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Protein & Cell

, Volume 3, Issue 6, pp 419–433 | Cite as

Minor fibrillar collagens, variable regions alternative splicing, intrinsic disorder, and tyrosine sulfation

  • Ming Fang
  • Reed Jacob
  • Owen McDougal
  • Julia Thom OxfordEmail author
Review

Abstract

Minor fibrillar collagen types V and XI, are those less abundant than the fibrillar collagen types I, II and III. The alpha chains share a high degree of similarity with respect to protein sequence in all domains except the variable region. Genomic variation and, in some cases, extensive alternative splicing contribute to the unique sequence characteristics of the variable region. While unique expression patterns in tissues exist, the functions and biological relevance of the variable regions have not been elucidated. In this review, we summarize the existing knowledge about expression patterns and biological functions of the collagen types V and XI alpha chains. Analysis of biochemical similarities among the peptides encoded by each exon of the variable region suggests the potential for a shared function. The alternative splicing, conservation of biochemical characteristics in light of low sequence conservation, and evidence for intrinsic disorder, suggest modulation of binding events between the surface of collagen fibrils and surrounding extracellular molecules as a shared function.

Keywords

minor fibrillar collagens variable regions alternative splicing fibrillogenesis heparan sulfate binding sites intrinsic disorder tyrosine sulfation 

Supplementary material

13238_2012_2917_MOESM1_ESM.pdf (533 kb)
Supplementary Material(PDF 533 kb)

References

  1. Andrikopoulos, K., Liu, X., Keene, D.R., Jaenisch, R., and Ramirez, F. (1995). Targeted mutation in the col5a2 gene reveals a regulatory role for type V collagen during matrix assembly. Nat Genet 9, 31–36.Google Scholar
  2. Andrikopoulos, K., Suzuki, H.R., Solursh, M., and Ramirez, F. (1992). Localization of pro-alpha 2(V) collagen transcripts in the tissues of the developing mouse embryo. Dev Dyn 195, 113–120.Google Scholar
  3. Annunen, S., Körkkö, J., Czarny, M., Warman, M.L., Brunner, H.G., Kääriäinen, H., Mulliken, J.B., Tranebjaerg, L., Brooks, D.G., Cox, G.F., et al. (1999). 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, 974–983.Google Scholar
  4. Ben-Dov, C., Hartmann, B., Lundgren, J., and Valcárcel, J. (2008). Genome-wide analysis of alternative pre-mRNA splicing. J Biol Chem 283, 1229–1233.Google Scholar
  5. Bi, W., Deng, J.M., Zhang, Z., Behringer, R.R., and de Crombrugghe, B. (1999). Sox9 is required for cartilage formation. Nat Genet 22, 85–89.Google Scholar
  6. Birk, D.E. (2001). Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly. Micron 32, 223–237.Google Scholar
  7. Blaschke, U.K., Eikenberry, E.F., Hulmes, D.J.S., Galla, H.-J., and Bruckner, P. (2000). Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J Biol Chem 275, 10370–10378.Google Scholar
  8. Bowman, K.G., and Bertozzi, C.R. (1999). Carbohydrate sulfotransferases: mediators of extracellular communication. Chem Biol 6, R9–R22.Google Scholar
  9. Bridgewater, L.C., Lefebvre, V., and de Crombrugghe, B. (1998). Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J Biol Chem 273, 14998–15006.Google Scholar
