The SUMO Pathway Promotes Basic Helix-Loop-Helix Proneural Factor Activity via a Direct Effect on the Zn Finger Protein Senseless

REFERENCES

• Abed M, et al. 2011. Degringolade, a SUMO-targeted ubiquitin ligase, inhibits Hairy/Groucho-mediated repression. EMBO J. 30:1289–1301.
   PubMedGoogle Scholar
• Abed M, Bitman-Lotan E, Orian A. 2011. A fly view of a SUMO-targeted ubiquitin ligase. Fly (Austin) 5(4):340–344. https://doi.org/10.4161/fly.5.4.17608.
   PubMed Web of Science ®Google Scholar
• Acar M, et al. 2006. Senseless physically interacts with proneural proteins and functions as a transcriptional co-activator. Development 133:1979–1989.
   PubMedGoogle Scholar
• Barad O, Hornstein E, Barkai N. 2011. Robust selection of sensory organ precursors by the Notch-Delta pathway. Curr. Opin. Cell Biol. 23:663–667.
   PubMedGoogle Scholar
• Barry KC, et al. 2011. The Drosophila STUbL protein Degringolade limits HES functions during embryogenesis. Development 138:1759–1769.
   PubMedGoogle Scholar
• Bedford L, Lowe J, Dick LR, Mayer RJ, Brownell JE. 2011. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat. Rev. Drug Discov. 10:29–46.
   PubMed Web of Science ®Google Scholar
• Bertrand N, Castro DS, Guillemot F. 2002. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3:517–530.
   PubMed Web of Science ®Google Scholar
• Bhaskar V, Smith M, Courey AJ. 2002. Conjugation of Smt3 to dorsal may potentiate the Drosophila immune response. Mol. Cell. Biol. 22:492–504.
   PubMed Web of Science ®Google Scholar
• Bhaskar V, Valentine SA, Courey AJ. 2000. A functional interaction between dorsal and components of the Smt3 conjugation machinery. J. Biol. Chem. 275:4033–4040.
   PubMedGoogle Scholar
• Bischof J, Maeda RK, Hediger M, Karch F, Basler K. 2007. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. U. S. A. 104:3312–3317.
   PubMed Web of Science ®Google Scholar
• Chakrabarti SR, Sood R, Nandi S, Nucifora G. 2000. Posttranslational modification of TEL and TEL/AML1 by SUMO-1 and cell-cycle-dependent assembly into nuclear bodies. Proc. Natl. Acad. Sci. U. S. A. 97:13281–13285.
   PubMed Web of Science ®Google Scholar
• Chen A, et al. 2006. SUMO regulates the cytoplasmonuclear transport of its target protein Daxx. J. Cell Biochem. 98:895–911.
   PubMed Web of Science ®Google Scholar
• Chien C-T, Hsiao C-D, Jan LY, Jan YN. 1996. Neuronal type information encoded in the basic-helix-loop-helix domain of proneural genes. Proc. Natl. Acad. Sci. U. S. A. 93:13239–13244.
   PubMedGoogle Scholar
• Costa MW, et al. 2011. Complex SUMO-1 regulation of cardiac transcription factor Nkx2-5. PLoS One 6:e24812. https://doi.org/10.1371/journal.pone.0024812.
   PubMed Web of Science ®Google Scholar
• Culi J, Modolell J. 1998. Proneural gene self-stimulation in neural precursors: an essential mechanism for sense organ development that is regulated by Notch signaling. Genes Dev. 12:2036–2047.
   PubMedGoogle Scholar
• Duan Z, et al. 2007. Epigenetic regulation of protein-coding and microRNA genes by the Gfi1-interacting tumor suppressor PRDM5. Mol. Cell. Biol. 27:6889–6902.
   PubMed Web of Science ®Google Scholar
• Duffy JB. 2002. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34:1–15.
   PubMed Web of Science ®Google Scholar
• Garcia-Dominguez M, Reyes JC. 2009. SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim. Biophys. Acta 1789:451–459.
   PubMed Web of Science ®Google Scholar
• Gareau JR, Lima CD. 2010. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 11:861–871.
   PubMed Web of Science ®Google Scholar
• Giagtzoglou N, Koumbanakis KA, Fullard J, Zarifi I, Delidakis C. 2005. Role of the Sc C terminus in transcriptional activation and E(spl) repressor recruitment. J. Biol. Chem. 280:1299–1305.
   PubMed Web of Science ®Google Scholar
• Girdwood DW, Tatham MH, Hay RT. 2004. SUMO and transcriptional regulation. Semin. Cell Dev. Biol. 15:201–210.
   PubMed Web of Science ®Google Scholar
• Grimes HL, Chan TO, Zweidler-McKay PA, Tong B, Tsichlis PN. 1996. The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal. Mol. Cell. Biol. 16:6263–6272.
   PubMed Web of Science ®Google Scholar
• Groth AC, Fish M, Nusse R, Calos MP. 2004. Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166:1775–1782.
