C-terminal clipping of chemokine ccl1/i-309 enhances ccr8-mediated intracellular calcium release and anti-apoptotic activity

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Denis, Catherine ^a   Deiteren, Kathleen ^a   Mortier, Anneleen ^b   Tounsi, Amel ^c,d   Fransen, Erik ^a   Proost, Paul ^b   Renauld, Jean Christophe ^c,d   Lambeir, Anne Marie ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d DE DUVE INSTITUTE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

2 MERCAPTOMETHYL 3 GUANIDO ETHYLTHIOPROPIONIC ACID; CALCIUM ION; CARBOXYPEPTIDASE; CARBOXYPEPTIDASE M; CCL1 CHEMOKINE; CHEMOKINE RECEPTOR CCR8; ENZYME INHIBITOR; UNCLASSIFIED DRUG; CALCIUM; CCL1 PROTEIN, HUMAN; CCL1 PROTEIN, MOUSE; CCR8 PROTEIN, HUMAN; CCR8 PROTEIN, MOUSE; DEXAMETHASONE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; METALLOPROTEINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BIOLOGICAL ACTIVITY; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; IN VITRO STUDY; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; RECEPTOR AFFINITY; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; GLYCOSYLATION; HUMAN; HYDROLYSIS; INFLAMMATION; METABOLISM; METHODOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CALCIUM; CELL LINE, TUMOR; CHEMOKINE CCL1; DEXAMETHASONE; GLYCOSYLATION; GPI-LINKED PROTEINS; HUMANS; HYDROLYSIS; INFLAMMATION; MASS SPECTROMETRY; METALLOENDOPEPTIDASES; MICE; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CCR8; SIGNAL TRANSDUCTION;

EID: 84858964996     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034199     Document Type: Article

References (48)

