Fibulin-5, an integrin-binding matricellular protein: its function in development and disease

Journal of Cell Communication and Signaling - Tập 3 Số 3-4 - Trang 337-347 - 2009
Hiromi Yanagisawa1, Marie K. Schluterman2, Rolf A. Brekken2
1Department of Molecular Biology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390-9148, USA
2Department of Surgery, Hamon Center for Therapeutic Oncology Research, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX, 75390-8593, USA

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Albig AR, Schiemann WP (2004) Fibulin-5 antagonizes vascular endothelial growth factor (VEGF) signaling and angiogenic sprouting by endothelial cells. DNA & Cell Biology 23:367–379

Albig AR, Schiemann WP (2005) Fibulin-5 function during tumorigenesis. Future Oncol 1:23–35

Albig AR, Neil JR, Schiemann WP (2006) Fibulins 3 and 5 antagonize tumor angiogenesis in vivo. Cancer Res 66:2621–2629

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

Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503–506

Bornstein P (2001) Thrombospondins as matricellular modulators of cell function. J Clin Invest 107:929–934

Brekken RA, Sage EH (2001) SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 19:816–827

Cai H, Harrison DG (2000) Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87:840–844

Carta L, Pereira L, Arteaga-Solis E, Lee-Arteaga SY, Lenart B, Starcher B et al (2006) Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J Biol Chem 281:8016–8023

Chailley-Heu B, Boucherat O, Barlier-Mur AM, Bourbon JR (2005) FGF-18 is upregulated in the postnatal rat lung and enhances elastogenesis in myofibroblasts. Am J Physiol Lung Cell Mol Physiol 288:L43–51

Charbonneau NL, Ono RN, Corson GM, Keene DR, Sakai LY (2004) Fine tuning of growth factor signals depends on fibrillin microfibril networks. Birth Defects Res C Embryo Today 72:37–50

Chiarugi P, Pani G, Giannoni E, Taddei L, Colavitti R, Raugei G et al (2003) Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J Cell Biol 161:933–944

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

Chu ML, Tsuda T (2004) Fibulins in development and heritable disease. Birth Defects Res C Embryo Today 72:25–36

Chua CC, Hamdy RC, Chua BH (1998) Upregulation of vascular endothelial growth factor by H2O2 in rat heart endothelial cells. Free Radic Biol Med 25:891–897

Cirulis JT, Bellingham CM, Davis EC, Hubmacher D, Reinhardt DP, Mecham RP et al (2008) Fibrillins, fibulins, and matrix-associated glycoprotein modulate the kinetics and morphology of in vitro self-assembly of a recombinant elastin-like polypeptide. Biochemistry 47:12601–12613

Claus S, Fischer J, Megarbane H, Megarbane A, Jobard F, Debret R et al (2008) A p.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

Davis GE, Bayless KJ, Davis MJ, Meininger GA (2000) Regulation of tissue injury responses by the exposure of matricryptic sites within extracellular matrix molecules. Am J Pathol 156:1489–1498

de Vega S, Iwamoto T, Nakamura T, Hozumi K, McKnight DA, Fisher LW et al (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

de Vega S, Iwamoto T, Yamada Y (2009) Fibulins: Multiple roles in matrix structures and tissue functions. Cell Mol Life Sci In Press

Drewes PG, Yanagisawa H, Starcher B, Hornstra IK, Csiszar K, Marinis SI et al (2007) Pelvic organ prolapse in Fibulin-5 knockout mice: pregnancy changes in elastic fiber homeostasis in mouse vagina. Am J Pathol 170:578–589

El-Hallous E, Sasaki T, Hubmacher D, Getie M, Tiedemann K, Brinckmann J et al (2007) Fibrillin-1 interactions with fibulins depend on the first hybrid domain and provide an adaptor function to tropoelastin. J Biol Chem 282:8935–8946

Elahi E, Kalhor R, Banihosseini SS, Torabi N, Pour-Jafari H, Houshmand M et al (2006) Homozygous missense mutation in fibulin-5 in an Iranian autosomal recessive cutis laxa pedigree and associated haplotype. J Invest Dermatol 126:1506–1509

