Fibulins: Multiple roles in matrix structures and tissue functions

Cellular and Molecular Life Sciences

Volumn 66, Issue 11-12, 2009, Pages 1890-1902

  De Vega, S ^a   Iwamoto, T ^a,b   Yamada, Y ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Elastogenesis; Embryonic development; Extracellular matrix network; Fibulins; Genetic disorders; Protein interactions

Indexed keywords

CALCIUM BINDING PROTEIN; FIBULIN;

AMINO ACID SEQUENCE; ANIMAL; BASEMENT MEMBRANE; CELL ADHESION; CELL MOTION; CHEMISTRY; EXTRACELLULAR MATRIX; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; BASEMENT MEMBRANE; CALCIUM-BINDING PROTEINS; CELL ADHESION; CELL MOVEMENT; EXTRACELLULAR MATRIX; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 69949132246     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-8632-6     Document Type: Review

References (105)

1. Argraves, W. S., Dickerson, K., Burgess, W. H. and Ruoslahti, E. (1989) Fibulin, a novel protein that interacts with the fibronectin receptor beta subunit cytoplasmic domain. Cell 58, 623-629
2. Godyna, S., Mann, D. M. and Argraves, W. S. (1995) A quantitative analysis of the incorporation of fibulin-1 into extracellular matrix indicates that fibronectin assembly is required. Matrix Biol. 14, 467-477
3. Kluge, M., Mann, K., Dziadek, M. and Timpl, R. (1990) Characterization of a novel calcium-binding 90-kDa glycoprotein (BM-90) shared by basement membranes and serum. Eur. J. Biochem. 193, 651-659
4. Pan, T. C., Kluge, M., Zhang, R. Z., Mayer, U., Timpl, R. and Chu, M. L. (1993) Sequence of extracellular mouse protein BM-90/fibulin and its calcium-dependent binding to other basement-membrane ligands. Eur. J. Biochem. 215, 733-740
5. Lecka-Czernik, B., Lumpkin, C. K. Jr. and Goldstein, S. (1995) An overexpressed gene transcript in senescent and quiescent human fibroblasts encoding a novel protein in the epidermal growth factor-like repeat family stimulates DNA synthesis. Mol. Cell. Biol. 15, 120-128
6. Giltay, R., Timpl, R. and Kostka, G. (1999) Sequence, recombinant expression and tissue localization of two novel extracellular matrix proteins, fibulin-3 and fibulin-4. Matrix Biol. 18, 469-480
7. Kowal, R. C., Richardson, J. A., Miano, J. M. and Olson, E. N. (1999) EVEC, a novel epidermal growth factor-like repeat-containing protein upregulated in embryonic and diseased adult vasculature. Circ. Res. 84, 1166-1176
8. Nakamura, T., Ruiz-Lozano, P., Lindner, V., Yabe, D., Taniwaki, M., Furukawa, Y., Kobuke, K., Tashiro, K., Lu, Z., Andon, N. L., Schaub, R., Matsumori, A., Sasayama, S., Chien, K. R. and Honjo, T. (1999) DANCE, a novel secreted RGD protein expressed in developing, atherosclerotic, and balloon-injured arteries. J. Biol. Chem. 274, 22476-22483
9. Vogel, B. E. and Hedgecock, E. M. (2001) Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 128, 883-894
10. de Vega, S., Iwamoto, T., Nakamura, T., Hozumi, K., McKnight, D. A., Fisher, L. W., Fukumoto, S. and Yamada, Y. (2007) TM14 is a new member of the fibulin family (fibulin-7) that interacts with extracellular matrix molecules and is active for cell binding. J. Biol. Chem. 282, 30878-30888
11. Barth, J. L., Argraves, K. M., Roark, E. F., Little, C. D. and Argraves, W. S. (1998) Identification of chicken and C. elegans fibulin-1 homologs and characterization of the C. elegans fibulin-1 gene. Matrix Biol. 17, 635-646
12. Chu, M. L. and Tsuda, T. (2004) Fibulins in development and heritable disease. Birth Defects Res. C Embryo Today 72, 25-36