   PubMed Web of Science ®Google Scholar
• Guruharsha KG, et al. A protein complex network of Drosophila melanogaster. Cell 147:690–703.
   PubMedGoogle Scholar
• Gutzwiller LM, et al. 2010. Proneural and abdominal Hox inputs synergize to promote sensory organ formation in the Drosophila abdomen. Dev. Biol. 348:231–243.
   PubMedGoogle Scholar
• Hannoun Z, Greenhough S, Jaffray E, Hay RT, Hay DC. 2010. Post-translational modification by SUMO. Toxicology 278:288–293.
   PubMed Web of Science ®Google Scholar
• Hay RT. 2005. SUMO: a history of modification. Mol. Cell 18:1–12.
   PubMed Web of Science ®Google Scholar
• Herrmann J, Lerman LO, Lerman A. 2007. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ. Res. 100:1276–1291.
   PubMed Web of Science ®Google Scholar
• Jafar-Nejad H, et al. 2003. Senseless acts as a binary switch during sensory organ precursor selection. Genes Dev. 17:2966–2978.
   PubMedGoogle Scholar
• Jafar-Nejad H, Bellen HJ. 2004. Gfi/Pag-3/senseless zinc finger proteins: a unifying theme? Mol. Cell. Biol. 24:8803–8812.
   PubMedGoogle Scholar
• Jarman AP, Ahmed I. 1998. The specificity of proneural genes in determining Drosophila sense organ identity. Mech. Dev. 76:117–125.
   PubMed Web of Science ®Google Scholar
• Jarman AP, Grau Y, Jan LY, Jan YN. 1993. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307–1321.
   PubMedGoogle Scholar
• Jennings B, Preiss A, Delidakis C, Bray S. 1994. The Notch signalling pathway is required for Enhancer of split bHLH protein expression during neurogenesis in the Drosophila embryo. Development 120:3537–3548.
   PubMed Web of Science ®Google Scholar
• Kazanjian A, et al. 2004. Growth factor independence-1 is expressed in primary human neuroendocrine lung carcinomas and mediates the differentiation of murine pulmonary neuroendocrine cells. Cancer Res. 64:6874–6882.
   PubMed Web of Science ®Google Scholar
• Kirjavainen A, et al. 2008. Prox1 interacts with Atoh1 and Gfi1, and regulates cellular differentiation in the inner ear sensory epithelia. Dev. Biol. 322:33–45.
   PubMedGoogle Scholar
• Klein UR, Haindl M, Nigg EA, Muller S. 2009. RanBP2 and SENP3 function in a mitotic SUMO2/3 conjugation-deconjugation cycle on Borealin. Mol. Biol. Cell 20:410–418.
   PubMed Web of Science ®Google Scholar
• Kroetz MB, Hochstrasser M. 2009. Identification of SUMO-interacting proteins by yeast two-hybrid analysis. Methods Mol. Biol. 497:107–120.
   PubMedGoogle Scholar
• Kunapuli P, Kasyapa CS, Chin SF, Caldas C, Cowell JK. 2006. ZNF198, a zinc finger protein rearranged in myeloproliferative disease, localizes to the PML nuclear bodies and interacts with SUMO-1 and PML. Exp. Cell Res. 312:3739–3751.
   PubMedGoogle Scholar
• Lage P, Jan YN, Jarman AP. 1997. Requirement for EGF receptor signalling in neural recruitment during formation of Drosophila chordotonal sense organ clusters. Curr. Biol. 7:166–175.
   PubMedGoogle Scholar
• Lee PS, Chang C, Liu D, Derynck R. 2003. Sumoylation of Smad4, the common Smad mediator of transforming growth factor-beta family signaling. J. Biol. Chem. 278:27853–27863.
   PubMed Web of Science ®Google Scholar
• Lehembre F, et al. 2000. Covalent modification of the transcriptional repressor tramtrack by the ubiquitin-related protein Smt3 in Drosophila flies. Mol. Cell. Biol. 20:1072–1082.
   PubMedGoogle Scholar
• Leyns L, Gomez-Skarmeta JL, Dambly-Chaudiere C. 1996. iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech. Dev. 59:63–72.
   PubMedGoogle Scholar
• Li-Kroeger D, Witt LM, Grimes HL, Cook TA, Gebelein B. 2008. Hox and senseless antagonism functions as a molecular switch to regulate EGF secretion in the Drosophila PNS. Dev. Cell 15:298–308.
   PubMedGoogle Scholar
• Lin DY, et al. 2006. Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24:341–354.
   PubMed Web of Science ®Google Scholar
• Lyst MJ, Stancheva I. 2007. A role for SUMO modification in transcriptional repression and activation. Biochem. Soc. Trans. 35:1389–1392.
   PubMed Web of Science ®Google Scholar
• Matunis MJ, Wu J, Blobel G. 1998. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 140:499–509.
   PubMed Web of Science ®Google Scholar
• Nolo R, Abbott LA, Bellen HJ. 2000. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102:349–362.
