Molecular Evolution of the Microfibril-Associated Proteins: The Fibulins and the MAGPs

Biology of Extracellular Matrix

Volumn Part F2618, Issue , 2013, Pages 163-190

  Segade, Fernando ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Basal Chordate; Dermal Connective Tissue; Elastic Fiber; Functional Partner; Genetic Module

Indexed keywords

EID: 84943663202     PISSN: 08873224     EISSN: 21911959     Source Type: Book Series    
DOI: 10.1007/978-3-642-36002-2_6     Document Type: Chapter

References (116)

1. Adkins RM (2008) Coevolution: molecular. In: Cooper DN, Kehrer-Sawatzki H (eds) Handbook of human molecular evolution. Wiley, Chichester, pp 322–328
2. Albig AR, Roy TG, Becenti DJ, Schiemann WP (2007) Transcriptome analysis of endothelial cell gene expression induced by growth on matrigel matrices: identification and characterization of MAGP-2 and lumican as novel regulators of angiogenesis. Angiogenesis 10:197–216
3. Albig AR, Becenti DJ, Roy TG, Schiemann WP (2008) Microfibril-associate glycoprotein 2 (MAGP-2) promotes angiogenic cell sprouting by blocking notch signaling in endothelial cells. Microvasc Res 76:7–14
4. Alvarez Y, Cederlund ML, Cottell DC, Bill BR, Ekker SC, Torres-Vazquez J, Weinstein BM, Hyde DR, Vihtelic TS, Kennedy BN (2007) Genetic determinants of hyaloid and retinal vasculature in zebrafish. BMC Dev Biol 7:114
5. Argraves WS, Greene LM, Cooley MA, Gallagher WM (2003) Fibulins: physiological and disease perspectives. EMBO Rep 4:1127–1131
6. Barth JL, Argraves KM, Roark EF, Little CD, Argraves WS (1998) Identification of chicken and C. elegans fibulin-1 homologs and characterization of the C. elegans fibulin-1 gene. Matrix Biol 17:635–646
7. Bellahcene A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS (2008) Small integrinbinding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8:212–226
8. Blair JE (2009) Animals (Metazoa). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 223–230
9. Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275–2284
10. Brown-Augsburger P, Broekelmann T, Rosenbloom J, Mecham RP (1996) Functional domains on elastin and microfibril-associated glycoprotein involved in elastic fibre assembly. Biochem J 318(pt 1):149–155
11. Brunet FG, Crollius HR, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M (2006) Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol Biol Evol 23:1808–1816
12. Chen Y, Dokholyan NV (2006) The coordinated evolution of yeast proteins is constrained by functional modularity. Trends Genet 22:416–419
13. Chen Y, Faraco J, Yin W, Germiller J, Francke U, Bonadio J (1993) Structure, chromosomal localization, and expression pattern of the murine Magp gene. J Biol Chem 268:27381–27389
14. Chen E, Larson JD, Ekker SC (2006) Functional analysis of zebrafish microfibril-associated glycoprotein-1 (Magp1) in vivo reveals roles for microfibrils in vascular development and function. Blood 107:4364–4374
15. Choi J, Bergdahl A, Zheng Q, Starcher B, Yanagisawa H, Davis EC (2009) Analysis of dermal elastic fibers in the absence of fibulin-5 reveals potential roles for fibulin-5 in elastic fiber assembly. Matrix Biol 28:211–220
16. Choudhury R, McGovern A, Ridley C, Cain SA, Baldwin A, Wang MC, Guo C, Mironov A Jr, Drymoussi Z, Trump D, Shuttleworth A, Baldock C, Kielty CM (2009) Differential regulation of elastic fiber formation by fibulin-4 and-5. J Biol Chem 284:24553–24567
17. Christoffels A, Koh EG, Chia JM, Brenner S, Aparicio S, Venkatesh B (2004) Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of rayfinned fishes. Mol Biol Evol 21:1146–1151
18. Cooley MA, Argraves WS (2011) The fibulins. In: Mecham RP (ed) The extracellular matrix: an overview. Springer, Berlin, pp 337–367
19. Craft CS, Zou W, Watkins M, Grimston S, Brodt MD, Broekelmann TJ, Weinbaum JS, Teitelbaum SL, Pierce RA, Civitelli R, Silva MJ, Mecham RP (2010) Microfibril-associated glycoprotein-1, an extracellular matrix regulator of bone remodeling. J Biol Chem 285:23858–23867
