Fragment-based identification of an inducible binding site on cell surface receptor CD44 for the design of protein-carbohydrate interaction inhibitors

Journal of Medicinal Chemistry

Volumn 57, Issue 6, 2014, Pages 2714-2725

  Liu, Li Kai ^a   Finzel, Barry C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; HERMES ANTIGEN; HYALURONIC ACID; ISOQUINOLINE DERIVATIVE; POLYMER; TETRASACCHARIDE;

ARTICLE; BINDING AFFINITY; DRUG BINDING SITE; DRUG DESIGN; DRUG SCREENING; IN VITRO STUDY; PHARMACOPHORE; PROTEIN CARBOHYDRATE INTERACTION; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIGENS, CD44; BINDING SITES; CARBOHYDRATES; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; HUMANS; INDICATORS AND REAGENTS; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; POLYSACCHARIDES; PROTEIN BINDING; PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84897460110     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm5000276     Document Type: Article

References (75)

1. Geiger, B.; Bershadsky, A.; Pankov, R.; Yamada, K. M. Transmembrane crosstalk between the extracellular matrix and the cytoskeleton Nat. Rev. Mol. Cell Biol. 2001, 2, 793-805
2. Sorokin, L. The impact of the extracellular matrix on inflammation Nat. Rev. Immunol. 2010, 10, 712-23
3. Joyce, J. A.; Pollard, J. W. Microenvironmental regulation of metastasis Nat. Rev. Cancer 2008, 9, 239-252
4. Lennon, F. E.; Singleton, P. A. Hyaluronan regulation of vascular integrity Am. J. Cardiovasc. Dis. 2011, 1, 200-13
5. Ponta, H.; Sherman, L.; Herrlich, P. A. CD44: From adhesion molecules to signalling regulators Nat. Rev. Mol. Cell Biol. 2003, 4, 33-45
6. Toole, B. P.; Wight, T. N.; Tammi, M. I. Hyaluronan-cell interactions in cancer and vascular disease J. Biol. Chem. 2002, 277, 4593-6
7. Hansson, G. K.; Libby, P. The immune response in atherosclerosis: a double-edged sword Nat. Rev. Immunol. 2006, 6, 508-19
8. Toole, B. P. Hyaluronan: From extracellular glue to pericellular cue Nat. Rev. Cancer 2004, 4, 528-39
9. Toole, B. P. Hyaluronan-CD44 Interactions in Cancer: Paradoxes and Possibilities Clin. Cancer Res. 2009, 15, 7462-7468
10. Jiang, D.; Liang, J.; Noble, P. W. Hyaluronan as an immune regulator in human diseases Physiol. Rev. 2011, 91, 221-64
11. Lebel, L.; Smith, L.; Risberg, B.; Laurent, T. C.; Gerdin, B. Increased lymphatic elimination of interstitial hyaluronan during E. coli sepsis in sheep Am. J. Physiol. 1989, 256, H1524-31
12. Takahashi, Y.; Li, L.; Kamiryo, M.; Asteriou, T.; Moustakas, A.; Yamashita, H.; Heldin, P. Hyaluronan fragments induce endothelial cell differentiation in a CD44- and CXCL1/GRO1-dependent manner J. Biol. Chem. 2005, 280, 24195-204
13. Slevin, M.; Kumar, S.; Gaffney, J. Angiogenic oligosaccharides of hyaluronan induce multiple signaling pathways affecting vascular endothelial cell mitogenic and wound healing responses J. Biol. Chem. 2002, 277, 41046-59
14. Matou-Nasri, S.; Gaffney, J.; Kumar, S.; Slevin, M. Oligosaccharides of hyaluronan induce angiogenesis through distinct CD44 and RHAMM-mediated signalling pathways involving Cdc2 and gamma-adducin Int. J. Oncol. 2009, 35, 761-73
15. Sugahara, K. N.; Murai, T.; Nishinakamura, H.; Kawashima, H.; Saya, H.; Miyasaka, M. Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44-expressing tumor cells J. Biol. Chem. 2003, 278, 32259-65
16. Sugahara, K. N.; Hirata, T.; Hayasaka, H.; Stern, R.; Murai, T.; Miyasaka, M. Tumor cells enhance their own CD44 cleavage and motility by generating hyaluronan fragments J. Biol. Chem. 2006, 281, 5861-8
