Advertisement

A Disintegrin and Metalloprotease (Adams) Family: Expression and Potential Roles in the Developing Heart

  • Thomas K. Borg
  • Angela De Almeida
  • Melissa Joy Loftis
  • Alex McFadden
  • Wayne Carver
Part of the Progress in Experimental Cardiology book series (PREC, volume 4)

Summary

The A Disintegrin And Metalloproteases (ADAMs) are a rather recently identified family of cell surface molecules which have a characteristic multidomain structure. The multiple domains found in these proteins include a metalloprotease domain that has been shown to proteolytically cleave extracellular matrix and cell surface proteins. These domains also include a disintegrin region which has been shown to participate in cell-cell binding in some cell types. Through these multiple functional domains, ADAMs have been shown to play roles in diverse developmental processes including cell-cell fusion and cell migration. The roles of these proteins in the developing cardiovascular system have not been examined. In the following discussion, we will summarize the current knowledge of these molecules in other systems and present novel data regarding their expression and potential function in the developing heart.

Key words

Disintegrin Metalloprotease Extracellular matrix Integrin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Wolfsberg TG, Primakoff P, Myles DG, White JM. 1995. ADAM, a novel family of membrane proteins containing A Disintegrin And Metalloprotease domain: multipotential functions in cell-cell and cell-matrix interactions. J Cell Biol 131:275–278.PubMedCrossRefGoogle Scholar
  2. 2.
    Wolfsberg TG, White JM. 1996. ADAMs in fertilization and development. Devel Biol 180:389–401.CrossRefGoogle Scholar
  3. 3.
    Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K. 1997. Molecular cloning of a gene encoding a new type of metalloproteinase-disintegrin family protein with thrombospondin motifs as an inflammation associated gene. J Biol Chem 272:556–562.PubMedCrossRefGoogle Scholar
  4. 4.
    Gilpin BJ, Loechel F, Mattei MG, Engvall E, Albrechtsen R, Wewer UM. 1998. A novel, secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo.. J Biol Chem 273:157–166.PubMedCrossRefGoogle Scholar
  5. 5.
    Millichip MI, Dallas DJ, Wu E, Dale S, McKie N. 1998. The metallo-disintegrin ADAM 10 (MADM) from bovine kidney has type IV collagenase activity in vitro.. Biochem Biophys Res Commun 245:594–598.PubMedCrossRefGoogle Scholar
  6. 6.
    Loechel F, Gilpin BJ, Engvall E, Albrechtsen R, Wewer UM. 1998. Human ADAM 12 (meltrin a) is an active metalloprotease. J Biol Chem 273:16993–16997.PubMedCrossRefGoogle Scholar
  7. 7.
    Hilenski LL, Terracio L, Sawyer R, Borg K. 1989. Effects of extracellular matrix on cytoskeletal and myfibrilar organization in vitro. Scan Microscopy 535.Google Scholar
  8. 8.
    Hilenski L, Terracio L, Borg TK. 1991. Myofibriliar and cytoskeletal assembly in neonatal rat cardiac myocytes cultured on laminin and collagen. Cell Tissue Res 264:577–587.PubMedCrossRefGoogle Scholar
  9. 9.
    Fassler R, Rohwedel J, Maltsev V, Bloch W, Lentini S, Guan K, Gullberg D, Hescheler J, Addicks K, Wobus AM. 1996. Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J Cell Science 109:2989–2999.PubMedGoogle Scholar
  10. 10.
    Simpson DG, Terracio L, Terracio M, Price RL, Turner DC, Borg TK. 1994. Modulation of cardiac myocyte phenotype in vitro. by the composition and orientation of the extracellular matrix. J Cell Physiol 161:89–105.PubMedCrossRefGoogle Scholar
  11. 11.
    Simpson DG, Reaves T, Shih ST, Burgess W, Borg TK, Terracio L. 1998. Cardiac integrins: The ties that bind. Cardiovasc Pathol 7:135–143.CrossRefGoogle Scholar
  12. 12.