Freeman LJ, Lomas A, Hodson N, Sherratt MJ, Mellody KT, Weiss AS et al (2005) Fibulin-5 interacts with fibrillin-1 molecules and microfibrils. Biochem J 388:1–5

Hirai M, Horiguchi M, Ohbayashi T, Kita T, Chien KR, Nakamura T (2007a) Latent TGF-beta-binding protein 2 binds to DANCE/fibulin-5 and regulates elastic fiber assembly. EMBO J 26:3283–3295

Hirai M, Ohbayashi T, Horiguchi M, Okawa K, Hagiwara A, Chien KR et al (2007b) Fibulin-5/DANCE has an elastogenic organizer activity that is abrogated by proteolytic cleavage in vivo. J Cell Biol 176:1061–1071

Hu Q, Loeys BL, Coucke PJ, De Paepe A, Mecham RP, Choi J et al (2006) Fibulin-5 mutations: mechanisms of impaired elastic fiber formation in recessive cutis laxa. Hum Mol Genet 15:3379–3386

Isogai Z, Ono RN, Ushiro S, Keene DR, Chen Y, Mazzieri R et al (2003) Latent transforming growth factor beta-binding protein 1 interacts with fibrillin and is a microfibril-associated protein. J Biol Chem 278:2750–2757

Jones RP, Wang M-C, Jowitt TA, Ridley C, Mellody KT, Howard M et al (2009) Fibulin 5 forms a compact dimer in physiological solutions. J Biol Chem In Press

Jung HJ, Jeon MJ, Yim GW, Kim SK, Choi JR, Bai SW (2009) Changes in expression of fibulin-5 and lysyl oxidase-like 1 associated with pelvic organ prolapse. Eur J Obstet Gynecol Reprod Biol

Karnik SK, Brooke BS, Bayes-Genis A, Sorensen L, Wythe JD, Schwartz RS et al (2003) A critical role for elastin signaling in vascular morphogenesis and disease. Development 130:411–423

Katsuta Y, Ogura Y, Iriyama S, Goetinck PF, Klement JF, Uitto J et al (2008) Fibulin-5 accelerates elastic fibre assembly in human skin fibroblasts. Exp Dermatol 17:837–842

Kapetanopoulos A, Fresser F, Millonig G, Shaul Y, Baier G, Utermann G (2002) Direct interaction of extracellular matrix protein DANCE with apolipoprotein (a) mediated by the kringle IV-type 2 domain. Mol. Genet. Genomics 267:440–460

Kelleher CM, McLean SE, Mecham RP (2004) Vascular extracellular matrix and aortic development. Curr Top Dev Biol 62:153–188

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

Kobayashi N, Kostka G, Garbe JH, Keene DR, Bächinger HP, Hanisch FG et al (2007) A comparative analysis of the fibulin protein family. Biochemical characterization, binding interactions, and tissue localization. J Biol Chem 282:11805–11816

Kowal RC, Richardson JA, Miano JM, Olson EN (1999) EVEC, a novel epidermal growth factor-like repeat-containing protein upregulated in embryonic and diseased adult vasculature. Circ Res 84:1166–1176

Kuang PP, Goldstein RH, Liu Y, Rishikof DC, Jean JC, Joyce-Brady M (2003) Coordinate expression of fibulin-5/DANCE and elastin during lung injury repair. Am J Physiol Lung Cell Mol Physiol 285:1147

Kuang PP, Joyce-Brady M, Zhang XH, Jean JC, Goldstein RH (2006) Fibulin-5 gene expression in human lung fibroblasts is regulated by TGF-beta and phosphatidylinositol 3-kinase activity. Am J Physiol Cell Physiol 291:C1412–1421

Lee YH, Albig AR, Regner M, Schiemann BJ, Schiemann WP (2008) Fibulin-5 initiates epithelial-mesenchymal transition (EMT) and enhances EMT induced by TGF-beta in mammary epithelial cells via a MMP-dependent mechanism. Carcinogenesis 29:2243–2251

Legate KR, Montanez E, Kudlacek O, Fassler R (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7:20–31