17. Gilg, A. G.; Tye, S. L.; Tolliver, L. B.; Wheeler, W. G.; Visconti, R. P.; Duncan, J. D.; Kostova, F. V.; Bolds, L. N.; Toole, B. P.; Maria, B. L. Targeting hyaluronan interactions in malignant gliomas and their drug-resistant multipotent progenitors Clin. Cancer Res. 2008, 14, 1804-13
18. Campo, G. M.; Avenoso, A.; Campo, S.; D'Ascola, A.; Nastasi, G.; Calatroni, A. Small hyaluronan oligosaccharides induce inflammation by engaging both toll-like-4 and CD44 receptors in human chondrocytes Biochem. Pharmacol. 2010, 80, 480-490
19. McKee, C. M.; Penno, M. B.; Cowman, M.; Burdick, M. D.; Strieter, R. M.; Bao, C.; Noble, P. W. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44 J. Clin. Invest. 1996, 98, 2403-13
20. Ghatak, S.; Misra, S.; Toole, B. P. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway J. Biol. Chem. 2002, 277, 38013-20
21. Slomiany, M. G.; Dai, L.; Bomar, P. A.; Knackstedt, T. J.; Kranc, D. A.; Tolliver, L.; Maria, B. L.; Toole, B. P. Abrogating drug resistance in malignant peripheral nerve sheath tumors by disrupting hyaluronan-CD44 interactions with small hyaluronan oligosaccharides Cancer Res. 2009, 69, 4992-8
22. Slomiany, M. G.; Dai, L.; Tolliver, L. B.; Grass, G. D.; Zeng, Y.; Toole, B. P. Inhibition of Functional Hyaluronan-CD44 Interactions in CD133-positive Primary Human Ovarian Carcinoma Cells by Small Hyaluronan Oligosaccharides Clin. Cancer Res. 2009, 15, 7593-7601
23. Lüke, H. J.; Prehm, P. Synthesis and shedding of hyaluronan from plasma membranes of human fibroblasts and metastatic and non-metastatic melanoma cells Biochem. J. 1999, 343 (Pt 1) 71-5
24. Yang, C.; Cao, M.; Liu, H.; He, Y.; Xu, J.; Du, Y.; Liu, Y.; Wang, W.; Cui, L.; Hu, J.; Gao, F. The High and Low Molecular Weight Forms of Hyaluronan Have Distinct Effects on CD44 Clustering J. Biol. Chem. 2012, 287, 43094-43107
25. Stern, R.; Asari, A. A.; Sugahara, K. N. Hyaluronan fragments: An information-rich system Eur. J. Cell Biol. 2006, 85, 699-715
26. Underhill, C. B.; Chi-Rosso, G.; Toole, B. P. Effects of detergent solubilization on the hyaluronate-binding protein from membranes of simian virus 40-transformed 3T3 cells J. Biol. Chem. 1983, 258, 8086-91
27. Lesley, J. Hyaluronan Binding by Cell Surface CD44 J. Biol. Chem. 2000, 275, 26967-26975
28. Ye, L.; Mora, R.; Akhayani, N.; Haudenschild, C. C.; Liau, G. Growth factor and cytokine-regulated hyaluronan-binding protein TSG-6 is localized to the injury-induced rat neointima and confers enhanced growth in vascular smooth muscle cells Circ. Res. 1997, 81, 289-96
29. Jackson, D. G. Immunological functions of hyaluronan and its receptors in the lymphatics Immunol. Rev. 2009, 230, 216-31
30. Gao, F.; Yang, C. X.; Mo, W.; Liu, Y. W.; He, Y. Q. Hyaluronan oligosaccharides are potential stimulators to angiogenesis via RHAMM mediated signal pathway in wound healing Clin. Invest. Med. 2008, 31, E106-16
31. Krettek, A.; Sjöberg, S. CD44-a new cardiovascular drug target or merely an innocent bystander? Cardiovasc Hematol. Disord. Drug Targets 2009, 9, 293-302
32. Kashima, Y.; Takahashi, M.; Shiba, Y.; Itano, N.; Izawa, A.; Koyama, J.; Nakayama, J.; Taniguchi, S. a. i.; Kimata, K.; Ikeda, U. Crucial role of hyaluronan in neointimal formation after vascular injury PloS One 2013, 8, e58760
33. Zeidler, A.; Bräuer, R.; Thoss, K.; Bahnsen, J.; Heinrichs, V.; Jablonski-Westrich, D.; Wroblewski, M.; Rebstock, S.; Hamann, A. Therapeutic effects of antibodies against adhesion molecules in murine collagen type II-induced arthritis Autoimmunity 1995, 21, 245-52
