Solution Characterization of the Extracellular Region of CD147 and Its Interaction with Its Enzyme Ligand Cyclophilin A

Journal of Molecular Biology

Volumn 391, Issue 3, 2009, Pages 518-535

  Schlegel, Jennifer ^a   Redzic, Jasmina S ^a   Porter, Christopher C ^b   Yurchenko, Vyacheslav ^c   Bukrinsky, Michael ^d   Labeikovsky, Wladimir ^e   Armstrong, Geoffrey S ^f   Zhang, Fengli ^g   Isern, Nancy G ^h   DeGregori, James ^a   Hodges, Robert ^a   Eisenmesser, Elan Zohar ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Children's Hospital Colorado   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d GEORGE WASHINGTON UNIVERSITY   (United States)

^e ROCKEFELLER UNIVERSITY   (United States)

^f UNIVERSITY OF COLORADO   (United States)

^g FLORIDA STATE UNIVERSITY   (United States)

^h PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

CD147; cyclophilin; extracellular matrix metalloproteinase inducer (EMMPRIN); isomerization; proline

Indexed keywords

CD147 ANTIGEN; CYCLOPHILIN A;

ARTICLE; BINDING SITE; CONTROLLED STUDY; GEL FILTRATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

EID: 67651158782     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.05.080     Document Type: Article

References (71)

