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Comparative Biology of the α2-Macroglobulin-Based Immune System

  • P. B. Armstrong
  • J. P. Quigley
Part of the Advances in Comparative and Environmental Physiology book series (COMPARATIVE, volume 24)

Abstract

Most multicellular organisms are subject during their lives to a nearly continual challenge by pathogenic microorganisms and multicellular parasites. In response, a variety of immune processes have evolved to suppress pathogens that have invaded the body. Some of these immune processes are phylogenetically unique. Perhaps the best-known example is the induced antibody response based on VDJ gene rearrangement of the immunoglobulin heavy and light chain genes, which apparently is present only in the vertebrates (Marchalonis and Schluter 1990). Other immune systems, such as the prophenoloxidase system (Söderhäll and Smith 1986), lysozyme (Engström et al. 1985), the pentraxins (Tennent et al. 1993), and α2-macroglobulin (Armstrong and Quigley 1995), are of more ancient origin, because they are present in modern representatives of diverse animal phyla. This chapter reviews the role of the α2-macroglobulin system in immunity.

Keywords

Horseshoe Crab Cytolytic Activity Comparative Biology Thiol Ester Glutamyl Residue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aimes RT, Quigley JP, Swarnakar S, Strickland DK, Armstrong PB (1995) Preliminary investigations on the scavenger receptors of the amebocyte of the American horseshoe crab, Limulus polyphemus. Biol Bull 189 (in press)Google Scholar
  2. Andersen GR, Jacobsen L, Thirup S, Nyborg J, Sottrup-Jensen L (1991) Crystallization and preliminary X-ray analysis of methylamine-treated α2-macroglobulin and 3 α2-macro-globulin-proteinase complexes. FEBS Lett 292: 267–270PubMedGoogle Scholar
  3. Andersen GR, Thirup S, Nyborg J, Dolmer K, Jacobsen L, Sottrup-Jensen L (1994) Low-resolution X-ray diffraction data obtained from hexagonal crystals of methylamine-treated α2-macroglobulin. Acta Cryst D50: 298–301Google Scholar
  4. Andreasen PA, Sottrup-Jensen L, Kjøller L, Nykjaer A, Moestrup SK, Petersen CM, Gliemann J (1994) Receptor-mediated endocytosis of plasminogen activators and activator/inhibitor complexes. FEBS Lett 338: 239–245PubMedGoogle Scholar
  5. Arakawa H, Urisaka T, Tsuruta H, Amemiya Y, Kihara H, Ikai A (1994) The kinetics of conformational changes of α2-macroglobulin determined by time resolved X-ray solution scattering. FEBS Lett 337: 171–174PubMedGoogle Scholar
  6. Armstrong PB, Quigley JP (1987) Limulus α2-macroglobulin. First evidence in an invertebrate for a protein containing an internal thiol ester bond. Biochem J 248: 703–707PubMedGoogle Scholar
  7. Armstrong PB, Quigley JP (1992) Humoral immunity: α2-macroglobulin activity in the plasma of mollusks. Veliger 35: 161–164Google Scholar
  8. Armstrong PB, Quigley JP (1995) Immune function of α2-macroglobulin in invertebrates. Prog Mol Subcell Biol. Springer, Berlin Heidelberg New York (in press)Google Scholar
  9. Armstrong PB, Rossner MT, Quigley JP (1985) An α2-macroglubulin-like in the blood of chelicerate and mandibulate arthropods. J Exp Zool 236: 1–9PubMedGoogle Scholar