Lelkes PI, Hahn KL, Sukovich DA, Karmiol S, Schmidt DH (1998) On the possible role of reactive oxygen species in angiogenesis. Adv Exp Med Biol 454:295–310

Lemaire R, Korn JH, Schiemann WP, Lafyatis R (2004) Fibulin-2 and fibulin-5 alterations in tsk mice associated with disorganized hypodermal elastic fibers and skin tethering. J Invest Dermatol 123:1063–1069

Liu X, Zhao Y, Gao J, Pawlyk B, Starcher B, Spencer JA et al (2004) Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat Genet 36:178–182

Loeys B, Van Maldergem L, Mortier G, Coucke P, Gerniers S, Naeyaert JM et al (2002) Homozygosity for a missense mutation in fibulin-5 (FBLN5) results in a severe form of cutis laxa. Hum Mol Genet 11:2113–2118

Lomas AC, Mellody KT, Freeman LJ, Bax DV, Shuttleworth CA, Kielty CM (2007) Fibulin-5 binds human smooth-muscle cells through alpha5beta1 and alpha4beta1 integrins, but does not support receptor activation. Biochem J 405:417–428

Lotery AJ, Baas D, Ridley C, Jones RP, Klaver CC, Stone E et al (2006) Reduced secretion of fibulin 5 in age-related macular degeneration and cutis laxa. Hum Mutat 27:568–574

Madsen CD, Sidenius N (2008) The interaction between urokinase receptor and vitronectin in cell adhesion and signalling. Eur J Cell Biol 87:617–629

Markova D, Zou Y, Ringpfeil F, Sasaki T, Kostka G, Timpl R et al (2003) Genetic heterogeneity of cutis laxa: a heterozygous tandem duplication within the fibulin-5 (FBLN5) gene. Am J Hum Genet 72:998–1004

Maurer P, Hohenester E (1997) Structural and functional aspects of calcium binding in extracellular matrix proteins. Matrix Biol 15:569–580 discussion 581cscs

McLaughlin PJ, Chen Q, Horiguchi M, Starcher BC, Stanton JB, Broekelmann TJ et al (2006) Targeted disruption of fibulin-4 abolishes elastogenesis and causes perinatal lethality in mice. Mol Cell Biol 26:1700–1709

McLaughlin PJ, Bakall B, Choi J, Liu Z, Sasaki T, Davis EC et al (2007) Lack of fibulin-3 causes early aging and herniation, but not macular degeneration in mice. Hum Mol Genet 16:3059–3070

Mullins RF, Olvera MA, Clark AF, Stone EM (2007) Fibulin-5 distribution in human eyes: relevance to age-related macular degeneration. Exp Eye Res 84:378–380

Nakamura T, Ruiz-Lozano P, Lindner V, Yabe D, Taniwaki M, Furukawa Y et al (1999) DANCE, a novel secreted RGD protein expressed in developing, atherosclerotic, and balloon-injured arteries. J Biol Chem 274:22476–22483

Nakamura T, Lozano PR, Ikeda Y, Iwanaga Y, Hinek A, Minamisawa S et al (2002) Fibulin-5/DANCE is essential for elastogenesis in vivo. Nature 415:171–175

Neptune ER, Frischmeyer PA, Arking DE, Myers L, Bunton TE, Gayraud B et al (2003) Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat Genet 33:407–411

Nguyen AD, Itoh S, Jeney V, Yanagisawa H, Fujimoto M, Ushio-Fukai M et al (2004) Fibulin-5 is a novel binding protein for extracellular superoxide dismutase. Circ Res 95:1067–1074

Nonaka R, Onoue S, Wachi H, Sato F, Urban Z, Starcher BC et al (2009) DANCE/fibulin-5 promotes elastic fiber formation in a tropoelastin isoform-dependent manner. Clin Biochem 42:713–721

Preis M, Cohen T, Sarnatzki Y, Ben Yosef Y, Schneiderman J, Gluzman Z et al (2006) Effects of fibulin-5 on attachment, adhesion, and proliferation of primary human endothelial cells. Biochem Biophys Res Commun 348:1024–1033