1. Guo H.M., Majmudar G., Jensen T.C., Biswas C., Toole B.P., and Gordon M.K. Characterization of the gene for human EMMPRIN, a tumor cell surface inducer of matrix metalloproteinases. Gene 220 (1998) 99-108
2. Schmidt R., Bültmann A., Fischel S., Gillitzer A., Cullen P., Walch A., et al. Extracellular matrix metalloproteinase inducer (CD147) is a novel receptor on platelets, activates platelets, and augments nuclear factor {kappa}B dependent inflammation in monocytes. Circ. Res. (2008) 107 10.1161/CIRCRESAHA.107.157990
3. Ruiz S., Castro-Castro A., and Bustelo X.R. CD147 inhibits the nuclear factor of activated T-cells by impairing vav1 and rac1 downstream signaling. J. Biol. Chem. 283 (2008) 5554-5566
4. Gabison E.E., Hoang-Xuan T., Mauviel A., and Menashi S. EMMPRIN/CD147, an MMP modulator in cancer, development and tissue repair. Biochimie 87 (2005) 361-368
5. Zheng H.C., Takahashi H., Murai Y., Cui Z.G., Nomoto K., Miwa S., et al. Upregulated EMMPRIN/CD147 might contribute to growth and angiogenesis of gastric carcinoma: a good marker for local invasion and prognosis. Br. J. Cancer 95 (2006) 1371-1378
6. Tang Y., Nakada M.T., Kesavan P., McCabe F., Millar H., Rafferty P., et al. Extracellular matrix metalloproteinase inducer stimulates tumor angiogenesis by elevating vascular endothelial cell growth factor and matrix metal loproteinases. Cancer Res. 65 (2005) 3193-3199
7. Velez W., and Kyprianou N. EMMPRIN is a biomarker of prostate cancer progression in TRAMP mice. FASEB J. 21 (2007) A621
8. Xu H.Y., Qian A.R., Shang P., Xu J., Kong L.M., Bian H.J., and Chen Z.N. siRNA targeted against HAb18G/CD147 inhibits MMP-2 secretion, actin and FAK expression in hepatocellular carcinoma cell line via ERK1/2 pathway. Cancer Lett. 247 (2007) 336-344
9. Millimaggi D., Mari M., D'Ascenzo S., Carosa E., Jannini E.A., Zucker S., et al. Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia 9 (2007) 349-357
10. Sidhu S.S., Mengistab A.T., Tauscher A.N., LaVail J., and Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 23 (2004) 956-963
11. Taylor P.M., Woodfield R.J., Hodgkin M.N., Pettitt T.R., Martin A., Kerr D.J., and Wakelam M.J.O. Breast cancer cell-derived EMMPRIN stimulates fibroblast MMP2 release through a phospholipase A(2) and 5-lipoxygenase catalyzed pathway. Oncogene 21 (2002) 5765-5772
12. Zhu P., Ding J., Zhou J., Dong W.J., Fan C.M., and Chen Z.N. Expression of CD147 on monocytes/macrophages in rheumatoid arthritis: its potential role in monocyte accumulation and matrix metalloproteinase production. Arthritis Res. Ther. 7 (2005) R1023-R1033
13. Zhu P., Lu N., Shi Z.G., Zhou J., Wu Z.B., Yang Y., et al. CD147 overexpression on synoviocytes in rheumatoid arthritis enhances matrix metalloproteinase production and invasiveness of synoviocytes. Arthritis Res. Ther. 8 (2006) 1-12
14. Belton R.J., Chen L., Mesquita F.S., and Nowak R.A. Basigin-2 is a cell surface receptor for soluble basigin ligand. J. Biol. Chem. 283 (2008) 17805-17814
15. Yoshida S., Shibata M., Yamamoto S., Hagihara M., Asai N., Takahashi M., et al. Homo-oligomer formation by basigin, an immunoglobulin superfamily member, via its N-terminal immunoglobulin domain. Eur. J. Biochem. 267 (2000) 4372-4380
16. Melchior A., Denys A., Deligny A., Mazurier J., and Allain F. Cyclophilin B induces integrin-mediated cell adhesion by a mechanism involving CD98-dependent activation of protein kinase C-delta and p44/42 mitogen-activated protein kinases. Exp. Cell Res. 314 (2008) 616-628
17. Pakula R., Melchior A., Denys A., Vanpouille C., Mazurier J., and Allain F. Syndecan-1/CD147 association is essential for cyclophilin B-induced activation of p44/42 mitogen-activated protein kinases and promotion of cell adhesion and chemotaxis. Glycobiology 17 (2007) 492-503
18. Yurchenko V., Constant S., and Bukrinsky M. Dealing with the family: CD147 interactions with cyclophilins. Immunology 117 (2006) 301-309
19. Andreotti A.H. Native state proline isomerization: an intrinsic molecular switch. Biochemistry 42 (2003) 9515-9524
20. Yao Q.Z., Li M., Yang H., Chai H., Fisher W., and Chen C.Y. Roles of cyclophilins in cancers and other organ systems. World J. Surg. 29 (2005) 276-280
21. Pap T. Cyclophilins in rheumatoid arthritis-stepping into an undiscovered country?. Clin. Immunol. 116 (2005) 199-201
22. Billich A., Winkler G., Aschauer H., Rot A., and Peichl P. Presence of cyclophilin A in synovial fluids of patients with rheumatoid arthritis. J. Exp. Med. 185 (1997) 975-980