20. Craft CS, Broekelmann TJ, Zou W, Chappel JC, Teitelbaum SL, Mecham RP (2011) Oophorectomy-induced bone loss is attenuated in MAGP1-deficient mice. J Cell Biochem 113:93–99
21. Davis EC (1994) Immunolocalization of microfibril and microfibril-associated proteins in the subendothelial matrix of the developing mouse aorta. J Cell Sci 107(pt 3):727–736
22. de Vega S, Iwamoto T, Nakamura T, Hozumi K, McKnight DA, Fisher LW, Fukumoto S, 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
23. de Vega S, Iwamoto T, Yamada Y (2009) Fibulins: multiple roles in matrix structures and tissue functions. Cell Mol Life Sci 66:1890–1902
24. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167
25. Dorus S, Anderson JR, Vallender EJ, Gilbert SL, Zhang L, Chemnick LG, Ryder OA, Li W, Lahn BT (2006) Sonic Hedgehog, a key development gene, experienced intensified molecular evolution in primates. Hum Mol Genet 15:2031–2037
26. Faraco J, Bashir M, Rosenbloom J, Francke U (1995) Characterization of the human gene for microfibril-associated glycoprotein (MFAP2), assignment to chromosome 1p36.1-p35, and linkage to D1S170. Genomics 25:630–637
27. Fares MA, Bezemer D, Moya A, Marin I (2003) Selection on coding regions determined Hox7 genes evolution. Mol Biol Evol 20:2104–2112
28. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Gordon L, Hendrix M, Hourlier T, Johnson N, Kahari AK, Keefe D, Keenan S, Kinsella R, Komorowska M, Koscielny G, Kulesha E, Larsson P, Longden I, McLaren W, Muffato M, Overduin B, Pignatelli M, Pritchard B, Riat HS, Ritchie GR, Ruffier M, Schuster M, Sobral D, Tang YA, Taylor K, Trevanion S, Vandrovcova J, White S, Wilson M, Wilder SP, Aken BL, Birney E, Cunningham F, Dunham I, Durbin R, Fernandez-Suarez XM, Harrow J, Herrero J, Hubbard TJ, Parker A, Proctor G, Spudich G, Vogel J, Yates A, Zadissa A, Searle SM (2012) Ensembl 2012. Nucleic Acids Res 40:D84–D90.
29. Frankfater C, Maus E, Gaal K, Segade F, Copeland NG, Gilbert DJ, Jenkins NA, Shipley JM (2000) Organization of the mouse microfibril-associated glycoprotein-2 (MAGP-2) gene. Mamm Genome 11:191–195
30. Fraser HB (2006) Coevolution, modularity and human disease. Curr Opin Genet Dev 16:637–644
31. Fraser HB, Hirsh AE, Wall DP, Eisen MB (2004) Coevolution of gene expression among interacting proteins. Proc Natl Acad Sci U S A 101:9033–9038
32. Gans C (1989) Stages in the origin of vertebrates: analysis by means of scenarios. Biol Rev Camb Philos Soc 64:221–268
33. Gibson MA, Hughes JL, Fanning JC, Cleary EG (1986) The major antigen of elastin-associated microfibrils is a 31-kDa glycoprotein. J Biol Chem 261:11429–11436
34. Gibson MA, Sandberg LB, Grosso LE, Cleary EG (1991) Complementary DNA cloning establishes microfibril-associated glycoprotein (MAGP) to be a discrete component of the elastin-associated microfibrils. J Biol Chem 266:7596–7601
35. Gibson MA, Hatzinikolas G, Kumaratilake JS, Sandberg LB, Nicholl JK, Sutherland GR, Cleary EG (1996) Further characterization of proteins associated with elastic fiber microfibrils including the molecular cloning of MAGP-2 (MP25). J Biol Chem 271:1096–1103
36. Gibson MA, Finnis ML, Kumaratilake JS, Cleary EG (1998) Microfibril-associated glycoprotein 2 (MAGP-2) is specifically associated with fibrillin-containing microfibrils but exhibits more restricted patterns of tissue localization and developmental expression than its structural relative MAGP-1. J Histochem Cytochem 46:871–886
37. Gibson MA, Leavesley DI, Ashman LK (1999) Microfibril-associated glycoprotein-2 specifically interacts with a range of bovine and human cell types via alphaVbeta3 integrin. J Biol Chem 274:13060–13065
38. Giltay R, Timpl R, 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
39. Gu X (1999) Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol 16:1664–1674
40. Gu X (2001) Maximum-likelihood approach for gene family evolution under functional divergence. Mol Biol Evol 18:453–464
41. Gu X (2006) A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. Mol Biol Evol 23:1937–1945