1. Skidgel RA, Davis RM, Tan F, (1989) Human carboxypeptidase M. Purification and characterization of a membrane-bound carboxypeptidase that cleaves peptide hormones. J Biol Chem 264: 2236-2241.
2. Deiteren K, Hendriks D, Scharpe S, Lambeir AM, (2009) Carboxypeptidase M: Multiple alliances and unknown partners. Clin Chim Acta 399: 24-39.
3. Charo IF, Ransohoff RM, (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354: 610-621.
4. Mortier A, Gouwy M, Van Damme J, Proost P, (2011) Effect of posttranslational processing on the in vitro and in vivo activity of chemokines. Exp Cell Res 317: 642-654.
5. Davis DA, Singer KE, De La Luz Sierra M, Narazaki M, Yang F, et al. (2005) Identification of carboxypeptidase N as an enzyme responsible for C-terminal cleavage of stromal cell-derived factor-1alpha in the circulation. Blood 105: 4561-4568.
6. Marquez-Curtis L, Jalili A, Deiteren K, Shirvaikar N, Lambeir AM, et al. (2008) Carboxypeptidase M expressed by human bone marrow cells cleaves the C-terminal lysine of stromal cell-derived factor-1alpha: another player in hematopoietic stem/progenitor cell mobilization? Stem Cells 26: 1211-1220.
7. De La Luz Sierra M, Yang F, Narazaki M, Salvucci O, Davis D, et al. (2004) Differential processing of stromal-derived factor-1alpha and stromal-derived factor-1beta explains functional diversity. Blood 103: 2452-2459.
8. Tan Y, Du J, Cai S, Li X, Ma W, et al. (2006) Cloning and characterizing mutated human stromal cell-derived factor-1 (SDF-1): C-terminal alpha-helix of SDF-1alpha plays a critical role in CXCR4 activation and signaling, but not in CXCR4 binding affinity. Exp Hematol 34: 1553-1562.
9. Iellem A, Mariani M, Lang R, Recalde H, Panina-Bordignon P, et al. (2001) Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med 194: 847-853.
10. Miller MD, Krangel MS, (1992) The human cytokine I-309 is a monocyte chemoattractant. Proc Natl Acad Sci U S A 89: 2950-2954.
11. Zingoni A, Soto H, Hedrick JA, Stoppacciaro A, Storlazzi CT, et al. (1998) The chemokine receptor CCR8 is preferentially expressed in Th2 but not Th1 cells. J Immunol 161: 547-551.
12. Goya I, Gutierrez J, Varona R, Kremer L, Zaballos A, et al. (1998) Identification of CCR8 as the specific receptor for the human beta-chemokine I-309: cloning and molecular characterization of murine CCR8 as the receptor for TCA-3. J Immunol 160: 1975-1981.
13. Roos RS, Loetscher M, Legler DF, Clark-Lewis I, Baggiolini M, et al. (1997) Identification of CCR8, the receptor for the human CC chemokine I-309. J Biol Chem 272: 17251-17254.
14. Tiffany HL, Lautens LL, Gao JL, Pease J, Locati M, et al. (1997) Identification of CCR8: a human monocyte and thymus receptor for the CC chemokine I-309. J Exp Med 186: 165-170.
15. Van Snick J, Houssiau F, Proost P, Van Damme J, Renauld JC, (1996) I-309/T cell activation gene-3 chemokine protects murine T cell lymphomas against dexamethasone-induced apoptosis. J Immunol 157: 2570-2576.
16. Louahed J, Struyf S, Demoulin JB, Parmentier M, Van Snick J, et al. (2003) CCR8-dependent activation of the RAS/MAPK pathway mediates anti-apoptotic activity of I-309/CCL1 and vMIP-I. Eur J Immunol 33: 494-501.
17. Spinetti G, Bernardini G, Camarda G, Mangoni A, Santoni A, et al. (2003) The chemokine receptor CCR8 mediates rescue from dexamethasone-induced apoptosis via an ERK-dependent pathway. J Leukoc Biol 73: 201-207.
18. Horuk R, Hesselgesser J, Zhou Y, Faulds D, Halks-Miller M, et al. (1998) The CC chemokine I-309 inhibits CCR8-dependent infection by diverse HIV-1 strains. J Biol Chem 273: 386-391.
19. Bernardini G, Spinetti G, Ribatti D, Camarda G, Morbidelli L, et al. (2000) I-309 binds to and activates endothelial cell functions and acts as an angiogenic molecule in vivo. Blood 96: 4039-4045.
20. Hoelzinger DB, Smith SE, Mirza N, Dominguez AL, Manrique SZ, et al. (2010) Blockade of CCL1 inhibits T regulatory cell suppressive function enhancing tumor immunity without affecting T effector responses. J Immunol 184: 6833-6842.
21. Ruckes T, Saul D, Van Snick J, Hermine O, Grassmann R, (2001) Autocrine antiapoptotic stimulation of cultured adult T-cell leukemia cells by overexpression of the chemokine I-309. Blood 98: 1150-1159.
22. Tamguney G, Van Snick J, Fickenscher H, (2004) Autocrine stimulation of rhadinovirus-transformed T cells by the chemokine CCL1/I-309. Oncogene 23: 8475-8485.
23. Skidgel RA, Deddish PA, Davis RM, (1988) Isolation and characterization of a basic carboxypeptidase from human seminal plasma. Arch Biochem Biophys 267: 660-667.
