Fibrillin-rich microfibrils: Elastic biopolymers of the extracellular matrix

Journal of Muscle Research and Cell Motility

Volumn 23, Issue 5-6, 2002, Pages 581-596

  Kielty, C M ^a   Wess, T J ^b   Haston, L ^b   Ashworth, Jane L ^a   Sherratt, M J ^a   Shuttleworth, C A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPOLYMER; CALCIUM; ELASTIN; FIBRILLIN; FIBRILLIN 1; UNCLASSIFIED DRUG;

AGING; AUTOMATION; BIOMECHANICS; CARDIOVASCULAR MALFORMATION; CRUSTACEA; ELASTIC FIBER; ELASTIC TISSUE; ELASTICITY; EXTRACELLULAR MATRIX; EYE MALFORMATION; HUMAN; MACROMOLECULE; MARFAN SYNDROME; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN ISOLATION; PROTEIN STRUCTURE; REVIEW; SKELETON MALFORMATION; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; TISSUE REPAIR; TOMOGRAPHY; ULTRASTRUCTURE; VERTEBRATE;

ANIMALS; BIOPOLYMERS; ELASTICITY; EXTRACELLULAR MATRIX PROTEINS; FORECASTING; HUMANS; MICROFIBRILS; MICROFILAMENT PROTEINS; MICROSCOPY, ATOMIC FORCE; PROTEIN FOLDING;

CRUSTACEA; VERTEBRATA;

EID: 0037907614     PISSN: 01424319     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1023479010889     Document Type: Review

References (101)

1. Abrams WR, Ma RI, Kucich U, Bashir MM, Decker S, Tsipouras P, McPherson JD, Wasmuth JJ and Rosenbloom J (1995) Molecular cloning of the microfibrillar protein MFAP3 and assignment of the gene to human-chromsosme 5q32-q33.2. Genomics 26: 47-54.
2. Ashworth JL, Kielty CM and McLeod DM (2000) Fibrillin and the eye. Brit J Ophthalmol 84: 1312-1317.
3. Ashworth JL, Kelly V, Rock MJ, Shuttleworth CA and Kielty CM (1999c) Regulation of fibrillin carboxy-terminal furin processing by N-glycosylation, and association of amino- and carboxy-terminal sequences. J Cell Sci 112: 4163-4171.
4. Ashworth JL, Kelly V, Wilson R, Shuttleworth CA and Kielty CM (1999b) Fibrillin assembly: dimer formation mediated by amino-terminal sequences. J Cell Sci 112: 3549-3558.
5. Ashworth JL, Sherratt MJ, Rock MJ, Murphy G, Shapiro SD, Shuttleworth CA and Kielty CM (1999a) Fibrillin turnover by metalloproteinases: implications for connective tissue remodelling. Biochem J 340: 171-181.
6. Baccarani-Contri M, Vincenzi D, Cicchetti F, Mori G and Pasquali-Ronchetti I (1990) Immunocytochemical localization of proteoglycans within normal elastic fibres. Eur J Cell Biol 53: 305-312.
7. Baldock C, Koster AJ, Ziese U, Sherratt MJ, Kadler KE, Shuttleworth CA and Kielty CM (2001) The supramolecular organisation of fibrillin-rich microfibrils. J Cell Biol 152: 1045-1056.
8. Bellingham CM, Woodhouse KA, Robson P, Rothstein SJ and Keeley FW (2001) Self-aggregation of recombinantly expressed human elastin polypeptides. Biochim Biophys Acta 1550: 6-19.
9. Borel A, Eichenberger D, Farjanel J, Kessler E, Gleyzal C, Hulmes DJS, Sommer P and Font B (2001) Lysyl oxidase-like protein from bovine aorta. J Biol Chem 276: 48,944-48,949.
10. Bressan GM, Daga G, Colombatti A, Castellani I, Marigo V and Volpin D (1993) Emilin, a component of elastic fibers preferentially located at the elastin-microfibril interface. J Cell Biol 121: 201-213.
11. Brown-Augsberger P, Broekelmann T, Mecham L, Mercer R, Gibson MA, Cleary EG, Abrams WR, Rosenbloom J and Mecham RP (1996) Microfibril-associated glycoprotein binds to the carboxyl-terminal domain of tropoelastin and is a substrate for transglutaminase. J Biol Chem 269: 28,423-28,449.