  10. Chang, W.C., Lee, T.Y., Shien, D.M., Hsu, J.B., Horng, J.T., Hsu, P.C., Wang, T.Y., Huang, H.D., and Pan, R.L. (2009). Incorporating support vector machine for identifying protein tyrosine sulfation sites. J Comput Chem 30, 2526–2537.Google Scholar
  11. Chanut-Delalande, H., Fichard, A., Bernocco, S., Garrone, R., Hulmes, D.J.S., and Ruggiero, F. (2001). Control of heterotypic fibril formation by collagen V is determined by chain stoichiometry. J Biol Chem 276, 24352–24359.Google Scholar
  12. Chen, Y., Sumiyoshi, H., Oxford, J.T., Yoshioka, H., Ramirez, F., and Morris, N.P. (2001). Cis-acting elements regulate alternative splicing of exons 6A, 6B and 8 of the α1(XI) collagen gene and contribute to the regional diversification of collagen XI matrices. Matrix Biol 20, 589–599.Google Scholar
  13. Davies, S.R., Chang, L.-W., Patra, D., Xing, X., Posey, K., Hecht, J., Stormo, G.D., and Sandell, L.J. (2007). Computational identification and functional validation of regulatory motifs in cartilage-expressed genes. Genome Res 17, 1438–1447.Google Scholar
  14. Erdman, R., Stahl, R.C., Rothblum, K., Chernousov, M.A., and Carey, D.J. (2002). Schwann cell adhesion to a novel heparan sulfate binding site in the N-terminal domain of alpha 4 type V collagen is mediated by syndecan-3. J Biol Chem 277, 7619–7625.Google Scholar
  15. Fabbri, M., Garzon, R., Cimmino, A., Liu, Z., Zanesi, N., Callegari, E., Liu, S., Alder, H., Costinean, S., Fernandez-Cymering, C., et al. (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 104, 15805–15810.Google Scholar
  16. Fernandes, R.J., Weis, M., Scott, M.A., Seegmiller, R.E., and Eyre, D.R. (2007). Collagen XI chain misassembly in cartilage of the chondrodysplasia (cho) mouse. Matrix Biol 26, 597–603.Google Scholar
  17. Fessler, L.I., Brosh, S., Chapin, S., and Fessler, J.H. (1986). Tyrosine sulfation in precursors of collagen V. J Biol Chem 261, 5034–5040.Google Scholar
  18. Fichard, A., Kleman, J.P., and Ruggiero, F. (1995). Another look at collagen V and XI molecules. Matrix Biol 14, 515–531.Google Scholar
  19. Fischer, H., Stenling, R., Rubio, C., and Lindblom, A. (2001). Colorectal carcinogenesis is associated with stromal expression of COL11A1 and COL5A2. Carcinogenesis 22, 875–878.Google Scholar
  20. Fletcher, R.B., Baker, J.C., and Harland, R.M. (2006). FGF8 spliceforms mediate early mesoderm and posterior neural tissue formation in Xenopus. Development 133, 1703–1714.Google Scholar
  21. Gregory, K.E., Oxford, J.T., Chen, Y., Gambee, J.E., Gygi, S.P., Aebersold, R., Neame, P.J., Mechling, D.E., Bächinger, H.P., and Morris, N.P. (2000). Structural organization of distinct domains within the non-collagenous N-terminal region of collagen type XI. J Biol Chem 275, 11498–11506.Google Scholar
  22. Grimson, A., Farh, K.K.-H., Johnston, W.K., Garrett-Engele, P., Lim, L.P., and Bartel, D.P. (2007). MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27, 91–105.Google Scholar
  23. Guo, Q., and Li, J.Y.H. (2007). Distinct functions of the major Fgf8 spliceform, Fgf8b, before and during mouse gastrulation. Development 134, 2251–2260.Google Scholar
  24. Halsted, K.C., Bowen, K.B., Bond, L., Luman, S.E., Jorcyk, C.L., Fyffe, W.E., Kronz, J.D., and Oxford, J.T. (2008). Collagen α1(XI) in normal and malignant breast tissue. Mod Pathol 21, 1246–1254.Google Scholar