24. Skidgel RA, Davis RM, Erdos EG, (1984) Purification of a human urinary carboxypeptidase (kininase) distinct from carboxypeptidases A, B, or N. Anal Biochem 140: 520-531.
25. McGwire GB, Skidgel RA, (1995) Extracellular conversion of epidermal growth factor (EGF) to des-Arg53-EGF by carboxypeptidase M. J Biol Chem 270: 17154-17158.
26. Michel B, Igic R, Leray V, Deddish PA, Erdos EG, (1996) Removal of Arg141 from the alpha chain of human hemoglobin by carboxypeptidases N and M. Circ Res 78: 635-642.
27. Miller MD, Hata S, De Waal Malefyt R, Krangel MS, (1989) A novel polypeptide secreted by activated human T lymphocytes. J Immunol 143: 2907-2916.
28. Inngjerdingen M, Damaj B, Maghazachi AA, (2000) Human NK cells express CC chemokine receptors 4 and 8 and respond to thymus and activation-regulated chemokine, macrophage-derived chemokine, and I-309. J Immunol 164: 4048-4054.
29. Sebastiani S, Allavena P, Albanesi C, Nasorri F, Bianchi G, et al. (2001) Chemokine receptor expression and function in CD4+ T lymphocytes with regulatory activity. J Immunol 166: 996-1002.
30. Haskell CA, Horuk R, Liang M, Rosser M, Dunning L, et al. (2006) Identification and characterization of a potent, selective nonpeptide agonist of the CC chemokine receptor CCR8. Mol Pharmacol 69: 309-316.
31. Fox JM, Najarro P, Smith GL, Struyf S, Proost P, et al. (2006) Structure/function relationships of CCR8 agonists and antagonists. Amino-terminal extension of CCL1 by a single amino acid generates a partial agonist. J Biol Chem 281: 36652-36661.
32. Jensen PC, Nygaard R, Thiele S, Elder A, Zhu G, et al. (2007) Molecular interaction of a potent nonpeptide agonist with the chemokine receptor CCR8. Mol Pharmacol 72: 327-340.
33. Gutierrez J, Kremer L, Zaballos A, Goya I, Martinez AC, et al. (2004) Analysis of post-translational CCR8 modifications and their influence on receptor activity. J Biol Chem 279: 14726-14733.
34. Luz JG, Yu M, Su Y, Wu Z, Zhou Z, et al. (2005) Crystal structure of viral macrophage inflammatory protein I encoded by Kaposi's sarcoma-associated herpesvirus at 1.7A. J Mol Biol 352: 1019-1028.
35. Clark-Lewis I, Kim KS, Rajarathnam K, Gong JH, Dewald B, et al. (1995) Structure-activity relationships of chemokines. J Leukoc Biol 57: 703-711.
36. Keizer DW, Crump MP, Lee TW, Slupsky CM, Clark-Lewis I, et al. (2000) Human CC chemokine I-309, structural consequences of the additional disulfide bond. Biochemistry 39: 6053-6059.
37. Johnson Z, Proudfoot AE, Handel TM, (2005) Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev 16: 625-636.
38. Mortier A, Van Damme J, Proost P, (2008) Regulation of chemokine activity by posttranslational modification. Pharmacol Ther 120: 197-217.
39. Marro ML, Daniels DA, Andrew DP, Chapman TD, Gearing KL, (2006) In vitro selection of RNA aptamers that block CCL1 chemokine function. Biochem Biophys Res Commun 349: 270-276.
40. Boffa MB, Hamill JD, Maret D, Brown D, Scott ML, et al. (2003) Acute phase mediators modulate thrombin-activable fibrinolysis inhibitor (TAFI) gene expression in HepG2 cells. J Biol Chem 278: 9250-9257.
41. de Saint-Vis B, Cupillard L, Pandrau-Garcia D, Ho S, Renard N, et al. (1995) Distribution of carboxypeptidase M on lymphoid and myeloid cells parallels the other zinc-dependent proteases CD10 and CD13. Blood 86: 1098-1105.
42. Sun X, Wiesner B, Lorenz D, Papsdorf G, Pankow K, et al. (2008) Interaction of angiotensin-converting enzyme (ACE) with membrane-bound carboxypeptidase M (CPM)- a new function of ACE. Biol Chem 389: 1477-1485.
43. Renauld JC, Vink A, Louahed J, Vansnick J, (1995) Interleukin-9 is a major anti-apoptotic factor for thymic lymphomas. Blood 85: 1300-1305.
44. Deiteren K, Surpateanu G, Gilany K, Willemse JL, Hendriks DF, et al. (2007) The role of the S1 binding site of carboxypeptidase M in substrate specificity and turn-over. Biochim Biophys Acta 1774: 267-277.
45. Grynkiewicz G, Poenie M, Tsien RY, (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450.
46. Landegren U, (1984) Measurement of cell numbers by means of the endogenous enzyme hexosaminidase- applications to detection of lymphokines and cell-surface antigens. J Immunol Methods 67: 379-388.
47. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
48. Skidgel RA, (1991) Assays for arginine/lysine carboxypeptidases: carboxypeptidase H (E; enkephalin convertase), M and N. In: Rawlings N, Barrett AJ, Woessner JF, editors. Methods in Neurosciences Toronto Academic Press pp. 373-385.