and cancer. Nature, 420(6917): 860–867 https://doi.org/10.1038/nature01322 pmid: 12490959
15	Croker B A, Kiu H, Nicholson S E (2008). SOCS regulation of the JAK/STAT signalling pathway. Seminars in cell & developmental biology, Elsevier.
16	Crosetto N, Bienko M, Dikic I (2006). Ubiquitin hubs in oncogenic networks. Mol Cancer Res, 4(12): 899–904 https://doi.org/10.1158/1541-7786.MCR-06-0328 pmid: 17189380
17	da Silva M A S,Peppelenbosch M P(2003). Size matters: the emerging role of ASB proteins in controlling cell fate decisions and cancer development. Werking en functie van ASB eiwitten in de regulatie van compartimentgrootte: 15. https://doi.org/10.1038/ncb1779
18	Debrincat M A, Zhang J G, Willson T A, Silke J, Connolly L M, Simpson R J, Alexander W S, Nicola N A, Kile B T, Hilton D J (2007). Ankyrin repeat and suppressors of cytokine signaling box protein asb-9 targets creatine kinase B for degradation. J Biol Chem, 282(7): 4728–4737 https://doi.org/10.1074/jbc.M609164200 pmid: 17148442
19	Diks S H, Bink R J, van de Water S, Joore J, van Rooijen C, Verbeek F J, den Hertog J, Peppelenbosch M P, Zivkovic D (2006). The novel gene asb11: a regulator of the size of the neural progenitor compartment. J Cell Biol, 174(4): 581–592 https://doi.org/10.1083/jcb.200601081 pmid: 16893969
20	Du W Y, Lu Z H, Ye W, Fu X, Zhou Y, Kuang C M, Wu J X, Pan Z Z, Chen S, Liu R Y, Huang W L (2017). The loss-of-function mutations and down-regulated expression of ASB3 gene promote the growth and metastasis of colorectal cancer cells. Chin J Cancer, 36(1): 11 https://doi.org/10.1186/s40880-017-0180-0 pmid: 28088228
21	Fei X, Gu X, Fan S, Yang Z, Li F, Zhang C, Gong W, Mao Y, Ji C (2012). Crystal structure of Human ASB9-2 and substrate-recognition of CKB. Protein J, 31(4): 275–284 https://doi.org/10.1007/s10930-012-9401-1 pmid: 22418839
22	Ferguson J 3rd,Wu Y(2007). Ankyrin repeat and SOCS Box Protein 4 (ASB4) is a hydroxylation substrate of factor inhibiting HIF1 {alpha}(FIH) and promotes vascular differentiation via an oxygen-dependent mechanism. Cell Signal, 19(6):1185–92
23	Ferguson J E 3rd, Wu Y, Smith K, Charles P, Powers K, Wang H, Patterson C (2007). ASB4 is a hydroxylation substrate of FIH and promotes vascular differentiation via an oxygen-dependent mechanism. Mol Cell Biol, 27(18): 6407–6419 https://doi.org/10.1128/MCB.00511-07 pmid: 17636018
24	Foord R, Taylor I A, Sedgwick S G, Smerdon S J (1999). X-ray structural analysis of the yeast cell cycle regulator Swi6 reveals variations of the ankyrin fold and has implications for Swi6 function. Nat Struct Biol, 6(2): 157–165 https://doi.org/10.1038/5845 pmid: 10048928
25	Groothuis T A, Dantuma N P, Neefjes J, Salomons F A (2006). Ubiquitin crosstalk connecting cellular processes. Cell Div, 1(1): 21 https://doi.org/10.1186/1747-1028-1-21 pmid: 17007633
26	Guibal F C, Moog-Lutz C, Smolewski P, Di Gioia Y, Darzynkiewicz Z, Lutz P G, Cayre Y E (2002). ASB-2 inhibits growth and promotes commitment in myeloid leukemia cells. J Biol Chem, 277(1): 218–224 https://doi.org/10.1074/jbc.M108476200 pmid: 11682484
27	Guo J H, Saiyin H, Wei Y H, Chen S, Chen L, Bi G, Ma L J, Zhou G J, Huang C Q, Yu L, Dai L (2004). Expression of testis specific ankyrin repeat and SOCS box-containing 17 gene. Arch Androl, 50(3): 155–161 https://doi.org/10.1080/01485010490425485 pmid: 15204681
28	Hilton D J (1999). Negative regulators of cytokine signal transduction. Cell Mol Life Sci, 55(12): 1568–1577 https://doi.org/10.1007/s000180050396 pmid: 10526574
29	Hilton D J, Richardson R T, Alexander W S, Viney E M, Willson T A, Sprigg N S, Starr R, Nicholson S E, Metcalf D, Nicola N A (1998). Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci USA, 95(1): 114–119 https://doi.org/10.1073/pnas.95.1.114 pmid: 9419338