34. Mikecz, K.; Brennan, F. R.; Kim, J. H.; Glant, T. T. Anti-CD44 treatment abrogates tissue oedema and leukocyte infiltration in murine arthritis Nat. Med. 1995, 1, 558-63
35. Rupp, U.; Schoendorf-Holland, E.; Eichbaum, M.; Schuetz, F.; Lauschner, I.; Schmidt, P.; Staab, A.; Hanft, G.; Huober, J.; Sinn, H.-P.; Sohn, C.; Schneeweiss, A. Safety and pharmacokinetics of bivatuzumab mertansine in patients with CD44v6-positive metastatic breast cancer: Final results of a phase I study Anticancer Drugs 2007, 18, 477-85
36. Riechelmann, H.; Sauter, A.; Golze, W.; Hanft, G.; Schroen, C.; Hoermann, K.; Erhardt, T.; Gronau, S. Phase I trial with the CD44v6-targeting immunoconjugate bivatuzumab mertansine in head and neck squamous cell carcinoma Oral Oncol. 2008, 44, 823-9
37. Hirota-Takahata, Y.; Harada, H.; Tanaka, I.; Nakata, T.; Nakajima, M.; Takahashi, M. F-19848 A, a novel inhibitor of hyaluronic acid binding to cellular receptor CD44 J. Antibiot. 2007, 60, 633-9
38. Zöller, M. CD44: Can a cancer-initiating cell profit from an abundantly expressed molecule? Nat. Rev. Cancer 2011, 11, 254-267
39. Teriete, P.; Banerji, S.; Noble, M.; Blundell, C. D.; Wright, A. J.; Pickford, A. R.; Lowe, E.; Mahoney, D. J.; Tammi, M. I.; Kahmann, J. D.; Campbell, I. D.; Day, A. J.; Jackson, D. G. Structure of the regulatory hyaluronan binding domain in the inflammatory leukocyte homing receptor CD44 Mol. Cell 2004, 13, 483-96
40. Banerji, S.; Wright, A. J.; Noble, M.; Mahoney, D. J.; Campbell, I. D.; Day, A. J.; Jackson, D. G. Structures of the Cd44-hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction Nat. Struct. Mol. Biol. 2007, 14, 234-9
41. Banerji, S.; Day, A. J.; Kahmann, J. D.; Jackson, D. G. Characterization of a functional hyaluronan-binding domain from the human CD44 molecule expressed in Escherichia coli Protein Expr. Purif. 1998, 14, 371-81
42. Alex, A.; Flocco, M. Fragment-based drug discovery: What has it achieved so far? Curr Top Med Chem 2007, 7, 1544-67
43. Coyne, A. G.; Scott, D. E.; Abell, C. Drugging challenging targets using fragment-based approaches Curr. Opin. Chem. Biol. 2010, 14, 299-307
44. Scott, D. E.; Ehebauer, M. T.; Pukala, T.; Marsh, M.; Blundell, T. L.; Venkitaraman, A. R.; Abell, C.; Hyvönen, M. Using a fragment-based approach to target protein-protein interactions ChemBioChem 2013, 14, 332-42
45. Takeda, M.; Ogino, S.; Umemoto, R.; Sakakura, M.; Kajiwara, M.; Sugahara, K. N.; Hayasaka, H.; Miyasaka, M.; Terasawa, H.; Shimada, I. Ligand-induced structural changes of the CD44 hyaluronan-binding domain revealed by NMR J. Biol. Chem. 2006, 281, 40089-40095
46. Ogino, S.; Nishida, N.; Umemoto, R.; Suzuki, M.; Takeda, M.; Terasawa, H.; Kitayama, J.; Matsumoto, M.; Hayasaka, H.; Miyasaka, M.; Shimada, I. Two-state conformations in the hyaluronan-binding domain regulate CD44 adhesiveness under flow condition Structure 2010, 18, 649-56
47. Tan, K. P.; Nguyen, T. B.; Patel, S.; Varadarajan, R.; Madhusudhan, M. S. Depth: a web server to compute depth, cavity sizes, detect potential small-molecule ligand-binding cavities and predict the pKa of ionizable residues in proteins Nucleic Acids Res. 2013, 41, W314-21
48. Peach, R. J.; Hollenbaugh, D.; Stamenkovic, I.; Aruffo, A. Identification of hyaluronic acid binding sites in the extracellular domain of CD44 J. Cell Biol. 1993, 122, 257-64
49. Jana, M.; Bandyopadhyay, S. Conformational flexibility of a protein-carbohydrate complex and the structure and ordering of surrounding water Phys. Chem. Chem. Phys. 2012, 14, 6628-38
50. Day, A. J. The structure and regulation of hyaluronan-binding proteins Biochem. Soc. Trans. 1999, 27, 115-121
