Molecular mechanism and structural basis of interactions of dipeptidyl peptidase IV with adenosine deaminase and human immunodeficiency virus type-1 transcription transactivator

European Journal of Cell Biology

Volumn 91, Issue 4, 2012, Pages 265-273

  Fan, Hua ^a   Tansi, Felista Lemnyui ^a   Weihofen, Wilhelm Andreas ^b   Böttcher, Christoph ^b   Hu, Jing ^a   Martinez, Jacobo ^b   Saenger, Wolfram ^b   Reutter, Werner ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Adenosine deaminase (ADA); CD26; Cryo electron microscopy (cryo EM), crystal structure; Dipeptidyl peptidase IV (DPPIV); HIV 1 transcription transactivator (Tat); Serine phosphorylation; Tyrosine phosphorylation

Indexed keywords

ADENOSINE DEAMINASE; DIPEPTIDYL PEPTIDASE IV; TRANSACTIVATOR PROTEIN; TYROSINE;

BIOCHEMISTRY; CELL DIFFERENTIATION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; LEPIDOPTERA; LYMPHOCYTE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SHORT SURVEY;

ADENOSINE DEAMINASE; ANIMALS; CATTLE; DIPEPTIDYL PEPTIDASE 4; HIV-1; HUMANS; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTIONAL ACTIVATION;

BOVINAE; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84857370202     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.06.001     Document Type: Short Survey

References (49)

