Home LiteratureArticle Details
PMID: 11390985 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Endogenous Msx1 antisense transcript: in vivo and in vitro evidences, structure, and potential involvement in skeleton development in mammals.

Blin-Wakkach C, Lezot F, Ghoul-Mazgar S, Hotton D, Monteiro S, Teillaud C, Pibouin L, Orestes-Cardoso S, Papagerakis P, Macdougall M, Robert B, Berdal A

Abstract

Msx1 is a key factor for the development of tooth and craniofacial skeleton and has been proposed to play a pivotal role in terminal cell differentiation. In this paper, we demonstrated the presence of an endogenous Msx1 antisense RNA (Msx1-AS RNA) in mice, rats, and humans. In situ analysis revealed that this RNA is expressed only in differentiated dental and bone cells with an inverse correlation with Msx1 protein. These in vivo data and overexpression of Msx1 sense and AS RNA in an odontoblastic cell line (MO6-G3) showed that the balance between the levels of the two Msx1 RNAs is related to the expression of Msx1 protein. To analyze the impact of this balance in the Msx-Dlx homeoprotein pathway, we analyzed the effect of Msx1, Msx2, and Dlx5 overexpression on proteins involved in skeletal differentiation. We showed that the Msx1-AS RNA is involved in crosstalk between the Msx-Dlx pathways because its expression was abolished by Dlx5. Msx1 was shown to down-regulate a master gene of skeletal cells differentiation, Cbfa1. All these data strongly suggest that the ratio between Msx1 sense and antisense RNAs is a very important factor in the control of skeletal terminal differentiation. Finally, the initiation site for Msx1-AS RNA transcription was located by primer extension in both mouse and human in an identical region, including a consensus TATA box, suggesting an evolutionary conservation of the AS RNA-mediated regulation of Msx1 gene expression.