  10. Armstrong PB, Mangle WF, Wall JS, Hainfield JF, Van Holde KE, Ikai A, Quigley JP (1991) Structure of Limulus α2-macroglobulin. J Biol Chem 266: 2526–2530PubMedGoogle Scholar
  11. Armstrong PB, Armstrong MT, Quigley JP (1993) Characterization of a complement-like hemolytic system in the arthropod, Limulus polyphemus: involvement of a2-macroglobulin and C-reactive protein. Mol Immunol 30: 929–934PubMedGoogle Scholar
  12. Armstrong PB, Misquith S, Srimal S, Melchior R, Quigley JP (1994a) Identification of limulin as a major cytolytic protein in the plasma of the American horseshoe crab, Limulus polyphemus. Biol Bull 187: 227–228PubMedGoogle Scholar
  13. Barrett AJ, Brown MA, Sayers CA (1979) The electrophoretically “slow” and “fast” forms of the α2-macroglobulin molecule. Biochem J 181: 401–418PubMedGoogle Scholar
  14. Barrett AJ, Starkey PM (1973) The interaction of α2-macroglobulin with proteinases. Characteristics and specificity of the reaction and a hypothesis concerning its molecular mechanism. Biochem J 133: 709–724PubMedGoogle Scholar
  15. Bender RC, Fryer SE, Bayne CK (1992) Proteinase inhibitory activity in the plasma of a mollusc. Evidence for the presence of α2-macroglobulin. Comp Biochem Physiol B102: 821–824Google Scholar
  16. Beith J, Pichoir M, Metais P (1970) The influence of α2-macroglobulin on the elastolytic and esterolytic activity of elastase. FEBS Lett 8: 319–321Google Scholar
  17. Bjork I, Fish WW (1982) Evidence for similar conformational changes in α2-macroglobulin on reaction with primary amines or proteolytic enzymes. Biochem J 207: 347–356PubMedGoogle Scholar
  18. Borth W (1992) α2-Macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J 6: 3345–3353PubMedGoogle Scholar
  19. Borth W, Luger TA (1989) Identification of α2-macroglobulin as a cytokine binding plasma protein. Binding of interleukin-1β to “F” α2-macroglobulin. J Biol Chem 264: 5818–5825PubMedGoogle Scholar
  20. Canicatti C (1990) Hemolysins: pore-forming proteins in invertebrates. Experientia 46: 239–244PubMedGoogle Scholar
  21. Chen BJ, Wang D, Yuan Al, Feinman RD (1992) Structure of α2-macroglobulin-protease complexes. Methylamine competition shows that proteases bridge two disulfide-bonded half molecules. Biochemistry 31: 8960–8966Google Scholar
  22. Christensen U, Simonsen M, Harrit N, Sottrup-Jensen L (1989) Pregnancy zone protein, a proteinase-binding macroglobulin. Interactions with proteinase and methylamine. Biochemistry 28: 9324–9331PubMedGoogle Scholar
  23. Comfort A (1961) The life span of animals. Sci Am 205 (2): 108–119PubMedGoogle Scholar
  24. Davidsen O, Christensen EI, Gliemann J (1985) The plasma clearance of human α2-macro- globulin-trypsin complexes in the rat is mainly accounted for by uptake into hepatocytes. Biochim Biophys Acta 846: 85–92PubMedGoogle Scholar
  25. Delain E, Pochon F, Barray M, Van Leuven F (1992) Ultrastructure of alpha 2-macroglobulins. Electron Microsc Rev 5: 231–281PubMedGoogle Scholar
  26. Devriendt K, van den Berghe H, Cassiman J-J, Marynen P (1991) Primary structure of pregnancy zone protein. Molecular cloning of a full length PZP cDNA clone by the polymerase chain reaction. Biochim Biophys Acta 1088: 95–103PubMedGoogle Scholar