13. Chu, M. L. and Tsuda, T. (2004) Fibulins in development and heritable disease. Birth Defects Res. C Embryo Today 72, 25-36
14. Argraves, W. S., Greene, L. M., Cooley, M. A. and Gallagher, W. M. (2003) Fibulins: Physiological and disease perspectives. EMBO Rep. 4, 1127-1131
15. Timpl, R., Sasaki, T., Kostka, G. and Chu, M. L. (2003) Fibulins: A versatile family of extracellular matrix proteins. Nat. Rev. Mol. Cell Biol. 4, 479-489
16. Argraves, W. S., Tran, H., Burgess, W. H. and Dickerson, K. (1990) Fibulin is an extracellular matrix and plasma glycoprotein with repeated domain structure. J. Cell Biol. 111, 3155-3164
17. Grassel, S., Sicot, F. X., Gotta, S. and Chu, M. L. (1999) Mouse fibulin-2 gene. Complete exon-intron organization and promoter characterization. Eur. J. Biochem. 263, 471-477
18. Gallagher, W. M., Greene, L. M., Ryan, M. P., Sierra, V., Berger, A., Laurent-Puig, P. and Conseiller, E. (2001) Human fibulin-4: Analysis of its biosynthetic processing and mRNA expression in normal and tumour tissues. FEBS Lett. 489, 59-66
19. Kobayashi, N., Kostka, G., Garbe, J. H., Keene, D. R., Bachinger, H. P., Hanisch, F. G., Markova, D., Tsuda, T., Timpl, R., Chu, M. L. and Sasaki, T. (2007) A comparative analysis of the fibulin protein family. Biochemical characterization, binding interactions, and tissue localization. J. Biol. Chem. 282, 11805-11816
20. Zhang, H. Y., Timpl, R., Sasaki, T., Chu, M. L. and Ekblom, P. (1996) Fibulin-1 and fibulin-2 expression during organogenesis in the developing mouse embryo. Dev. Dyn. 205, 348-364
21. Roark, E. F., Keene, D. R., Haudenschild, C. C., Godyna, S., Little, C. D. and Argraves, W. S. (1995) The association of human fibulin-1 with elastic fibers: An immunohistological, ultrastructural, and RNA study. J. Histochem. Cytochem. 43, 401-411
22. Reinhardt, D. P., Sasaki, T., Dzamba, B. J., Keene, D. R., Chu, M. L., Gohring, W., Timpl, R. and Sakai, L. Y. (1996) Fibrillin-1 and fibulin-2 interact and are colocalized in some tissues. J. Biol. Chem. 271, 19489-19496
23. Mao, Y. and Schwarzbauer, J. E. (2005) Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24, 389-399
24. Larsen, M., Artym, V. V., Green, J. A. and Yamada, K. M. (2006) The matrix reorganized: Extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18, 463-471
25. Sasaki, T., Wiedemann, H., Matzner, M., Chu, M. L. and Timpl, R. (1996) Expression of fibulin-2 by fibroblasts and deposition with fibronectin into a fibrillar matrix. J. Cell Sci. 109, 2895-2904
26. Balbona, K., Tran, H., Godyna, S., Ingham, K. C., Strickland, D. K. and Argraves, W. S. (1992) Fibulin binds to itself and to the carboxyl-terminal heparin-binding region of fibronectin. J. Biol. Chem. 267, 20120-20125
27. Tran, H., VanDusen, W. J. and Argraves, W. S. (1997) The self-association and fibronectin-binding sites of fibulin-1 map to calcium-binding epidermal growth factor-like domains. J. Biol. Chem. 272, 22600-22606
28. Pfaff, M., Sasaki, T., Tangemann, K., Chu, M. L. and Timpl, R. (1995) Integrin-binding and cell-adhesion studies of fibulins reveal a particular affinity for alpha IIb beta 3. Exp. Cell Res. 219, 87-92
29. Miner, J. H. and Yurchenco, P. D. (2004) Laminin functions in tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 20, 255-284
30. Timpl, R., Tisi, D., Talts, J. F., Andac, Z., Sasaki, T. and Hohenester, E. (2000) Structure and function of laminin LG modules. Matrix Biol. 19, 309-317
31. 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
