An antimicrobial peptide tachyplesin acts as a secondary secretagogue and amplifies lipopolysaccharide-induced hemocyte exocytosis

FEBS Journal

Volumn 272, Issue 15, 2005, Pages 3863-3871

  Ozaki, Aya ^a   Ariki, Shigeru ^a   Kawabata, Shun Ichiro ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Exocytosis; Horseshoe crab; Innate immunity; Secretagogue; Tachyplesin

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; BACTERIUM LIPOPOLYSACCHARIDE; MASTOPARAN; PERTUSSIS TOXIN; PHOSPHOLIPASE C INHIBITOR; TACHYPLESIN;

ARTICLE; BLOOD CELL; CELL DENSITY; CELL SECRETION; CONTROLLED STUDY; DRUG PROTEIN BINDING; EXOCYTOSIS; FEEDBACK SYSTEM; INNATE IMMUNITY; LIMULUS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CATTLE; DNA-BINDING PROTEINS; EXOCYTOSIS; GTP-BINDING PROTEINS; HEMOCYTES; HORSESHOE CRABS; LIPOPOLYSACCHARIDES; PEPTIDES; PEPTIDES, CYCLIC; SIGNAL TRANSDUCTION; WASP VENOMS;

BOVINAE; MEROSTOMATA;

EID: 23644449048     PISSN: 1742464X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04800.x     Document Type: Article

References (53)

1. Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harbor Symp Quant Biol 54, 1-13.
2. Hoffmann JA, Kafatos FC, Janeway CA & Ezekowitz RAB (1999) Phylogenetic perspectives in innate immunity. Science 284, 1313-1318.
3. Lemaitre B, Nicolas E, Michaut L, Reichhart JM & Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983.
4. Medzhitov R, Preston-Hurlburt P & Janeway CA Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388, 394-397.
5. Anderson KV & Nüsslein-Volhard C (1984) Information for the dorsal-ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature 311, 223-227.
6. Ligoxygakis P, Pelte N, Hoffmann JA & Reichhart JM (2002) Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 297, 114-116.
7. Levashina EA, Langley E, Green C, Gubb D, Ashburner M, Hoffmann JA & Reichhart JM (1999) Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila. Science 285, 1917-1919.
8. Leulier F, Parquet C, Pili-Floury S, Ryu J-H, Caroff M, Lee W-J, Mengin-Lecreulx D & Lemaitre B (2003) The Drosophila immune system detects bacteria through specific peptideglycan recognition. Nat Immunol 4, 478-484.
9. Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T & Kurata S (2002) Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc Natl Acad Sci USA 99, 13705-13710.
10. Akira S, Takeda K & Kaisho T (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2, 675-680.
11. Rowley AF & Ratcliffe NA (1981) Insects. In Invertebrate Blood Cells 2 (Ratcliffe NA & Rowley AF, eds), pp. 421-488. Academic Press, London.
12. Iwanaga S, Kawabata S & Muta T (1998) New types of clotting factors and defense molecules found in horse-shoe crab hemolymph: their structures and functions. J Biochem 123, 1-15.
13. Kawabata S, Osaki T & Iwanaga S (2003) Innate immunity in the horseshoe crab. In Infectious Disease: Innate Immunity (Ezekowitz RAB & Hoffman JA, eds), pp. 109-125. Humana Press, New Jersey.
14. Kawabata S & Tsuda R (2002) Molecular basis of non-self recognition by the horseshoe crab tachylectins. Biochim Biophys Acta 1572, 414-421.
15. Levin J & Bang FB (1964) Roll of endotoxin in extracellular coagulation of limulus blood. Bull Johns Hopkins Hosp 115, 265-274.
16. Armstrong PB (1985) Adhesion and motility of the blood cells of Limulus. In: Blood Cells of Marine Invertebrates: Experimental Systems in Cell Biology and Comparative Physiology (Cohen WD, ed), pp. 77-124. Alan R. Liss, New York.
17. Ariki S, Koori K, Osaki T, Motoyama K, Inamori K & Kawabata S (2004) A serine protease zymogen functions as a pattern-recognition receptor for lipopolysaccharides. Proc Natl Acad Sci USA 101, 953-958.
18. Inamori K, Ariki S & Kawabata S (2004) A toll-like receptor in horseshoe crabs. Immunol Rev 198, 106-115.
19. Bell JK, Mullen GED, Leifer CA, Mazzoni A, Davies DR & Segal DM (2003) Leucine-rich repeats and pathogen recognition in toll-like receptors. Trends Immunol 24, 528-533.
20. Nakamura T, Tokunaga F, Morita T, Iwanaga S, Kusumoto S, Shiba T & Inoue K (1988) Intracellular serine-protease zymogen, factor C, from horseshoe crab hemocytes. Its activation by synthetic lipid A analogues and acidic phospholipids. Eur J Biochem 176, 89-94.
21. Nakamura T, Furunaka H, Miyata T, Tokunaga F, Muta T & Iwanaga S (1988) Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horse-shoe crab (Tachypleus tridentatus). J Biol Chem 263, 16709-16713.
22. Higashijima T, Uzu S, Nakajima T & Ross EM (1988) Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J Biol Chem 263, 6491-6494.
23. o by mastoparan, related amphiphilic peptides, and hydrophobic amines. J Biol Chem 265, 14176-14186.
24. Kawano K, Yoneya T, Miyata T, Yoshikawa K, Tokunaga F, Terada Y & Iwanaga S (1990) Antimicrobial peptide, tachyplesin I, isolated from hemocytes of the horseshoe crab (Tachypleus tridentatus). J Biol Chem 265, 15365-15367.
25. Nagai T, Osaki T & Kawabata S (2001) Functional conversion of hemocyanin to phenoloxidase by horse-shoe crab antimicrobial peptides. J Biol Chem 276, 27166-27170.
26. Kawabata S, Nagayama R, Hirata M, Shigenaga T, Agarwala KL, Saito T, Cho J, Nakajima H, Takagi T & Iwanaga S (1996) Tachycitin, a small granular component in horseshoe crab hemocytes, is an antimicrobial protein with chitin-binding activity. J Biochem 120, 1253-1260.
27. Saito T, Kawabata S, Shigenaga T, Takayenoki Y, Cho J, Nakajima H, Hirata M & Iwanaga S (1995) A novel big defensin identified in horseshoe crab hemocytes: isolation, amino acid sequence, and antimicrobial activity. J Biochem 117, 1131-1137.
