Broad complex isoforms have unique distributions during central nervous system metamorphosis in Drosophila melanogaster

Rebecca F. Spokony, Linda L Restifo

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Broad Complex (BRC) is a highly conserved, ecdysone-pathway gene essential for metamorphosis in Drosophila melanogaster, and possibly all holometabolous insects. Alternative splicing among duplicated exons produces several BRC isoforms, each with one zinc-finger DNA-binding domain (Z1, Z2, Z3, or Z4), highly expressed at the onset of metamorphosis. BRC-Z1, BRC-Z2, and BRC-Z3 represent distinct genetic functions (BRC complementation groups rbp, br, and 2Bc, respectively) and are required at discrete stages spanning final-instar larva through very young pupa. We showed previously that morphogenetic movements necessary for adult CNS maturation require BRC-Z1, -Z2, and -Z3, but not at the same time: BRC-Z1 is required in the mid-prepupa, BRC-Z2 and -Z3 are required earlier, at the larval-prepupal transition. To explore how BRC isoforms controlling the same morphogenesis events do so at different times, we examined their central nervous system (CNS) expression patterns during the ≈16 hours bracketing the hormone-regulated start of metamorphosis. Each isoform had a unique pattern, with BRC-Z3 being the most distinctive. There was some colocalization of isoform pairs, but no three-way overlap of BRC-Z1, -Z2, and -Z3. Instead, their most prominent expression was in glia (BRC-Z1), neuroblasts (BRC-Z2), or neurons (BRC-Z3). Despite sequence similarity to BRC-Z1, BRC-Z4 was expressed in a unique subset of neurons. These data suggest a switch in BRC isoform choice, from BRC-Z2 in proliferating cells to BRC-Z1, BRC-Z3, or BRC-Z4 in differentiating cells. Together with isoform-selective temporal requirements and phenotype considerations, this cell-type-selective expression suggests a model of BRC-dependent CNS morphogenesis resulting from intercellular interactions, culminating in BRCZ1-controlled, glia-mediated CNS movements in late prepupa.

Original languageEnglish (US)
Pages (from-to)15-36
Number of pages22
JournalJournal of Comparative Neurology
Volume517
Issue number1
DOIs
StatePublished - 2009

Fingerprint

Drosophila melanogaster
Protein Isoforms
Central Nervous System
Morphogenesis
Neuroglia
Ecdysone
Neurons
Pupa
Essential Genes
Zinc Fingers
Alternative Splicing
Larva
Insects
Exons
Hormones
Phenotype
DNA

Keywords

  • Duplicated exons
  • Ecdysone cascade
  • Glia
  • Insect
  • Morphogenesis
  • Neuroblast
  • Neuron
  • Subfunctionalization

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Broad complex isoforms have unique distributions during central nervous system metamorphosis in Drosophila melanogaster. / Spokony, Rebecca F.; Restifo, Linda L.

In: Journal of Comparative Neurology, Vol. 517, No. 1, 2009, p. 15-36.

Research output: Contribution to journalArticle

@article{a6d315093c00415f964248cdb0e496e7,
title = "Broad complex isoforms have unique distributions during central nervous system metamorphosis in Drosophila melanogaster",
abstract = "Broad Complex (BRC) is a highly conserved, ecdysone-pathway gene essential for metamorphosis in Drosophila melanogaster, and possibly all holometabolous insects. Alternative splicing among duplicated exons produces several BRC isoforms, each with one zinc-finger DNA-binding domain (Z1, Z2, Z3, or Z4), highly expressed at the onset of metamorphosis. BRC-Z1, BRC-Z2, and BRC-Z3 represent distinct genetic functions (BRC complementation groups rbp, br, and 2Bc, respectively) and are required at discrete stages spanning final-instar larva through very young pupa. We showed previously that morphogenetic movements necessary for adult CNS maturation require BRC-Z1, -Z2, and -Z3, but not at the same time: BRC-Z1 is required in the mid-prepupa, BRC-Z2 and -Z3 are required earlier, at the larval-prepupal transition. To explore how BRC isoforms controlling the same morphogenesis events do so at different times, we examined their central nervous system (CNS) expression patterns during the ≈16 hours bracketing the hormone-regulated start of metamorphosis. Each isoform had a unique pattern, with BRC-Z3 being the most distinctive. There was some colocalization of isoform pairs, but no three-way overlap of BRC-Z1, -Z2, and -Z3. Instead, their most prominent expression was in glia (BRC-Z1), neuroblasts (BRC-Z2), or neurons (BRC-Z3). Despite sequence similarity to BRC-Z1, BRC-Z4 was expressed in a unique subset of neurons. These data suggest a switch in BRC isoform choice, from BRC-Z2 in proliferating cells to BRC-Z1, BRC-Z3, or BRC-Z4 in differentiating cells. Together with isoform-selective temporal requirements and phenotype considerations, this cell-type-selective expression suggests a model of BRC-dependent CNS morphogenesis resulting from intercellular interactions, culminating in BRCZ1-controlled, glia-mediated CNS movements in late prepupa.",
keywords = "Duplicated exons, Ecdysone cascade, Glia, Insect, Morphogenesis, Neuroblast, Neuron, Subfunctionalization",
author = "Spokony, {Rebecca F.} and Restifo, {Linda L}",
year = "2009",
doi = "10.1002/cne.22119",
language = "English (US)",
volume = "517",
pages = "15--36",
journal = "Journal of Comparative Neurology",
issn = "0021-9967",
publisher = "Wiley-Liss Inc.",
number = "1",

}

TY - JOUR

T1 - Broad complex isoforms have unique distributions during central nervous system metamorphosis in Drosophila melanogaster

AU - Spokony, Rebecca F.