Rahn DD, Ruff MD, Brown S, Tibbals HF, Word RA (2008) Biomechanical properties of the mouse vagina: changes seen in pregnancy and with elastinopathy. Am J Obstet Gynecol 198:590e591-596

Raines EW (2000) The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int J Exp Pathol 81:173–182

Ruoslahti E, Pierschbacher MD (1987) New perspectives in cell adhesion: RGD and integrins. Science 238:491–497

Schiemann WP, Blobe GC, Kalume DE, Pandey A, Lodish HF (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

Schluterman MK, Chapman SL, Korpanty G, Ozumi K, Fukai T, Yanagisawa H, Brekken RA (2009) Loss of fibulin-5 binding to β1 integrins inhibits tumor growth by increasing the level of ROS. Disease Models and Mechanisms In Press

Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK et al (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3:289–300

Soderberg MW, Bystrom B, Kalamajski S, Malmstrom A, Ekman-Ordeberg G (2009) Gene expressions of small leucine-rich repeat proteoglycans and fibulin-5 are decreased in pelvic organ prolapse. Mol Hum Reprod 15:251–257

Spencer JA, Hacker SL, Davis EC, Mecham RP, Knutsen RH, Li DY et al (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

Stone EM, Braun TA, Russell SR, Kuehn MH, Lotery AJ, Moore PA et al (2004) Missense variations in the fibulin 5 gene and age-related macular degeneration. N Engl J Med 351:346–353

Sullivan KM, Bissonnette R, Yanagisawa H, Hussain SN, Davis EC (2007) Fibulin-5 functions as an endogenous angiogenesis inhibitor. Lab Invest 87:818–827

ten Dijke P, Arthur HM (2007) Extracellular control of TGFbeta signalling in vascular development and disease. Nat Rev Mol Cell Biol 8:857–869

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

Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, Alexander RW (2005) Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation 111:2347–2355

Touyz RM, Schiffrin EL (2004) Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 122:339–352

Ushio-Fukai M (2007) VEGF signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 9:731–739

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

Wachi H, Sato F, Nakazawa J, Nonaka R, Szabo Z, Urban Z et al (2007) Domains 16 and 17 of tropoelastin in elastic fibre formation. Biochem J 402:63–70

Wachi H, Nonaka R, Sato F, Shibata-Sato K, Ishida M, Iketani S et al (2008) Characterization of the molecular interaction between tropoelastin and DANCE/fibulin-5. J Biochem 143:633–639

Wu C, Keivens VM, O'Toole TE, McDonald JA, Ginsberg MH (1995) Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83:715–724

Wu WS (2006) The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev 25:695–705

Xie L, Palmsten K, MacDonald B, Kieran MW, Potenta S, Vong S et al (2008) Basement membrane derived fibulin-1 and fibulin-5 function as angiogenesis inhibitors and suppress tumor growth. Exp Biol Med (Maywood) 233:155–162

Yanagisawa H, Davis EC, Starcher BC, Ouchi T, Yanagisawa M, Richardson JA et al (2002) Fibulin-5 is an elastin-binding protein essential for elastic fibre development in vivo. Nature 415:168–171

Yang Z, Mu Z, Dabovic B, Jurukovski V, Yu D, Sung J et al (2007) Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice. J Cell Biol 176:787–793

Zanetti M, Braghetta P, Sabatelli P, Mura I, Doliana R, Colombatti A, Volpin D, Bonaldo P, Bressan GM (2004) Emilin-1 deficiency induces elastogenesis and vascular cell defects. Mol. Cell. Biol 24:638–650

Zheng Q, Choi J, Rouleau L, Leask RL, Richardson JA, Davis EC et al (2006) Normal Wound Healing in Mice Deficient for Fibulin-5, an Elastin Binding Protein Essential for Dermal Elastic Fiber Assembly. J Invest Dermatol

Zheng Q, Davis EC, Richardson JA, Starcher BC, Li T, Gerard RD et al (2007) Molecular analysis of fibulin-5 function during de novo synthesis of elastic fibers. Mol Cell Biol 27:1083–1095