  25. Heller, H., Schaefer, M., and Schulten, K. (1993). Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid-crystal phases. J Phys Chem 97, 8343–8360.Google Scholar
  26. Holmes, D.F., and Kadler, K.E. (2006). The 10+4 microfibril structure of thin cartilage fibrils. Proc Natl Acad Sci U S A 103, 17249–17254.Google Scholar
  27. Huang, S.C., Yu, D.H., Wank, S.A., Mantey, S., Gardner, J.D., and Jensen, R.T. (1989). Importance of sulfation of gastrin or cholecystokinin (CCK) on affinity for gastrin and CCK receptors. Peptides 10, 785–789.Google Scholar
  28. Imamura, Y., Scott, I.C., and Greenspan, D.S. (2000). The pro-alpha3(V) collagen chain. Complete primary structure, expression domains in adult and developing tissues, and comparison to the structures and expression domains of the other types V and XI procollagen chains. J Biol Chem 275, 8749–8759.Google Scholar
  29. Imhof, M., and Trueb, B. (2001). Alternative splicing of the first F3 domain from chicken collagen XIV affects cell adhesion and heparin binding. J Biol Chem 276, 9141–9148.Google Scholar
  30. Kadler, K.E., Baldock, C., Bella, J., and Boot-Handford, R.P. (2007). Collagens at a glance. J Cell Sci 120, 1955–1958.Google Scholar
  31. Kadler, K.E., Hill, A., and Canty-Laird, E.G. (2008). Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr Opin Cell Biol 20, 495–501.Google Scholar
  32. Kahler, R.A., Yingst, S.M.C., Hoeppner, L.H., Jensen, E.D., Krawczak, D., Oxford, J.T., and Westendorf, J.J. (2008). Collagen 11a1 is indirectly activated by lymphocyte enhancer-binding factor 1 (Lef1) and negatively regulates osteoblast maturation. Matrix Biol 27, 330–338.Google Scholar
  33. Kato, M., Zhang, J., Wang, M., Lanting, L., Yuan, H., Rossi, J.J., and Natarajan, R. (2007). MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-β-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 104, 3432–3437.Google Scholar
  34. Kinoshita, A., Greenwel, P., Tanaka, S., Di Liberto, M., Yoshioka, H., and Ramirez, F. (1997). A transcription activator with restricted tissue distribution regulates cell-specific expression of alpha1(XI) collagen. J Biol Chem 272, 31777–31784.Google Scholar
  35. Krek, A., Grün, D., Poy, M.N., Wolf, R., Rosenberg, L., Epstein, E.J., MacMenamin, P., da Piedade, I., Gunsalus, K.C., Stoffel, M., et al. (2005). Combinatorial microRNA target predictions. Nat Genet 37, 495–500.Google Scholar
  36. Ladd, A., and Cooper, T. (2002). Finding signals that regulate alternative splicing in the post-genomic era. Genome Biol 3, reviews0008.0001 reviews0008.0016.Google Scholar
  37. Lee, S., and Greenspan, D.S. (1995). Transcriptional promoter of the human alpha 1(V) collagen gene (COL5A1). Biochem J 310, 15–22.Google Scholar
  38. Leitinger, B., and Hohenester, E. (2007). Mammalian collagen receptors. Matrix Biol 26, 146–155.Google Scholar
  39. Leyte, A., van Schijndel, H.B., Niehrs, C., Huttner, W.B., Verbeet, M.P., Mertens, K., and van Mourik, J.A. (1991). Sulfation of Tyr1680 of human blood coagulation factor VIII is essential for the interaction of factor VIII with von Willebrand factor. J Biol Chem 266, 740–746.Google Scholar