1. Abbott C.A., McCaughan G.W., Gorrell M.D. Two highly conserved glutamic acid residues in the predicted beta propeller domain of dipeptidyl peptidase IV are required for its enzyme activity. FEBS Lett. 1999, 458:278-284.
2. Aertgeerts K., Ye S., Shi L., Prasad S.G., Witmer D., Chi E., Sang B.C., Wijnands R.A., Webb D.R., Swanson R.V. N-linked glycosylation of dipeptidyl peptidase IV (CD26): effects on enzyme activity, homodimer formation, and adenosine deaminase binding. Protein Sci. 2004, 13:145-154.
3. Ansorge S., Nordhoff K., Bank U., Heimburg A., Julius H., Breyer D., Thielitz A., Reinhold D., Täger M. Novel aspects of cellular action of dipeptidyl peptidase IV/CD26. Biol. Chem. 2011, 392:153-168.
4. Augustyns K., Bal G., Thonus G., Belyaev A., Zhang X.M., Bollaert W., Lambeir A.M., Durinx C., Goossens F., Haemers A. The unique properties of dipeptidyl-peptidase IV (DPP IV/CD26) and the therapeutic potential of DPP IV inhibitors. Curr. Med. Chem. 1999, 6:311-327.
5. Boggiano M.M., Chandler P.C., Oswald K.D., Rodgers R.J., Blundell J.E., Ishii Y., Beattie A.H., Holch P., Allison D.B., Schindler M., et al. PYY3-36 as an anti-obesity drug target. Obes. Rev. 2005, 6:307-322.
6. Campbell G.R., Watkins J.D., Esquieu D., Pasquier E., Loret E.P., Spector S.A. The C terminus of HIV-1 Tat modulates the extent of CD178-mediated apoptosis of T cells. J. Biol. Chem. 2005, 280:38376-38382.
7. Cheng H.C., Abdel-Ghany M., Pauli B.U. A novel consensus motif in fibronectin mediates dipeptidyl peptidase IV adhesion and metastasis. J. Biol. Chem. 2003, 278:24600-24607.
8. Dayton A.I., Sodroski J.G., Rosen C.A., Goh W.C., Haseltine W.A. The trans-activator gene of the human T cell lymphotropic virus type III is required for replication. Cell 1986, 44:941-947.
9. De Meester I., Korom S., Van Damme J., Scharpe S. CD26, let it cut or cut it down. Immunol. Today 1999, 20:367-375.
10. De Meester I., Vanham G., Kestens L., Vanhoof G., Bosmans E., Gigase P., Scharpe S. Binding of adenosine deaminase to the lymphocyte surface via CD26. Eur. J. Immunol. 1994, 24:566-570.
11. Demuth H.U., McIncosh C.H., Pederson R.A. Type 2 diabetes-therapy with dipeptidyl peptidase IV inhibitors. Biochim. Biophys. Acta 2005, 1751:33-44.
12. Dobers J., Grams S., Reutter W., Fan H. Roles of cysteines in rat dipeptidyl peptidase IV/CD26 in processing and proteolytic activity. Eur. J. Biochem. 2000, 267:5093-5100.
13. Dobers J., Zimmermann-Kordmann M., Leddermann M., Schewe T., Reutter W., Fan H. Expression, purification, and characterization of human dipeptidyl peptidase IV/CD26 in Sf9 insect cells. Protein Expr. Purif. 2002, 25:527-532.
14. Dong R.P., Kameoka J., Hegen M., Tanaka T., Xu Y., Schlossman S.F., Morimoto C. Characterization of adenosine deaminase binding to human CD26 on T cells and its biologic role in immune response. J. Immunol. 1996, 156:1349-1355.
15. Engel M., Hoffmann T., Wagner L., Wermann M., Heiser U., Kiefersauer R., Huber R., Bode W., Demuth H.U., Brandstetter H. The crystal structure of dipeptidyl peptidase IV (CD26) reveals its functional regulation and enzymatic mechanism. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:5063-5068.
16. Fan H., Meng W., Kilian C., Grams S., Reutter W. Domain-specific N-glycosylation of the membrane glycoprotein dipeptidylpeptidase IV (CD26) influences its subcellular trafficking, biological stability, enzyme activity and protein folding. Eur. J. Biochem. 1997, 246:243-251.
17. Fan H., Yan S., Stehling S., Marguet D., Schuppaw D., Reutter W. Dipeptidyl peptidase IV/CD26 in T cell activation, cytokine secretion and immunoglobulin production. Adv. Exp. Med. Biol. 2003, 524:165-174.
18. Franco R., Valenzuela A., Lluis C., Blanco J. Enzymatic and extraenzymatic role of ecto-adenosine deaminase in lymphocytes. Immunol. Rev. 1998, 161:27-42.
19. Gines S., Marino M., Mallol J., Canela E.I., Morimoto C., Callebaut C., Hovanessian A., Casado V., Lluis C., Franco R. Regulation of epithelial and lymphocyte cell adhesion by adenosine deaminase-CD26 interaction. Biochem. J. 2002, 361:203-209.
20. Gorrell M.D. First bite. Nat. Struct. Biol. 2003, 10:3-5.
21. Gutheil W.G., Subramanyam M., Flentke G.R., Sanford D.G., Munoz E., Huber B.T., Bachovchin W.W. Human immunodeficiency virus 1 Tat binds to dipeptidyl aminopeptidase IV (CD26): a possible mechanism for Tat's immunosuppressive activity. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:6594-6598.
22. Hanski C., Huhle T., Reutter W. Involvement of plasma membrane dipeptidyl peptidase IV in fibronectin-mediated adhesion of cell on collagen. Biol. Chem. Hoppe Seyler 1985, 366:1169-1176.
23. Herrera C., Morimoto C., Blanco J., Mallol J., Arenzana F., Lluis C., Franco R. Comodulation of CXCR4 and CD26 in human lymphocytes. J. Biol. Chem. 2001, 276:19532-19539.
24. Ishii T., Ohnuma K., Murakami A., Takasawa N., Kobayashi S., Dang N.H., Schlossman S.F., Morimoto C. CD26-mediated signaling for T cell activation occurs in lipid rafts through its association with CD45RO. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:12138-12143.
25. Kameoka J., Tanaka T., Nojima Y., Schlossman S.F., Morimoto C. Direct association of adenosine deaminase with a T cell activation antigen CD26. Science 1993, 261:466-469.
