TnaA, an SP-RING protein, interacts with Osa, a subunit of the chromatin remodeling complex BRAHMA and with the SUMOylation pathway in Drosophila melanogaster

Juan Monribot-Villanueva; R Alejandro Juárez-Uribe; Zoraya Palomera-Sánchez; Lucía Gutiérrez-Aguiar; Mario Zurita; James A Kennison; Martha Vázquez

doi:10.1371/journal.pone.0062251

TnaA, an SP-RING protein, interacts with Osa, a subunit of the chromatin remodeling complex BRAHMA and with the SUMOylation pathway in Drosophila melanogaster

PLoS One. 2013 Apr 19;8(4):e62251. doi: 10.1371/journal.pone.0062251. Print 2013.

Authors

Juan Monribot-Villanueva¹, R Alejandro Juárez-Uribe, Zoraya Palomera-Sánchez, Lucía Gutiérrez-Aguiar, Mario Zurita, James A Kennison, Martha Vázquez

Affiliation

¹ Departamento de Fisiología Molecular y Genética del Desarrollo, Instituto de Biotecnología-Universidad Nacional Autónoma de México, Cuernavaca, Morelos, México.

Abstract

Tonalli A (TnaA) is a Drosophila melanogaster protein with an XSPRING domain. The XSPRING domain harbors an SP-RING zinc-finger, which is characteristic of proteins with SUMO E3 ligase activity. TnaA is required for homeotic gene expression and is presumably involved in the SUMOylation pathway. Here we analyzed some aspects of the TnaA location in embryo and larval stages and its genetic and biochemical interaction with SUMOylation pathway proteins. We describe that there are at least two TnaA proteins (TnaA130 and TnaA123) differentially expressed throughout development. We show that TnaA is chromatin-associated at discrete sites on polytene salivary gland chromosomes of third instar larvae and that tna mutant individuals do not survive to adulthood, with most dying as third instar larvae or pupae. The tna mutants that ultimately die as third instar larvae have an extended life span of at least 4 to 15 days as other SUMOylation pathway mutants. We show that TnaA physically interacts with the SUMO E2 conjugating enzyme Ubc9, and with the BRM complex subunit Osa. Furthermore, we show that tna and osa interact genetically with SUMOylation pathway components and individuals carrying mutations for these genes show a phenotype that can be the consequence of misexpression of developmental-related genes.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Carrier Proteins / chemistry
Carrier Proteins / metabolism*
Cell Cycle Proteins / metabolism*
Chromatin / metabolism
Chromatin Assembly and Disassembly*
DNA-Binding Proteins / metabolism*
Drosophila Proteins / chemistry
Drosophila Proteins / metabolism*
Drosophila melanogaster / genetics
Drosophila melanogaster / growth & development
Drosophila melanogaster / metabolism*
Epistasis, Genetic
Genes, Insect / genetics
Larva / growth & development
Larva / metabolism
Phenotype
Polytene Chromosomes / metabolism
Protein Binding
Protein Structure, Tertiary
Protein Subunits / metabolism*
Salivary Glands / metabolism
Signal Transduction
Sumoylation*
Time Factors
Trans-Activators / metabolism*
Ubiquitin-Conjugating Enzymes / metabolism
Wings, Animal / anatomy & histology

Substances

Carrier Proteins
Cell Cycle Proteins
Chromatin
DNA-Binding Proteins
Drosophila Proteins
Protein Subunits
Trans-Activators
brm protein, Drosophila
osa protein, Drosophila
tna protein, Drosophila
Ubiquitin-Conjugating Enzymes
ubiquitin-conjugating enzyme UBC9

Grants and funding

This work was supported by funds from Dirección General Asuntos del Personal Académico (DGAPA) grant IN208808 (http://dgapa.unam.mx/html/papiit/papit.html), and Consejo Nacional Ciencia y Tecnología (CONACyT) grant 99654 (http://www.conacyt.gob.mx) to M. V. and in part by the Intramural Research Program of the United States National Institutes of Health, National Institute of Child Health and Human Development (NICHD) (http://dir.nichd.nih.gov/dirweb/home.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.