Collagen 11a1 is indirectly activated by lymphocyte enhancer-binding factor 1 (Lef1) and negatively regulates osteoblast maturation

Matrix Biology

Volumn 27, Issue 4, 2008, Pages 330-338

  Kahler, Rachel A ^a   Yingst, Sorcha M C ^b   Hoeppner, Luke H ^a   Jensen, Eric D ^a   Krawczak, David ^a   Oxford, Julia T ^b   Westendorf, Jennifer J ^c,d  

^a UNIVERSITY OF MINNESOTA   (United States)

^b BOISE STATE UNIVERSITY   (United States)

^c MAYO CLINIC   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

Author keywords

Beta catenin; Collagen 11a1; Lef1; Osteoblasts; V1b; VO; Wnt

Indexed keywords

ALKALINE PHOSPHATASE; ANTISENSE OLIGONUCLEOTIDE; BETA CATENIN; COLLAGEN TYPE 11; COLLAGEN TYPE 11A1; DNA BINDING PROTEIN; LYMPHOCYTE ENHANCER BINDING FACTOR 1; WNT PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL MATURATION; CELL STRAIN 3T3; CONTROLLED STUDY; GENE ACTIVATION; GENE TARGETING; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ALKALINE PHOSPHATASE; ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL LINE; COLLAGEN TYPE XI; GENE EXPRESSION REGULATION; LYMPHOID ENHANCER-BINDING FACTOR 1; MICE; OSTEOBLASTS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING;

EID: 43049146483     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2008.01.002     Document Type: Article

References (54)

