CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts

Noritaka Matsuo, Shizuko Tanaka, Marion Gordon, Manuel Koch, Hidekatsu Yoshioka, Francesco Ramirez

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

Collagen XXIV is a newly discovered and poorly characterized member of the fibril-forming family of collagen molecules, which displays unique structural features of invertebrate fibrillar collagens and is expressed predominantly in bone tissue. Here we report the characterization of the proximal promoter of the mouse gene (Col24a1) and its regulation in osteoblastic cells. Using well characterized murine models of osteoblast differentiation, we found that the Col24a1 gene is activated sometime before onset of the late differentiation marker osteocalcin. Additional analyses revealed that Col24a1 produces equal amounts of two alternatively spliced products with different 5′-untranslated sequences that originate from distinct transcriptional start sites. Cell transfection experiments in combination with DNA binding assays demonstrated that Col24a1 promoter activity in ROS17/2.8 osteosarcoma cells is under the control of an upstream cis-acting element, which is shared by both transcripts and is recognized by specific combinations of c-Jun, CREB1, ATF1, and ATF2 dimers. Consistent with these results, overexpression of c-Jun, ATF1, ATF2, or CREB1 in transiently transfected osteoblastic cells stimulated transcription from reporter gene constructs driven by the Col24a1 promoter to different degrees. Moreover, chromatin immunoprecipitation experiments showed that these nuclear factors bind the same upstream sequence of the endogenous Col24a1 gene. Collectively these data provide new information about transcriptional control of collagen fibrillogenesis, in addition to implicating for the first time CREB-AP1 protein complexes in the regulation of collagen gene expression in osteoblasts.

Original languageEnglish (US)
Pages (from-to)5445-5452
Number of pages8
JournalJournal of Biological Chemistry
Volume281
Issue number9
DOIs
StatePublished - Mar 3 2006

Fingerprint

Cyclic AMP Response Element-Binding Protein
Osteoblasts
Transcription
Genes
Collagen
Proteins
Fibrillar Collagens
Chromatin Immunoprecipitation
Osteocalcin
Differentiation Antigens
Gene Expression Regulation
Osteosarcoma
Invertebrates
Reporter Genes
Gene expression
Dimers
Chromatin
Transfection
Assays
Bone

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Matsuo, Noritaka ; Tanaka, Shizuko ; Gordon, Marion ; Koch, Manuel ; Yoshioka, Hidekatsu ; Ramirez, Francesco. / CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts. In: Journal of Biological Chemistry. 2006 ; Vol. 281, No. 9. pp. 5445-5452.
@article{d71e3cc001904e66b49b9780cbc96f20,
title = "CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts",
abstract = "Collagen XXIV is a newly discovered and poorly characterized member of the fibril-forming family of collagen molecules, which displays unique structural features of invertebrate fibrillar collagens and is expressed predominantly in bone tissue. Here we report the characterization of the proximal promoter of the mouse gene (Col24a1) and its regulation in osteoblastic cells. Using well characterized murine models of osteoblast differentiation, we found that the Col24a1 gene is activated sometime before onset of the late differentiation marker osteocalcin. Additional analyses revealed that Col24a1 produces equal amounts of two alternatively spliced products with different 5′-untranslated sequences that originate from distinct transcriptional start sites. Cell transfection experiments in combination with DNA binding assays demonstrated that Col24a1 promoter activity in ROS17/2.8 osteosarcoma cells is under the control of an upstream cis-acting element, which is shared by both transcripts and is recognized by specific combinations of c-Jun, CREB1, ATF1, and ATF2 dimers. Consistent with these results, overexpression of c-Jun, ATF1, ATF2, or CREB1 in transiently transfected osteoblastic cells stimulated transcription from reporter gene constructs driven by the Col24a1 promoter to different degrees. Moreover, chromatin immunoprecipitation experiments showed that these nuclear factors bind the same upstream sequence of the endogenous Col24a1 gene. Collectively these data provide new information about transcriptional control of collagen fibrillogenesis, in addition to implicating for the first time CREB-AP1 protein complexes in the regulation of collagen gene expression in osteoblasts.",
author = "Noritaka Matsuo and Shizuko Tanaka and Marion Gordon and Manuel Koch and Hidekatsu Yoshioka and Francesco Ramirez",
year = "2006",
month = "3",
day = "3",
doi = "10.1074/jbc.M509923200",
language = "English (US)",
volume = "281",
pages = "5445--5452",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "9",

}

CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts. / Matsuo, Noritaka; Tanaka, Shizuko; Gordon, Marion; Koch, Manuel; Yoshioka, Hidekatsu; Ramirez, Francesco.