42. Hanada K, Vermeij M, Garinis GA, de Waard MC, Kunen MG, Myers L, Maas A, Duncker DJ, Meijers C, Dietz HC, Kanaar R, Essers J (2007) Perturbations of vascular homeostasis and aortic valve abnormalities in fibulin-4 deficient mice. Circ Res 100:738–746
43. Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999) From molecular to modular cell biology. Nature 402:C47–C52
44. Hatzinikolas G, Gibson MA (1998) The exon structure of the human MAGP-2 gene. Similarity with the MAGP-1 gene is confined to two exons encoding a cysteine-rich region. J Biol Chem 273:29309–29314
45. Hedges SB (2009) Vertebrates (Vertebrata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 309–314
46. Henderson M, Polewski R, Fanning JC, Gibson MA (1996) Microfibril-associated glycoprotein-1 (MAGP-1) is specifically located on the beads of the beaded-filament structure for fibrillincontaining microfibrils as visualized by the rotary shadowing technique. J Histochem Cytochem 44:1389–1397
47. Hesselson D, Newman C, Kim KW, Kimble J (2004) GON-1 and fibulin have antagonistic roles in control of organ shape. Curr Biol 14:2005–2010
48. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61:995–1016
49. Horiguchi M, Inoue T, Ohbayashi T, Hirai M, Noda K, Marmorstein LY, Yabe D, Takagi K, Akama TO, Kita T, Kimura T, Nakamura T (2009) Fibulin-4 conducts proper elastogenesis via interaction with cross-linking enzyme lysyl oxidase. Proc Natl Acad Sci U S A 106:19029–19034
50. Hubmacher D, Reinhardt DP (2011) Microfibrils and fibrillin. In: Mecham RP (ed) The extracellular matrix: an overview. Springer, Berlin, pp 233–266
51. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957
52. Kasahara M (2007) The 2R hypothesis: an update. Curr Opin Immunol 19:547–552
53. Kawasaki K (2011) The SCPP gene family and the complexity of hard tissues in vertebrates. Cells Tissues Organs 194:108–112
54. Kielty CM, Sherratt MJ, Shuttleworth CA (2002) Elastic fibres. J Cell Sci 115:2817–2828
55. Kielty CM, Sherratt MJ, Marson A, Baldock C (2005) Fibrillin microfibrils. Adv Protein Chem 70:405–436
56. King N, Hittinger CT, Carroll SB (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301:361–363
57. Kobayashi N, Kostka G, Garbe JH, Keene DR, Bachinger HP, Hanisch FG, Markova D, Tsuda T, Timpl R, Chu ML, Sasaki T (2007) A comparative analysis of the fibulin protein family. Biochemical characterization, binding interactions, and tissue localization. J Biol Chem 282:11805–11816
58. Kortschak RD, Tamme R, Lardelli M (2001) Evolutionary analysis of vertebrate Notch genes. Dev Genes Evol 211:350–354
59. Kozel BA, Mecham RP, Rosenbloom J (2011) Elastin. In: Mecham RP (ed) Extracellular matrix: an overview. Springer, Berlin, pp 267–301
60. Kubota Y, Kuroki R, Nishiwaki K (2004) A fibulin-1 homolog interacts with an ADAM protease that controls cell migration in C. elegans. Curr Biol 14:2011–2018
61. Kumaratilake JS, Gibson MA, Fanning JC, Cleary EG (1989) The tissue distribution of microfibrils reacting with a monospecific antibody to MAGP, the major glycoprotein antigen of elastin-associated microfibrils. Eur J Cell Biol 50:117–127
62. Lemaire R, Bayle J, Mecham RP, Lafyatis R (2007) Microfibril-associated MAGP-2 stimulates elastic fiber assembly. J Biol Chem 282(1):800–808
63. McConnell CJ, Wright GM, DeMont ME (1996) The modulus of elasticity of lobster aorta microfibrils. Experientia 52:918–921
64. McConnell CJ, DeMont ME, Wright GM (1997) Microfibrils provide non-linear elastic behaviour in the abdominal artery of the lobster Homarus americanus. J Physiol 499(pt 2):513–526
65. McLaughlin PJ, Chen Q, Horiguchi M, Starcher BC, Stanton JB, Broekelmann TJ, Marmorstein AD, McKay B, Mecham R, Nakamura T, Marmorstein LY (2006) Targeted disruption of fibulin-4 abolishes elastogenesis and causes perinatal lethality in mice. Mol Cell Biol 26:1700–1709