    Hooper NM, Karran EH, Turner AJ. 1997. Membrane protein secretases. Biochem J 321:265–279.PubMedGoogle Scholar
  13. 13.
    Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, Castner BJ, Stocking KL, Reddy P, Srinivasan S, Nelson N, Boiani N, Schooley KA, Gerhart M, Davis R, Fitzner JN, Johnson RS, Paxton RJ, March CJ, Cerretti DP. 1997. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385:729–733.PubMedCrossRefGoogle Scholar
  14. 14.
    Moss ML, Jin SL, Milk ME, Bickett DM, Burkhart W, Carter HL, Chen WJ, Clay WC, Didsbury JR, Hassler D. 1997. Nature 385:729–733.CrossRefGoogle Scholar
  15. 15.
    Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, Russel WE, Castner BJ, Johnson RS, Fitzner JN, Boyce RW, Nelson N, Kozlosky CJ, Wolfson MF, Rauch CT, Cerretti DP, Paxton RJ, March CJ, Black RA. 1998. An essential role for ectodomain shedding in mammalian development. Science 282:1281–1284.PubMedCrossRefGoogle Scholar
  16. 16.
    Blobel C. 1997. Metalloprotease-disintegrins: Links to cell adhesion and cleavage of TNF-OC and Notch. Cell 90:589–592.PubMedCrossRefGoogle Scholar
  17. 17.
    Black RA, White JM. 1998. ADAMs: Focus on the protease domains. Curr Opin Cell Biol 10: 654–659.PubMedCrossRefGoogle Scholar
  18. 18.
    Borland G, Murphy G, Ager A. 1999. Tissue inhibitor of metalloproteinases-3 inhibits shedding of L-selectin fromleukocytes. J Biol Chem 274:2810–2815.PubMedCrossRefGoogle Scholar
  19. 19.
    Lammich S, Kojro E, Postina R, Gilbert S, Pfeiffer R, Jasionowski M, Haass C, Fahrenhok F. 1999. Constitutive and regukted α-secretase cleavage of Akheimer’s amyloid precursor protein by a disintegrin and metalloprotease. Proc Natl Acad Sci USA 96:3922–3927.PubMedCrossRefGoogle Scholar
  20. 20.
    Izumi Y, Hirata M, Hasuwa H, Iwamoto R, Umata T, Miyado K, Tamai Y, Kurisaki T, Sehara-Fujisawa A, Ohno A, Mekada E. 1998. A metalloprotease-disintegrin, MDC 9/meltrin-γ/ADAM 9 and PKC δ are involved in TPA-indiuced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor. EMBO J 17:7260–7272.PubMedCrossRefGoogle Scholar
  21. 21.
    Shakibaei M, Marker H-J. 1999. β1-integrins in the cartikge matrix. Cell Tissue Res 296:565–573.PubMedCrossRefGoogle Scholar
  22. 22.
    Albelda AM, Buck CA. 1990. Integrins and other cell adhesion molecules. FASEB J 4:2868–2880.PubMedGoogle Scholar
  23. 23.
    Humphries MJ. 1990. The molecular basis and specificity of integrin-ligand interactions. J Cell Sci 97:585–592.PubMedGoogle Scholar
  24. 24.
    Hynes RO. 1992. Integrins: Versatility, modulation and signaling in cell adhesion. Cell 69:11–25.PubMedCrossRefGoogle Scholar
  25. 25.
    Baldwin HS, Buck CA. 1994. Integrins and other cell adhesion molecules in cardiac development. Trends Cardiovasc Med 4:178–187.PubMedCrossRefGoogle Scholar
  26. 26.
    Ding B, Price RL, Goldsmith EC, Borg TK,Yan X, Douglas MD, Weinberg EO, Thielen T, Didenko W, Lorell BH. 2000. Left ventricular hypertrophy in ascending aortic stenosis mice: Anoikis and the progression to early failure. Circulation 101:2854–2862.PubMedCrossRefGoogle Scholar
  27. 27.
    Blobel CP, Wolfsberg TG, Turk CW, Myles DG, Primakoff P, White JM. 1992. A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature 356:248–252.PubMedCrossRefGoogle Scholar
  28. 28.
    Evans J, Schwartz R, Kopf G. 1995. Mouse sperm-egg plasma membrane interactions: Analysis of roles of egg integrins and the mouse sperm homologue of PH-30 (fertilin). J Cell Sci 108:3267–3278.PubMedGoogle Scholar
  29. 29.
    Snell WJ, White JM. 1996. The molecules of mammalian fertilization. Cell 85:629–637.PubMedCrossRefGoogle Scholar
  30. 30.
    Evans JP, Schultz RM, Kopf GS. 1998. Roles of the disintegrin domains of mouse fertilins alpha and beta in fertilization. Biol Reprod 59:145–152.PubMedCrossRefGoogle Scholar
  31. 31.