32. Sasaki, T., Gohring, W., Mann, K., Brakebusch, C., Yamada, Y., Fassler, R. and Timpl, R. (2001) Short arm region of laminin-5 gamma2 chain: Structure, mechanism of processing and binding to heparin and proteins. J. Mol. Biol. 314, 751-763
33. Talts, J. F., Andac, Z., Gohring, W., Brancaccio, A. and Timpl, R. (1999) Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. EMBO J. 18, 863-870
34. Sasaki, T., Kostka, G., Gohring, W., Wiedemann, H., Mann, K., Chu, M. L. and Timpl, R. (1995) Structural characterization of two variants of fibulin-1 that differ in nidogen affinity. J. Mol. Biol. 245, 241-250
35. Sasaki, T., Gohring, W., Pan, T. C., Chu, M. L. and Timpl, R. (1995) Binding of mouse and human fibulin-2 to extracellular matrix ligands. J. Mol. Biol. 254, 892-899
36. Adam, S., Gohring, W., Wiedemann, H., Chu, M. L., Timpl, R. and Kostka, G. (1997) Binding of fibulin-1 to nidogen depends on its C-terminal globular domain and a specific array of calcium-binding epidermal growth factor-like (EG) modules. J. Mol. Biol. 272, 226-236
37. Hopf, M., Gohring, W., Kohfeldt, E., Yamada, Y. and Timpl, R. (1999) Recombinant domain IV of perlecan binds to nidogens, laminin-nidogen complex, fibronectin, fibulin-2 and heparin. Eur. J. Biochem. 259, 917-925
38. Aspberg, A., Adam, S., Kostka, G., Timpl, R. and Heinegard, D. (1999) Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican. J. Biol. Chem. 274, 20444-20449
39. Olin, A. I., Morgelin, M., Sasaki, T., Timpl, R., Heinegard, D. and Aspberg, A. (2001) The proteoglycans aggrecan and Versican form networks with fibulin-2 through their lectin domain binding. J. Biol. Chem. 276, 1253-1261
40. Lee, N. V., Rodriguez-Manzaneque, J. C., Thai, S. N., Twal, W. O., Luque, A., Lyons, K. M., Argraves, W. S. and Iruela-Arispe, M. L. (2005) Fibulin-1 acts as a cofactor for the matrix metalloprotease ADAMTS-1. J. Biol. Chem. 280, 34796-34804
41. Ng, K. M., Catalano, M. G., Pinos, T., Selva, D. M., Avvakumov, G. V., Munell, F. and Hammond, G. L. (2006) Evidence that fibulin family members contribute to the steroid-dependent extravascular sequestration of sex hormone- binding globulin. J. Biol. Chem. 281, 15853-15861
42. Tran, H., Tanaka, A., Litvinovich, S. V., Medved, L. V., Haudenschild, C. C. and Argraves, W. S. (1995) The interaction of fibulin-1 with fibrinogen. A potential role in hemostasis and thrombosis. J. Biol. Chem. 270, 19458-19464
43. Godyna, S., Diaz-Ricart, M. and Argraves, W. S. (1996) Fibulin-1 mediates platelet adhesion via a bridge of fibrinogen. Blood 88, 2569-2577
44. Perbal, B., Martinerie, C., Sainson, R., Werner, M., He, B. and Roizman, B. (1999) The C-terminal domain of the regulatory protein NOVH is sufficient to promote interaction with fibulin 1C: A clue for a role of NOVH in cell-adhesion signaling. Proc. Natl. Acad. Sci. USA 96, 869-874
45. Brooke, J. S., Cha, J. H. and Eidels, L. (2002) Latent transforming growth factor beta-binding protein-3 and fibulin-1C interact with the extracellular domain of the heparinbinding EGF-like growth factor precursor. BMC Cell Biol. 3, 2
46. Ohsawa, I., Takamura, C. and Kohsaka, S. (2001) Fibulin-1 binds the amino-terminal head of beta-amyloid precursor protein and modulates its physiological function. J. Neurochem. 76, 1411-1420
47. Zhang, H., Gao, X., Weng, C. and Xu, Z. (2008) Interaction between angiogenin and fibulin 1: Evidence and implication. Acta Biochim. Biophys. Sin. (Shanghai) 40, 375-380