23. Yurchenko V., O'Connor M., Dai W.W., Guo H.M., Toole B., Sherry B., and Bukrinsky M. CD147 is a signaling receptor for cyclophilin B. Biochem. Biophys. Res. Commun. 288 (2001) 786-788
24. Yurchenko V., Zybarth G., O'Connor M., Dai W.W., Franchin G., Hao T., et al. Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J. Biol. Chem. 277 (2002) 22959-22965
25. Jin Z.G., Lungu A.O., Xie L., Wang M., Wong C., and Berk B.C. Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 1186-1191
26. Arora K., Gwinn W.M., Bower M.A., Watson A., Okwumabua I., MacDonald H.R., et al. Extracellular cyclophilins contribute to the regulation of inflammatory responses. J. Immunol. 175 (2005) 517-522
27. Gwinn W.M., Damsker J.M., Falahati R., Okwumabua I., Kelly-Welch A., Keegan A.D., et al. Novel approach to inhibit asthma-mediated lung inflammation using anti-CD147 intervention. J. Immunol. 177 (2006) 4870-4879
28. Damsker J.M., Okwumabua I., Bukrinsky M.I., and Constant S.L. Contribution of cyclophilin-CD147 interactions in rheumatoid arthritis. J. Immunol. 176 (2006) S47
29. Bose S., Mathur M., Bates P., Joshi N., and Banerjee A.K. Requirement for cyclophilin A for the replication of vesicular stomatitis virus New Jersey serotype. J. Gen. Virol. 84 (2003) 1687-1699
30. Castro A.P.V., Carvalho T.M.U., Moussatche N., and Damaso C.R.A. Redistribution of cyclophilin A to viral factories during vaccinia virus infection and its incorporation into mature particles. J. Virol. 77 (2003) 9052-9068
31. Sorin M., and Kalpana G.V. Dynamics of virus-host interplay in HIV-1 replication. Curr. HIV Res. 4 (2006) 117-130
32. Chen Z.N., Mi L., Xu J., Yu J.Y., Wang X.H., Jiang J.L., et al. Function of HAb18G/CD147 in invasion of host cells by severe acute respiratory syndrome coronavirus. J. Infect. Dis. 191 (2005) 755-760
33. Pushkarsky T., Zybarth G., Dubrovsky L., Yurchenko V., Tang H., Guo H.M., et al. CD147 facilitates HIV-1 infection by interacting with virus-associated cyclophilin A. Proc. Natl Acad. Sci. USA 98 (2001) 6360-6365
34. Yu X.L., Hu T., Du J.M., Ding J.P., Yang X.M., Zhang J., et al. Crystal structure of HAb18g/CD147-implications for immunoglobulin superfamily homophilic adhesion. J. Biol. Chem. 283 (2008) 18056-18065
35. Yang H., Chen J., Yang J., Qiao S., Zhao S., and Yu L. Cyclophilin A is upregulated in small cell lung cancer and activates ERK1/2 signal. Biochem. Biophys. Res. Commun. 361 (2007) 763-767
36. Bosco D.A., Eisenmesser E.Z., Pochapsky S., Sundquist W.I., and Kern D. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc. Natl Acad. Sci. USA 99 (2002) 5247-5252
37. Campos-Olivas R., and Summers M.F. Backbone dynamics of the N-terminal domain of the HIV-1 capsid protein and comparison with the G94D mutant conferring cyclosporin resistance/dependence. Biochemistry 38 (1999) 10262-10271
38. Sun J.X., and Hemler M.E. Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions. Cancer Res. 61 (2001) 2276-2281
39. Jia L., Wang H.J., Zhou H.M., Cao J., Hu Y.C., and Zhang J.N. Caveolin-1 up-regulates CD 147 glycosylation and the invasive capability of murine hepatocarcinoma cell lines. Int. J. Biochem. Cell Biol. 38 (2006) 1584-1593
40. Jia L., Zhou H.M., Wang S.J., Cao J., Wei W., and Zhang J.N. Deglycosylation of CD147 down-regulates matrix metalloproteinase-11 expression and the adhesive capability of murine hepatocarcinoma cell HcaF in vitro. IUBMB Life 58 (2006) 209-216
41. Markovic I., Stantchev T.S., Fields K.H., Tiffany L.J., Tomic M., Weiss C.D., et al. Thiol/disulfide exchange is a prerequisite for CXCR4-tropic HIV-1 envelope-mediated T-cell fusion during viral entry. Blood 103 (2004) 1586-1594
42. Iacono K.T., Brown A.L., Greene M.I., and Saouaf S.J. CD147 immunoglobulin superfamily receptor function and role in pathology. Exp. Mol. Pathol. 83 (2007) 283-295
43. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
44. Larsson G., Martinez G., Schleucher J., and Wijmenga S.S. Detection of nano-second internal motion and determination of the overall tumbling times independent of the time scale of internal motion in proteins from NMR relaxation data. J. Biomol. NMR 27 (2003) 291-312
45. Cole R., and Loria J.P. FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data. J. Biomol. NMR 26 (2003) 203-213
46. Yurchenko V., Pushkarsky T., Li J.H., Dai W.W., Sherry B., and Bukrinsky M. Regulation of CD147 cell surface expression-involvement of the proline residue in the CD147 transmembrane domain. J. Biol. Chem. 280 (2005) 17013-17019
