Inhibition of Smurf2 translation by miR-322/503 modulates TGF-β/Smad2 signaling and intestinal epithelial homeostasis

Molecular Biology of the Cell

Volumn 25, Issue 8, 2014, Pages 1234-1243

  Cao, Shan ^a,b   Xiao, Lan ^a,b   Rao, Jaladanki N ^a,b   Zou, Tongtong ^a,b   Liu, Lan ^a,b   Zhang, Dee ^a,b   Turner, Douglas J ^a,b   Gorospec, Myriam ^c   Wang, Jian Ying ^a,b,d  

^a Cell Biology Group Department of Surgery ^*  (United States)

^b BALTIMORE VA MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE ON AGING   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 322; MICRORNA 503; PROTEIN SMURF2; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CYCLOHEXIMIDE; MADH2 PROTEIN, RAT; MESSENGER RNA; MIRN322 MICRORNA, RAT; MIRN503 MICRORNA, RAT; SMURF2 PROTEIN, RAT; UBIQUITIN PROTEIN LIGASE;

3' UNTRANSLATED REGION; ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE; GENE REPRESSION; HOMEOSTASIS; INTESTINE EPITHELIUM CELL; MOLECULAR INTERACTION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; RNA TRANSLATION; SIGNAL TRANSDUCTION; SMURF2 GENE; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; GENETICS; INTESTINE MUCOSA; METABOLISM; PHOSPHORYLATION; PROTEIN SYNTHESIS;

3' UNTRANSLATED REGIONS; ANIMALS; APOPTOSIS; CELL LINE; CYCLOHEXIMIDE; INTESTINAL MUCOSA; MICRORNAS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN-PROTEIN LIGASES;

EID: 84902667628     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-09-0560     Document Type: Article

References (57)

