Interaction with calmodulin is important for the secretion of thimet oligopeptidase following stimulation

FEBS Journal

Volumn 276, Issue 16, 2009, Pages 4358-4371

  Russo, Lilian C ^a   Goñi, Camila N ^a   Castro, Leandro M ^a   Asega, Amanda F ^b   Camargo, Antonio C M ^b   Trujillo, Cleber A ^a   Ulrich, Henning ^a   Glucksman, Marc J ^c   Scavone, Cristoforo ^a   Ferro, Emer S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

^c ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

14 3 3 ; Calmodulin; Protein kinase A; Protein protein interaction; Unconventional secretion

Indexed keywords

CALCIMYCIN; CALCIUM IONOPHORE; CALMIDAZOLIUM; CALMODULIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; KT 5720; THIMET OLIGOPEPTIDASE;

ARTICLE; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; DRUG INHIBITION; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE;

CALCIMYCIN; CALCIUM; CALMODULIN; CELL LINE; CYTOSOL; FORSKOLIN; HUMANS; METALLOENDOPEPTIDASES; PROTEIN BINDING;

EID: 68749107347     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07144.x     Document Type: Article

References (64)

1. Blobel G Sabatini DD (1970) Controlled proteolysis of nascent polypeptides in rat liver cell fractions I. Location of the polypeptides within ribosomes. J Cell Biol 45, 130 145.
2. Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189, 867.
3. Nickel W (2003) The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 270, 2109 2119.
4. Carreno FR, Goni CN, Castro LM Ferro ES (2005) 14-3-3 epsilon modulates the stimulated secretion of endopeptidase 24.15. J Neurochem 93, 10 25.
5. Ferro ES, Tullai JW, Glucksman MJ Roberts JL (1999) Secretion of metalloendopeptidase 24.15 (EC 3.4.24.15). DNA Cell Biol 18, 781 789.
6. Vincent B, Jiracek J, Noble F, Loog M, Roques B, Dive V, Vincent JP Checler F (1997) Contribution of endopeptidase 3.4.24.15 to central neurotensin inactivation. Eur J Pharmacol 334, 49 53.
7. Zhou X, Engel T, Goepfert C, Erren M, Assmann G von Eckardstein A (2002) The ATP binding cassette transporter A1 contributes to the secretion of interleukin 1beta from macrophages but not from monocytes. Biochem Biophys Res Commun 291, 598 604.
8. Cooper DN Barondes SH (1990) Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol 110, 1681 1691.
9. Dauch P, Vincent JP Checler F (1991) Specific inhibition of endopeptidase 24.16 by dipeptides. Eur J Biochem 202, 269 276.
10. Denny PW, Gokool S, Russell DG, Field MC Smith DF (2000) Acylation-dependent protein export in Leishmania. J Biol Chem 275, 11017 11025.
11. Flinn HM, Rangarajan D Smith DF (1994) Expression of a hydrophilic surface protein in infective stages of Leishmania major. Mol Biochem Parasitol 65, 259 270.
12. Sacks DL, Saraiva EM, Rowton E, Turco SJ Pimenta PF (1994) The role of the lipophosphoglycan of Leishmania in vector competence. Parasitology 108 (Suppl S55 S62.
13. Hughes RC (1999) Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim Biophys Acta 1473, 172 185.
14. Sato S, Burdett I Hughes RC (1993) Secretion of the baby hamster kidney 30-kDa galactose-binding lectin from polarized and nonpolarized cells: a pathway independent of the endoplasmic reticulum-Golgi complex. Exp Cell Res 207, 8 18.
15. Levi SK Glick BS (2007) GRASPing unconventional secretion. Cell 130, 407 409.
16. Lew RA, Cowley M, Clarke IJ Smith AI (1997) Peptidases that degrade gonadotropin-releasing hormone: influence on LH secretion in the ewe. J Neuroendocrinol 9, 707 712.
17. Roberts JL, Mani SK, Woller MJ, Glucksman MJ Wu TJ (2007) LHRH-(1-5): a bioactive peptide regulating reproduction. Trends Endocrinol Metab 18, 386 392.
18. Wu TJ, Pierotti AR, Jakubowski M, Sheward WJ, Glucksman MJ, Smith AI, King JC, Fink G Roberts JL (1997) Endopeptidase EC 3.4.24.15 presence in the rat median eminence and hypophysial portal blood and its modulation of the luteinizing hormone surge. J Neuroendocrinol 9, 813 822.