47. Hanoulle X., Melchior A., Sibille N., Parent B., Denys A., Wieruszeski J.M., et al. Structural and functional characterization of the interaction between cyclophilin B and a heparin-derived oligosaccharide. J. Biol. Chem. 282 (2007) 34148-34158
48. Ottiger M., Zerbe O., Guntert P., and Wuthrich K. The NMR solution conformation of unligated human cyclophilin A. J. Mol. Biol. 272 (1997) 64-81
49. Eisenmesser E.Z., Bosco D.A., Akke M., and Kern D. Enzyme dynamics during catalysis. Science 295 (2002) 1520-1523
50. Piotukh K., Gu W., Kofler M., Labudde D., Helms V., and Freund C. Cyclophilin a binds to linear peptide motifs containing a consensus that is present in many human proteins. J. Biol. Chem. 280 (2005) 23668-23674
51. Brazin K.N., Mallis R.J., Fulton D.B., and Andreotti A.H. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc. Natl Acad. Sci. USA 99 (2002) 1899-1904
52. Grathwohl C., and Wuthrich K. NMR studies of the rates of proline cis-trans isomerization in oligopeptides. Biopolymers 20 (1981) 2623-2633
53. Liu J., Chen C.M., and Walsh C.T. Human and Escherichia coli cyclophilins-sensitivity to inhibition by the immunosuppressant cyclosporin A correlates with a specific tryptophan residue. Biochemistry 30 (1991) 2306-2310
54. Hanna S.M., Kirk P., Holt O.J., Puklavec M.J., Brown M.H., and Barclay A.N. A novel form of the membrane protein CD147 that contains an extra Ig-like domain and interacts homophilically. BMC Biochem. 4 (2003) 17
55. Kern D., Kern G., Scherer G., Fischer G., and Drakenberg T. Kinetic analysis of cyclophilin-catalyzed prolyl cis/trans isomerization by dynamic NMR spectroscopy. Biochemistry 34 (1995) 13594-13602
56. Yap A.S., Crampton M.S., and Hardin J. Making and breaking contacts: the cellular biology of cadherin regulation. Curr. Opin. Cell Biol. 19 (2007) 508-514
57. Guerrini M., Hricovini M., and Torri G. Interaction of heparins with fibroblast growth factors: conformational aspects. Curr. Pharm. Des. 13 (2007) 2045-2056
58. Wilson M.C., Meredith D., Fox J.E.M., Manoharan C., Davies A.J., and Halestrap A.P. Basigin (CD147) is the target for organomercurial inhibition of monocarboxylate transporter isoforms 1 and 4-the ancillary protein for the insensitive MCT2 is embigin (gp70). J. Biol. Chem. 280 (2005) 27213-27221
59. Barclay A.N., and Brown M.H. The SIRP family of receptors and immune regulation. Nat. Rev. Immunol. 6 (2006) 457-464
60. Lands W.E.M. A review of alcohol clearance in humans. Alcohol 15 (1998) 147-160
61. Ke H., Mayrose D., and Cao W. Crystal structure of cyclophilin A complexed with substrate Ala-Pro suggests a solvent-assisted mechanism of cis-trans isomerization. Proc. Natl Acad. Sci. USA 90 (1993) 3324-3328
62. Zhao Y., and Ke H. Crystal structure implies that cyclophilin predominantly catalyzes the trans to cis isomerization. Biochemistry 35 (1996) 7356-7361
63. Eisenmesser E.Z., Millet O., Labeikovsky W., Korzhnev D.M., Wolf-Watz M., Bosco D.A., et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438 (2005) 117-121
64. Pushkarsky T., Yurchenko V., Laborico A., and Bukrinsky M. CD147 stimulates HIV-1 infection in a signal-independent fashion. Biochem. Biophys. Res. Commun. 363 (2007) 495-499
65. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe-a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
66. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas P., et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins: Struct., Funct., Bioinform. 59 (2005) 687-696
67. Sattler M., Schleucher J., and Griesinger C. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magn. Reson. Spectrosc. 34 (1999) 93-158
68. d'Auvergne E.J., and Gooley P.R. Optimisation of NMR dynamic models. I. Minimisation algorithms and their performance within the model-free and Brownian rotational diffusion spaces. J. Biomol. NMR 40 (2008) 107-119
69. Farrow N.A., Zhang O.W., Formankay J.D., and Kay L.E. A heteronuclear correlation experiment for simultaneous determination of N-15 longitudinal decay and chemical-exchange rates of systems in slow equilibrium. J. Biomol. NMR 4 (1994) 727-734
70. Farrow N.A., Zhang O.W., Formankay J.D., and Kay L.E. Comparison of the backbone dynamics of a folded and an unfolded Sh3 domain existing in equilibrium in aqueous buffer. Biochemistry 34 (1995) 868-878
71. Sarkar P., Reichman C., Saleh T., Birge R.B., and Kalodimos C.G. Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol. Cell 25 (2007) 413-426