  40. Li, S.-W., Takanosu, M., Arita, M., Bao, Y., Ren, Z.-X., Maier, A., Prockop, D.J., and Mayne, R. (2001). Targeted disruption of Col11a2 produces a mild cartilage phenotype in transgenic mice: comparison with the human disorder otospondylomegaepiphyseal dysplasia (OSMED). Dev Dyn 222, 141–152.Google Scholar
  41. Li, X.-Y., Mantovani, R., Hooft van Huijsduijnen, R., Andre, I., Benoist, C., and Mathis, D. (1992). Evolutionary variation of the CCAAT-binding transcription factor NF-Y. Nucleic Acids Res 20, 1087–1091.Google Scholar
  42. 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. (1995). A fibrillar collagen gene, Col11a1, is essential for skeletal morphogenesis. Cell 80, 423–430.Google Scholar
  43. Lincoln, J., Florer, J.B., Deutsch, G.H., Wenstrup, R.J., and Yutzey, K.E. (2006a). ColVa1 and ColXIa1 are required for myocardial morphogenesis and heart valve development. Dev Dyn 235, 3295–3305.Google Scholar
  44. Lincoln, J., Florer, J.B., Deutsch, G.H., Wenstrup, R.J., and Yutzey, K.E. (2006b). ColVa1 and ColXIa1 are required for myocardial morphogenesis and heart valve development. Dev Dyn 235, 3295–3305.Google Scholar
  45. Lincoln, J., Kist, R., Scherer, G., and Yutzey, K.E. (2007). Sox9 is required for precursor cell expansion and extracellular matrix organization during mouse heart valve development. Dev Biol 305, 120–132.Google Scholar
  46. Liu, M.C., and Lipmann, F. (1985). Isolation of tyrosine-O-sulfate by Pronase hydrolysis from fibronectin secreted by Fujinami sarcoma virus-infected rat fibroblasts. Proc Natl Acad Sci U S A 82, 34–37.Google Scholar
  47. Lui, V.C., Kong, R.Y., Nicholls, J., Cheung, A.N., and Cheah, K.S. (1995). 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, 511–516.Google Scholar
  48. Lui, V.C., Ng, L.J., Sat, E.W., Nicholls, J., and Cheah, K.S. (1996). Extensive alternative splicing within the amino-propeptide coding domain of alpha2(XI) procollagen mRNAs. Expression of transcripts encoding truncated pro-alpha chains. J Biol Chem 271, 16945–16951.Google Scholar
  49. Luparello, C., and Sirchia, R. (2005). Type V collagen regulates the expression of apoptotic and stress response genes by breast cancer cells. J Cell Physiol 202, 411–421.Google Scholar
  50. Makeyev, E.V., and Maniatis, T. (2008). Multilevel regulation of gene expression by microRNAs. Science 319, 1789–1790.Google Scholar
  51. Marchant, J.K., Hahn, R.A., Linsenmayer, T.F., and Birk, D.E. (1996). Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. J Cell Biol 135, 1415–1426.Google Scholar
  52. Matlin, A.J., Clark, F., and Smith, C.W.J. (2005). Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 6, 386–398.Google Scholar
  53. Matsui, Y., Chansky, H.A., Barahmand-Pour, F., Zielinska-Kwiatkowska, A., Tsumaki, N., Myoui, A., Yoshikawa, H., Yang, L., and Eyre, D.R. (2003). COL11A2 collagen gene transcription is differentially regulated by EWS/ERG sarcoma fusion protein and wild-type ERG. J Biol Chem 278, 11369–11375.Google Scholar
  54. Matsuo, N., Yu-Hua, W., Sumiyoshi, H., Sakata-Takatani, K., Nagato, H., Sakai, K., Sakurai, M., and Yoshioka, H. (2003). The transcription factor CCAAT-binding factor CBF/NF-Y regulates the proximal promoter activity in the human α1(XI) collagen gene (COL11A1). J Biol Chem 278, 32763–32770.Google Scholar