12. Brown-Augsburger P, Tisdale C, Broekelmann T, Sloan C and Mecham RP (1995) Identification of an elastin cross-linking domain that joins three peptide chains. J Biol Chem 270: 17,778-17,783.
13. Cardy CM and Handford PA (1998) Metal ion dependency of microfibrils supports a rod-like conformation for fibrillin-1 calcium-binding epidermal growth factor-like domains. J Mol Biol 276: 855-860.
14. Colombatti A, Doliana R, Bot S, Canton A, Mongiat M, Mungiguerra G, Paron-Cilli S and Spessotto P (2000) The EMILIN protein family. Matrix Biol 19: 289-301.
15. Csiszar K (2001) Lysyl oxidases: a novel multifunctional amine oxidase family. Prog Nucleic Acid Res Mol Biol 70: 1-32.
16. Dallas SL, Keene DR, Saharinen J, Sakai LY, Mundy GR and Bonewald LF (2000) Role of the latent transforming growth factor beta binding protein family in fibrillin-containing microfibrils in bone cells in vitro and in vivo. J Bone Mineral Res 15: 68-81.
17. Dahlbäck K, Ljungquist A, Lofberg H, Dahlbäck B, Engvall E and Sakai LY (1990) Fibrillin immunoreactive fibers constitute a unique network in the human dermis: immunohistochemical comparison of the distributions of fibrillin, vitronectin, amyloid P component, and orcein stainable structures in normal skin and elastosis. J Invest Dermatol 94: 284-291.
18. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE and Iozzo RV (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743.
19. Doliana R, Bot S, Mungiguerra G, Canton A, Cilli SP and Colombatti A (2001) Isolation and characterization of EMILIN-2, a new component of the growing EMILINs family and a member of the EMI domain-containing superfamily. J Biol Chem 276: 12,003-12,011.
20. Doliana R, Bucciotti F, Giacomello E, Deutzmann R, Volpin D, Bressan GM and Colombatti A (1999) EMILIN, a component of the elastic fiber and a new member of the Clq/Tumor necrosis factor superfamily of proteins. J Biol Chem 274: 16,773-16,781.
21. Downing AK, Knott V, Werner JM, Cardy CM, Campbell ID and Handford PA (1996) Solution structure of a pair of calcium-binding epidermal growth factor-like domains: implications for the Marfan syndrome and other genetic disorders. Cell 85: 597-605.
22. 2+ for the mechanical properties of fibrillin. Proteins: Str Funct Genet 45: 90-95.
23. Faury G (2001) Function-structure relationship of elastic arteries in evolution: from microfibrils to elastin and elastic fibres. Pathol Biol (Paris) 49: 310-325.
24. Gibson MA, Finnis ML, Kumaratilake JL and Cleary EG (1998) Microfibril-associated glycoprotein-2 (MAGP-2) is specifically associated with fibrillin-containing microfibrils and exhibits more restricted patterns of tissue localisation and developmental expression than its structural relative MAGP-1. J Histochem Cytochem 46: 871-885.
25. Gibson MA, Hatzinikolas G, Davis EC, Baker E, Sutherland GR and Mecham RP (1995) Bovine latent transforming growth factor β1-binding protein-2: molecular cloning, identification of tissue isoforms, and immunolocalization to elastin-associated microfibrils. Mol Cell Biol 15: 6932-6942.
26. Gibson MA, Kumaratilake JS and Cleary EG (1989) The protein components of the 12-nanometer microfibrils of elastic and non-elastic tissues. J Biol Chem 264: 4590-4598.
27. Gibson MA, Kumaratilake JS and Cleary EG (1997) Immunohistochemical and ultrastructural localization of MP 78/70 (beta ig-H3) in extracellular matrix of developing and mature bovine tissues. J Histochem Cytochem 45: 1683-1696.
28. Gibson MA, Leavesley DI and Ashman LK (1999) Microfibril-associated glycoprotein-2 specifically interacts with a range of bovine and human cell types via alpha Vbeta3 integrin. J Biol Chem 274: 13,060-13,065.
29. Grässel S, Unsold C, Schacke H, Brucner-Tuderman L and Bruckner P (1999) Collagen XVI is expressed by human dermal fibroblasts and keratinocytes and is associated with the microfibrillar apparatus in the upper papillary dermis. Matrix Biol 18: 309-317.
