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

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Evolution of Extracellular Matrix

Part of the book series: Biology of Extracellular Matrix ((BEM))

Abstract

This chapter reviews the evolutionary histories of two representative families of microfibril-associated proteins as distinctive examples of adding evolutionary novelty to the ancient microfibril genetic module. The microfibril-associated glycoproteins (MAGPs), a recent addition to the microfibril, evolved from a MAGP1-like gene in basal vertebrates. The extant MAGP1 and MAGP2 genes arose in a multigene duplication event, with functional divergence mediated by relaxation of natural selection and correlated evolution between MAGP2 and Notch1. Unique MAGP1 functions in bony vertebrates likely evolved by gain of function at the N-terminus. The fibulins (FBLNs) appeared at the base of the metazoans, contemporaneously with the Fibrillin gene. Diversification accelerated in chordates and vertebrates, to a total of nine FBLN genes. The vertebrate FBLN3/4/5 clade of elastogenic FBLNs evolved from a chordate ancestor by two gene duplication events in quick succession. Accelerated evolution in sequence and expression patterns occurred preferentially on the FBLN5 branch. Coevolution of functional motifs in FBLN3/4/5 with their partners in elastic fiber deposition contributed to the nonredundant specialization of the elastogenic FBLNs.

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References

  • Adkins RM (2008) Coevolution: molecular. In: Cooper DN, Kehrer-Sawatzki H (eds) Handbook of human molecular evolution. Wiley, Chichester, pp 322–328

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Argraves WS, Greene LM, Cooley MA, Gallagher WM (2003) Fibulins: physiological and disease perspectives. EMBO Rep 4:1127–1131

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bellahcene A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS (2008) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8:212–226

    PubMed  CAS  Google Scholar 

  • Blair JE (2009) Animals (Metazoa). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 223–230

    Google Scholar 

  • Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275–2284

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Chen Y, Dokholyan NV (2006) The coordinated evolution of yeast proteins is constrained by functional modularity. Trends Genet 22:416–419

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 ray-finned fishes. Mol Biol Evol 21:1146–1151

    PubMed  CAS  Google Scholar 

  • Cooley MA, Argraves WS (2011) The fibulins. In: Mecham RP (ed) The extracellular matrix: an overview. Springer, Berlin, pp 337–367

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • de Vega S, Iwamoto T, Yamada Y (2009) Fibulins: multiple roles in matrix structures and tissue functions. Cell Mol Life Sci 66:1890–1902

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Fares MA, Bezemer D, Moya A, Marin I (2003) Selection on coding regions determined Hox7 genes evolution. Mol Biol Evol 20:2104–2112

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Fraser HB (2006) Coevolution, modularity and human disease. Curr Opin Genet Dev 16:637–644

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gans C (1989) Stages in the origin of vertebrates: analysis by means of scenarios. Biol Rev Camb Philos Soc 64:221–268

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gu X (1999) Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol 16:1664–1674

    PubMed  CAS  Google Scholar 

  • Gu X (2001) Maximum-likelihood approach for gene family evolution under functional divergence. Mol Biol Evol 18:453–464

    PubMed  CAS  Google Scholar 

  • Gu X (2006) A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. Mol Biol Evol 23:1937–1945

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999) From molecular to modular cell biology. Nature 402:C47–C52

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hedges SB (2009) Vertebrates (Vertebrata). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 309–314

    Google Scholar 

  • 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 fibrillin-containing microfibrils as visualized by the rotary shadowing technique. J Histochem Cytochem 44:1389–1397

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61:995–1016

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hubmacher D, Reinhardt DP (2011) Microfibrils and fibrillin. In: Mecham RP (ed) The extracellular matrix: an overview. Springer, Berlin, pp 233–266

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Kasahara M (2007) The 2R hypothesis: an update. Curr Opin Immunol 19:547–552

    PubMed  CAS  Google Scholar 

  • Kawasaki K (2011) The SCPP gene family and the complexity of hard tissues in vertebrates. Cells Tissues Organs 194:108–112