  27. Enghild JJ, Salvesen G, Thøgersen IB, Pizzo SV (1989a) Proteinase-binding and inhibition by the monomeric α-macroglobulin rat α-inhibitor-3. J Biol Chem 264: 11428–11435PubMedGoogle Scholar
  28. Enghild JI, Thøgersen IB, Roche PA, Pizzo SV (1989b) A conserved region in α-macroglobulins participates in binding to the mammalian α-macroglobulin receptor. Biochemistry 28: 1406–1412PubMedGoogle Scholar
  29. Enghild JJ, Salvesen G, Brew K, Nagase H (1989c) Interaction of human rheumatoid synovial collagenase (matrix metalloproteinase 1) and stromolysin (matrix metalloproteinase 3)with human α2-macroglobulin and chicken ovostatin. Binding kinetics and identification of matrix metalloproteinase cleavage sites. J Biol Chem 264: 8779–8785PubMedGoogle Scholar
  30. Engstrom Å, Xanthopoulos K, Boman HG, Bennich H (1985) Amino acid and cDNA sequences of lysozyme from Halophora cecropia. EMBO J 4: 2119–2122PubMedGoogle Scholar
  31. Feldman SR, Pizzo SV (1984) Comparison of the binding of chicken α2-macroglobulin and ovomacroglobulin to the mammalian α2-macroglobulin receptor. Arch Biochem Biophys 235: 267–275PubMedGoogle Scholar
  32. Finch CE (1990) Longevity, senescence and the genome. The University of Chicago Press, Chicago, 922 pp + xvGoogle Scholar
  33. Furie B, Furie BC (1992) Molecular and cellular biology of blood coagulation. N Engl J Med 326: 800–806PubMedGoogle Scholar
  34. Gliemann J, Larsen TR, Sottrup-Jensen L (1983) Cell association and degradation of a2- macroglobulin-trypsin complexes in hepatocytes and adipocytes. Biochim Biophys Acta 756: 230– 237PubMedGoogle Scholar
  35. Gonias SL (1992) α2-Macroglobulin: a protein at the interface of fibrinolysis and cellular growth regulation. Exp Hematol 20: 302–311PubMedGoogle Scholar
  36. Gonias SL, Reynolds JA, Pizzo SV (1982) Physical properties of human α2-macroglobulin following reaction with methylamine and trypsin. Biochim Biophys Acta 705: 306–314PubMedGoogle Scholar
  37. Grenningloh G, Bieber AJ, Rehm EJ, Snow PM, Tarquina ZR, Hortsch M, Patel NH, Goodman CS (1990) Molecular genetics of neuronal recognition in Drosophila. Evolution and function of immunoglobulin superfamily cell adhesion molecules. Cold Spring Harbor Symp Quant Biol 55: 327–340PubMedGoogle Scholar
  38. Hall M, Söderhäll K, Sottrup-Jensen L (1989) Amino acid sequence around the thiolester of α2-macroglobulin from plasma of the crayfish, Pacifastacus leniusculus. FEBS Lett 254: 111–114PubMedGoogle Scholar
  39. Hall PK, Roberts RC (1978) Physical and chemical properties of human plasma α20-macro-globulin. Biochem J 173: 27–38PubMedGoogle Scholar
  40. Harpel PC (1973) Studies on human plasma α2-macroglobulin-enzyme interactions. Evidence for proteolytic modification of the subunit chain structure. J Exp Med 138: 508–521PubMedGoogle Scholar
  41. Havermann K, Janoff A (1978) Neutral proteases of human polymorphonuclear leukocytes. Urbran and Schwarzenberg, BaltimoreGoogle Scholar
  42. Hergenhahn HG, Aspan A, Söderhäll K (1987) Purification and characterization of a high-Mr proteinase inhibitor of prophenoloxidase activation from crayfish plasma. Biochem J 248: 223–228PubMedGoogle Scholar
  43. Hergenhahn HG, Hall M, Söderhäll K (1988) Purification and characterization of an α2-macroglobulin-likeproteinase inhibitor from plasma of the crayfish Pacifastacus leniusculus. Biochem J 255: 801–806PubMedGoogle Scholar