   PubMed Web of Science ®Google Scholar
• Pauley S, Kopecky B, Beisel K, Soukup G, Fritzsch B. 2008. Stem cells and molecular strategies to restore hearing. Panminerva Med. 50:41–53.
   PubMedGoogle Scholar
• Powell LM, Deaton AM, Wear MA, Jarman AP. 2008. Specificity of Atonal and Scute bHLH factors: analysis of cognate E box binding sites and the influence of Senseless. Genes Cells 13:915–929.
   PubMedGoogle Scholar
• Ramain P, Heitzler P, Haenlin M, Simpson P. 1993. pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development 119:1277–1291.
   PubMed Web of Science ®Google Scholar
• Rodriguez MS, Dargemont C, Hay RT. 2001. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276:12654–12659.
   PubMed Web of Science ®Google Scholar
• Saitoh H, Hinchey J. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275:6252–6258.
   PubMed Web of Science ®Google Scholar
• Salzberg A, et al. 1994. Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron 13:269–287.
   PubMedGoogle Scholar
• Schmidt D, Muller S. 2002. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc. Natl. Acad. Sci. U. S. A. 99:2872–2877.
   PubMed Web of Science ®Google Scholar
• Shroyer NF, Wallis D, Venken KJ, Bellen HJ, Zoghbi HY. 2005. Gfi1 functions downstream of Math1 to control intestinal secretory cell subtype allocation and differentiation. Genes Dev. 19:2412–2417.
   PubMed Web of Science ®Google Scholar
• Smet-Nocca C, Wieruszeski JM, Leger H, Eilebrecht S, Benecke A. 2011. SUMO-1 regulates the conformational dynamics of thymine-DNA glycosylase regulatory domain and competes with its DNA binding activity. BMC Biochem. 12:4. https://doi.org/10.1186/1471-2091-12-4.
   PubMedGoogle Scholar
• Smith M, Bhaskar V, Fernandez J, Courey AJ. 2004. Drosophila Ulp1, a nuclear pore-associated SUMO protease, prevents accumulation of cytoplasmic SUMO conjugates. J. Biol. Chem. 279:43805–43814.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Hatakeyama S, Saitoh H, Nakayama KI. 2005. Noncovalent SUMO-1 binding activity of thymine DNA glycosylase (TDG) is required for its SUMO-1 modification and colocalization with the promyelocytic leukemia protein. J. Biol. Chem. 280:5611–5621.
   PubMedGoogle Scholar
• Takanaka Y, Courey AJ. 2005. SUMO enhances vestigial function during wing morphogenesis. Mech. Dev. 122:1130–1137.
   PubMedGoogle Scholar
• Tatham MH, et al. 2001. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276:35368–35374.
   PubMed Web of Science ®Google Scholar
• Terui Y, Saad N, Jia S, McKeon F, Yuan J. 2004. Dual role of sumoylation in the nuclear localization and transcriptional activation of NFAT1. J. Biol. Chem. 279:28257–28265.
   PubMedGoogle Scholar
• Verger A, Perdomo J, Crossley M. 2003. Modification with SUMO. A role in transcriptional regulation. EMBO Rep. 4:137–142.
   PubMed Web of Science ®Google Scholar
• Wallis D, et al. 2003. The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. Development 130:221–232.
   PubMed Web of Science ®Google Scholar
• Wei F, Scholer HR, Atchison ML. 2007. Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J. Biol. Chem. 282:21551–21560.
   PubMedGoogle Scholar
• Witt LM, et al. 2010. Atonal, Senseless, and Abdominal-A regulate rhomboid enhancer activity in abdominal sensory organ precursors. Dev. Biol. 344:1060–1070.
   PubMedGoogle Scholar
• Yang Z, Ding K, Pan L, Deng M, Gan L. 2003. Math5 determines the competence state of retinal ganglion cell progenitors. Dev. Biol. 264:240–254.
   PubMedGoogle Scholar
• Yoon H, Lee DJ, Kim MH, Bok J. 2011. Identification of genes concordantly expressed with Atoh1 during inner ear development. Anat. Cell Biol. 44:69–78.
   PubMedGoogle Scholar
• Zhong S, et al. 2000. Role of SUMO-1-modified PML in nuclear body formation. Blood 95:2748–2752.
   PubMed Web of Science ®Google Scholar
• zur Lage PI, Powell LM, Prentice DR, McLaughlin P, Jarman AP. 2004. EGF receptor signaling triggers recruitment of Drosophila sense organ precursors by stimulating proneural gene autoregulation. Dev. Cell 7:687–696.
   PubMed Web of Science ®Google Scholar
• zur Lage PI, Prentice DR, Holohan EE, Jarman AP. 2003. The Drosophila proneural gene amos promotes olfactory sensillum formation and suppresses bristle formation. Development 130:4683–4693.
   PubMedGoogle Scholar
• Zweidler-Mckay PA, Grimes HL, Flubacher MM, Tsichlis PN. 1996. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol. Cell. Biol. 16:4024–4034.
   PubMed Web of Science ®Google Scholar