19. Garrido PA, Vandenbulcke F, Ramjaun AR, Vincent B, Checler F, Ferro E Beaudet A (1999) Confocal microscopy reveals thimet oligopeptidase (EC 3.4.24.15) and neurolysin (EC 3.4.24.16) in the classical secretory pathway. DNA Cell Biol 18, 323 331.
20. Crack PJ, Wu TJ, Cummins PM, Ferro ES, Tullai JW, Glucksman MJ Roberts JL (1999) The association of metalloendopeptidase EC 3.4.24.15 at the extracellular surface of the AtT-20 cell plasma membrane. Brain Res 835, 113 124.
21. Fontenele-Neto JD, Massarelli EE, Gurgel Garrido PA, Beaudet A Ferro ES (2001) Comparative fine structural distribution of endopeptidase 24.15 (EC3.4.24.15) and 24.16 (EC3.4.24.16) in rat brain. J Comp Neurol 438, 399 410.
22. Ferro ES, Carreno FR, Goni C, Garrido PA, Guimaraes AO, Castro LM, Oliveira V, Araujo MC, Rioli V, Gomes MD et al. (2004) The intracellular distribution and secretion of endopeptidases 24.15 (EC 3.4.24.15) and 24.16 (EC 3.4.24.16). Protein Pept Lett 11, 415 421.
23. Tullai JW, Cummins PM, Pabon A, Roberts JL, Lopingco MC, Shrimpton CN, Smith AI, Martignetti JA, Ferro ES Glucksman MJ (2000) The neuropeptide processing enzyme EC 3.4.24.15 is modulated by protein kinase A phosphorylation. J Biol Chem 275, 36514 36522.
24. Gunnarsson K (2001) Affinity-based biosensors for biomolecular interaction analysis. In Current Protocols in Immunology (Richard Coico, ed) Chapter 18, Unit 18 16, John Wiley and Sons, Inc., Hoboken, New Jersey.
25. Murphy M, Jason-Moller L Bruno J (2006) Using Biacore to measure the binding kinetics of an antibody-antigen interaction. In Current Protocols in Protein Science (Gween Taylor, ed) Chapter 19, Unit 19 14, John Wiley and Sons, Inc., Hoboken, New Jersey.
26. Sakaba T Neher E (2001) Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32, 1119 1131.
27. Yamniuk AP Vogel HJ (2004) Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 27, 33 57.
28. Cardozo C Orlowski M (1993) Evidence that enzymatic conversion of N-[1(R,S)-carboxy-3-phenylpropyl]-Ala-Ala-Phe-p-aminobenzoate, a specific inhibitor of endopeptidase 24.15, to N-[1(R,S)-carboxy-3-phenylpropyl]-Ala-Ala is necessary for inhibition of angiotensin converting enzyme. Peptides 14, 1259 1262.
29. Jeske NA, Berg KA, Cousins JC, Ferro ES, Clarke WP, Glucksman MJ Roberts JL (2006) Modulation of bradykinin signaling by EP24.15 and EP24.16 in cultured trigeminal ganglia. J Neurochem 97, 13 21.
30. Kest B, Orlowski M Bodnar RJ (1992) Endopeptidase 24.15 inhibition and opioid antinociception. Psychopharmacology (Berl) 106, 408 416.
31. Kest B, Orlowski M, Molineaux CJ Bodnar RJ (1991) Antinociceptive properties of inhibitors of endopeptidase 24.15. Int J Neurosci 56, 141 149.
32. Molineaux CJ Ayala JM (1990) An inhibitor of endopeptidase-24.15 blocks the degradation of intraventricularly administered dynorphins. J Neurochem 55, 611 618.
33. Orlowski M, Michaud C Chu TG (1983) A soluble metalloendopeptidase from rat brain. Purification of the enzyme and determination of specificity with synthetic and natural peptides. Eur J Biochem 135, 81 88.
34. Pierotti AR, Lasdun A, Ayala JM, Roberts JL Molineaux CJ (1991) Endopeptidase-24.15 in rat hypothalamic/pituitary/gonadal axis. Mol Cell Endocrinol 76, 95 103.
35. Smith AI, Shrimpton CN, Norman UM, Clarke IJ, Wolfson AJ Lew RA (2000) Neuropeptidases regulating gonadal function. Biochem Soc Trans 28, 430 434.
36. Pierotti A, Dong KW, Glucksman MJ, Orlowski M Roberts JL (1990) Molecular cloning and primary structure of rat testes metalloendopeptidase EC 3.4.24.15. Biochemistry 29, 10323 10329.
37. Mishra S Joshi PG (2007) Lipid raft heterogeneity: an enigma. J Neurochem 103 (Suppl 1 135 142.
38. Jeske NA, Glucksman MJ Roberts JL (2003) EP24.15 is associated with lipid rafts. J Neurosci Res 74, 468 473.
39. Jeske NA, Glucksman MJ Roberts JL (2004) Metalloendopeptidase EC3.4.24.15 is constitutively released from the exofacial leaflet of lipid rafts in GT1-7 cells. J Neurochem 90, 819 828.