  44. Huang JS, Huang SS, Deuel TF (1984) Specific covalent binding of platelet derived growth factor to human plasma α2-macroglobulin. Proc Natl Acad Sci USA 81: 342–347PubMedGoogle Scholar
  45. Hussain MM, Maxfield FR, Más-Oliva J, Tabas I, Ji Z-S, Innerarity TL, Mahley RW (1991) Clearance of chylomicron remnants by the low density lipoprotein receptor-related protein/α2-macroglobulin receptor. J Biol Chem 266: 13936–13940PubMedGoogle Scholar
  46. Ikai A, Ditamoto T, Nishigai M (1983) Alpha-2-macroglobulin-like protease inhibitor from the egg white of Cuban crocodile (Crocodylas rhombifer). J Biochem (Tokyo) 93: 121–127Google Scholar
  47. Ikai A, Kiruchi M, Nishigai M (1990) Interval structure of ovomacroglobulin studied by electron microscopy. J Biol Chem 265: 8280–8284PubMedGoogle Scholar
  48. Iwanaga S, Miyata T, Tokunaga F, Muta T (1992) Molecular mechanism of hemolymph clotting system in Limulus. Thromb Res 68: 1–32PubMedGoogle Scholar
  49. James K (1990) Interactions between cytokines and α2-macroglobulin. Immunol Today 11: 163–167PubMedGoogle Scholar
  50. Jiang H, Siegel JN, Gewurz H (1991) Binding and complement activation by C-reactive protein via the collagen-like region of Clq and inhibition of these reactions by monoclonal antibodies to C-reactive protein and Clq. J Immunol 146: 2324–2330PubMedGoogle Scholar
  51. Kitano T, Nakashima M, Ikai A (1982) Hen egg white ovomacroglobulin has a protease inhibitory activity. J Biochem 92: 1679–1682Google Scholar
  52. Kristensen T, Moestrup SK, Gliemann J, Bendtsen L, Sand O, Sottrup-Jensen L (1990) Evidence that the newly cloned low-density-lipporotein receptor related protein (LRP) is the α2-macroglobulin receptor. FEBS Lett 276: 151–155PubMedGoogle Scholar
  53. Laskowski M, Kato I (1980) Protein inhibitors of proteases. Annu Rev Biochem 49: 593–626PubMedGoogle Scholar
  54. Law SK, Levine RP (1977) Interaction between the third complement protein and cell surface macromolecules. Proc Natl Acad Sci USA 74: 2701–2705PubMedGoogle Scholar
  55. Law SK, Reid KBM (1988) Complement. IRL Press, Oxford, 72 ppGoogle Scholar
  56. Liang Z, Lindblad P, Beauvais A, Johansson MW, Latage J-P, Hall M, Cerenius L, Söderhäll K (1992) Crayfish α2-macroglobulin and 76 kDa protein; their biosynthesis and subcellular localization of the 76kDa protein. J Insect Physiol 38: 987–995Google Scholar
  57. Marchalonis JJ, Schluter SF (1990) Origins of immunoglobulins and immune recognition molecules. Bioscience 40: 758–768Google Scholar
  58. McKerrow JH, Sun E, Rosenthal PJ, Bouvier J (1993) The proteases and pathogenicity of parasitic protozoa. Annu Rev Microbiol 47: 821–853PubMedGoogle Scholar
  59. Miyazawa K, Inoue K (1990) Complement activation induced by human C-reactive protein in mildly acidic conditions. J Immunol 145: 650–654PubMedGoogle Scholar
  60. Melchior R, Quigley JP, Armstrong PB (1995) α2-Macroglobulin-mediated clearance of proteases from the plasma of the American horseshoe crab, Limulus polyphemus. J Biol Chem (in press)Google Scholar
  61. Nagase H, Harris ED (1983) Ovostatin: a novel proteinase inhibitor from chicken egg white II. Mechanism of inhibition studied with collagenase and thermolysin. J Biol Chem 258: 7490–7498PubMedGoogle Scholar