MeSH Terms
Amino Acid Sequence Animals Cattle Cell Line Chickens Conserved Sequence Embryonic and Fetal Development Evolution, Molecular Gene Expression Regulation, Developmental Heterozygote Homeodomain Proteins/genetics,physiology Humans MSX1 Transcription Factor Mammals Mice Mice, Knockout Molecular Sequence Data Odontoblasts/cytology,physiology Osteogenesis Protein Biosynthesis RNA, Antisense/genetics Rats Sequence Alignment Sequence Homology, Amino Acid Transcription Factors Transcription, Genetic
Chemicals
Homeodomain Proteins MSX1 Transcription Factor Msx1 protein, rat RNA, Antisense Transcription Factors
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Blin-Wakkach C
Laboratory of Biology-Odontology, Institut National de la Santé et de la Recherche Médicale, E 0110, Institut des Cordeliers, IFR 58, 75006 Paris, France. biol_odonto_fr@yahoo.com
Lezot F
Ghoul-Mazgar S
Hotton D
Monteiro S
Teillaud C
Pibouin L
Orestes-Cardoso S
Papagerakis P
Macdougall M
Robert B
Berdal A
References (43)
43 references, click to expand
  1. Regulation of organogenesis. Common molecular mechanisms regulating the development of teeth and other organs.
    Int J Dev Biol. 1995 Feb;39(1):35-50 PMID: 7626420
  2. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5.
    Development. 1999 Sep;126(17):3795-809 PMID: 10433909
  3. In situ hybridization of calbindin-D 28 k transcripts in undecalcified sections of the rat continuously erupting incisor.
    Connect Tissue Res. 1995;32(1-4):137-43 PMID: 7554910
  4. Temperature sensitive simian virus 40 large T antigen immortalization of murine odontoblast cell cultures: establishment of clonal odontoblast cell line.
    Connect Tissue Res. 1995;33(1-3):97-103 PMID: 7554969
  5. A PEBP2 alpha/AML-1-related factor increases osteocalcin promoter activity through its binding to an osteoblast-specific cis-acting element.
    J Biol Chem. 1995 Dec 29;270(52):30973-9 PMID: 8537354
  6. An AML-1 consensus sequence binds an osteoblast-specific complex and transcriptionally activates the osteocalcin gene.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):4968-73 PMID: 8643513
  7. A human MSX1 homeodomain missense mutation causes selective tooth agenesis.
    Nat Genet. 1996 Aug;13(4):417-21 PMID: 8696335
  8. Biomineralization, life-time of odontogenic cells and differential expression of the two homeobox genes MSX-1 and DLX-2 in transgenic mice.
    J Bone Miner Res. 2000 Mar;15(3):430-41 PMID: 10750557
  9. The uniqueness of the imprinting mechanism.
    Curr Opin Genet Dev. 2000 Apr;10(2):229-33 PMID: 10753780
  10. Dedifferentiation of mammalian myotubes induced by msx1.
    Cell. 2000 Dec 22;103(7):1099-109 PMID: 11163185
  11. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  12. A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1.
    Genes Dev. 1989 Jan;3(1):26-37 PMID: 2565278
  13. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis.
    EMBO J. 1989 Jan;8(1):91-100 PMID: 2565810
  14. Fast and sensitive multiple sequence alignments on a microcomputer.
    Comput Appl Biosci. 1989 Apr;5(2):151-3 PMID: 2720464
  15. Msx1 controls inductive signaling in mammalian tooth morphogenesis.
    Development. 1996 Oct;122(10):3035-44 PMID: 8898217
  16. Study of osteoblast-specific expression of one mouse osteocalcin gene: characterization of the factor binding to OSE2.
    Connect Tissue Res. 1996;35(1-4):7-14 PMID: 9084638
  17. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation.
    Cell. 1997 May 30;89(5):747-54 PMID: 9182762
  18. Msx1 antagonizes the myogenic activity of Pax3 in migrating limb muscle precursors.
    Development. 1999 Nov;126(22):4965-76 PMID: 10529415
  19. MSX1 mutation is associated with orofacial clefting and tooth agenesis in humans.
    Nat Genet. 2000 Apr;24(4):342-3 PMID: 10742093
  20. An antisense transcript from the Xenopus laevis bFGF gene coding for an evolutionarily conserved 24 kd protein.
    EMBO J. 1989 Oct;8(10):2983-8 PMID: 2479540
  21. N-myc mRNA forms an RNA-RNA duplex with endogenous antisense transcripts.
    Mol Cell Biol. 1990 Aug;10(8):4180-91 PMID: 1695323
  22. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  23. The homeobox gene Hox 7.1 has specific regional and temporal expression patterns during early murine craniofacial embryogenesis, especially tooth development in vivo and in vitro.
    Development. 1991 Feb;111(2):269-85 PMID: 1680043
  24. Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation.
    Nature. 1992 Dec 3;360(6403):477-81 PMID: 1360150
  25. The expression pattern of the chicken homeobox-containing gene GHox-7 in developing polydactylous limb buds suggests its involvement in apical ectodermal ridge-directed outgrowth of limb mesoderm and in programmed cell death.
    Differentiation. 1993 Jan;52(2):129-37 PMID: 8097171
  26. Characterization of the human HOX 7 cDNA and identification of polymorphic markers.
    Hum Mol Genet. 1992 Sep;1(6):407-10 PMID: 1284527
  27. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development.
    Cell. 1993 Oct 8;75(1):45-58 PMID: 8104708
  28. Antisense RNA and p53 regulation in induced murine cell differentiation.
    Ann N Y Acad Sci. 1992 Oct 28;660:77-87 PMID: 1340159
  29. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development.
    Nat Genet. 1994 Apr;6(4):348-56 PMID: 7914451
  30. Msx-2/Hox 8.1: a transcriptional regulator of the rat osteocalcin promoter.
    Mol Endocrinol. 1994 Nov;8(11):1484-93 PMID: 7877617
  31. Experimental analysis of Msx-1 and Msx-2 gene expression during chick mandibular morphogenesis.
    Dev Dyn. 1995 Feb;202(2):195-214 PMID: 7734736
  32. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts.
    Cell. 1997 May 30;89(5):755-64 PMID: 9182763
  33. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia.
    Cell. 1997 May 30;89(5):773-9 PMID: 9182765
  34. Insertional mutation of the mouse Msx1 homeobox gene by an nlacZ reporter gene.
    Mech Dev. 1997 Jul;65(1-2):123-33 PMID: 9256350
  35. Stage-specific expression of Dlx-5 during osteoblast differentiation: involvement in regulation of osteocalcin gene expression.
    Mol Endocrinol. 1997 Oct;11(11):1681-94 PMID: 9328350
  36. Haploinsufficiency of MSX1: a mechanism for selective tooth agenesis.
    Mol Cell Biol. 1998 Oct;18(10):6044-51 PMID: 9742121
  37. FGFs and BMP4 induce both Msx1-independent and Msx1-dependent signaling pathways in early tooth development.
    Development. 1998 Nov;125(21):4325-33 PMID: 9753686
  38. Reciprocal regulation of osteocalcin transcription by the homeodomain proteins Msx2 and Dlx5.
    Biochemistry. 1998 Nov 17;37(46):16360-8 PMID: 9819228
  39. Antisense RNA: function and fate of duplex RNA in cells of higher eukaryotes.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1415-34 PMID: 9841677
  40. Tsix, a gene antisense to Xist at the X-inactivation centre.
    Nat Genet. 1999 Apr;21(4):400-4 PMID: 10192391
  41. Expression of DLX5 during human embryonic craniofacial development.
    Mech Dev. 1999 Mar;81(1-2):183-6 PMID: 10330497
  42. The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb.
    Development. 1999 Jun;126(12):2689-701 PMID: 10331980
  43. MSX1 inhibits myoD expression in fibroblast x 10T1/2 cell hybrids.
    Cell. 1995 Aug 25;82(4):611-20 PMID: 7664340
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-06-19
Epub
2001-00-05
Pages
7336-41
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC34669
Subset
IM
Databases
GENBANK
AF267728
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com