    Primakoff P, Hyatt H, Tredick-Kline J. 1987. Identification and purification of a sperm surface protein with a potential role in sperm-egg membrane fusion. J Cell Biol 104:141–149.PubMedCrossRefGoogle Scholar
  32. 32.
    Blobel CP, White JM. 1992. Structure, function and evolutionary relationship of proteins containing a disintegrin domain. Curr Opin Cell Biol 4:760–765.PubMedCrossRefGoogle Scholar
  33. 33.
    Myles DG, Kimmel LH, Blobel CP, White JM, Primakoff P. 1994. Identification of a binding site in the disintegrin domain of fertilin required for sperm-egg fusion. Proc Natl Acad Sci USA 91:4195–4198.PubMedCrossRefGoogle Scholar
  34. 34.
    Cho C, Bunch DO, Faure JE, Goulding EH, Eddy EM, Primakoff P, Myles DG. 1998. Fertilization defects in sperm from mice lacking fertilin β. Science 281:1857–1859.PubMedCrossRefGoogle Scholar
  35. 35.
    Almeida E, Huovila A-P, Sutherland AE, Stephens L, Calaraco P, Shaw L, Mercurio A, Sonnenberg A, Primakoff P, Myles DG. 1999. Mouse egg integrin α6βl functions as a sperm receptor. Cell 81:1095–1104.CrossRefGoogle Scholar
  36. 36.
    Chen MS, Almeida EA, Huovila A, Takahashi Y, Shaw LM, Mercurio AM, White JM. 1999. Evidence that distinct states of the integrin α6βl interact with laminin and an ADAM. J Cell Biol 144: 549–561.PubMedCrossRefGoogle Scholar
  37. 37.
    Zhang XP, Kamamata T, Yokoyama K, Puzon-McLaughlin W, Takada Y. 1998. Specific interaction of the recombinant disintegrin-like domain of MDC-15 (metargidin,ADAM-15) with integrin alphav-beta 3. J Biol Chem 273:7345–7350.PubMedCrossRefGoogle Scholar
  38. 38.
    Yagami-Hiromasa T, Sato T, Kurisaki T, Karnijo K, Nabeshima Y, Fujisawa-Sehara A. 1995. A metalloprotease-disintegrin participating in myoblast fusion. Nature 377:652–656.PubMedCrossRefGoogle Scholar
  39. 39.
    Bjarnason JB, Fox JW. 1995. Snake venom metalloendopeptidases: Reprolysins. Methods Enzymol 248:345–368.PubMedCrossRefGoogle Scholar
  40. 40.
    Tselepis VH, Green LJ, Humphries MJ. 1997. An RGD to LDV conversion within the disintegrin kistrin generates an integrin antagonist that retains potency but exhibits altered receptor specificity. J Biol Chem 272:21341–21348.PubMedCrossRefGoogle Scholar
  41. 41.
    Thiery JP, Duband JL, Trucker GC. 1985. Cell migration in the vertebrate embryo: Role of cell adhesion and tissue environment in pattern formation. Annu Rev Cell Biol 1:91–113.PubMedCrossRefGoogle Scholar
  42. 42.
    Rees DA, Couchman JR, Smith CG, Woods A, Wilson G. 1983. Cell-substratum interactions in the adhesion and locomotion of fibroblasts. Philosophical Trans Royal Soc London 299:169–176. 11–4–82.03Google Scholar
  43. 43.
    Potts JD, Dagle JM, Walder JA, Weeks DL, Runyan RB. 1991. Epithelial-mesenchymal transformation of embryonic cardiac endothelial cells is inhibited by a modified antisense oligodeoxynucleotide to transforming growth factor beta 3. Proc Nat Acad Sci USA 88:1516–1520.PubMedCrossRefGoogle Scholar
  44. 44.
    Potts JD, Vincent EB, Runyan RB, Weeks DL. 1992. Sense and antisense TGF beta 3 mRNA levels correlate with cardiac valve induction. Devel Dynamics 193:340–345.CrossRefGoogle Scholar
  45. 45.
    Schiro JA, Chan BMC, Roswit WT, Kassner PD, Pentland AP, Hemler ME, Eisen AZ, Kupper TS. 1991. Integrin α2β1 (VLA-2) mediates reorganization and contraction of collagen matrices by human cells. Cell 67:403–410.PubMedCrossRefGoogle Scholar
  46. 46.
    Carver W, Molano I, Reaves T, Borg TK, Terracio L. 1995. Role of the α1β1 integrin complex in collagen gel contraction in vitro. by heart fibroblasts. J Cell Physiol 165:425–437.PubMedCrossRefGoogle Scholar
  47. 47.
    Woessner JF. 1991. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154.PubMedGoogle Scholar
  48. 48.