  55. Mayne, R., Brewton, R.G., Mayne, P.M., and Baker, J.R. (1993). Isolation and characterization of the chains of type V/type XI collagen present in bovine vitreous. J Biol Chem 268, 9381–9386.Google Scholar
  56. McAlinden, A., Havlioglu, N., Liang, L., Davies, S.R., and Sandell, L.J. (2005). Alternative splicing of type II procollagen exon 2 is regulated by the combination of a weak 5′ splice site and an adjacent intronic stem-loop cis element. J Biol Chem 280, 32700–32711.Google Scholar
  57. McAlinden, A., Liang, L., Mukudai, Y., Imamura, T., and Sandell, L.J. (2007). Nuclear protein TIA-1 regulates COL2A1 alternative splicing and interacts with precursor mRNA and genomic DNA. J Biol Chem 282, 24444–24454.Google Scholar
  58. McDougal, O.M., Mallory, C., Warner, L.R., and Oxford, J.T. (2011). Predicted structure and binding motifs of collagen α1(XI). J BioInformatics BioTech (In press).Google Scholar
  59. McGuirt, W.T., Prasad, S.D., Griffith, A.J., Kunst, H.P.M., Green, G.E., Shpargel, K.B., Runge, C., Huybrechts, C., Mueller, R.F., Lynch, E., et al. (1999). Mutations in COL11A2 cause non-syndromic hearing loss (DFNA13). Nat Genet 23, 413–419.Google Scholar
  60. Medeck, R.J., Sosa, S., Morris, N., and Oxford, J.T. (2003). BMP-1-mediated proteolytic processing of alternatively spliced isoforms of collagen type XI. Biochem J 376, 361–368.Google Scholar
  61. Melkoniemi, M., Brunner, H.G., Manouvrier, S., Hennekam, R., Superti-Furga, A., Kääriäinen, H., Pauli, R.M., van Essen, T., Warman, M.L., Bonaventure, J., et al. (2000). Autosomal recessive disorder otospondylomegaepiphyseal dysplasia is associated with loss-of-function mutations in the COL11A2 gene. Am J Hum Genet 66, 368–377.Google Scholar
  62. Michalickova, K., Susic, M., Willing, M.C., Wenstrup, R.J., and Cole, W.G. (1998). Mutations of the alpha2(V) chain of type V collagen impair matrix assembly and produce ehlers-danlos syndrome type I. Hum Mol Genet 7, 249–255.Google Scholar
  63. Morris, N.P., Oxford, J.T., Davies, G.B.M., Smoody, B.F., and Keene, D.R. (2000). Developmentally regulated alternative splicing of the α1(XI) collagen chain: spatial and temporal segregation of isoforms in the cartilage of fetal rat long bones. J Histochem Cytochem 48, 725–741.Google Scholar
  64. Nagato, H., Matsuo, N., Sumiyoshi, H., Sakata-Takatani, K., Nasu, M., and Yoshioka, H. (2004). The transcription factor CCAAT-binding factor CBF/NF-Y and two repressors regulate the core promoter of the human pro-α3(V) collagen gene (COL5A3). J Biol Chem 279, 46373–46383.Google Scholar
  65. Onnerfjord, P., Heathfield, T.F., and Heinegård, D. (2004). Identification of tyrosine sulfation in extracellular leucine-rich repeat proteins using mass spectrometry. J Biol Chem 279, 26–33.Google Scholar
  66. Oxford, J.T., Doege, K.J., and Morris, N.P. (1995). Alternative exon splicing within the amino-terminal nontriple-helical domain of the rat pro-α 1(XI) collagen chain generates multiple forms of the mRNA transcript which exhibit tissue-dependent variation. J Biol Chem 270, 9478–9485.Google Scholar
  67. Pankov, R., and Yamada, K.M. (2002). Fibronectin at a glance. J Cell Sci 115, 3861–3863.Google Scholar
  68. Park, S.-Y., Lee, J.H., Ha, M., Nam, J.-W., and Kim, V.N. (2009). miR-29 miRNAs activate p53 by targeting p85α and CDC42. Nat Struct Mol Biol 16, 23–29.Google Scholar