30. Hanssen E, Franc S and Garrone R (1998) Atomic force microscopy and modelling of natural elastic fibrillin polymers. Biol Cell 90: 223-228.
31. Henderson M, Polewski R, Fanning JC and Gibson MA (1996) Microfibril-associated glycoprotein-1 (MAGP-1) is specifically located on the beads of the beaded-flament structure for fibrillin-containing microfibrils as visualized by the rotary shadowing technique. J Histochem Cytochem 44: 1389-1397.
32. Hindson VJ, Ashworth JL, Rock M, Shuttleworth CA and Kielty CM (1999) Fibrillin catabolism by matrix metalloproteinases: characterisation of amino- and carboxy-terminal cleavage sites. FEBS Lett 452: 195-198.
33. Hirano E, Fujimoto N, Tajima S, Akiyama M, Ishibashi R and Okamoto K (2002) Expression of 36-kDa microfibril-associated glycoprotein (MAGP-36) in human keratinocytes and its localization in skin. J Dermatol Sci 28: 60-67.
34. Horrigan SK, Rich CB, Streeten BW, Li ZY and Foster JA (1992) Characterization of an associated microfibril protein through recombinant DNA techniques. J Biol Chem 267: 10,087-10,095.
35. Isogai Z, Aspberg A, Keene DR, Ono RN, Reinhardt DP and Sakai LY (2002) Versican interacts with fibrillin-1 and links extracellular microfibrils to other connective tissue networks. J Biol Chem 277: 4565-4572.
36. Jensen SA, Reinhardt DP, Gibson MA and Weiss AS (2001) Protein interaction studies of MAGP-1 with tropoelastin and fibrillin-1. J Biol Chem 276: 39,661-39,666.
37. Keene DR, Maddox BK, Kuo H-J, Sakai LY and Glanville RW (1991) Extraction of extensible beaded structure and their identification as extracellular matrix fibrillin-containing microfibrils. J Histochem Cytochem 39: 441-449.
38. Kielty CM and Shuttleworth CA (1993) The role of calcium in the organisation of fibrillin microfibrils. FEBS Lett 336: 323-326.
39. Kielty CM and Shuttleworth CA (1997) Microfibrillar elements of the dermal matrix. Microsc Res Tech 38: 407-427.
40. Kielty CM, Baldock C, Lee D, Rock MJ, Sherratt MJ, Ashworth JL and Shuttleworth CA (2002) Fibrillin: from microfibril assembly to biomechanical function. Philos Trans Roy Soc B 357: 207-217.
41. Kielty CM, Whittaker SP and Shuttleworth CA (1996) Fibrillin: evidence that chondroitin sulphate proteoglycans are components of microfibrils and associate with newly synthesised monomers. FEBS Lett 386: 169-173.
42. Kielty CM, Woolley DE, Whittaker SP and Shuttleworth CA (1994) Catabolism of intact fibrillin microfibrils by neutrophil elastase, chymotrypsin and trypsin. FEBS Lett 351: 85-89.
43. Kitahama S, Gibson MA, Hatzinikolas G, Hay S, Kuliwaba JL, Evdokiou A, Atkins GJ and Findlay DM (2000) Expression of fibrillins and other microfibril-associated proteins in human bone and osteoblast-like cells. Bone 27: 61-67.
44. Kocsis E, Trus BL, Steer CJ, Bisher ME and Steven AC (1991). Image averaging of flexible fibrous macromolecules: the clathrin triskelion has an elastic proximal segment. J Struct Biol 107: 6-14.
45. Kogake S, Hall SM, Kielty CM and Haworth SG (2002) Fibrillin-1 remodelling in the pulmonary arterial wall during development. Am J Physiol-Lung Cell Mol Physiol (under review).
46. Kostka G, Giltay R, Bloch W, Addicks K, Timpl R, Fassler R and Chu M-L (2001) Perinatal lethality and endothelial cell abnormalities in several vessel compartments of fibulin-1-deficient mice. Mol Cell Biol 21: 7025-7034.