30	Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009). Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol, 10(10): 682–696 https://doi.org/10.1038/nrm2774 pmid: 19773780
31	Hotamisligil G S (2006). Inflammation and metabolic disorders. Nature, 444(7121): 860–867 https://doi.org/10.1038/nature05485 pmid: 17167474
32	Jang C Y, Wong J, Coppinger J A, Seki A, Yates J R 3rd, Fang G (2008). DDA3 recruits microtubule depolymerase Kif2a to spindle poles and controls spindle dynamics and mitotic chromosome movement. J Cell Biol, 181(2): 255–267 https://doi.org/10.1083/jcb.200711032 pmid: 18411309
33	Johnson D G, Walker C L (1999). Cyclins and cell cycle checkpoints. Annu Rev Pharmacol Toxicol, 39(1): 295–312 https://doi.org/10.1146/annurev.pharmtox.39.1.295 pmid: 10331086
34	Kamura T, Sato S, Haque D, Liu L, Kaelin W G Jr, Conaway R C, Conaway J W (1998). The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev, 12(24): 3872–3881 https://doi.org/10.1101/gad.12.24.3872 pmid: 9869640
35	Keller K E, Wirtz M K (2016). Working your SOCS off: The role of ASB10 and protein degradation pathways in glaucoma. Exp Eye Res pmid: 27296073
36	Kile B T, Schulman B A, Alexander W S, Nicola N A, Martin H M, Hilton D J (2002). The SOCS box: a tale of destruction and degradation. Trends Biochem Sci, 27(5): 235–241 https://doi.org/10.1016/S0968-0004(02)02085-6 pmid: 12076535
37	Kim K S, Kim M S, Kim S K, Baek K H (2004). Murine Asb-17 expression during mouse testis development and spermatogenesis. Zygote, 12(2): 151–156 https://doi.org/10.1017/S0967199404002722 pmid: 15460110
38	Kim S K, Rhim S Y, Lee M R,Kim J S, Kim H J, Lee D R, Kim K S (2008). Stage-specific expression of ankyrin and SOCS box protein-4 (Asb-4) during spermatogenesis. Mol Cell, 25(2):317–21
39	Kohroki J, Nishiyama T, Nakamura T, Masuho Y (2005). ASB proteins interact with Cullin5 and Rbx2 to form E3 ubiquitin ligase complexes. FEBS Lett, 579(30): 6796–6802 https://doi.org/10.1016/j.febslet.2005.11.016 pmid: 16325183
40	Lai K C, Chang K W, Liu C J, Lee T C (2006). Enhanced expression of ASB6 and IFIT2 in oral squamous cell carcinoma, AACR.
41	Lamsoul I, Burande C F, Razinia Z, Houles T C, Menoret D, Baldassarre M, Erard M, Moog-Lutz C, Calderwood D A, Lutz P G (2011). Functional and structural insights into ASB2a, a novel regulator of integrin-dependent adhesion of hematopoietic cells. J Biol Chem, 286(35): 30571–30581 https://doi.org/10.1074/jbc.M111.220921 pmid: 21737450
42	Lee M R,Kim S K, Kim J S, Rhim S Y,Kim K S (2008). Expression of murine Asb-9 during mouse spermatogenesis. Mol Cell, 26(6):621–4
43	Lee N P, Leung K W, Cheung N, Lam B Y, Xu M Z, Sham P C, Lau G K, Poon R T, Fan S T, Luk J M (2008). Comparative proteomic analysis of mouse livers from embryo to adult reveals an association with progression of hepatocellular carcinoma. Proteomics, 8(10): 2136–2149 https://doi.org/10.1002/pmic.200700590 pmid: 18425728
44	Li J, Mahajan A, Tsai M D (2006). Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry, 45(51): 15168–15178 https://doi.org/10.1021/bi062188q pmid: 17176038
45	Li J Y, Chai B, Zhang W, Wu X, Zhang C, Fritze D, Xia Z, Patterson C, Mulholland M W (2011). Ankyrin repeat and SOCS box containing protein 4 (Asb-4) colocalizes with insulin receptor substrate 4 (IRS4) in the hypothalamic neurons and mediates IRS4 degradation. BMC Neurosci, 12(1): 95 https://doi.org/10.1186/1471-2202-12-95 pmid: 21955513
46	Linossi E M, Nicholson S E (2012). The SOCS box-adapting proteins for ubiquitination and proteasomal degradation. IUBMB Life, 64(4): 316–323 https://doi.org/10.1002/iub.1011 pmid: 22362562