  62. Nagase J, Harris ED, Woessner JF, Brew K (1983) Ovostatin: a novel proteinase inhibitor from chicken egg white I. Purification, physicochemical properties and tissue distribution of ovostatin. J Biol Chem 258: 7481–7489PubMedGoogle Scholar
  63. Nielsen KL, Sottrup-Jensen L, Nagase H, Thögersen HC, Etzerodt M (1994) Amino acid sequence of hen ovomacroglobulin (ovostatin) deduced from cloned cDNA. DNA Sequencing 5: 111 - 119Google Scholar
  64. Nykjaer A, Bengtsson-Olivecrona G, Lookene A, Moestrup SK, Petersen CM, Weber W, Beisiegel U, Gliemann J (1993) The α2-macroglobulin receptor/low density lipoprotein receptor-related protein binds lipoprotein lipase and β-migrating very low density lipoprotein associated with the lipase. J Biol Chem 268: 15048–15055PubMedGoogle Scholar
  65. O’Connor-Court MD, Wakefield LM (1987) Latent transforming growth factor-β in serum. J Biol Chem 262: 14090–14099Google Scholar
  66. Ogata H, Kouyoumdjian M, Borges DR (1993) Comparison between clearance rates of plasma kallikrein and of plasma kallikrein-α2-macroglobulin complexes by the liver. Int J Biochem 25: 1047–1051PubMedGoogle Scholar
  67. Ohlsson K (1971) Elimination of [125]-trypsin α2-macroglobulin complexes from blood by the reticuloendothelial cells in dog. Acta Physiol Scand 81: 269–272PubMedGoogle Scholar
  68. Osada T, Nishigai M, Ikai A (1986) Open quaternary structure of the hagfish proteinase inhibitor with similar properties to human α2-macroglobulin. J Ultrastruct Mol Struct Res 96: 136–145PubMedGoogle Scholar
  69. Perlmutter DH, Pierce JA (1989) The α1-antitrypsin gene and emphysema. Am J Physiol 257: L147–L162PubMedGoogle Scholar
  70. Quigley JP, Armstrong PB (1983) An endopeptidase inhibitor, similar to mammalian α 2- macroglobulin, detected in the hemolymph of an invertebrate, Limulus polyphemus. J Biol Chem 258: 7903–7906PubMedGoogle Scholar
  71. Quigley JP, Armstrong PB (1985) A homologue of α2-macroglobulin purified from the hemolymph of the horseshoe crab Limulus. J Biol Chem 260: 12715–12719PubMedGoogle Scholar
  72. Quigley JP, Armstrong PB, Gallant P, Rickles FR, Troll W (1982) An endopeptidase inhibitor, similar to vertebrate α2-macroglobulin, present in the plasma of Limulus polyphemus. Biol Bull 163: 402Google Scholar
  73. Quigley JP, Ikai A, Arakawa H, Osada T, Armstrong PB (1991) Reaction of proteinases with α2-macroglobulin from the American horseshoe crab, Limulus. J Biol Chem 266: 19426–19431PubMedGoogle Scholar
  74. Reid KBM, Porter RR (1981) The proteolytic activation systems of complement. Annu Rev Biochem 50: 433–464PubMedGoogle Scholar
  75. Runnegar B (1982) The Cambrian explosion: animals or fossils? J Geol Soc Aust 29: 395–411Google Scholar
  76. Salvesen GS, Sayers CA, Barrett AJ (1981) Further characterization of the covalent linking reaction of α2-macroglobulin. Biochem J 195: 453–461PubMedGoogle Scholar
  77. Sepkoski JJ (1978) A kinetic model of phanerozoic taxonomic diversity I. Analysis of marine orders. Paleobiology 4: 223–251Google Scholar
  78. Söderhäll K, Smith VJ (1986) Prophenoloxidase-activating cascade as a recognition and defense system in arthropods, In: Gupta AP (ed) Hemocytic and humoral immunity in arthropods. Wiley, New York, pp 251–285Google Scholar