  69. Paul, J.I., and Hynes, R.O. (1984). Multiple fibronectin subunits and their post-translational modifications. J Biol Chem 259, 13477–13487.Google Scholar
  70. Pelisch, F., Blaustein, M., Kornblihtt, A.R., and Srebrow, A. (2005). Cross-talk between signaling pathways regulates alternative splicing: a novel role for JNK. J Biol Chem 280, 25461–25469.Google Scholar
  71. Penkov, D., Tanaka, S., Di Rocco, G., Berthelsen, J., Blasi, F., and Ramirez, F. (2000). Cooperative interactions between PBX, PREP, and HOX proteins modulate the activity of the alpha 2(V) collagen (COL5A2) promoter. J Biol Chem 275, 16681–16689.Google Scholar
  72. Pihlajamaa, T., Prockop, D.J., Faber, J., Winterpacht, A., Zabel, B., Giedion, A., Wiesbauer, P., Spranger, J., and Ala-Kokko, L. (1998). Heterozygous glycine substitution in the COL11A2 gene in the original patient with the Weissenbacher-Zweymüller syndrome demonstrates its identity with heterozygous OSMED (nonocular Stickler syndrome). Am J Med Genet 80, 115–120.Google Scholar
  73. Pucci-Minafra, I., Carella, C., Cirincione, R., Chimenti, S., Minafra, S., and Luparello, C. (2000). Type V collagen induces apoptosis of 8701-BC breast cancer cells and enhances m-calpain expression. Breast Cancer Res 2, E008.Google Scholar
  74. Ricard-Blum, S., and Ruggiero, F. (2005). The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol Biol (Paris) 53, 430–442.Google Scholar
  75. Richards, A.J., Martin, S., Nicholls, A.C., Harrison, J.B., Pope, F.M., and Burrows, N.P. (1998). A single base mutation in COL5A2 causes Ehlers-Danlos syndrome type II. J Med Genet 35, 846–848.Google Scholar
  76. Romero, P., Obradovic, Z., Li, X., Garner, E.C., Brown, C.J., and Dunker, A.K. (2001). Sequence complexity of disordered protein. Proteins 42, 38–48.Google Scholar
  77. Romero, P.R., Zaidi, S., Fang, Y.Y., Uversky, V.N., Radivojac, P., Oldfield, C.J., Cortese, M.S., Sickmeier, M., LeGall, T., Obradovic, Z., et al. (2006). Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci U S A 103, 8390–8395.Google Scholar
  78. Roulet, M., Ruggiero, F., Karsenty, G., and LeGuellec, D. (2007). A comprehensive study of the spatial and temporal expression of the col5a1 gene in mouse embryos: a clue for understanding collagen V function in developing connective tissues. Cell Tissue Res 327, 323–332.Google Scholar
  79. Sakata-Takatani, K., Matsuo, N., Sumiyoshi, H., Tsuda, T., and Yoshioka, H. (2004). Identification of a functional CBF-binding CCAAT-like motif in the core promoter of the mouse pro-α 1(V) collagen gene (Col5a1). Matrix Biol 23, 87–99.Google Scholar
  80. Schwarze, U., Atkinson, M., Hoffman, G.G., Greenspan, D.S., and Byers, P.H. (2000). Null alleles of the COL5A1 gene of type V collagen are a cause of the classical forms of Ehlers-Danlos syndrome (types I and II). Am J Hum Genet 66, 1757–1765.Google Scholar
  81. Seibert, C., Cadene, M., Sanfiz, A., Chait, B. T., and Sakmar, T.P. (2002). Tyrosine sulfation of CCR5 N-terminal peptide by tyrosylprotein sulfotransferases 1 and 2 follows a discrete pattern and temporal sequence. Proc Natl Acad Sci USA 99, 11031–11036.Google Scholar
  82. Sengupta, S., den Boon, J.A., Chen, I.H., Newton, M.A., Stanhope, S.A., Cheng, Y.-J., Chen, C.-J., Hildesheim, A., Sugden, B., and Ahlquist, P. (2008). MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci USA 105, 5874–2000, 5878.Google Scholar