48. Fujimoto, N., Terlizzi, J., Brittingham, R., Fertala, A., McGrath, J. A. and Uitto, J. (2005) Extracellular matrix protein 1 interacts with the domain III of fibulin-1C and 1D variants through its central tandem repeat 2. Biochem. Biophys. Res. Commun. 333, 1327-1333
49. Zheng, Q., Davis, E. C., Richardson, J. A., Starcher, B. C., Li, T., Gerard, R. D. and Yanagisawa, H. (2007) Molecular analysis of fibulin-5 function during de novo synthesis of elastic fibers. Mol. Cell. Biol. 27, 1083-1095
50. Wachi, H., Nonaka, R., Sato, F., Shibata-Sato, K., Ishida, M., Iketani, S., Maeda, I., Okamoto, K., Urban, Z., Onoue, S. and Seyama, Y. (2008) Characterization of the molecular interaction between tropoelastin and DANCE/fibulin-5. J. Biochem. 143, 633-639
51. Liu, X., Zhao, Y., Gao, J., Pawlyk, B., Starcher, B., Spencer, J. A., Yanagisawa, H., Zuo, J. and Li, T. (2004) Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat. Genet. 36, 178-182
52. Hirai, M., Ohbayashi, T., Horiguchi, M., Okawa, K., Hagiwara, A., Chien, K. R., Kita, T. and Nakamura, T. (2007) Fibulin-5/DANCEhas an elastogenic organizer activity that is abrogated by proteolytic cleavage in vivo. J. Cell Biol. 176, 1061-1071
53. Hirai, M., Horiguchi, M., Ohbayashi, T., Kita, T., Chien, K. R. and Nakamura, T. (2007) Latent TGF-beta-binding protein 2 binds to DANCE/fibulin-5 and regulates elastic fiber assembly. EMBO J. 26, 3283-3295
54. Koski, C., Saharinen, J. and Keski-Oja, J. (1999) Independent promoters regulate the expression of two amino terminally distinct forms of latent transforming growth factor-beta binding protein-1 (LTBP-1) in a cell type-specific manner. J. Biol. Chem. 274, 32619-32630
55. Gibson, M. A., Hatzinikolas, G., Davis, E. C., Baker, E., Sutherland, G. R. and Mecham, R. P. (1995) Bovine latent transforming growth factor beta 1-binding protein 2: Molecular cloning, identification of tissue isoforms, and immunolocalization to elastin-associated microfibrils. Mol. Cell. Biol. 15, 6932-6942
56. Miosge, N., Gotz, W., Sasaki, T., Chu, M. L., Timpl, R. and Herken, R. (1996) The extracellular matrix proteins fibulin-1 and fibulin-2 in the early human embryo. Histochem. J. 28, 109-116
57. Zhang, H. Y., Chu, M. L., Pan, T. C., Sasaki, T., Timpl, R. and Ekblom, P. (1995) Extracellular matrix protein fibulin-2 is expressed in the embryonic endocardial cushion tissue and is a prominent component of valves in adult heart. Dev. Biol. 167, 18-26
58. 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. Dev. Dyn. 222, 89-100
59. Ehlermann, J., Weber, S., Pfisterer, P. and Schorle, H. (2003) Cloning, expression and characterization of the murine Efemp1, a gene mutated in Doyne-Honeycomb retinal dystrophy. Gene Expr. Patterns 3, 441-447
60. McLaughlin, P. J., Bakall, B., Choi, J., Liu, Z., Sasaki, T., Davis, E. C., Marmorstein, A. D. and Marmorstein, L. Y. (2007) Lack of fibulin-3 causes early aging and herniation, but not macular degeneration in mice. Hum. Mol. Genet.16, 3059-3070
61. Xiang, Y., Sekine, T., Nakamura, H., Imajoh-Ohmi, S., Fukuda, H., Yudoh, K., Masuko-Hongo, K., Nishioka, K. and Kato, T. (2006) Fibulin-4 is a target of autoimmunity predominantly in patients with osteoarthritis. J. Immunol. 176, 3196-3204
62. Schultz, D. W., Klein, M. L., Humpert, A. J., Luzier, C. W., Persun, V., Schain, M., Mahan, A., Runckel, C., Cassera, M., Vittal, V., Doyle, T. M., Martin, T. M., Weleber, R. G., Francis, P. J. and Acott, T. S. (2003) Analysis of the ARMD1 locus: Evidence that a mutation in HEMICENTIN-1 is associated with age-related macular degeneration in a large family. Hum. Mol. Genet. 12, 3315-3323
