SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres

Alan P. Kenny, David J Kozlowski, David W. Oleksyn, Lynne M. Angerer, Robert C. Angerer

Research output: Contribution to journalArticle

67 Citations (Scopus)

Abstract

We have identified a Sox family transcription factor, SpSoxB1, that is asymmetrically distributed among blastomeres of the sea urchin embryo during cleavage, beginning at 4th cleavage. SpSoxB1 interacts with a cis element that is essential for transcription of SpAN, a gene that is activated cell autonomously and expressed asymmetrically along the animal-vegetal axis. In vitro translated SpSoxB1 forms a specific complex with this cis element whose mobility is identical to that formed by a protein in nuclear extracts. An anti-SpSoxB1 rabbit polyclonal antiserum specifically supershifts this DNA-protein complex and recognizes a single protein on immunoblots of nuclear proteins that comigrates with in vitro translated SpSoxB1. Developmental immunoblots of total proteins at selected early developmental stages, as well as EMSA of egg and 16-cell stage proteins, show that SpSoxB1 present at low levels in unfertilized eggs and progressively accumulates during cleavage. SpSoxB1 maternal transcripts are uniformly distributed in the unfertilized egg and the protein accumulates to similar, high concentrations in all nuclei of 4- and 8-cell embryos. However, at fourth cleavage, the micromeres, which are partitioned by asymmetric division of the vegetal 4 blastomeres, have reduced nuclear levels of the protein, while high levels persist in their sister macromeres and in the mesomeres. During cleavage, the uniform maternal SpSoxB1 transcript distribution is replaced by a zygotic nonvegetal pattern that reinforces the asymmetric SpSoxB1 protein distribution and reflects the corresponding domain of SpAN mRNA accumulation at early blastula stage (~ 150 cells). The vegetal region lacking nuclear SpSoxB1 gradually expands so that, after blastula stage, only cells in differentiating ectoderm accumulate this protein in their nuclei. The results reported here support a model in which SpSoxB1 is a major regulator of the initial phase of asymmetric transcription of SpAN in the nonvegetal domain by virtue of its distribution at 4th cleavage and is subsequently an important spatial determinant of expression in the early blastula. This factor is the earliest known spatially restricted regulator of transcription along the animal-vegetal axis of the sea urchin embryo.

Original languageEnglish (US)
Pages (from-to)5473-5483
Number of pages11
JournalDevelopment
Volume126
Issue number23
StatePublished - Dec 1 1999
Externally publishedYes

Fingerprint

Blastomeres
Sea Urchins
Transcription Factors
Blastula
Nuclear Proteins
Ovum
Proteins
Embryonic Structures
Mothers
Egg Proteins
Ectoderm
Immune Sera
Rabbits
Messenger RNA
DNA
Genes

Keywords

  • Animal-vegetal axis
  • Gene regulation
  • Sea urchin
  • Sox
  • SpaN

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Kenny, A. P., Kozlowski, D. J., Oleksyn, D. W., Angerer, L. M., & Angerer, R. C. (1999). SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. Development, 126(23), 5473-5483.

SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. / Kenny, Alan P.; Kozlowski, David J; Oleksyn, David W.; Angerer, Lynne M.; Angerer, Robert C.

In: Development, Vol. 126, No. 23, 01.12.1999, p. 5473-5483.

Research output: Contribution to journalArticle

Kenny, AP, Kozlowski, DJ, Oleksyn, DW, Angerer, LM & Angerer, RC 1999, 'SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres', Development, vol. 126, no. 23, pp. 5473-5483.
Kenny, Alan P. ; Kozlowski, David J ; Oleksyn, David W. ; Angerer, Lynne M. ; Angerer, Robert C. / SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres. In: Development. 1999 ; Vol. 126, No. 23. pp. 5473-5483.
@article{9b17a6476d8f4bb095b370b19e0feae8,
title = "SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres",
abstract = "We have identified a Sox family transcription factor, SpSoxB1, that is asymmetrically distributed among blastomeres of the sea urchin embryo during cleavage, beginning at 4th cleavage. SpSoxB1 interacts with a cis element that is essential for transcription of SpAN, a gene that is activated cell autonomously and expressed asymmetrically along the animal-vegetal axis. In vitro translated SpSoxB1 forms a specific complex with this cis element whose mobility is identical to that formed by a protein in nuclear extracts. An anti-SpSoxB1 rabbit polyclonal antiserum specifically supershifts this DNA-protein complex and recognizes a single protein on immunoblots of nuclear proteins that comigrates with in vitro translated SpSoxB1. Developmental immunoblots of total proteins at selected early developmental stages, as well as EMSA of egg and 16-cell stage proteins, show that SpSoxB1 present at low levels in unfertilized eggs and progressively accumulates during cleavage. SpSoxB1 maternal transcripts are uniformly distributed in the unfertilized egg and the protein accumulates to similar, high concentrations in all nuclei of 4- and 8-cell embryos. However, at fourth cleavage, the micromeres, which are partitioned by asymmetric division of the vegetal 4 blastomeres, have reduced nuclear levels of the protein, while high levels persist in their sister macromeres and in the mesomeres. During cleavage, the uniform maternal SpSoxB1 transcript distribution is replaced by a zygotic nonvegetal pattern that reinforces the asymmetric SpSoxB1 protein distribution and reflects the corresponding domain of SpAN mRNA accumulation at early blastula stage (~ 150 cells). The vegetal region lacking nuclear SpSoxB1 gradually expands so that, after blastula stage, only cells in differentiating ectoderm accumulate this protein in their nuclei. The results reported here support a model in which SpSoxB1 is a major regulator of the initial phase of asymmetric transcription of SpAN in the nonvegetal domain by virtue of its distribution at 4th cleavage and is subsequently an important spatial determinant of expression in the early blastula. This factor is the earliest known spatially restricted regulator of transcription along the animal-vegetal axis of the sea urchin embryo.",
keywords = "Animal-vegetal axis, Gene regulation, Sea urchin, Sox, SpaN",
author = "Kenny, {Alan P.} and Kozlowski, {David J} and Oleksyn, {David W.} and Angerer, {Lynne M.} and Angerer, {Robert C.}",
year = "1999",
month = "12",
day = "1",
language = "English (US)",
volume = "126",
pages = "5473--5483",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "23",