In: Journal of Biological Chemistry, Vol. 281, No. 9, 03.03.2006, p. 5445-5452.

Research output: Contribution to journalArticle

TY - JOUR

T1 - CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts

AU - Matsuo, Noritaka

AU - Tanaka, Shizuko

AU - Gordon, Marion

AU - Koch, Manuel

AU - Yoshioka, Hidekatsu

AU - Ramirez, Francesco

PY - 2006/3/3

Y1 - 2006/3/3

N2 - Collagen XXIV is a newly discovered and poorly characterized member of the fibril-forming family of collagen molecules, which displays unique structural features of invertebrate fibrillar collagens and is expressed predominantly in bone tissue. Here we report the characterization of the proximal promoter of the mouse gene (Col24a1) and its regulation in osteoblastic cells. Using well characterized murine models of osteoblast differentiation, we found that the Col24a1 gene is activated sometime before onset of the late differentiation marker osteocalcin. Additional analyses revealed that Col24a1 produces equal amounts of two alternatively spliced products with different 5′-untranslated sequences that originate from distinct transcriptional start sites. Cell transfection experiments in combination with DNA binding assays demonstrated that Col24a1 promoter activity in ROS17/2.8 osteosarcoma cells is under the control of an upstream cis-acting element, which is shared by both transcripts and is recognized by specific combinations of c-Jun, CREB1, ATF1, and ATF2 dimers. Consistent with these results, overexpression of c-Jun, ATF1, ATF2, or CREB1 in transiently transfected osteoblastic cells stimulated transcription from reporter gene constructs driven by the Col24a1 promoter to different degrees. Moreover, chromatin immunoprecipitation experiments showed that these nuclear factors bind the same upstream sequence of the endogenous Col24a1 gene. Collectively these data provide new information about transcriptional control of collagen fibrillogenesis, in addition to implicating for the first time CREB-AP1 protein complexes in the regulation of collagen gene expression in osteoblasts.

AB - Collagen XXIV is a newly discovered and poorly characterized member of the fibril-forming family of collagen molecules, which displays unique structural features of invertebrate fibrillar collagens and is expressed predominantly in bone tissue. Here we report the characterization of the proximal promoter of the mouse gene (Col24a1) and its regulation in osteoblastic cells. Using well characterized murine models of osteoblast differentiation, we found that the Col24a1 gene is activated sometime before onset of the late differentiation marker osteocalcin. Additional analyses revealed that Col24a1 produces equal amounts of two alternatively spliced products with different 5′-untranslated sequences that originate from distinct transcriptional start sites. Cell transfection experiments in combination with DNA binding assays demonstrated that Col24a1 promoter activity in ROS17/2.8 osteosarcoma cells is under the control of an upstream cis-acting element, which is shared by both transcripts and is recognized by specific combinations of c-Jun, CREB1, ATF1, and ATF2 dimers. Consistent with these results, overexpression of c-Jun, ATF1, ATF2, or CREB1 in transiently transfected osteoblastic cells stimulated transcription from reporter gene constructs driven by the Col24a1 promoter to different degrees. Moreover, chromatin immunoprecipitation experiments showed that these nuclear factors bind the same upstream sequence of the endogenous Col24a1 gene. Collectively these data provide new information about transcriptional control of collagen fibrillogenesis, in addition to implicating for the first time CREB-AP1 protein complexes in the regulation of collagen gene expression in osteoblasts.

UR - http://www.scopus.com/inward/record.url?scp=33646836641&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33646836641&partnerID=8YFLogxK

U2 - 10.1074/jbc.M509923200

DO - 10.1074/jbc.M509923200

M3 - Article

C2 - 16373341

AN - SCOPUS:33646836641

VL - 281

SP - 5445

EP - 5452

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 9

ER -