26. Liu Z., Christensson M., Forslow A., De Meester I., Sundqvist K.G. A CD26-controlled cell surface cascade for regulation of T cell motility and chemokine signals. J. Immunol. 2009, 183:3616-3624.
27. Lorey S., Stockel-Maschek A., Faust J., Brandt W., Stiebitz B., Gorrell M.D., Kahne T., Mrestani-Klaus C., Wrenger S., Reinhold D., et al. Different modes of dipeptidyl peptidase IV (CD26) inhibition by oligopeptides derived from the N-terminus of HIV-1 Tat indicate at least two inhibitor binding sites. Eur. J. Biochem. 2003, 270:2147-2156.
28. Ludwig K., Fan H., Dobers J., Berger M., Reutter W., Bottcher C. 3D structure of the CD26-ADA complex obtained by cryo-EM and single particle analysis. Biochem. Biophys. Res. Commun. 2004, 313:223-229.
29. Ludwig K., Yan S., Fan H., Reutter W., Bottcher C. The 3D structure of rat DPPIV/CD26 as obtained by cryo-TEM and single particle analysis. Biochem. Biophys. Res. Commun. 2003, 304:73-77.
30. Martinez-Navio J.M., Casanova V., Pacheco R., Naval-Macabuhay I., Climent N., Garcia F., Gatell J.M., Mallol J., Gallart T., Lluis C., Franco R. Adenosine deaminase potentiates the generation of effector, memory, and regulatory CD4+ T cells. J. Leukoc. Biol. 2011, 89:127-136.
31. Mentlein R. Dipeptidyl-peptidase IV (CD26)-role in the inactivation of regulatory peptides. Regul. Pept. 1999, 85:9-24.
32. Mentlein R. Therapeutic assessment of glucagon-like peptide-1 agonists compared with dipeptidyl peptidase IV inhibitors as potential antidiabetic drugs. Expert Opin. Investig. Drugs 2005, 14:57-64.
33. Morimoto C., Schlossman S.F. The structure and function of CD26 in the T-cell immune response. Immunol. Rev. 1998, 161:55-70.
34. Ohnuma K., Dang N.H., Morimoto C. Revisiting an old acquaintance: CD26 and its molecular mechanisms in T cell function. Trends Immunol. 2008, 29:295-301.
35. Ohnuma K., Uchiyama M., Yamochi T., Nishibashi K., Hosono O., Takahashi N., Kina S., Tanaka H., Lin X., Dang N.H., et al. Caveolin-1 triggers T-cell activation via CD26 in association with CARMA1. J. Biol. Chem. 2007, 282:10117-10131.
36. Ohtsuki T., Tsuda H., Morimoto C. Good or evil: CD26 and HIV infection. J. Dermatol. Sci. 2000, 22:152-160.
37. Pacheco R., Martinez-Navio J.M., Lejeune M., Climent N., Oliva H., Gatell J.M., Gallart T., Mallol J., Lluis C., Franco R. CD26, adenosine deaminase, and adenosine receptors mediate costimulatory signals in the immunological synapse. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9583-9588.
38. Pospisilik J.A., Martin J., Doty T., Ehses J.A., Pamir N., Lynn F.C., Piteau S., Demuth H.U., McIntosh C.H., Pederson R.A. Dipeptidyl peptidase IV inhibitor treatment stimulates beta-cell survival and islet neogenesis in streptozotocin-induced diabetic rats. Diabetes 2003, 52:741-750.
39. Rasmussen H.B., Branner S., Wiberg F.C., Wagtmann N. Crystal structure of human dipeptidyl peptidase IV/CD26 in complex with a substrate analog. Nat. Struct. Biol. 2003, 10:19-25.
40. Richard E., Alam S.M., Arredondo-Vega F.X., Patel D.D., Hershfield M.S. Clustered charged amino acids of human adenosine deaminase comprise a functional epitope for binding the adenosine deaminase complexing protein CD26/dipeptidyl peptidase IV. J. Biol. Chem. 2002, 277:19720-19726.
41. Sodroski J., Rosen C., Wong-Staal F., Salahuddin S.Z., Popovic M., Arya S., Gallo R.C., Haseltine W.A. Trans-acting transcriptional regulation of human T-cell leukemia virus type III long terminal repeat. Science 1985, 227:171-173.
42. Struyf S., Proost P., Van Damme J. Regulation of the immune response by the interaction of chemokines and proteases. Adv. Immunol. 2003, 81:1-44.
43. Tansi F.L., Blanchard V., Berger M., Tauber R., Reutter W., Fan H. Interaction of human dipeptidyl peptidase IV and human immunodeficiency virus type-1 transcription transactivator in Sf9 cells. Virol. J. 2011, 7:267.
44. Valenzuela A., Blanco J., Callebaut C., Jacotot E., Lluis C., Hovanessian A.G., Franco R. Adenosine deaminase binding to human CD26 is inhibited by HIV-1 envelope glycoprotein gp120 and viral particles. J. Immunol. 1997, 158:3721-3729.
45. von Bonin A., Huhn J., Fleischer B. Dipeptidyl-peptidase IV/CD26 on T cells: analysis of an alternative T-cell activation pathway. Immunol. Rev. 1998, 161:43-53.
46. Weihofen W.A., Liu J., Reutter W., Saenger W., Fan H. Crystal structure of CD26/dipeptidyl-peptidase IV in complex with adenosine deaminase reveals a highly amphiphilic interface. J. Biol. Chem. 2004, 279:43330-43335.
47. Wrenger S., Reinhold D., Hoffmann T., Kraft M., Frank R., Faust J., Neubert K., Ansorge S. The N-terminal X-X-Pro sequence of the HIV-1 Tat protein is important for the inhibition of dipeptidyl peptidase IV (DP IV/CD26) and the suppression of mitogen-induced proliferation of human T cells. FEBS Lett. 1996, 383:145-149.
48. Wriggers W., Birmanns S. Using situs for flexible and rigid-body fitting of multiresolution single-molecule data. J. Struct. Biol. 2001, 133:193-202.
49. Yan S., Marguet D., Dobers J., Reutter W., Fan H. Deficiency of CD26 results in a change of cytokine and immunoglobulin secretion after stimulation by pokeweed mitogen. Eur. J. Immunol. 2003, 33:1519-1527.