1. Bakirtzi K, Hatziapostolou M, Karagiannides I, Polytarchou C, Jaeger S, Iliopoulos D, Pothoulakis C (2011). Neurotensin signaling activates microRNAs-21 and-155 and Akt, promotes tumor growth in mice, and is increased in human colon tumors. Gastroenterology 141, 1749-1761.
2. Blank M, Tang Y, Yamashita M, Burkett SS, Cheng SY, Zhang YE (2012). A tumor suppressor function of Smurf2 associated with controlling chromatin landscape and genome stability through RNF20. Nat Med 18, 227-234.
3. Buchan JR, Parker R (2009). Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36, 932-941.
4. Cui YH, Xiao L, Rao JN, Zou T, Liu L, Chen Y, Turner DJ, Gorospe M, Wang JY (2012). miR-503 represses CUG-binding protein 1 translation by recruiting CUGBP1 mRNA to processing bodies. Mol Biol Cell 23, 151-162.
5. David D, Nair SA, Pillai MR (2013). Smurf E3 ubiquitin ligases at the cross roads of oncogenesis and tumor suppression. Biochim Biophys Acta 1835, 119-128.
6. Eulalio A, Huntzinger E, Izaurralde E (2008). Getting to the root of miRNA-mediated gene silencing. Cell 132, 9-14.
7. Gamez B, Rodriguez-Carballo E, Bartrons R, Rosa JL, Ventura F (2013). MicroRNA-322 (miR-322) and its target protein Tob2 modulate Osterix (Osx) mRNA stability. J Biol Chem 288, 14264-14275.
8. Gao S, Alarcon C, Sapkota G, Rahman S, Chen PY, Goerner N, Macias MJ, Erdjument-Bromage H, Tempst P, Massague J (2009). Ubiquitin ligase Nedd4L targets activated Smad2/3 to limit TGF-β signaling. Mol Cell 36, 457-468.
9. Garneau NL, Wilusz J, Wilusz CJ (2007). The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8, 113-126.
10. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006). miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34, D140-D144.
11. Harter JL (1960). Critical values for Duncan's new multiple range tests. Biometric 671-685.
12. Hershko A, Ciechanover A (1998). The ubiquitin system. Annu Rev Biochem 67, 425-479.
13. Hoeller D, Hecker CM, Dikic I (2006). Ubiquitin and ubiquitin-like proteins in cancer pathogenesis. Nat Rev Cancer 6, 776-788.
14. Izzi L, Attisano L (2004). Regulation of the TGF-β signalling pathway by ubiquitin-mediated degradation. Oncogene 23, 2071-2078.
15. Kamato D, Burch ML, Piva TJ, Rezaei HB, Rostam MA, Xu S, Zheng W, Little PJ, Osman N (2013). Transforming growth factor-β signaling: role and consequences of Smad linker region phosphorylation. Cell Signal 25, 2017-2024.
16. Kedde M et al. (2007). RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131, 1273-1286.
17. Kulkarni M, Ozgur S, Stoecklin G (2010). On track with P-bodies. Biochem Soc Trans 38, 242-251.
18. Leung AK, Sharp PA (2010). MicroRNA functions in stress responses. Mol Cell 40, 205-215.
19. Li H, Seth A (2004). An RNF11: Smurf2 complex mediates ubiquitination of the AMSH protein. Oncogene 23, 1801-1808.
20. Li L, Rao JN, Bass BL, Wang JY (2001). NF-κB activation and susceptibility to apoptosis after polyamine depletion in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 280, G992-G1004.
21. Lin X, Liang M, Feng XH (2000). Smurf2 is an ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-β signaling. J Biol Chem 275, 36818-36822.
22. Liu L, Rao JN, Zou T, Xiao L, Wang PY, Turner DJ, Gorospe M, Wang JY (2009). Polyamines regulate c-Myc translation through Chk2-dependent HuR phosphorylation. Mol Biol Cell 20, 4885-4898.
23. Liu L, Santora R, Rao JN, Guo X, Zou T, Zhang HM, Turner DJ, Wang JY (2003). Activation of TGF-β-Smad signaling pathway following polyamine depletion in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 285, G1056-G1067.
24. Lo RS, Massague J (1999). Ubiquitin-dependent degradation of TGF-β-activated smad2. Nat Cell Biol 1, 472-478.
25. Lönn P, Moren A, Raja E, Dahl M, Moustakas A (2009). Regulating the stability of TGF-β receptors and Smads. Cell Res 19, 21-35.
26. Massague J, Seoane J, Wotton D (2005). Smad transcription factors. Genes Dev 19, 2783-2810.
27. Mendell JT, Olson EN (2012). MicroRNAs in stress signaling and human disease. Cell 148, 1172-1187.
28. Merlet E, Atassi F, Motiani RK, Mougenot N, Jacquet A, Nadaud S, Capiod T, Trebak M, Lompre AM, Marchand A (2013). miR-424/322 regulates vascular smooth muscle cell phenotype and neointimal formation in the rat. Cardiovasc Res 98, 458-468.
29. Nie J, Xie P, Liu L, Xing G, Chang Z, Yin Y, Tian C, He F, Zhang L (2010). Smad ubiquitylation regulatory factor 1/2 (Smurf1/2) promotes p53 degradation by stabilizing the E3 ligase MDM2. J Biol Chem 285, 22818-22830.
30. Nonne N, Ameyar-Zazoua M, Souidi M, Harel-Bellan A (2010). Tandem affinity purification of miRNA target mRNAs (TAP-Tar). Nucleic Acids Res 38, e20.