  79. Sottrup-Jensen L (1987) α2-Macroglobulin and related thiol ester plasma proteins. In: Putnam FW (ed) The plasma proteins. Structure, function, and genetic control, 2nd edn, vol 5. Academic Press, Orlando, pp 191–291Google Scholar
  80. Sottrup-Jensen L, Petersen TE, Magnusson S (1980) A thiol-ester in α2-macroglobulin cleaved during proteinase complex formation. FEBS Lett 121: 275–279PubMedGoogle Scholar
  81. Sottrup-Jensen L, Lonblad PB, Stephanik TM, Peterson TE, Magnusson S, Jornvall H (1981) Primary structure of the “bait” region for proteinases in α2-macroglobulin. Nature of the complex. FEBS Lett 127: 167–173PubMedGoogle Scholar
  82. Sottrup-Jensen L, Gliemann J, Van Leuven F (1986) Domain structure of human α2-macro-globulin. Characterization of a receptor-binding domain obtained by digestion with papain. FEBS Lett 205: 20–24PubMedGoogle Scholar
  83. Sottrup-Jensen L, Sand O, Dristensen L, Fey GH (1989) The α;2;-macroglobulin bait region. Sequence diversity and localization of cleavage sites for proteinases in five mammalian α;2;-macroglobulins. J Biol Chem 264: 15781–15789PubMedGoogle Scholar
  84. Sottrup-Jensen L, Borth W, Hall M, Quigley JP, Armstrong PB (1990a) Sequence similarity between α;2;-macroglobulin from the horseshoe crab, Limulus polyphemus, and proteins of the α;2;-macroglobulin family from mammals. Comp Biochem Physiol 96B: 621–625Google Scholar
  85. Sottrup-Jensen L, Hansen JF, Pedersen HS, Kristensen L (1990b) Localization of lysyl-γ-glutamyl cross-links in five human α;2;-macroglobulin-proteinase complexes.Nature of the high molecular weight cross-linked products. J Biol Chem 265: 17727–17737PubMedGoogle Scholar
  86. Sporn MB, Roberts AB (1990) Peptide growth factors, vols I and I I. Springer, Berlin Heidelberg New YorkGoogle Scholar
  87. Spycher SE, Arya S, Isenman DE, Painter H (1987) A functional, thioester-containing α2-macroglobulin homologue isolated from the hemolymph of the American lobster (Homarus americanus). J Biol Chem 262: 14606–14611PubMedGoogle Scholar
  88. Srimal S. Quigley JP, Armstrong PB (1993) Limulin and C-reactive protein from the plasma of Limulus polyphemus are different proteins. Biol Bull 185: 325Google Scholar
  89. Starkey PM, Barrett AJ (1977) α2-Macroglobulin, a physiological regulator of proteinase activity. In: Barrett AJ (ed) Proteinases in mammalian cells and tissues. Elsevier, Amsterdam, pp 663–696Google Scholar
  90. Starkey PM, Barrett AJ (1982) Evolution of α2-macroglobulin. The demonstration in a variety of vertebrate species of a protein resembling human α2-macroglobulin. Biochem J 205: 91–95PubMedGoogle Scholar
  91. Steinbuch M, Pejaudier L, Quentin M, Martin V (1968) Molecular alteration of α2-macro-globulin by aliphatic amines. Biochim Biophys Acta 154: 228–231PubMedGoogle Scholar
  92. Strickland DK, Ashcom JD, Williams S, Burgess WH, Migliorini M, Argraves WS (1990) Sequence identity between the α2-maeroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem 265: 17401–404PubMedGoogle Scholar
  93. Swenson RP, Howard JB (1979) Characterization of alkylamine-sensitive site in α2-macro-globulin. Proc Natl Acad Sci USA 76: 4313–4316PubMedGoogle Scholar