    Werb Z. 1993. Proteinases and matrix degradation. Textbook of Rlieumatology. pp 248–264.Google Scholar
  49. 49.
    Birkedal-Hansen H, Moore WE, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A, Engler JA. 1993. Matrix metalloproteinases: A review Crit Rev Oral Biol Med 4:197–250.Google Scholar
  50. 50.
    McGuire PG, Orkin RW. 1992. Urokinase activity in the developing avian heart: a spatial and temporal analysis. Devel Dynamics 193:24–33.CrossRefGoogle Scholar
  51. 51.
    McGuire PG, Alexander SM. 1993. Inhibition of urokinase synthesis and cell surface binding alters the motile behavior of embryonic endocardial-derived mesenchymal cells in vitro.. Development 118:931–939.PubMedGoogle Scholar
  52. 52.
    Nakagawa W, Terracio L, Carver W, Birkedal-Hansen H, Borg TK. 1992. Expression of collagenase and IL-1 alpha in developing rat hearts. Devel Dynamics 195:87–99.CrossRefGoogle Scholar
  53. 53.
    Alexander SM, Jackson KJ, Bushnell KM, McGuire PG. 1997. Spatial and temporal expression of the 72-kDa type IV collagenase (MMP-2) correlates with development and differentiation of valves in the embryonic avian heart. Devel Dynamics 209:261—268.Google Scholar
  54. 54.
    Borg K, Burgess W, Terracio L, Borg TK. 1998. Expression of metalloproteases by cardiac myocytes and fibroblasts in vitro. Cardiovasc Pathol 6:261–269.CrossRefGoogle Scholar
  55. 55.
    Dettman RW, Denetclaw WJ, Ordahl CP, Bristow J. 1998. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Devel Biol 193:169–181.CrossRefGoogle Scholar
  56. 56.
    Gittenberger-de Groot AC, Vrancken PM, Mentink MM, Gourdie RG, Poelmann RE. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82:1043–1052.PubMedCrossRefGoogle Scholar
  57. 57.
    Nath D, Slocombe PM, Webster A, Stephens PE, Docherty AJP, Murphy G. 2000. Meltrin γ (ADAM-9) mediates cell adhesion through α6βl integrin, leading to a marked induction of fibroblast cell motility. J Cell Sci 113:2319–2328.PubMedGoogle Scholar
  58. 58.
    Horwitz A, Duggan K, Buck C, Becherle MC, Burridge K. 1986. Interaction of plasma membrane fibronectin receptor with talin- a transmembrane linkage. Nature 320:531–533.PubMedCrossRefGoogle Scholar
  59. 59.
    Otey CA, Pavalko FM, Burridge K. 1990. An interaction between α-actinin and the β integrin subunit in vitro.. J Cell Biol 111:721–729.PubMedCrossRefGoogle Scholar
  60. 60.
    Liliental J, Chang DD. 1998. Rack 1, a receptor for activated protein kinase C, interacts with integrin β subunit. J Biol Chem 273:2379–2383.PubMedCrossRefGoogle Scholar
  61. 61.
    Hemler MN. 1998. Integrin associated proteins. Curr Opin Cell Biol 10:578–585.PubMedCrossRefGoogle Scholar
  62. 62.
    Borg TK, Terracio L. 1990. Interaction of the extracellular matrix with cardiac myocytes during development and disease. In: (Robinson T, ed.) Issues in Biomedicine. Basel, Karger.Google Scholar
  63. 63.
    Iba K, Albrechtsen R, Gilpin BJ, Loechel F, Wewer UM. 1999. Cysteine-rich domain of human ADAM 12 (meltrin a) supports tumor cell adhesion. Amer J Pathol 154:1489–1501.CrossRefGoogle Scholar
  64. 64.
    Iba K, Albrechtsen, Gilpin B, Frohlich C, Loechel F, Zolkiewska A, Ishguro K, Kojima T, Liu W, Langford K, Sanderson RD, Brakebusch C, Fassler R, Wewer DM. 2000. The cysteine-rich domain of human ADAM 12 supports cell adhesion through syndecans and triggers signaling events that lead to β1 integrin-dependent cell spreading. J Cell Biol 149:1143–1155.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Thomas K. Borg
    • 1
  • Angela De Almeida
    • 1
  • Melissa Joy Loftis
    • 1
  • Alex McFadden
    • 1
  • Wayne Carver
    • 1
  1. 1.Department of Developmental Biology and Anatomy, School of MedicineUniversity of South CarolinaColumbiaUSA

Personalised recommendations