    PubMed  Google Scholar 

  • Kielty CM, Sherratt MJ, Shuttleworth CA (2002) Elastic fibres. J Cell Sci 115:2817–2828

    PubMed  CAS  Google Scholar 

  • Kielty CM, Sherratt MJ, Marson A, Baldock C (2005) Fibrillin microfibrils. Adv Protein Chem 70:405–436

    PubMed  CAS  Google Scholar 

  • King N, Hittinger CT, Carroll SB (2003) Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301:361–363

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kortschak RD, Tamme R, Lardelli M (2001) Evolutionary analysis of vertebrate Notch genes. Dev Genes Evol 211:350–354

    PubMed  CAS  Google Scholar 

  • Kozel BA, Mecham RP, Rosenbloom J (2011) Elastin. In: Mecham RP (ed) Extracellular matrix: an overview. Springer, Berlin, pp 267–301

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lemaire R, Bayle J, Mecham RP, Lafyatis R (2007) Microfibril-associated MAGP-2 stimulates elastic fiber assembly. J Biol Chem 282(1):800–808

    PubMed  CAS  Google Scholar 

  • McConnell CJ, Wright GM, DeMont ME (1996) The modulus of elasticity of lobster aorta microfibrils. Experientia 52:918–921

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • McLysaght A, Hokamp K, Wolfe KH (2002) Extensive genomic duplication during early chordate evolution. Nat Genet 31:200–204

    PubMed  CAS  Google Scholar 

  • Mecham RP, Davis EC (1994) In: Yurchenko PD, Mecham RP (eds) Extracellular matrix assembly and structure. Academic, San Diego

    Google Scholar 

  • Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27:937–945

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Miyata T, Suga H (2001) Divergence pattern of animal gene families and relationship with the Cambrian explosion. Bioessays 23:1018–1027

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Morris PJ (1993) The developmental role of the extracellular-matrix suggests a monophyletic origin of the kingdom Animalia. Evolution 47:152–165

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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, Gibson-Brown 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Ramirez F, Dietz HC (2007) Fibrillin-rich microfibrils: structural determinants of morphogenetic and homeostatic events. J Cell Physiol 213:326–330

    PubMed  CAS  Google Scholar 

  • Ramirez F, Sakai LY, Rifkin DB, Dietz HC (2007) Extracellular microfibrils in development and disease. Cell Mol Life Sci 64:2437–2446

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Segade F (2009) Functional evolution of the microfibril-associated glycoproteins. Gene 439:43–54

    PubMed  CAS  Google Scholar 

  • Segade F (2010) Molecular evolution of the fibulins: implications on the functionality of the elastic fibulins. Gene 464:17–31

    PubMed  CAS  Google Scholar 

  • Segade F, Mecham RP (2005) Regulatory elements of microfibril-associated glycoprotein-1 gene expression in muscle cells. Biochim Biophys Acta 1731:215–224

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Segade F, Trask BC, Broekelmann TJ, Pierce RA, Mecham RP (2002) Identification of a matrix-binding domain in MAGP1 and MAGP2 and intracellular localization of alternative splice forms. J Biol Chem 277:11050–11057

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Shimeld SM, Holland PWH (2000) Vertebrate innovations. Proc Natl Acad Sci U S A 97:4449–4452

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Vogel BE, Muriel JM, Dong C, Xu X (2006) Hemicentins: what have we learned from worms? Cell Res 16:872–878

    PubMed  CAS  Google Scholar 

  • Wagenseil JE, Mecham RP (2007) New insights into elastic fiber assembly. Birth Defects Res C Embryo Today 81:229–240

    PubMed  CAS  Google Scholar 

  • Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89:957–989

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297(pt 2):249–260

    PubMed  CAS  Google Scholar 

  • Yan Q, Sage EH (1999) SPARC, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 47:1495–1506

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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Correspondence to Fernando Segade .

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Segade, F. (2013). Molecular Evolution of the Microfibril-Associated Proteins: The Fibulins and the MAGPs. In: Keeley, F., Mecham, R. (eds) Evolution of Extracellular Matrix. Biology of Extracellular Matrix. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36002-2_6

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