  94. Tack BF (1983) The β-Cys-γ -Glu thiolester bond in human C3, C4 and α2-macroglobulin. Springer Semin Immunopathol 6: 259-282PubMedGoogle Scholar
  95. Tack BF, Harrison RA, Janatova J, Thomas ML, Prahl JW (1980) Evidence for presence of an internal thiolester bond in third component of human complement. Proc Natl Acad Sci USA 77: 5764–5768PubMedGoogle Scholar
  96. Tennent GA, Butler PJG, Hutton T, Woolfitt AR, Harvey DJ, Rademacher TW, Pepys MB (1993) Molecular characterization of Limulus polyphemus C-reactive protein. 1. Subunit composition. Eur J Biochem 214: 91–97PubMedGoogle Scholar
  97. Testa JE, Quigley JP (1990) The role of urokinase-type plasminogen activator in aggressive tumor cell behavior. Cancer Metast Rev 9: 353–367Google Scholar
  98. Thøgersen IB, Salvesen G, Brucato FH, Pizzo SV, Enghild JJ (1992) Purification and characterization of an α-macroglobulin proteinase inhibitor from the mollusc Octopus vulgaris. Biochem J 285: 521–527PubMedGoogle Scholar
  99. Travis J, and Salvesen GS (1983) Human plasma proteinase inhibitors. Annu Rev Biochem 52: 655–709PubMedGoogle Scholar
  100. Van Dijk MCM, Boers W, Linthorst C, van Berkel TJC (1992) Role of the scavenger receptor in the uptake of methylamine-activated α2-macroglobulin by rat liver. Biochem J 287: 447–455PubMedGoogle Scholar
  101. Van Leuven F (1984) Human α2-macroglobulin. Primary amines and the mechanisms of endoprotease inhibition and receptor-mediated endocytosis. Mol Cell Biochem 58: 121–128PubMedGoogle Scholar
  102. Van Leuven F, Cassiman J-J, Van Den Berghe J (1981) Functional modifications of α2-macroglobulin by primary amines II. Inhibition of covalent binding of trypsin to α2M by methylamine and other primary amines. J Biol Chem 256: 9023–9027PubMedGoogle Scholar
  103. Van Leuven F, Marynen P, Sottrup-Jensen L, Cassiman J-J, Van Den Berghe H (1986) Receptor-binding domain of human α2-macroglobulin. Isolation after limited proteolysis with a bacterial proteinase. J Biol Chem 261: 11369–11373PubMedGoogle Scholar
  104. Vu T-K, Hung DT, Wheaton VI, Coughlin SR (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64: 1057–1068PubMedGoogle Scholar
  105. Waldman TA (1988) Immunodeficiency diseases. In: Samter M, Talmage DW, Frank MM, Austen KF, Claman HN (eds) Immunological diseases, 4th edn. Little, Brown & Co, Boston, pp 411–465Google Scholar
  106. Werb Z (1993) Proteases and matrix degradation. In: Kelley WN, Harris ED, Ruddy S, Sledge CB (eds) Textbook of rheumatology, 4th edn. Saunders, Philadelphia, pp 300–321Google Scholar
  107. Wu K, Wang D, Feinman RD (1981) Inhibition of proteases by α2-macroglobulin. The role of lysyl amino groups of trypsin in covalent complex formation. J Biol Chem 256: 10409–10414PubMedGoogle Scholar
  108. Yochem J, Greenwald I (1993) A gene for a low density lipoprotein-related protein in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 90: 4572–4576PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • P. B. Armstrong
    • 1
    • 2
  • J. P. Quigley
    • 2
    • 3
  1. 1.Department of Molecular and Cellular BiologyUniversity of CaliforniaDavisUSA
  2. 2.Marine Biological LaboratoryWoods HoleUSA
  3. 3.Department of Pathology, Health Sciences CenterState University of New YorkUSA

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