47. Lausen M, Lynch N, Schlosser A, Tornoe I, Sackmose SG, Teisner B, Willis AC, Crouch E, Schwaeble W and Holmskov U (1999) Microfibril-associated protein 4 is present in lung washings and binds to the collagen region of lung surfactant protein D. J Biol Chem 274: 32,234-32,240.
48. Liu WG, Faraco J, Qian CP and Francke U (1997) The gene for microfibril-associated protein-1 (MFAP1) is located several megabases centromeric to FBN1 and is not mutated in Marfan syndrome. Human Genet 99: 578-584.
49. McConnell CJ, DeMont ME and Wright GM (1997) Microfibrils provide non-linear behaviour in the abdominal artery of the lobster Homarus americanus. J Physiol 499: 513-526.
50. McConnell CJ, Wright Gm and DeMont ME (1996) The modulus of elasticity of lobster aorta microfibrils. Experientia 52: 918-921.
51. Mecham RP and Davis EC (1994) Elastic fiber structure and assembly. In: Yurchenco PD, Birk DE and Mecham RP (eds) Extracellular Matrix Assembly and Structure. (pp. 281-314) Academic Press, New York.
52. Miyazono K, Hellman U, Wernstedt C and Heldin CH (1988) Latent high molecular-weight complex of transforming growth factor-β1-purification from human-platelets and structural characterization. J Biol Chem 263: 6407-6415.
53. Milewicz DM, Urban Z and Boyd C (2000) Genetic disorders of the elastic fiber system. Matrix Biol 19: 471-480.
54. Miosge N, Sasaki T and Timpl R (1999) Angiogenesis inhibitor endostatin is a distinct component of elastic fibers in vessel walls. FASEB J 13: 1743-1750.
55. Nagase T, Nakayama M, Nakajima D, Kikuno R and Ohara O (2001) Prediction of the coding sequences of unidentified human genes. XX. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res 8: 85-95.
56. Nakamura T, Lozano PR, Ikeda Y, Iwanaga Y, Hinek A, Minamisawa S, Cheng C-F, Kobuke K, Dalton N, Takada Y, Tashiro K, Ross J, Honjo T and Chien KR (2002) Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature 415: 171-175.
57. Oklu R and Hesketh R (2000) The latent transforming growth factor beta binding protein (LTBP) family. Biochem J 352: 601-610.
58. Pereira L, D'Alessio M, Ramirez F, Lynch JR, Sykes B, Pangilinan T and Bonadio J (1993) Genomic organization of the sequence coding for fibrillin, the defective gene product in Marfan syndrome. Hum Mol Genet 2: 961-968.
59. Pfaff M, Reinhardt DP, Sakai LY and Timpl R (1996) Cell adhesion and integrin binding to recombinant human fibrillin-1. FEBS Lett 384: 247-250.
60. Prody PS, Callahan JW and Hinek A (1998) The 67-kDa enzymatically inactive alternatively spliced variant of beta-galactosidase is identical to the elastin/laminin-binding protein. J Biol Chem 273: 6319-6326.
61. Qian R and Glanville RW (1997) Alignment of fibrillin molecules in elastic microfibrils is defined by transglutaminase-derived crosslinks. Biochemistry 36: 15,841-15,847.
62. Raghunath M, Putnam EA, Ritty T, Hamstra D, Park ES, Tschodrich-Rotter M, Peters R, Rehemtulla A and Milewicz DM (1999) Carboxy-terminal conversion of profibrillin to fibrillin at a basic site by PACE/furin-like activity required for incorporation in the matrix. J Cell Sci 112: 1093-1100.
63. Raghunath M, Tschodrich-Rotter M, Sasaki T, Meuli M, Chu M-L and Timpl R (1999) Confocal laser scanning analysis of the association of fibulin-2 with fibrillin-1 and fibronectin define different stages of skin regeneration. J Invest Dermatol 112: 97-101.
64. Raghunath M, Unsold C, Kubitscheck U, Bruckner-Tuderman L, Peters R and Meuli M (1998) The cutaneous microfibrillar apparatus contains latent transforming growth factor-beta binding protein-1 (LTBP-1) and is a repository for latent TGF-beta 1. J Invest Dermatol 111: 559-564.
65. Reber-Muller S, Spissinger T, Schubert P, Spring J and Schmid V (1995) An extracellular matrix protein of jellyfish homologous to mammalian fibrillins forms different fibrils depending on the life stage of the animal. Dev Biol 169: 662-672.