66. McLaughlin PJ, Bakall B, Choi J, Liu Z, Sasaki T, Davis EC, Marmorstein AD, Marmorstein LY (2007) Lack of fibulin-3 causes early aging and herniation, but not macular degeneration in mice. Hum Mol Genet 16:3059–3070
67. McLysaght A, Hokamp K, Wolfe KH (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31:200–204
68. Mecham RP, Davis EC (1994) In: Yurchenko PD, Mecham RP (eds) Extracellular matrix assembly and structure. Academic, San Diego
69. Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27:937–945
70. Miyamoto A, Lau R, Hein PW, Shipley JM, Weinmaster G (2006) Microfibrillar proteins MAGP-1 and MAGP-2 induce Notch1 extracellular domain dissociation and receptor activation. J Biol Chem 281:10089–10097
71. Miyata T, Suga H (2001) Divergence pattern of animal gene families and relationship with the Cambrian explosion. Bioessays 23:1018–1027
72. Moltzer E, te Riet L, Swagemakers SM, van Heijningen PM, Vermeij M, van Veghel R, Bouhuizen AM, van Esch JH, Lankhorst S, Ramnath NW, de Waard MC, Duncker DJ, van der Spek PJ, Rouwet EV, Danser AH, Essers J (2011) Impaired vascular contractility and aortic wall degeneration in fibulin-4 deficient mice: effect of angiotensin II type 1 (AT1) receptor blockade. PLoS One 6:e23411
73. Morris PJ (1993) The developmental role of the extracellular-matrix suggests a monophyletic origin of the kingdom Animalia. Evolution 47:152–165
74. Muriel JM, Dong C, Hutter H, Vogel BE (2005) Fibulin-1C and Fibulin-1D splice variants have distinct functions and assemble in a hemicentin-dependent manner. Development 132:4223–4234
75. Muriel JM, Xu X, Kramer JM, Vogel BE (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
76. Nakamura T, Lozano PR, Ikeda Y, Iwanaga Y, Hinek A, Minamisawa S, Cheng CF, Kobuke K, Dalton N, Takada Y, Tashiro K, Ross J Jr, Honjo T, Chien KR (2002) Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature 415:171–175
77. Nehring LC, Miyamoto A, Hein PW, Weinmaster G, Shipley JM (2005) The extracellular matrix protein MAGP-2 interacts with Jagged1 and induces its shedding from the cell surface. J Biol Chem 280:20349–20355
78. Pan TC, Sasaki T, Zhang RZ, Fassler R, Timpl R, Chu ML (1993) Structure and expression of fibulin-2, a novel extracellular matrix protein with multiple EGF-like repeats and consensus motifs for calcium binding. J Cell Biol 123:1269–1277
79. Pazos F, Juan D, Izarzugaza JM, Leon E, Valencia A (2008) Prediction of protein interaction based on similarity of phylogenetic trees. Methods Mol Biol 484:523–535
80. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94
81. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, GibsonBrown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071
82. Rahn DD, Acevedo JF, Roshanravan S, Keller PW, Davis EC, Marmorstein LY, Word RA (2009) Failure of pelvic organ support in mice deficient in fibulin-3. Am J Pathol 174:206–215
83. Ramirez F, Dietz HC (2007) Fibrillin-rich microfibrils: structural determinants of morphogenetic and homeostatic events. J Cell Physiol 213:326–330
84. Ramirez F, Sakai LY, Rifkin DB, Dietz HC (2007) Extracellular microfibrils in development and disease. Cell Mol Life Sci 64:2437–2446
85. Reber-Muller S, Spissinger T, Schuchert P, Spring J, 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
86. Reinhardt DP, Sasaki T, Dzamba BJ, Keene DR, Chu ML, Gohring W, Timpl R, Sakai LY (1996) Fibrillin-1 and fibulin-2 interact and are colocalized in some tissues. J Biol Chem 271:19489–19496
87. Roark EF, Keene DR, Haudenschild CC, Godyna S, Little CD, Argraves WS (1995) The association of human fibulin-1 with elastic fibers: an immunohistological, ultrastructural, and RNA study. J Histochem Cytochem 43:401–411
88. Robertson I, Jensen S, Handford P (2011) TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs. Biochem J 433:263–276
89. Robson P, Wright GM, Youson JH, Keeley FW (2000) The structure and organization of lamprin genes: multiple-copy genes with alternative splicing and convergent evolution with insect structural proteins. Mol Biol Evol 17:1739–1752