28. Holmblad T & Söderhäll K (1999) Cell adhesion molecules and antioxidative enzymes in a crustacean, possible role in immunity. Aquaculture 172, 111-123.
29. Kobayashi M, Johansson MW & Söderhäll K (1990) The 76 kD cell-adhesion factor from crayfish haemocytes promotes encapsulation in vitro. Cell Tissue Res 260, 13-18.
30. Sacca R, Cuff CA & Ruddle NH (1997) Mediators of inflammation. Curr Opin Immunol 9, 851-857.
31. Luster AD (2002) The role of chemokines in linking innate and adaptive immunity. Curr Opin Immunol 14, 129-135.
32. Basset A, Khush RS, Braun A, Gardan L, Boccard F, Hoffmann JA & Lemaitre B (2000) The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci USA 97, 3376-3381.
33. Hirai Y, Kuwada M, Yasuhara T, Yoshida H & Nakajima T (1979) A new mast cell degranulating peptide 'mastoparan' in the venom of Vespula lewisii. Chem Pharm Bull 27, 1942-1944.
34. Jones PM, Mann FM, Persaud SJ & Wheeler-Jones CPD (1993) Mastoparan stimulates insulin secretion from pancreatic β-cells by effects at a late stage in thesecretory pathway. Mol Cell Endocrinol 94, 97-103.
35. 2+-independent late site in stimulus-secretion coupling. J Biol Chem 268, 23297-23306.
36. Ozaki Y, Maysumto Y, Yatomi Y, Higashihara M, Kariya T & Kume S (1990) Mastoparan, a wasp venom, activates platelets via pertussis toxin-sensitive GTP-binding proteins. Biochem Biophys Res Commun 170, 779-785.
37. Wheeler-Jones CPD, Saermark T, Kakkar VV & Authi KS (1991) Activation of human platelets by mastoparan. Biochem Soc Trans 19, 114S.
38. Wheeler-Jones CPD, Saermark T, Kakkar VV & Authi KS (1992) Mastoparan promotes exocytosis and increase intracellular cyclic AMP in human platelets. Biochem J 281, 465-472.
39. Norgauer J, Eberle M, Lemke HD & Aktories K (1992) Activation of human neutrophils by mastoparan. Biochem J 282, 393-397.
40. Joyce-Brady M, Rubins JB, Panchenko MP, Bernardo J, Steele MP, Kolm L, Simons ER & Dickey BF (1991) Mechanisms of mastoparan-stimulated surfactant secretion from isolated pulmonary alveolar type 2 cells. J Biol Chem 266, 6859-6865.
41. i. J Biol Chem 265, 11044-11049.
42. Tanaka T, Kohno T, Konoshita S, Mukai H, Itoh H, Ohya M, Miyazawa T, Higashijima T & Wakanatsu K (1998) α helix content of G protein α subunit is decreased upon activation by receptor mime tics. J Biol Chem 273, 3247-3252.
43. Ferry X, Brehin S, Kamel R & Landry Y (2002) G protein-dependent activation of mast cell by peptides and basic secretagogues. Peptide 23, 1507-1515.
44. Befus AD, Mowat C, Gilchrist M, Hu J, Solomon S & Bateman A (1999) Neutrophil defensins induce histamine secretion from mast cells: mechanisms of action. J Immunol 163, 947-953.
45. Mousli M, Bueb J, Bronner C, Rouot B & Landry Y (1990) G protein activation: a receptor-independent mode of action for cationic amphiphilic neuropeptides and venom peptides. Trends Pharma Sci 11, 358-362.
46. Ayabe T, Satchell DP, Willson CL, Parks WC, Selsted ME & Ouellette AJ (2000) Secretion of microbial α-defensins by intestinal paneth cells in response to bacteria. Nat Immunol 1, 113-118.
47. 2+-activated, intermediate conductance potassium chanel. J Biol Chem 277, 3793-3800.
48. Porter EM, Bevins CL, Ghosh D & Ganz T (2002) The multifaceted paneth cell. Cell Mol Life Sci 59, 156-170.
49. Lin PW, Simon PO, JrGewirtz AT, Neish AS, Ouellette AJ, Madara JL & Lencer WI (2004) Paneth cell cryptidins act in vitro as apical paracrine regulators of the innate inflammatory response. J Biol Chem 279, 19902-19907.
50. Lencer WI, Cheung G, Currie MG, Ouellette AJ, Selsted ME & Madra JL (1997) Induction of epithelial chloride secretion by channel-forming cryptdins 2 and 3. Proc Natl Acad Sci USA 94, 8585-8589.
51. Shigenaga T, Takayenoki Y, Kawasaki S, Seki N, Muta T, Toh Y, Ito A & Iwanaga S (1993) Separation of large and small granules from horseshoe crab (tachypleus tridentatus) hemocytes and characterization of their components. J Biochem 114, 307-316.
52. Inamori K, Saito T, Iwaki D, Nagira T, Iwanaga S, Arisaka F & Kawabata S (1999) A newly identified horseshoe crab lectin with specificity for blood group A antigen recognizes specific O-antigens of bacterial lipopolysaccharides. J Biol Chem 274, 3272-3278.
53. Patthy L & Smith EL (1975) Identification of functional arginine residues in ribonuclease A and lysozyme. J Biol Chem 250, 565-569.