47	Liu Y, Li J, Zhang F, Qin W, Yao G, He X, Xue P, Ge C, Wan D, Gu J (2003). Molecular cloning and characterization of the human ASB-8 gene encoding a novel member of ankyrin repeat and SOCS box containing protein family. Biochem Biophys Res Commun, 300(4): 972–979 https://doi.org/10.1016/S0006-291X(02)02971-6 pmid: 12559969
48	Lux S E, John K M, Bennett V (1990). Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature 344(6261):36–42
49	Marcotte E M, Pellegrini M, Yeates T O, Eisenberg D (1999). A census of protein repeats. J Mol Biol, 293(1): 151–160 https://doi.org/10.1006/jmbi.1999.3136 pmid: 10512723
50	Maxwell P H, Wiesener M S, Chang G W, Clifford S C, Vaux E C, Cockman M E, Wykoff C C, Pugh C W, Maher E R, Ratcliffe P J (1999). The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature, 399(6733): 271–275 https://doi.org/10.1038/20459 pmid: 10353251
51	McDaneld T G, Hannon K, Moody D E (2006). Ankyrin repeat and SOCS box protein 15 regulates protein synthesis in skeletal muscle. Am J Physiol Regul Integr Comp Physiol, 290(6): R1672–R1682 https://doi.org/10.1152/ajpregu.00239.2005 pmid: 16424087
52	McDaneld T G, Spurlock D M (2008). Ankyrin repeat and suppressor of cytokine signaling (SOCS) box-containing protein (ASB) 15 alters differentiation of mouse C2C12 myoblasts and phosphorylation of mitogen-activated protein kinase and Akt. J Anim Sci, 86(11): 2897–2902 https://doi.org/10.2527/jas.2008-1076 pmid: 18641171
53	Mocellin S, Rossi C R, Pilati P, Nitti D (2005). Tumor necrosis factor, cancer and anticancer therapy. Cytokine Growth Factor Rev, 16(1): 35–53 https://doi.org/10.1016/j.cytogfr.2004.11.001 pmid: 15733831
54	Morris L G, Veeriah S, Chan T A (2010). Genetic determinants at the interface of cancer and neurodegenerative disease. Oncogene, 29(24): 3453–3464 https://doi.org/10.1038/onc.2010.127 pmid: 20418918
55	Mosavi L K, Cammett T J, Desrosiers D C, Peng Z Y (2004). The ankyrin repeat as molecular architecture for protein recognition. Protein Sci, 13(6): 1435–1448 https://doi.org/10.1110/ps.03554604 pmid: 15152081
56	Mosavi L K, Minor D L Jr, Peng Z Y (2002). Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA, 99(25): 16029–16034 https://doi.org/10.1073/pnas.252537899 pmid: 12461176
57	Nie L, Zhao Y, Wu W, Yang Y Z, Wang H C, Sun X H (2011). Notch-induced Asb2 expression promotes protein ubiquitination by forming non-canonical E3 ligase complexes. Cell Res, 21(5): 754–769 https://doi.org/10.1038/cr.2010.165 pmid: 21119685
58	Okumura F, Matsuzaki M, Nakatsukasa K, Kamura T (2012).The role of elongin BC-containing ubiquitin ligases. Front Oncol, 2: 10
59	Pahl H L (1999). Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene, 18(49): 6853–6866 https://doi.org/10.1038/sj.onc.1203239 pmid: 10602461
60	Plum L, Belgardt B F, Brüning J C (2006). Central insulin action in energy and glucose homeostasis. J Clin Invest, 116(7): 1761–1766 https://doi.org/10.1172/JCI29063 pmid: 16823473
61	Seki A, Coppinger J A, Jang C Y, Yates J R, Fang G (2008). Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science, 320(5883): 1655–1658 https://doi.org/10.1126/science.1157425 pmid: 18566290
62	Sonnhammer E L, Von Heijne G, Krogh A (1998). A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol, 6:175–82
63	Tee J M, Peppelenbosch M P (2010). Anchoring skeletal muscle development and disease: the role of ankyrin repeat domain containing proteins in muscle physiology. Crit Rev Biochem Mol Biol, 45(4): 318–330 https://doi.org/10.3109/10409238.2010.488217 pmid: 20515317
64	Tee J M, Sartori da Silva M A, Rygiel A M, Muncan V, Bink R, van den Brink G R, van Tijn P, Zivkovic D, Kodach L L, Guardavaccaro D, Diks S H, Peppelenbosch M P (2012). asb11 is a regulator of embryonic and adult regenerative myogenesis. Stem Cells Dev, 21(17): 3091–3103 https://doi.org/10.1089/scd.2012.0123 pmid: 22512762