AU - Restifo, Linda L

PY - 2009

Y1 - 2009

N2 - Broad Complex (BRC) is a highly conserved, ecdysone-pathway gene essential for metamorphosis in Drosophila melanogaster, and possibly all holometabolous insects. Alternative splicing among duplicated exons produces several BRC isoforms, each with one zinc-finger DNA-binding domain (Z1, Z2, Z3, or Z4), highly expressed at the onset of metamorphosis. BRC-Z1, BRC-Z2, and BRC-Z3 represent distinct genetic functions (BRC complementation groups rbp, br, and 2Bc, respectively) and are required at discrete stages spanning final-instar larva through very young pupa. We showed previously that morphogenetic movements necessary for adult CNS maturation require BRC-Z1, -Z2, and -Z3, but not at the same time: BRC-Z1 is required in the mid-prepupa, BRC-Z2 and -Z3 are required earlier, at the larval-prepupal transition. To explore how BRC isoforms controlling the same morphogenesis events do so at different times, we examined their central nervous system (CNS) expression patterns during the ≈16 hours bracketing the hormone-regulated start of metamorphosis. Each isoform had a unique pattern, with BRC-Z3 being the most distinctive. There was some colocalization of isoform pairs, but no three-way overlap of BRC-Z1, -Z2, and -Z3. Instead, their most prominent expression was in glia (BRC-Z1), neuroblasts (BRC-Z2), or neurons (BRC-Z3). Despite sequence similarity to BRC-Z1, BRC-Z4 was expressed in a unique subset of neurons. These data suggest a switch in BRC isoform choice, from BRC-Z2 in proliferating cells to BRC-Z1, BRC-Z3, or BRC-Z4 in differentiating cells. Together with isoform-selective temporal requirements and phenotype considerations, this cell-type-selective expression suggests a model of BRC-dependent CNS morphogenesis resulting from intercellular interactions, culminating in BRCZ1-controlled, glia-mediated CNS movements in late prepupa.

AB - Broad Complex (BRC) is a highly conserved, ecdysone-pathway gene essential for metamorphosis in Drosophila melanogaster, and possibly all holometabolous insects. Alternative splicing among duplicated exons produces several BRC isoforms, each with one zinc-finger DNA-binding domain (Z1, Z2, Z3, or Z4), highly expressed at the onset of metamorphosis. BRC-Z1, BRC-Z2, and BRC-Z3 represent distinct genetic functions (BRC complementation groups rbp, br, and 2Bc, respectively) and are required at discrete stages spanning final-instar larva through very young pupa. We showed previously that morphogenetic movements necessary for adult CNS maturation require BRC-Z1, -Z2, and -Z3, but not at the same time: BRC-Z1 is required in the mid-prepupa, BRC-Z2 and -Z3 are required earlier, at the larval-prepupal transition. To explore how BRC isoforms controlling the same morphogenesis events do so at different times, we examined their central nervous system (CNS) expression patterns during the ≈16 hours bracketing the hormone-regulated start of metamorphosis. Each isoform had a unique pattern, with BRC-Z3 being the most distinctive. There was some colocalization of isoform pairs, but no three-way overlap of BRC-Z1, -Z2, and -Z3. Instead, their most prominent expression was in glia (BRC-Z1), neuroblasts (BRC-Z2), or neurons (BRC-Z3). Despite sequence similarity to BRC-Z1, BRC-Z4 was expressed in a unique subset of neurons. These data suggest a switch in BRC isoform choice, from BRC-Z2 in proliferating cells to BRC-Z1, BRC-Z3, or BRC-Z4 in differentiating cells. Together with isoform-selective temporal requirements and phenotype considerations, this cell-type-selective expression suggests a model of BRC-dependent CNS morphogenesis resulting from intercellular interactions, culminating in BRCZ1-controlled, glia-mediated CNS movements in late prepupa.

KW - Duplicated exons

KW - Ecdysone cascade

KW - Glia

KW - Insect

KW - Morphogenesis

KW - Neuroblast

KW - Neuron

KW - Subfunctionalization

UR - http://www.scopus.com/inward/record.url?scp=70349843230&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=70349843230&partnerID=8YFLogxK

U2 - 10.1002/cne.22119

DO - 10.1002/cne.22119

M3 - Article

C2 - 19711379

AN - SCOPUS:70349843230

VL - 517

SP - 15

EP - 36

JO - Journal of Comparative Neurology

JF - Journal of Comparative Neurology

SN - 0021-9967

IS - 1

ER -