63. Schultz, D. W., Weleber, R. G., Lawrence, G., Barral, S., Majewski, J., Acott, T. S. and Klein, M. L. (2005) HEMICENTIN-1 (FIBULIN-6) and the 1q31 AMD locus in the context of complex disease: Review and perspective. Ophthalmic Genet. 26, 101-105
64. Gallagher, W. M., Currid, C. A. and Whelan, L. C. (2005) Fibulins and cancer: Friend or foe? Trends Mol. Med. 11, 336-340
65. Roger, P., Pujol, P., Lucas, A., Baldet, P. and Rochefort, H. (1998) Increased immunostaining of fibulin-1, an estrogen-regulated protein in the stroma of human ovarian epithelial tumors. Am. J. Pathol. 153, 1579-1588
66. Forti, S., Scanlan, M. J., Invernizzi, A., Castiglioni, F., Pupa, S., Agresti, R., Fontanelli, R., Morelli, D., Old, L. J., Pupa, S. M. and Menard, S. (2002) Identification of breast cancer-restricted antigens by antibody screening of SKBR3 cDNA library using a preselected patient's serum. Breast Cancer Res. Treat. 73, 245-256
67. Greene, L. M., Twal, W. O., Duffy, M. J., McDermott, E. W., Hill, A. D., O'Higgins, N. J., McCann, A. H., Dervan, P. A., Argraves, W. S. and Gallagher, W. M. (2003) Elevated expression and altered processing of fibulin-1 protein in human breast cancer. Br. J. Cancer 88, 871-878
68. Pupa, S. M., Argraves, W. S., Forti, S., Casalini, P., Berno, V., Agresti, R., Aiello, P., Invernizzi, A., Baldassari, P., Twal, W. O., Mortarini, R., Anichini, A. and Menard, S. (2004) Immunological and pathobiological roles of fibulin-1 in breast cancer. Oncogene 23, 2153-2160
69. Qing, J., Maher, V. M., Tran, H., Argraves, W. S., Dunstan, R. W. and McCormick, J. J. (1997) Suppression of anchorage-independent growth and matrigel invasion and delayed tumor formation by elevated expression of fibulin-1D in human fibrosarcoma-derived cell lines. Oncogene 15, 2159-2168
70. Moll, F., Katsaros, D., Lazennec, G., Hellio, N., Roger, P., Giacalone, P. L., Chalbos, D., Maudelonde, T., Rochefort, H. and Pujol, P. (2002) Estrogen induction and overexpression of fibulin-1C mRNA in ovarian cancer cells. Oncogene 21, 1097-1107
71. Schiemann, W. P., Blobe, G. C., Kalume, D. E., Pandey, A. and Lodish, H. F. (2002) Context-specific effects of fibulin-5 (DANCE/EVEC) on cell proliferation, motility, and invasion. Fibulin-5 is induced by transforming growth factor-beta and affects protein kinase cascades. J. Biol. Chem. 277, 27367-27377
72. Debeer, P., Schoenmakers, E. F., Twal, W. O., Argraves, W. S., De Smet, L., Fryns, J. P. and Van De Ven, W. J. (2002) The fibulin-1 gene (FBLN1) is disrupted in a t(12;22) associated with a complex type of synpolydactyly. J. Med. Genet. 39, 98-104
73. Miner, J. H., Cunningham, J. and Sanes, J. R. (1998) Roles for laminin in embryogenesis: Exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J. Cell Biol. 143, 1713-1723
74. Putnam, E. A., Zhang, H., Ramirez, F. and Milewicz, D. M. (1995) Fibrillin-2 (FBN2) mutations result in the Marfan-like disorder, congenital contractural arachnodactyly. Nat. Genet. 11, 456-458
75. Toren, A., Rozenfeld-Granot, G., Heath, K. E., Amariglio, N., Rocca, B., Crosson, J., Epstein, C. J., Laghi, F., Landolfi, R., Carlsson, L. E., Argraves, S., Bizzaro, N., Moxey-Mims, M., Brok-Simoni, F., Martignetti, J. A., Greinacher, A. and Rechavi, G. (2003) MYH9 spectrum of autosomal-dominant giant platelet syndromes: Unexpected association with fibulin-1 variant-D inactivation. Am. J. Hematol. 74, 254-262