1. Annunen S., Korkko J., Czarny M., Warman M.L., Brunner H.G., Kaariainen H., Mulliken J.B., Tranebjaerg L., Brooks D.G., Cox G.F., Cruysberg J.R., Curtis M.A., Davenport S.L., Friedrich C.A., Kaitila I., Krawczynski M.R., Latos-Bielenska A., Mukai S., Olsen B.R., Shinno N., Somer M., Vikkula M., Zlotogora J., Prockop D.J., and Ala-Kokko L. Splicing mutations of 54-bp exons in the COL11A1 gene cause Marshall syndrome, but other mutations cause overlapping Marshall/Stickler phenotypes. Am. J. Hum. Genet. 65 (1999) 974-983
2. Ayme S., and Preus M. The Marshall and Stickler syndromes: objective rejection of lumping. J. Med. Genet. 21 (1984) 34-38
3. Baron R., Rawadi G., and Roman-Roman S. Wnt signaling: a key regulator of bone mass. Curr. Top. Dev. Biol. 76 (2006) 103-127
4. Behrens J., von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., and Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382 (1996) 638-642
5. Bi Y., Stuelten C.H., Kilts T., Wadhwa S., Iozzo R.V., Robey P.G., Chen X.D., and Young M.F. Extracellular matrix proteoglycans control the fate of bone marrow stromal cells. J. Biol. Chem. 280 (2005) 30481-30489
6. Bix G., and Iozzo R.V. Matrix revolutions: "tails" of basement-membrane components with angiostatic functions. Trends Cell Biol. 15 (2005) 52-60
7. Clevers H., and van de Wetering M. TCF/LEF factor earn their wings. Trends Genet. 13 (1997) 485-489
8. Comper W.D. Extracellular Matrix (1996), Harwood Academic Publishers, Amsterdam, The Netherlands
9. Davies G.B., Oxford J.T., Hausafus L.C., Smoody B.F., and Morris N.P. Temporal and spatial expression of alternative splice-forms of the alpha1(XI) collagen gene in fetal rat cartilage. Dev. Dyn. 213 (1998) 12-26
10. Fichard A., Kleman J.P., and Ruggiero F. Another look at collagen V and XI molecules. Matrix Biol. 14 (1995) 515-531
11. Fischer H., Salahshor S., Stenling R., Bjork J., Lindmark G., Iselius L., Rubio C., and Lindblom A. COL11A1 in FAP polyps and in sporadic colorectal tumors. BMC Cancer 1 (2001) 17
12. Galceran J., Sustmann C., Hsu S.C., Folberth S., and Grosschedl R. LEF1-mediated regulation of Delta-like1 links Wnt and Notch signaling in somitogenesis. Genes Dev. 18 (2004) 2718-2723
13. Gelse K., Poschl E., and Aigner T. Collagens-structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55 (2003) 1531-1546
14. Glass II D.A., and Karsenty G. In vivo analysis of Wnt signaling in bone. Endocrinology 148 (2007) 2630-2634
15. Gokhale J.A., Robey P.G., and Boskey A.L. The biochemistry of bone. Osteoporosis (2001), San Diego, CA, Academic Press
16. Gregory K.E., Oxford J.T., Chen Y., Gambee J.E., Gygi S.P., Aebersold R., Neame P.J., Mechling D.E., Bachinger H.P., and Morris N.P. Structural organization of distinct domains within the non-collagenous N-terminal region of collagen type XI. J. Biol. Chem. 275 (2000) 11498-11506
17. Griffith A.J., Sprunger L.K., Sirko-Osadsa D.A., Tiller G.E., Meisler M.H., and Warman M.L. Marshall syndrome associated with a splicing defect at the COL11A1 locus. Am. J. Hum. Genet. 62 (1998) 816-823
18. Iozzo R.V. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev., Mol. Cell Biol. 6 (2005) 646-656
19. Iyama K., Sumiyoshi H., Khaleduzzaman M., Matsuo N., Ninomiya Y., and Yoshioka H. Differential expression of two exons of the alpha1(XI) collagen gene (Col11a1) in the mouse embryo. Matrix Biol. 20 (2001) 53-61
20. Jakkula E., Melkoniemi M., Kiviranta I., Lohiniva J., Raina S.S., Perala M., Warman M.L., Ahonen K., Kroger H., Goring H.H., and Ala-Kokko L. The role of sequence variations within the genes encoding collagen II, IX and XI in non-syndromic, early-onset osteoarthritis. Osteoarthr. Cartil. 13 (2005) 497-507
21. Kahler R.A., and Westendorf J.J. Lymphoid enhancer factor-1 and beta-catenin inhibit Runx2-dependent transcriptional activation of the osteocalcin promoter. J. Biol. Chem. 278 (2003) 11937-11944
22. Kahler R.A., Galindo M., Lian J., Stein G.S., van Wijnen A.J., and Westendorf J.J. Lymphocyte enhancer-binding factor 1 (Lef1) inhibits terminal differentiation of osteoblasts. J. Cell. Biochem. 97 (2006) 969-983
23. Kim S.W., Park J.I., Spring C.M., Sater A.K., Ji H., Otchere A.A., Daniel J.M., and McCrea P.D. Non-canonical Wnt signals are modulated by the Kaiso transcriptional repressor and p120-catenin. Nat. Cell Biol. 6 (2004) 1212-1220
24. Kinoshita A., Greenwel P., Tanaka S., Di Liberto M., Yoshioka H., and Ramirez F. A transcription activator with restricted tissue distribution regulates cell-specific expression of alpha1(XI) collagen. J. Biol. Chem. 272 (1997) 31777-31784
25. Li Y., Lacerda D.A., Warman M.L., Beier D.R., Yoshioka H., Ninomiya Y., Oxford J.T., Morris N.P., Andrikopoulos K., Ramirez F., et al. A fibrillar collagen gene, Col11a1, is essential for skeletal morphogenesis. Cell 80 (1995) 423-430
26. Lui V.C., Kong R.Y., Nicholls J., Cheung A.N., and Cheah K.S. The mRNAs for the three chains of human collagen type XI are widely distributed but not necessarily co-expressed: implications for homotrimeric, heterotrimeric and heterotypic collagen molecules. Biochem. J. 311 Pt 2 (1995) 511-516
27. Martin S., Richards A.J., Yates J.R., Scott J.D., Pope M., and Snead M.P. Stickler syndrome: further mutations in COL11A1 and evidence for additional locus heterogeneity. Eur. J. Hum. Genet. 7 (1999) 807-814