}

TY - JOUR

T1 - SpSoxB1, a maternally encoded transcription factor asymmetrically distributed among early sea urchin blastomeres

AU - Kenny, Alan P.

AU - Kozlowski, David J

AU - Oleksyn, David W.

AU - Angerer, Lynne M.

AU - Angerer, Robert C.

PY - 1999/12/1

Y1 - 1999/12/1

N2 - We have identified a Sox family transcription factor, SpSoxB1, that is asymmetrically distributed among blastomeres of the sea urchin embryo during cleavage, beginning at 4th cleavage. SpSoxB1 interacts with a cis element that is essential for transcription of SpAN, a gene that is activated cell autonomously and expressed asymmetrically along the animal-vegetal axis. In vitro translated SpSoxB1 forms a specific complex with this cis element whose mobility is identical to that formed by a protein in nuclear extracts. An anti-SpSoxB1 rabbit polyclonal antiserum specifically supershifts this DNA-protein complex and recognizes a single protein on immunoblots of nuclear proteins that comigrates with in vitro translated SpSoxB1. Developmental immunoblots of total proteins at selected early developmental stages, as well as EMSA of egg and 16-cell stage proteins, show that SpSoxB1 present at low levels in unfertilized eggs and progressively accumulates during cleavage. SpSoxB1 maternal transcripts are uniformly distributed in the unfertilized egg and the protein accumulates to similar, high concentrations in all nuclei of 4- and 8-cell embryos. However, at fourth cleavage, the micromeres, which are partitioned by asymmetric division of the vegetal 4 blastomeres, have reduced nuclear levels of the protein, while high levels persist in their sister macromeres and in the mesomeres. During cleavage, the uniform maternal SpSoxB1 transcript distribution is replaced by a zygotic nonvegetal pattern that reinforces the asymmetric SpSoxB1 protein distribution and reflects the corresponding domain of SpAN mRNA accumulation at early blastula stage (~ 150 cells). The vegetal region lacking nuclear SpSoxB1 gradually expands so that, after blastula stage, only cells in differentiating ectoderm accumulate this protein in their nuclei. The results reported here support a model in which SpSoxB1 is a major regulator of the initial phase of asymmetric transcription of SpAN in the nonvegetal domain by virtue of its distribution at 4th cleavage and is subsequently an important spatial determinant of expression in the early blastula. This factor is the earliest known spatially restricted regulator of transcription along the animal-vegetal axis of the sea urchin embryo.

AB - We have identified a Sox family transcription factor, SpSoxB1, that is asymmetrically distributed among blastomeres of the sea urchin embryo during cleavage, beginning at 4th cleavage. SpSoxB1 interacts with a cis element that is essential for transcription of SpAN, a gene that is activated cell autonomously and expressed asymmetrically along the animal-vegetal axis. In vitro translated SpSoxB1 forms a specific complex with this cis element whose mobility is identical to that formed by a protein in nuclear extracts. An anti-SpSoxB1 rabbit polyclonal antiserum specifically supershifts this DNA-protein complex and recognizes a single protein on immunoblots of nuclear proteins that comigrates with in vitro translated SpSoxB1. Developmental immunoblots of total proteins at selected early developmental stages, as well as EMSA of egg and 16-cell stage proteins, show that SpSoxB1 present at low levels in unfertilized eggs and progressively accumulates during cleavage. SpSoxB1 maternal transcripts are uniformly distributed in the unfertilized egg and the protein accumulates to similar, high concentrations in all nuclei of 4- and 8-cell embryos. However, at fourth cleavage, the micromeres, which are partitioned by asymmetric division of the vegetal 4 blastomeres, have reduced nuclear levels of the protein, while high levels persist in their sister macromeres and in the mesomeres. During cleavage, the uniform maternal SpSoxB1 transcript distribution is replaced by a zygotic nonvegetal pattern that reinforces the asymmetric SpSoxB1 protein distribution and reflects the corresponding domain of SpAN mRNA accumulation at early blastula stage (~ 150 cells). The vegetal region lacking nuclear SpSoxB1 gradually expands so that, after blastula stage, only cells in differentiating ectoderm accumulate this protein in their nuclei. The results reported here support a model in which SpSoxB1 is a major regulator of the initial phase of asymmetric transcription of SpAN in the nonvegetal domain by virtue of its distribution at 4th cleavage and is subsequently an important spatial determinant of expression in the early blastula. This factor is the earliest known spatially restricted regulator of transcription along the animal-vegetal axis of the sea urchin embryo.

KW - Animal-vegetal axis

KW - Gene regulation

KW - Sea urchin

KW - Sox

KW - SpaN

UR - http://www.scopus.com/inward/record.url?scp=0033385941&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0033385941&partnerID=8YFLogxK

M3 - Article

VL - 126

SP - 5473

EP - 5483

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 23

ER -