66. Reinboth B, Hanssen E, Cleary EG and Gibson MA (2001) Molecular interactions of biglycan and decorin with elastic fiber components. Biglycan forms a ternary complex with tropoelastin and MAGP-1. J Biol Chem 277: 3950-3957.
67. Reinhardt DP, Keene DR, Corson GM, Pöschl E, Bächinger HP, Gambee JE and Sakai LY (1996a) Fibrillin-1: organization in microfibrils and structural properties. J Mol Biol 258: 104-114.
68. Reinhardt DP, Mechling DE, Boswell BA, Keene DR, Sakai LY and Bächinger HP (1997) Calcium determines the shape of fibrillin. J Biol Chem 272: 7368-7373.
69. Reinhardt DP, Sasaki T, Dzamba BJ, Keene DR, Chu M-L, Göhring W, Timpl R and Sakai LY (1996b) Fibrillin-1 and fibulin-2 interact and are colocalized in some tissues. J Biol Chem 271: 19,489-19,496.
70. Rief M, Gautel M, Oesterhelt F, Fernandez JM and Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112.
71. Ritty TM, Broekelmann T, Tisdale C, Milewicz DM and Mecham RP (1999) Processing of the fibrillin-1 carboxyl-terminal domain. J Biol Chem 274: 8933-8940.
72. Robb BW, Wachi H, Schaub T, Mecham RP and Davis EC (1999) Characterization of an in vitro model of elastic fiber formation. Mol Biol Cell 10: 3595-3605.
73. Robinson PN and Godfrey M (2000) The molecular genetics of Marfan Syndrome and related microfibrillopathies. J Med Genet 37: 9-25.
74. Sadawa H and Konomi H (1991) The alpha 1 chain of type VIII collagen is associated with many but not all microfibrils of elastic fiber system. Cell Struct Funct 16: 455-466.
75. Sakamoto H, Broekelmann T, Cheresh DA, Ramirez F, Rosenbloom J and Mecham RP (1996) Cell-type specific recognition of RGD- and non-RGD-containing cell binding domains in fibrillin-1. J Biol Chem 271: 4916-4922.
76. Schorderet DF, Menasche M, Morand S, Bonnel S, Buchillier V, Marchant D, Auderset K, Bonny C, Abitbol M and Munier FL (2000) Genomic characterisation and embryonic expression of the mouse BigH3 (Tgfbi) gene. Biochim Biophys Acta 274: 267-274.
77. Sechler JL, Rao H, Cumiskey AM, Vega-Colón I, Smith MS, Murata T and Schwarzbauer JE (2001) A novel fibronectin binding site required for fibronectin fibril growth during matrix assembly. J Cell Biol 154: 1081-1088.
78. Segade F, Trask BC, Broekelmann TJ, Pierce RA and Mecham RP (2002) Identification of a matrix binding domain in the microfibril-associated glycoproteins 1 and 2 (MAGP1 and 2) and intracellular localization of alternative splice forms. J Biol Chem (in press).
79. Sherratt MJ, Wess TJ, Baldock C, Ashworth JL, Purslow PP, Shuttleworth CA and Kielty CM (2001) Fibrillin-rich microfibrils of the extracellular matrix: ultrastructure and assembly. Micron 32: 185-200.
80. Sinha S, Nevett C, Shuttleworth CA and Kielty CM (1998) Cellular and extracellular biology of the latent transforming growth factor-beta binding proteins. Matrix Biol 17: 529-545.
81. Sinha S, Shuttleworth CA, Heagerty AM and Kielty CM (2002) Expression of latent TGFbeta binding proteins and association with TGFbeta-1 and fibrillin-1 in the response to arterial injury. Cardiovasc Res 53: 971-983.
82. Taipale J, Saharinen J, Hedman K and Keski-Oja J (1996) Latent transforming growth-factor-β1 and its binding-protein are components of extracellular-matrix microfibrils. J Histochem Cytochem 44: 875-889.
83. Tassabehji M, Metcalfe K, Hurst J, Ashcroft GS, Kielty CM, Wilmot C, Donnai D, Read AP and Jones CJP (1998) An elastin gene mutation producing abnormal tropoelastin and abnormal elastic fibres in a patient with autosomal dominant cutis laxa. Hum Mol Genet 7: 1021-1028.