28. Matsuo N., Yu-Hua W., Sumiyoshi H., Sakata-Takatani K., Nagato H., Sakai K., Sakurai M., and Yoshioka H. The transcription factor CCAAT-binding factor CBF/NF-Y regulates the proximal promoter activity in the human alpha 1(XI) collagen gene (COL11A1). J. Biol. Chem. 278 (2003) 32763-32770
29. Medeck R.J., Sosa S., Morris N., and Oxford J.T. BMP-1-mediated proteolytic processing of alternatively spliced isoforms of collagen type XI. Biochem. J. 376 (2003) 361-368
30. Meisler M.H., Griffith A.J., Warman M., Tiller G., and Sprunger L.K. Gene symbol: COL11A1. Disease: Marshall Syndrome. Hum. Genet. vol. 102 (1998) 498
31. Melkoniemi M., Koillinen H., Mannikko M., Warman M.L., Pihlajamaa T., Kaariainen H., Rautio J., Hukki J., Stofko J.A., Cisneros G.J., Krakow D., Cohn D.H., Kere J., and Ala-Kokko L. Collagen XI sequence variations in nonsyndromic cleft palate, Robin sequence and micrognathia. Eur. J. Hum. Genet. 11 (2003) 265-270
32. Morris N.P., Oxford J.T., Davies G.B., Smoody B.F., and Keene D.R. Developmentally regulated alternative splicing of the alpha1(XI) collagen chain: spatial and temporal segregation of isoforms in the cartilage of fetal rat long bones. J. Histochem. Cytochem. 48 (2000) 725-741
33. Noponen-Hietala N., Kyllonen E., Mannikko M., Ilkko E., Karppinen J., Ott J., and Ala-Kokko L. Sequence variations in the collagen IX and XI genes are associated with degenerative lumbar spinal stenosis. Ann. Rheum. Dis. 62 (2003) 1208-1214
34. Olsen B.R. Mutations in collagen genes resulting in metaphyseal and epiphyseal dysplasias. Bone 17 (1995) 45S-49S
35. Park J.I., Kim S.W., Lyons J.P., Ji H., Nguyen T.T., Cho K., Barton M.C., Deroo T., Vleminckx K., Moon R.T., and McCrea P.D. Kaiso/p120-catenin and TCF/beta-catenin complexes coordinately regulate canonical Wnt gene targets. Dev. Cell 8 (2005) 843-854
36. Robey P.G., and Boskey A.L. Extracellular matrix and biomineralization of bone. Primer on the Metabolic Bone Diseases Disorders and Mineral Metabolism (2003), American Society for Bone and Mineral Research, Washington, D.C
37. Rodriguez R.R., Seegmiller R.E., Stark M.R., and Bridgewater L.C. A type XI collagen mutation leads to increased degradation of type II collagen in articular cartilage. Osteoarthr. Cartil. 12 (2004) 314-320
38. Scott P.G., Dodd C.M., and Pringle G.A. Mapping the locations of the epitopes of five monoclonal antibodies to the core protein of dermatan sulfate proteoglycan II (decorin). J. Biol. Chem. 268 (1993) 11558-11564
39. Seegmiller R., Fraser F.C., and Sheldon H. A new chondrodystrophic mutant in mice. Electron microscopy of normal and abnormal chondrogenesis. J. Cell Biol. 48 (1971) 580-593
40. Snead M.P., and Yates J.R. Clinical and molecular genetics of Stickler syndrome. J. Med. Genet. 36 (1999) 353-359
41. Snead M.P., Yates J.R., Williams R., Payne S.J., Pope F.M., and Scott J.D. Stickler syndrome type 2 and linkage to the COL11A1 gene. Ann. N.Y. Acad. Sci. 785 (1996) 331-332
42. So C.L., Kaluarachchi K., Tam P.P., and Cheah K.S. Impact of mutations of cartilage matrix genes on matrix structure, gene activity and chondrogenesis. Osteoarthr. Cartil. 9 (2001) S160-S173 Suppl A
43. Spring C.M., Kelly K.F., O'Kelly I., Graham M., Crawford H.C., and Daniel J.M. The catenin p120ctn inhibits Kaiso-mediated transcriptional repression of the beta-catenin/TCF target gene matrilysin. Exp. Cell Res. 305 (2005) 253-265
44. Stratton R.F., Lee B., and Ramirez F. Marshall syndrome. Am. J. Med. Genet. 41 (1991) 35-38
45. Thom J.R., and Morris N.P. Biosynthesis and proteolytic processing of type XI collagen in embryonic chick sterna. J. Biol. Chem. 266 (1991) 7262-7269
46. Tran K.T., Griffith L., and Wells A. Extracellular matrix signaling through growth factor receptors during wound healing. Wound Repair Regen. 12 (2004) 262-268
47. Tran K.T., Lamb P., and Deng J.S. Matrikines and matricryptins: implications for cutaneous cancers and skin repair. J. Dermatol. Sci. 40 (2005) 11-20
48. van Genderen C., Okamura R.M., Farinas I., Quo R.G., Parslow T.G., Bruhn L., and Grosschedl R. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8 (1994) 2691-2703
49. Warner L.R., Blasick C.M., Brown R.J., and Oxford J.T. Expression, purification, and refolding of recombinant collagen alpha1(XI) amino terminal domain splice variants. Protein Expr. Purif. 52 (2007) 403-409
50. Waterman M.L. Lymphoid enhancer factor/T cell factor expression in colorectal cancer. Cancer Metastasis Rev. 23 (2004) 41-52
51. Westendorf J.J., Kahler R.A., and Schroeder T.M. Wnt signaling in osteoblasts and bone diseases. Gene 341 (2004) 19-39
52. Winter R.M., Baraitser M., Laurence K.M., Donnai D., and Hall C.M. The Weissenbacher-Zweymuller, Stickler, and Marshall syndromes: further evidence for their identity. Am. J. Med. Genet. 16 (1983) 189-199
53. Yoshioka H., Greenwel P., Inoguchi K., Truter S., Inagaki Y., Ninomiya Y., and Ramirez F. Structural and functional analysis of the promoter of the human alpha 1(XI) collagen gene. J. Biol. Chem. 270 (1995) 418-424
54. Yoshioka H., Iyama K., Inoguchi K., Khaleduzzaman M., Ninomiya Y., and Ramirez F. Developmental pattern of expression of the mouse alpha 1 (XI) collagen gene (Col11a1). Dev. Dyn. 204 (1995) 41-47