40. 2+ stimulation of adenylyl cyclase generates dynamic oscillations in cyclic AMP. J Cell Sci 119, 828 836.
41. Walsh DA, Perkins JP Krebs EG (1968) An adenosine 3′,5′- monophosphate-dependent protein kinase from rabbit skeletal muscle. J Biol Chem 243, 3763 3765.
42. Seino S Shibasaki T (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85, 1303 1342.
43. Tasken K Aandahl EM (2004) Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev 84, 137 167.
44. Luk SC, Ngai SM, Tsui SK, Fung KP, Lee CY Waye MM (1999) In vivo and in vitro association of 14-3-3 epsilon isoform with calmodulin: implication for signal transduction and cell proliferation. J Cell Biochem 73, 31 35.
45. Jurado LA, Chockalingam PS Jarrett HW (1999) Apocalmodulin. Physiol Rev 79, 661 682.
46. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 31, 5269 5278.
47. Vogel HJ (1994) The Merck Frosst Award Lecture 1994. Calmodulin: a versatile calcium mediator protein. Biochem Cell Biol 72, 357 376.
48. Yap KL, Kim J, Truong K, Sherman M, Yuan T Ikura M (2000) Calmodulin target database. J Struct Funct Genomics 1, 8 14.
49. 2+/CaM-dependent protein kinase cascade in health and disease. Subcell Biochem 45, 169 214.
50. Chamberlain LH, Roth D, Morgan A Burgoyne RD (1995) Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis. J Cell Biol 130, 1063 1070.
51. 2+)-stimulated secretion by modulating membrane-attached exocytic machinery. J Biol Chem 274, 26469 26476.
52. 2+ -releasing channel. J Cell Biol 162, 211 222.
53. Colombo MI, Beron W Stahl PD (1997) Calmodulin regulates endosome fusion. J Biol Chem 272, 7707 7712.
54. Peters C, Bayer MJ, Buhler S, Andersen JS, Mann M Mayer A (2001) Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409, 581 588.
55. ++)-calmodulin-dependent phosphorylation and dephosphorylation of rat parotid secretion granules. Biochem Biophys Res Commun 215, 75 81.
56. Berti DA, Morano C, Russo LC, Castro LM, Cunha FM, Zhang X, Sironi J, Klitzke CF, Ferro ES Fricker LD (2009) Analysis of intracellular substrates and products of thimet oligopeptidase (EC 3.4.24.15) in human embryonic kidney 293 cells. J Biol Chem 284, 14105 14116.
57. Cunha FM, Berti DA, Ferreira ZS, Klitzke CF, Markus RP Ferro ES (2008) Intracellular peptides as natural regulators of cell signaling. J Biol Chem 283, 24448 24459.
58. Rioli V, Kato A, Portaro FC, Cury GK, te Kaat K, Vincent B, Checler F, Camargo AC, Glucksman MJ, Roberts JL et al. (1998) Neuropeptide specificity and inhibition of recombinant isoforms of the endopeptidase 3.4.24.16 family: comparison with the related recombinant endopeptidase 3.4.24.15. Biochem Biophys Res Commun 250, 5 11.
59. Steer D, Lew R, Perlmutter P, Smith AI Aguilar MI (2002) Inhibitors of metalloendopeptidase EC 3.4.24.15 and EC 3.4.24.16 stabilized against proteolysis by the incorporation of beta-amino acids. Biochemistry 41, 10819 10826.
60. Rioli V, Gozzo FC, Heimann AS, Linardi A, Krieger JE, Shida CS, Almeida PC, Hyslop S, Eberlin MN Ferro ES (2003) Novel natural peptide substrates for endopeptidase 24.15, neurolysin, and angiotensin-converting enzyme. J Biol Chem 278, 8547 8555.
61. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248 254.
62. van de Loosdrecht AA, Nennie E, Ossenkoppele GJ, Beelen RH Langenhuijsen MM (1991) Cell mediated cytotoxicity against U 937 cells by human monocytes and macrophages in a modified colorimetric MTT assay. A methodological study. J Immunol Methods 141, 15 22.
63. Martins AH, Alves JM, Trujillo CA, Schwindt TT, Barnabe GF, Motta FL, Guimaraes AO, Casarini DE, Mello LE, Pesquero JB et al. (2008) Kinin-B2 receptor expression and activity during differentiation of embryonic rat neurospheres. Cytometry A 73, 361 368.
64. Pattnaik P (2005) Surface plasmon resonance: applications in understanding receptor-ligand interaction. Appl Biochem Biotechnol 126, 79 92.