  83. Sirko-Osadsa, D.A., Murray, M.A., Scott, J.A., Lavery, M.A., Warman, M.L., and Robin, N.H. (1998). Stickler syndrome without eye involvement is caused by mutations in COL11A2, the gene encoding the α2(XI) chain of type XI collagen. J Pediatr 132, 368–371.Google Scholar
  84. Söderhäll, C., Marenholz, I., Kerscher, T., Rüschendorf, F., Esparza-Gordillo, J., Worm, M., Gruber, C., Mayr, G., Albrecht, M., Rohde, K., et al. (2007). Variants in a novel epidermal collagen gene (COL29A1) are associated with atopic dermatitis. PLoS Biol 5, e242.Google Scholar
  85. Srebrow, A., Blaustein, M., and Kornblihtt, A.R. (2002). Regulation of fibronectin alternative splicing by a basement membrane-like extracellular matrix. FEBS Lett 514, 285–289.Google Scholar
  86. Stamm, S., Ben-Ari, S., Rafalska, I., Tang, Y., Zhang, Z., Toiber, D., Thanaraj, T.A., and Soreq, H. (2005). Function of alternative splicing. Gene 344, 1–20.Google Scholar
  87. Sugimoto, M., Kimura, T., Tsumaki, N., Matsui, Y., Nakata, K., Kawahata, H., Yasui, N., Kitamura, Y., Nomura, S., and Ochi, T. (1998). Differential in situ expression of alpha2(XI) collagen mRNA isoforms in the developing mouse. Cell Tissue Res 292, 325–332.Google Scholar
  88. Surmann-Schmitt, C., Dietz, U., Kireva, T., Adam, N., Park, J., Tagariello, A., Önnerfjord, P., Heinegård, D., Schlötzer-Schrehardt, U., Deutzmann, R., et al. (2008). Ucma, a novel secreted cartilage-specific protein with implications in osteogenesis. J Biol Chem 283, 7082–7093.Google Scholar
  89. Tanaka, K., Tsumaki, N., Kozak, C.A., Matsumoto, Y., Nakatani, F., Iwamoto, Y., and Yamada, Y. (2002). A Krüppel-associated box-zinc finger protein, NT2, represses cell-type-specific promoter activity of the α 2(XI) collagen gene. Mol Cell Biol 22, 4256–4267.Google Scholar
  90. Tanaka, S., Antoniv, T.T., Liu, K., Wang, L., Wells, D.J., Ramirez, F., and Bou-Gharios, G. (2004). Cooperativity between far upstream enhancer and proximal promoter elements of the human α2(I) collagen (COL1A2) gene instructs tissue specificity in transgenic mice. J Biol Chem 279, 56024–56031.Google Scholar
  91. Tompson, S.W., Bacino, C.A., Safina, N.P., Bober, M.B., Proud, V.K., Funari, T., Wangler, M.F., Nevarez, L., Ala-Kokko, L., Wilcox, W.R., et al. (2010). Fibrochondrogenesis results from mutations in the COL11A1 type XI collagen gene. Am J Hum Genet 87, 708–712.Google Scholar
  92. Tsumaki, N., and Kimura, T. (1995). Differential expression of an acidic domain in the amino-terminal propeptide of mouse pro-alpha 2(XI) collagen by complex alternative splicing. J Biol Chem 270, 2372–2378.Google Scholar
  93. Tsumaki, N., Kimura, T., Matsui, Y., Nakata, K., and Ochi, T. (1996). Separable cis-regulatory elements that contribute to tissue- and site-specific alpha 2(XI) collagen gene expression in the embryonic mouse cartilage. J Cell Biol 134, 1573–1582.Google Scholar
  94. Tsumaki, N., Kimura, T., Tanaka, K., Kimura, J.H., Ochi, T., and Yamada, Y. (1998). Modular arrangement of cartilage- and neural tissue-specific cis-elements in the mouse alpha2(XI) collagen promoter. J Biol Chem 273, 22861–22864.Google Scholar