65	Thomas J C, Matak-Vinkovic D, Van Molle I, Ciulli A (2013). Multimeric complexes among ankyrin-repeat and SOCS-box protein 9 (ASB9), ElonginBC, and Cullin 5: insights into the structure and assembly of ECS-type Cullin-RING E3 ubiquitin ligases. Biochemistry, 52(31): 5236–5246 https://doi.org/10.1021/bi400758h pmid: 23837592
66	Thottakara T, Friedrich F W, Reischmann S, Braumann S, Schlossarek S, Krämer E, Juhr D, Schlüter H, van der Velden J, Münch J, Patten M, Eschenhagen T, Moog-Lutz C, Carrier L (2015). The E3 ubiquitin ligase Asb2b is downregulated in a mouse model of hypertrophic cardiomyopathy and targets desmin for proteasomal degradation. J Mol Cell Cardiol, 87: 214–224 https://doi.org/10.1016/j.yjmcc.2015.08.020 pmid: 26343497
67	Tokuoka M, Miyoshi N, Hitora T, Mimori K, Tanaka F, Shibata K, Ishii H, Sekimoto M, Doki Y, Mori M (2010). Clinical significance of ASB9 in human colorectal cancer. Int J Oncol, 37(5): 1105–1111 pmid: 20878058
68	Townley-Tilson W H, Wu Y, Ferguson J E 3rd, Patterson C (2014). The ubiquitin ligase ASB4 promotes trophoblast differentiation through the degradation of ID2. PLoS One, 9(2): e89451 https://doi.org/10.1371/journal.pone.0089451 pmid: 24586788
69	Uematsu K, Okumura F, Tonogai S, Joo-Okumura A, Alemayehu D H, Nishikimi A, Fukui Y, Nakatsukasa K, Kamura T (2016). ASB7 regulates spindle dynamics and genome integrity by targeting DDA3 for proteasomal degradation. J Cell Biol, 215(1): 95–106 https://doi.org/10.1083/jcb.201603062 pmid: 27697924
70	van Kouwenhove M, Kedde M, Agami R (2011). MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer, 11(9): 644–656 https://doi.org/10.1038/nrc3107 pmid: 21822212
71	Wajant H, Pfizenmaier K, Scheurich P (2003). Tumor necrosis factor signaling. Cell Death Differ, 10(1): 45–65 https://doi.org/10.1038/sj.cdd.4401189 pmid: 12655295
72	Wang J, Muntean A G, Hess J L (2012). ECSASB2 mediates MLL degradation during hematopoietic differentiation. Blood, 119(5): 1151–1161 https://doi.org/10.1182/blood-2011-06-362079 pmid: 22174154
73	Wauman J, De Smet A S, Catteeuw D, Belsham D, Tavernier J (2008). Insulin receptor substrate 4 couples the leptin receptor to multiple signaling pathways. Mol Endocrinol, 22(4): 965–977 https://doi.org/10.1210/me.2007-0414 pmid: 18165436
74	Wilcox A, Katsanakis K D, Bheda F, Pillay T S (2004). Asb6, an adipocyte-specific ankyrin and SOCS box protein, interacts with APS to enable recruitment of elongins B and C to the insulin receptor signaling complex. J Biol Chem, 279(37): 38881–38888 https://doi.org/10.1074/jbc.M406101200 pmid: 15231829
75	Wilcox G (2005). Insulin and insulin resistance. Clin Biochem Rev, 26(2): 19–39 pmid: 16278749
76	Yang X Y, Ren C P, Wang L, Li H, Jiang C J, Zhang H B, Zhao M, Yao K T (2005). Identification of differentially expressed genes in metastatic and non-metastatic nasopharyngeal carcinoma cells by suppression subtractive hybridization. Cell Oncol, 27(4): 215–223 pmid: 16308470
77	Yuan J H, Yang F, Chen B F, Lu Z, Huo X S, Zhou W P, Wang F, Sun S H (2011). The histone deacetylase 4/SP1/microrna-200a regulatory network contributes to aberrant histone acetylation in hepatocellular carcinoma. Hepatology, 54(6): 2025–2035 https://doi.org/10.1002/hep.24606 pmid: 21837748
78	Ziemin-van der Poel S, McCabe N R, Gill H J, Espinosa R 3rd, Patel Y, Harden A, Rubinelli P, Smith S D, LeBeau M M, Rowley J D (1991). Identification of a gene, MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Proc Natl Acad Sci USA, 88(23): 10735–10739 https://doi.org/10.1073/pnas.88.23.10735 pmid: 1720549

[1]	Dingcheng Gao, Vivek Mittal, Yi Ban, Ana Rita Lourenco, Shira Yomtoubian, Sharrell Lee. Metastatic tumor cells – genotypes and phenotypes[J]. Front. Biol., 2018, 13(4): 277-286.