90. Rychel AL, Smith SE, Shimamoto HT, Swalla BJ (2006) Evolution and development of the chordates: collagen and pharyngeal cartilage. Mol Biol Evol 23:541–549
91. Santini F, Harmon LJ, Carnevale G, Alfaro ME (2009) Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol Biol 9:194
92. Satou Y, Kawashima T, Shoguchi E, Nakayama A, Satoh N (2005) An integrated database of the ascidian, Ciona intestinalis: towards functional genomics. Zoolog Sci 22:837–843
93. Segade F (2009) Functional evolution of the microfibril-associated glycoproteins. Gene 439:43–54
94. Segade F (2010) Molecular evolution of the fibulins: implications on the functionality of the elastic fibulins. Gene 464:17–31
95. Segade F, Mecham RP (2005) Regulatory elements of microfibril-associated glycoprotein-1 gene expression in muscle cells. Biochim Biophys Acta 1731:215–224
96. Segade F, Broekelmann TJ, Pierce RA, Mecham RP (2000) Revised genomic structure of the human MAGP1 gene and identification of alternate transcripts in human and mouse tissues. Matrix Biol 19:671–682
97. Segade F, Trask BC, Broekelmann TJ, Pierce RA, Mecham RP (2002) Identification of a matrixbinding domain in MAGP1 and MAGP2 and intracellular localization of alternative splice forms. J Biol Chem 277:11050–11057
98. Segade F, Suganuma N, Mychaleckyj JC, Mecham RP (2007) The intracellular form of human MAGP1 elicits a complex and specific transcriptional response. Int J Biochem Cell Biol 39:2303–2313
99. Shimeld SM, Holland PWH (2000) Vertebrate innovations. Proc Natl Acad Sci U S A 97:4449–4452
100. Spencer JA, Hacker SL, Davis EC, Mecham RP, Knutsen RH, Li DY, Gerard RD, Richardson JA, Olson EN, 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 U S A 102:2946–2951
101. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 9:678–687
102. Timpl R, Sasaki T, Kostka G, Chu ML (2003) Fibulins: a versatile family of extracellular matrix proteins. Nat Rev Mol Cell Biol 4:479–489
103. Trask BC, Broekelmann T, Ritty TM, Trask TM, Tisdale C, Mecham RP (2001) Posttranslational modifications of microfibril associated glycoprotein-1 (MAGP-1). Biochemistry 40:4372–4380
104. Vandepoele K, De Vos W, Taylor JS, Meyer A, Van de Peer Y (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci U S A 101:1638–1643
105. Vogel BE, Hedgecock EM (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
106. Vogel BE, Muriel JM, Dong C, Xu X (2006) Hemicentins: what have we learned from worms? Cell Res 16:872–878
107. Wagenseil JE, Mecham RP (2007) New insights into elastic fiber assembly. Birth Defects Res C Embryo Today 81:229–240
108. Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89:957–989
109. Weinbaum JS, Broekelmann TJ, Pierce RA, Werneck CC, Segade F, Craft CS, Knutsen RH, Mecham RP (2008) Deficiency in microfibril-associated glycoprotein-1 leads to complex phenotypes in multiple organ systems. J Biol Chem 283:25533–25543
110. Werneck CC, Trask BC, Broekelmann TJ, Trask TM, Ritty TM, Segade F, Mecham RP (2004) Identification of a major microfibril-associated glycoprotein-1-binding domain in fibrillin-2. J Biol Chem 279:23045–23051
111. Werneck CC, Vicente CP, Weinberg JS, Shifren A, Pierce RA, Broekelmann TJ, Tollefsen DM, Mecham RP (2008) Mice lacking the extracellular matrix protein MAGP1 display delayed thrombotic occlusion following vessel injury. Blood 111:4137–4144
112. Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297(pt 2):249–260
113. Yan Q, Sage EH (1999) SPARC, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 47:1495–1506
114. Yanagisawa H, Davis EC (2010) Unraveling the mechanism of elastic fiber assembly: the roles of short fibulins. Int J Biochem Cell Biol 42:1084–1093
115. Yanagisawa H, Davis EC, Starcher BC, Ouchi T, Yanagisawa M, Richardson JA, Olson EN (2002) Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 415:168–171
116. Zheng Q, Davis EC, Richardson JA, Starcher BC, Li T, Gerard RD, Yanagisawa H (2007) Molecular analysis of fibulin-5 function during de novo synthesis of elastic fibers. Mol Cell Biol 27:1083–1095