84. Thurmond FA and Trotter JA (1996) Morphology and biomechanics of the microfibrillar network of sea cucumber dermis. J Exptl Biol 199: 1817-1828.
85. Tiedemann K, Bätge B, Müller PK and Reinhardt DP (2001) Interactions of fibrillin-1 with heparin/heparan sulphate, implications for microfibrillar assembly. J Biol Chem 276: 36,035-36,042.
86. Toonkool P, Jensen SA, Maxwell AL and Weiss AS (2001) Hydrophobic domains of human tropoelastin interact in a context-dependent manner. J Biol Chem 275: 44,575-44,580.
87. Toyashima T, Yamashita K, Shishibori T, Itano T and Kobayashi R (1999) Ultrastructural distribution of 36-kDa microfibril-associated glycoprotein (MAGP-36) in human and bocvine tissues. J Histichem Cytochem 47: 1049-1056.
88. Trask TM, Ritty TM, Broekelmann T, Tisdale C and Mecham RP (1999) N-terminal domains of fibrillin 1 and fibrillin 2 direct the formation of homodimers: a possible first step in microfibril assembly. Biochem J 340: 693-701.
89. Trask BC, Trask TM, Broekelmann T and Mecham RP (2000a) The microfibrillar proteins MAGP-1 and fibrillin-1 form a ternary complex with the chondroitin sulfate proteoglycan decorin. Molec Biol Cell 11: 1499-1507.
90. Trask TM, Trask BC, Ritty TM, Abrams WR, Rosenbloom J and Mecham RP (2000b) Interaction of tropoelastin with the amino-terminal domains of fibrillin-1 and fibrillin-2 suggests a role for the fibrillins in elastic fiber formation. J Biol Chem 275: 24,400-24,406.
91. Tsuda T, Wang H, Timpl R and Chu M-L (2001) Fibulin-2 expression marks transformed mesenchymal cells in developing cardiac valves, aortic arch vessels, and coronary vessels. Devel Dynam 222: 89-100.
92. Utani A, Nomizu M and Yamada Y (1997) Fibulin-2 binds to the short arms of laminin-5 and laminin-1 via conserved amino acid sequences. J Biol Chem 272: 2814-2820.
93. Wess TJ, Purslow P and Kielty CM (1997) Fibrillin-rich microfibrils: an X-ray diffraction study and elastomeric properties. FEBS Lett 413: 424-428.
94. Wess TJ, Purslow PP, Sherratt MJ, Ashworth JL, Shuttleworth CA and Kielty CM (1998a) Calcium determines the supramolecular organization of fibrillin- rich microfibrils. J Cell Biol 141: 829-837.
95. Wess TJ, Purslow PP and Kielty CM (1998b) X-ray diffraction studies of fibrillin-rich microfibrils: effects of tissue extension on axial and lateral packing. J Struct Biol 122: 123-127.
96. Wright DM, Duance VC, Wess TJ, Kielty CM and Purslow PP (1999) The supramolecular organisation of fibrillin-rich microfibrils determines the mechanical properties of bovine zonular filaments. J Exp Biol 202: 3011-3020.
97. Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, Goldstein S, Bonadio J, Boskey A, Heegaard AM, Sommer B, Satomura K, Dominguez P, Zhao C, Kulkarni AB, Robey PG and Young MF (1998) Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat Genet 20: 78-82.
98. Yanagisawa H, Davis EC, Starcher BC, Ouchi T, Yanagisawa M, Richardson JA and Olsen EN (2002) Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 415: 168-171.
99. Zhang H, Apfelroth SD, Hu W, Davis EC, Sanguineti C, Bonadio J, Mecham RP and Ramirez F (1994) Structure and expression of fibrillin-2, a novel microfibrillar component preferentially located in elastic matrices. J Cell Biol 124: 855-863.
100. Zhang H, Hu W and Ramirez F (1995) Developmental expression of fibrillin genes suggests heterogeneity of extracellular microfibrils. J Cell Biol 129: 1165-1176.
101. Zimmermann DR, Dours-Zimmermann M, Schubert M and Bruckner-Tuderman L (1994) Versican is expressed in the proliferating zone in the epidermis and in association with the elastic network of the dermis. J Cell Biol 124: 817-825.