[2]	Soumya Nair, Sandra Suresh, Arya Kaniyassery, Panchami Jaya, Jayanthi Abraham. A review on melatonin action as therapeutic agent in cancer[J]. Front. Biol., 2018, 13(3): 180-189.
[3]	Muhammad Naveed, Mohammad Raees, Irfan Liaqat, Mohammad Kashif. Clastogenic ROS and biophotonics in precancerous diagnosis[J]. Front. Biol., 2018, 13(2): 103-122.
[4]	D. Brooke Widner, D. Clark Files, Kathryn E. Weaver, Yusuke Shiozawa. Preclinical and clinical studies on cancer-associated cachexia[J]. Front. Biol., 2018, 13(1): 11-18.
[5]	Razia Rahman, Lokesh Kumar Gahlot, Yasha Hasija. miRACA: A database for miRNAs associated with cancers and age related disorders (ARD)[J]. Front. Biol., 2018, 13(1): 36-50.
[6]	Amir Abdoli. High salt and fat intake, inflammation, and risk of cancer[J]. Front. Biol., 2017, 12(6): 387-391.
[7]	Pang-Kuo Lo,Benjamin Wolfson,Qun Zhou. Cellular, physiological and pathological aspects of the long non-coding RNA NEAT1[J]. Front. Biol., 2016, 11(6): 413-426.
[8]	Sahar Al Seesi,Alok Das Mohapatra,Arpita Pawashe,Ion I. Mandoiu,Fei Duan. Finding neoepitopes in mouse models of personalized cancer immunotherapy[J]. Front. Biol., 2016, 11(5): 366-375.
[9]	Gahana Advani,Anderly C. Chueh,Ya Chee Lim,Amardeep Dhillon,Heung-Chin Cheng. Csk-homologous kinase (Chk/Matk): a molecular policeman suppressing cancer formation and progression[J]. Front. Biol., 2015, 10(3): 195-202.
[10]	Caiguo ZHANG. The correlation between iron homeostasis and telomere maintenance[J]. Front. Biol., 2014, 9(5): 347-355.
[11]	Qingguo ZHAO,Fei LIU. Mesenchymal stem cells in progression and treatment of cancers[J]. Front. Biol., 2014, 9(3): 186-194.
[12]	Baoxiang GUAN,Ashraful HOQUE,Xiaochun XU. *Amiloride and guggulsterone suppression of esophageal cancer cell growth in vitro* and in nude mouse xenografts**[J]. Front. Biol., 2014, 9(1): 75-81.
[13]	Noor GAMMOH,Simon WILKINSON. Autophagy in cancer biology and therapy[J]. Front. Biol., 2014, 9(1): 35-50.
[14]	Merlin LOPUS, Rao SETHUMADHAVAN, P. CHANDRASEKARAN, K. SREEVISHNUPRIYA, A.W. VARSHA, V. SHANTHI, K. RAMANATHAN, R. RAJASEKARAN. A computational approach to explore the functional missense mutations in the spindle check point protein Mad1[J]. Front Biol, 2013, 8(6): 618-625.
[15]	Olga KSIONDA, Andre LIMNANDER, Jeroen P. ROOSE. RasGRP Ras guanine nucleotide exchange factors in cancer[J]. Front Biol, 2013, 8(5): 508-532.

Viewed

Full text

Abstract

Cited

Shared

Discussed