TY - JOUR

T1 - Gaga regulates border cell migration in drosophila

AU - Ogienko, Anna A.

AU - Yarinich, Lyubov A.

AU - Fedorova, Elena V.

AU - Dorogova, Natalya V.

AU - Bayborodin, Sergey I.

AU - Baricheva, Elina M.

AU - Pindyurin, Alexey V.

PY - 2020/10/2

Y1 - 2020/10/2

N2 - Collective cell migration is a complex process that happens during normal development of many multicellular organisms, as well as during oncological transformations. In Drosophila oogenesis, a small set of follicle cells originally located at the anterior tip of each egg chamber become motile and migrate as a cluster through nurse cells toward the oocyte. These specialized cells are referred to as border cells (BCs) and provide a simple and convenient model system to study collective cell migration. The process is known to be complexly regulated at different levels and the product of the slow border cells (slbo) gene, the C/EBP transcription factor, is one of the key elements in this process. However, little is known about the regulation of slbo expression. On the other hand, the ubiquitously expressed transcription factor GAGA, which is encoded by the Trithorax-like (Trl) gene was previously demonstrated to be important for Drosophila oogenesis. Here, we found that Trl mutations cause substantial defects in BC migration. Partially, these defects are explained by the reduced level of slbo expression in BCs. Additionally, a strong genetic interaction between Trl and slbo mutants, along with the presence of putative GAGA binding sites within the slbo promoter and enhancer, suggests the direct regulation of this gene by GAGA. This idea is supported by the reduction in the slbo-Gal4-driven GFP expression within BC clusters in Trl mutant background. However, the inability of slbo overexpression to compensate defects in BC migration caused by Trl mutations suggests that there are other GAGA target genes contributing to this process. Taken together, the results define GAGA as another important regulator of BC migration in Drosophila oogenesis.

AB - Collective cell migration is a complex process that happens during normal development of many multicellular organisms, as well as during oncological transformations. In Drosophila oogenesis, a small set of follicle cells originally located at the anterior tip of each egg chamber become motile and migrate as a cluster through nurse cells toward the oocyte. These specialized cells are referred to as border cells (BCs) and provide a simple and convenient model system to study collective cell migration. The process is known to be complexly regulated at different levels and the product of the slow border cells (slbo) gene, the C/EBP transcription factor, is one of the key elements in this process. However, little is known about the regulation of slbo expression. On the other hand, the ubiquitously expressed transcription factor GAGA, which is encoded by the Trithorax-like (Trl) gene was previously demonstrated to be important for Drosophila oogenesis. Here, we found that Trl mutations cause substantial defects in BC migration. Partially, these defects are explained by the reduced level of slbo expression in BCs. Additionally, a strong genetic interaction between Trl and slbo mutants, along with the presence of putative GAGA binding sites within the slbo promoter and enhancer, suggests the direct regulation of this gene by GAGA. This idea is supported by the reduction in the slbo-Gal4-driven GFP expression within BC clusters in Trl mutant background. However, the inability of slbo overexpression to compensate defects in BC migration caused by Trl mutations suggests that there are other GAGA target genes contributing to this process. Taken together, the results define GAGA as another important regulator of BC migration in Drosophila oogenesis.

KW - Border cells

KW - Cell migration

KW - Drosophila melanogaster

KW - GAGA

KW - Slbo

KW - Trl

KW - ENCODES

KW - C/EBP

KW - PROTEIN

KW - CHROMATIN

KW - ANTERIOR-POSTERIOR AXIS

KW - TRITHORAX-LIKE GENE

KW - border cells

KW - HYPOMORPHIC MUTATION

KW - slbo

KW - JAK/STAT PATHWAY

KW - OOGENESIS

KW - cell migration

KW - BINDING

UR - http://www.scopus.com/inward/record.url?scp=85092361223&partnerID=8YFLogxK

U2 - 10.3390/ijms21207468

DO - 10.3390/ijms21207468

M3 - Article

C2 - 33050455

AN - SCOPUS:85092361223

VL - 21

SP - 1

EP - 16

JO - International Journal of Molecular Sciences

JF - International Journal of Molecular Sciences

SN - 1661-6596

IS - 20

M1 - 7468

ER -