76. Michaelides, M., Jenkins, S. A., Brantley, M. A. Jr., Andrews, R. M., Waseem, N., Luong, V., Gregory-Evans, K., Bhattacharya, S. S., Fitzke, F. W. and Webster, A. R. (2006) Maculopathy due to the R345W substitution in fibulin-3: Distinct clinical features, disease variability, and extent of retinal dysfunction. Invest. Ophthalmol. Vis. Sci. 47, 3085-3097
77. Hucthagowder, V., Sausgruber, N., Kim, K. H., Angle, B., Marmorstein, L. Y. and Urban, Z. (2006) Fibulin-4: A novel gene for an autosomal recessive cutis laxa syndrome. Am. J. Hum. Genet. 78, 1075-1080
78. Loeys, B., Van Maldergem, L., Mortier, G., Coucke, P., Gerniers, S., Naeyaert, J. M. and De Paepe, A. (2002) Homozygosity for a missense mutation in fibulin-5 (FBLN5) results in a severe form of cutis laxa. Hum. Mol. Genet. 11, 2113-2118
79. Claus, S., Fischer, J., Megarbane, H., Megarbane, A., Jobard, F., Debret, R., Peyrol, S., Saker, S., Devillers, M., Sommer, P. and Damour, O. (2008) Ap.C217R mutation in fibulin-5 from cutis laxa patients is associated with incomplete extracellular matrix formation in a skin equivalent model. J. Invest. Dermatol. 128, 1442-1450
80. Hu, Q., Loeys, B. L., Coucke, P. J., De Paepe, A., Mecham, R. P., Choi, J., Davis, E. C. and Urban, Z. (2006) Fibulin-5 mutations: Mechanisms of impaired elastic fiber formation in recessive cutis laxa. Hum. Mol. Genet. 15, 3379-3386
81. Lotery, A. J., Baas, D., Ridley, C., Jones, R. P., Klaver, C. C., Stone, E., Nakamura, T., Luff, A., Griffiths, H., Wang, T., Bergen, A. A. and Trump, D. (2006) Reduced secretion of fibulin 5 in age-related macular degeneration and cutis laxa. Hum. Mutat. 27, 568-574
82. Markova, D., Zou, Y., Ringpfeil, F., Sasaki, T., Kostka, G., Timpl, R., Uitto, J. and Chu, M. L. (2003) Genetic heterogeneity of cutis laxa: A heterozygous tandem duplication within the fibulin-5 (FBLN5) gene. Am. J. Hum. Genet. 72, 998-1004
83. Fisher, S. A., Rivera, A., Fritsche, L. G., Keilhauer, C. N., Lichtner, P., Meitinger, T., Rudolph, G. and Weber, B. H. (2007) Case-control genetic association study of fibulin-6 (FBLN6 or HMCN1) variants in age-related macular degeneration (AMD). Hum. Mutat. 28, 406-413
84. 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
85. Cooley, M. A., Kern, C. B., Fresco, V. M., Wessels, A., Thompson, R. P., McQuinn, T. C., Twal, W. O., Mjaatvedt, C. H., Drake, C. J. and Argraves, W. S. (2008) Fibulin-1 is required for morphogenesis of neural crest-derived structures. Dev. Biol. 319, 336-345
86. Muriel, J. M., Dong, C., Hutter, H. and Vogel, B. E. (2005) Fibulin-1C and Fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner. Development 132, 4223-4234
87. Kubota, Y., Kuroki, R. and Nishiwaki, K. (2004) A fibulin-1 homolog interacts with an ADAM protease that controls cell migration in C. elegans. Curr. Biol.14, 2011-2018
88. Hesselson, D., Newman, C., Kim, K. W. and Kimble, J. (2004) GON-1 and fibulin have antagonistic roles in control of organ shape. Curr. Biol. 14, 2005-2010
89. Nishiwaki, K., Hisamoto, N. and Matsumoto, K. (2000) A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans. Science 288, 2205-2208
90. Blelloch, R. and Kimble, J. (1999) Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans. Nature 399, 586-590
91. Muriel, J. M., Xu, X., Kramer, J. M. and Vogel, B. E. (2006) Selective assembly of fibulin-1 splice variants reveals distinct extracellular matrix networks and novel functions for perlecan/UNC-52 splice variants. Dev. Dyn. 235, 2632-2640