31. Omer AD, Janas MM, Novina CD (2009). The chicken or the egg: microRNA-mediated regulation of mRNA translation or mRNA stability. Mol Cell 35, 739-740.
32. Orom UA, Lund AH (2007). Isolation of microRNA targets using biotinylated synthetic microRNAs. Methods 43, 162-165.
33. Quaroni A, Wands J, Trelstat RL, Isselbacher KJ (1979). Epithelial cell cultures from rat small intestine. J Cell Biol 80, 248-265.
34. Rao JN, Wang JY (2011). Regulation of gastrointestinal mucosal growth. In: Molecule to Function to Disease, ed. DN Granger and JP Granger, Princeton, NJ: Morgan & Claypool, 11-114.
35. Sapkota G, Alarcon C, Spagnoli FM, Brivanlou AH, Massague J (2007). Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25, 441-454.
36. Sarkar S, Dey BK, Dutta A (2010). MiR-322/424 and-503 are induced during muscle differentiation and promote cell cycle quiescence and differentiation by down-regulation of Cdc25A. Mol Biol Cell 21, 2138-2149.
37. Sato T, Clevers H (2013). Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340, 1190-1194.
38. Schwamborn JC, Muller M, Becker AH, Puschel AW (2007). Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J 26, 1410-1422.
39. Seiler N, Raul F (2007). Polyamines and the intestinal tract. Crit Rev Clin Lab Sci 44, 365-411.
40. Shi Y, Massague J (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700.
41. Ten Dijke P, Hill CS (2004). New insights into TGF-β-Smad signalling. Trends Biochem Sci 29, 265-273.
42. Wang JY, McCormack SA, Viar MJ, Johnson LR (1991). Stimulation of proximal small intestinal mucosal growth by luminal polyamines. Am J Physiol Gastrointest Liver Physiol 261, G504-G511.
43. Wang JY, Wang H, Johnson LR (1995). Gastrin stimulates expression of protooncogene c-myc through a process involving polyamines in IEC-6 cells. Am J Physiol Cell Physiol 269, C1474-C1481.
44. Wang PY, Rao JN, Zou T, Liu L, Xiao L, Yu TX, Turner DJ, Gorospe M, Wang JY (2010). Post-transcriptional regulation of MEK-1 by polyamines through the RNA-binding protein HuR modulating intestinal epithelial apoptosis. Biochem J 426, 293-306.
45. Xiao L, Cui YH, Rao JN, Zou T, Liu L, Smith A, Turner DJ, Gorospe M, Wang JY (2011). Regulation of cyclin-dependent kinase 4 translation through CUG-binding protein 1 and microRNA-222 by polyamines. Mol Biol Cell 22, 3055-3069.
46. Xiao L, Rao JN, Zou T, Liu L, Cao S, Martindale JL, Su W, Chung HK, Gorospe M, Wang JY (2013). miR-29b represses intestinal mucosal growth by inhibiting translation of cyclin-dependent kinase 2. Mol Biol Cell 24, 3038-3046.
47. Xiao L, Rao JN, Zou T, Liu L, Marasa BS, Chen J, Turner DJ, Zhou H, Gorospe M, Wang JY (2007). Polyamines regulate the stability of activating transcription factor-2 mRNA through RNA-binding protein HuR in intestinal epithelial cells. Mol Biol Cell 18, 4579-4590.
48. Xu P, Liu J, Derynck R (2012). Post-translational regulation of TGF-β receptor and Smad signaling. FEBS Lett 586, 1871-1884.
49. Ye D, Guo S, Al-Sadi R, Ma TY (2011). MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology 141, 1323-1333.
50. Yu TX, Rao JN, Zou T, Liu L, Xiao L, Ouyang M, Cao S, Gorospe M, Wang JY (2012). Competitive binding of CUGBP1 and HuR to occludin mRNA controls its translation and modulates epithelial barrier function. Mol Biol Cell 24, 85-99.
51. Yu TX, Wang PY, Rao JN, Zou T, Liu L, Xiao L, Gorospe M, Wang JY (2011). Chk2-dependent HuR phosphorylation regulates occludin mRNA translation and epithelial barrier function. Nucleic Acids Res 39, 8472-8487.
52. Zhang Y, Chang C, Gehling DJ, Hemmati-Brivanlou A, Derynck R (2001). Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc Natl Acad Sci USA 98, 974-979.
53. Zhang HM, Rao JN, Guo X, Liu L, Zou T, Turner DJ, Wang JY (2004). Akt kinase activation blocks apoptosis in intestinal epithelial cells by inhibiting caspase-3 after polyamine depletion. J Biol Chem 279, 22539-22547.
54. Zhang X, Zou T, Rao JN, Liu L, Xiao L, Wang PY, Cui YH, Gorospe M, Wang JY (2009). Stabilization of XIAP mRNA through the RNA binding protein HuR regulated by cellular polyamines. Nucleic Acids Res 37, 7623-7637.
55. Zhuang R, Rao JN, Zou T, Liu L, Xiao L, Cao S, Hansraj NZ, Gorospe M, Wang JY (2013). miR-195 competes with HuR to modulate stim1 mRNA stability and regulate cell migration. Nucleic Acids Res 41, 7905-7919.
56. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH (1999). A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400, 687-693.
57. Zou T, Rao JN, Liu L, Xiao L, Yu TX, Jiang P, Gorospe M, Wang JY (2010). Polyamines regulate the stability of JunD mRNA by modulating the competitive binding of its 3′ untranslated region to HuR and AUF1. Mol Cell Biol 30, 5021-5032.