  95. Valcourt, U., Gouttenoire, J., Aubert-Foucher, E., Herbage, D., and Mallein-Gerin, F. (2003). Alternative splicing of type II procollagen pre-mRNA in chondrocytes is oppositely regulated by BMP-2 and TGF-beta1. FEBS Lett 545, 115–119.Google Scholar
  96. Wahl, M.C., Will, C.L., and Lührmann, R. (2009). The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701–718.Google Scholar
  97. Warner, L.R., Brown, R.J., Yingst, S.M.C., and Oxford, J.T. (2006). Isoform-specific heparan sulfate binding within the amino-terminal noncollagenous domain of collagen alpha1(XI). J Biol Chem 281, 39507–39516.Google Scholar
  98. Wenstrup, R.J., Florer, J.B., Cole, W.G., Willing, M.C., and Birk, D.E. (2004). Reduced type I collagen utilization: a pathogenic mechanism in COL5A1 haplo-insufficient Ehlers-Danlos syndrome. J Cell Biochem 92, 113–124.Google Scholar
  99. Wenstrup, R.J., Florer, J.B., Willing, M.C., Giunta, C., Steinmann, B., Young, F., Susic, M. and Cole, W.G. (2000). COL5A1 haploinsufficiency is a common molecular mechanism underlying the classical form of EDS. Am J Hum Genet 66, 1766–1776.Google Scholar
  100. Xu, L., Peng, H., Wu, D., Hu, K., Goldring, M.B., Olsen, B.R., and Li, Y. (2005). Activation of the discoidin domain receptor 2 induces expression of matrix metalloproteinase 13 associated with osteoarthritis in mice. J Biol Chem 280, 548–555.Google Scholar
  101. Yamaguchi, K., Matsuo, N., Sumiyoshi, H., Fujimoto, N., Iyama, K.-I., Yanagisawa, S., and Yoshioka, H. (2005). Pro-α3(V) collagen chain is expressed in bone and its basic N-terminal peptide adheres to osteosarcoma cells. Matrix Biol 24, 283–294.Google Scholar
  102. Yoshioka, H., Greenwel, P., Inoguchi, K., Truter, S., Inagaki, Y., Ninomiya, Y., and Ramirez, F. (1995a). Structural and functional analysis of the promoter of the human alpha 1(XI) collagen gene. J Biol Chem 270, 418–424.Google Scholar
  103. Yoshioka, H., Iyama, K.-I., Inoguchi, K., Khaleduzzaman, M., Ninomiya, Y., and Ramirez, F. (1995b). Developmental pattern of expression of the mouse alpha 1 (XI) collagen gene (Col11a1). Dev Dyn 204, 41–47.Google Scholar
  104. Zhang, X., Boot-Handford, R.P., Huxley-Jones, J., Forse, L.N., Mould, A.P., Robertson, D.L., Li, L., Athiyal, M., and Sarras, M.P. Jr. (2007). The Collagens of Hydra Provide Insight into the Evolution of Metazoan Extracellular Matrices. J Biol Chem 282, 6792–6802.Google Scholar
  105. Zhu, Y., Oganesian, A., Keene, D.R., and Sandell, L.J. (1999). Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta1 and BMP-2. J Cell Biol 144, 1069–1080.Google Scholar
  106. Zoppi, N., Gardella, R., De Paepe, A., Barlati, S., and Colombi, M. (2004). Human fibroblasts with mutations in COL5A1 and COL3A1 genes do not organize collagens and fibronectin in the extracellular matrix, down-regulate α2β1 integrin, and recruit alphavbeta3 Instead of α5β1 integrin. J Biol Chem 279, 18157–18168.Google Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Ming Fang
    • 1
    • 3
  • Reed Jacob
    • 2
    • 3
  • Owen McDougal
    • 2
    • 3
  • Julia Thom Oxford
    • 1
    • 3
    Email author
  1. 1.Department of Biological SciencesBoise State UniversityBoiseUSA
  2. 2.Department of Chemistry and BiochemistryBoise State UniversityBoiseUSA
  3. 3.Biomolecular Research CenterBoise State UniversityBoiseUSA

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