92. Hesselson, D. and Kimble, J. (2006) Growth control by EGF repeats of the C. elegans Fibulin-1C isoform. J. Cell Biol. 175, 217-223
93. Sicot, F. X., Tsuda, T., Markova, D., Klement, J. F., Arita, M., Zhang, R. Z., Pan, T. C., Mecham, R. P., Birk, D. E. and Chu, M. L. (2008) Fibulin-2 is dispensable for mouse development and elastic fiber formation. Mol. Cell. Biol. 28, 1061-1067
94. Marmorstein, L. Y., McLaughlin, P. J., Peachey, N. S., Sasaki, T. and Marmorstein, A. D. (2007) Formation and progression of sub-retinal pigment epithelium deposits in Efemp1 mutation knock-in mice: A model for the early pathogenic course of macular degeneration. Hum. Mol. Genet. 16, 2423-2432
95. Fu, L., Garland, D., Yang, Z., Shukla, D., Rajendran, A., Pearson, E., Stone, E. M., Zhang, K. and Pierce, E. A. (2007) The R345W mutation in EFEMP1 is pathogenic and causes AMD-like deposits in mice. Hum. Mol. Genet. 16, 2411-2422
96. Roybal, C. N., Marmorstein, L. Y., Vander Jagt, D. L. and Abcouwer, S. F. (2005) Aberrant accumulation of fibulin-3 in the endoplasmic reticulum leads to activation of the unfolded protein response and VEGF expression. Invest. Ophthalmol. Vis. Sci. 46, 3973-3979
97. Stone, E. M., Braun, T. A., Russell, S. R., Kuehn, M. H., Lotery, A. J., Moore, P. A., Eastman, C. G., Casavant, T. L. and Sheffield, V. C. (2004) Missense variations in the fibulin 5 gene and age-related macular degeneration. N. Engl. J. Med. 351, 346-353
98. McLaughlin, P. J., Chen, Q., Horiguchi, M., Starcher, B. C., Stanton, J. B., Broekelmann, T. J., Marmorstein, A. D., McKay, B., Mecham, R., Nakamura, T. and Marmorstein, L. Y. (2006) Targeted disruption of fibulin-4 abolishes elastogenesis and causes perinatal lethality in mice. Mol. Cell. Biol. 26, 1700-1709
99. Hanada, K., Vermeij, M., Garinis, G. A., de Waard, M. C., Kunen, M. G., Myers, L., Maas, A., Duncker, D. J., Meijers, C., Dietz, H. C., Kanaar, R. and Essers, J. (2007) Perturbations of vascular homeostasis and aortic valve abnormalities in fibulin-4 deficient mice. Circ. Res. 100, 738-746
100. Yanagisawa, H., Davis, E. C., Starcher, B. C., Ouchi, T., Yanagisawa, M., Richardson, J. A. and Olson, E. N. (2002) Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 415, 168-171
101. Nakamura, T., Lozano, P. R., Ikeda, Y., Iwanaga, Y., Hinek, A., Minamisawa, S., Cheng, C. F., Kobuke, K., Dalton, N., Takada, Y., Tashiro, K., Ross Jr, J., Honjo, T. and Chien, K. R. (2002) Fibulin-5/DANCEis essential for elastogenesis in vivo. Nature 415, 171-175
102. Twal, W. O., Czirok, A., Hegedus, B., Knaak, C., Chintalapudi, M. R., Okagawa, H., Sugi, Y. and Argraves, W. S. (2001) Fibulin-1 suppression of fibronectin-regulated cell adhesion and motility. J. Cell Sci. 114, 4587-4598
103. Lomas, A. C., Mellody, K. T., Freeman, L. J., Bax, D. V., Shuttleworth, C. A. and Kielty, C. M. (2007) Fibulin-5 binds human smooth-muscle cells through alpha5beta1 and alpha4-beta1 integrins, but does not support receptor activation. Biochem. J. 405, 417-428
104. Spencer, J. A., Hacker, S. L., Davis, E. C., Mecham, R. P., Knutsen, R. H., Li, D. Y., Gerard, R. D., Richardson, J. A., Olson, E. N. and Yanagisawa, H. (2005) Altered vascular remodeling in fibulin-5-deficient mice reveals a role of fibulin-5 in smooth muscle cell proliferation and migration. Proc. Natl. Acad. Sci. USA 102, 2946-2951
105. Albig, A. R. and Schiemann, W. P. (2004) Fibulin-5 antagonizes vascular endothelial growth factor (VEGF) signaling and angiogenic sprouting by endothelial cells. DNA Cell Biol. 23, 367-379