51. Higman, V. A.; Blundell, C. D.; Mahoney, D. J.; Redfield, C.; Noble, M. E. M.; Day, A. J. Plasticity of the TSG-6 HA-binding loop and mobility in the TSG-6-HA complex revealed by NMR and X-ray crystallography J. Mol. Biol. 2007, 371, 669-84
52. Ween, M. P.; Hummitzsch, K.; Rodgers, R. J.; Oehler, M. K.; Ricciardelli, C. Versican induces a pro-metastatic ovarian cancer cell behavior which can be inhibited by small hyaluronan oligosaccharides Clin. Exp. Metastasis 2011, 28, 113-25
53. Midgley, A. C.; Rogers, M.; Hallett, M. B.; Clayton, A.; Bowen, T.; Phillips, A. O.; Steadman, R. Transforming Growth Factor-1 (TGF-1)-stimulated Fibroblast to Myofibroblast Differentiation Is Mediated by Hyaluronan (HA)-Facilitated Epidermal Growth Factor Receptor (EGFR) and CD44 Co-localization in Lipid Rafts J. Biol. Chem. 2013, 288, 14824-14838
54. Fujii, K.; Fujii, Y.; Hubscher, S.; Tanaka, Y. CD44 is the physiological trigger of Fas up-regulation on rheumatoid synovial cells J. Immunol. 2001, 167, 1198-203
55. Fitzgerald, K. A.; Bowie, A. G.; Skeffington, B. S.; O'Neill, L. A. Ras, protein kinase C zeta, and I kappa B kinases 1 and 2 are downstream effectors of CD44 during the activation of NF-kappa B by hyaluronic acid fragments in T-24 carcinoma cells J. Immunol. 2000, 164, 2053-63
56. Bourguignon, L. Y. W.; Gilad, E.; Rothman, K.; Peyrollier, K. Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression J. Biol. Chem. 2005, 280, 11961-72
57. Hamilton, S. R.; Fard, S. F.; Paiwand, F. F.; Tolg, C.; Veiseh, M.; Wang, C.; McCarthy, J. B.; Bissell, M. J.; Koropatnick, J.; Turley, E. A. The hyaluronan receptors CD44 and Rhamm (CD168) form complexes with ERK1,2 that sustain high basal motility in breast cancer cells J. Biol. Chem. 2007, 282, 16667-80
58. Kouvidi, K.; Berdiaki, A.; Nikitovic, D.; Katonis, P.; Afratis, N.; Hascall, V. C.; Karamanos, N. K.; Tzanakakis, G. N. Role of receptor for hyaluronic acid-mediated motility (RHAMM) in low molecular weight hyaluronan (LMWHA)-mediated fibrosarcoma cell adhesion J. Biol. Chem. 2011, 286, 38509-20
59. Xu, Y.; Stamenkovic, I.; Yu, Q. CD44 attenuates activation of the hippo signaling pathway and is a prime therapeutic target for glioblastoma Cancer Res. 2010, 70, 2455-64
60. Bourguignon, L. Y. W. Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression Semin. Cancer Biol. 2008, 18, 251-9
61. Harada, H.; Takahashi, M. CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and -2 J. Biol. Chem. 2007, 282, 5597-607
62. Zaytseva, Y. Y.; Rychahou, P. G.; Gulhati, P.; Elliott, V. A.; Mustain, W. C.; O'Connor, K.; Morris, A. J.; Sunkara, M.; Weiss, H. L.; Lee, E. Y.; Evers, B. M. Inhibition of fatty acid synthase attenuates CD44-associated signaling and reduces metastasis in colorectal cancer Cancer Res. 2012, 72, 1504-17
63. Tian, X.; Azpurua, J.; Hine, C.; Vaidya, A.; Myakishev-Rempel, M.; Ablaeva, J.; Mao, Z.; Nevo, E.; Gorbunova, V.; Seluanov, A. High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat Nature 2013, 499, 346-9
64. Mahoney, D. J.; Aplin, R. T.; Calabro, A.; Hascall, V. C.; Day, A. J. Novel methods for the preparation and characterization of hyaluronan oligosaccharides of defined length Glycobiology 2001, 11, 1025-33
65. Giannetti, A. M. From experimental design to validated hits a comprehensive walk-through of fragment lead identification using surface plasmon resonance Methods Enzymol. 2011, 493, 169-218
66. Elinder, M.; Geitmann, M.; Gossas, T.; Kallblad, P.; Winquist, J.; Nordstrom, H.; Hamalainen, M.; Danielson, U. H. Experimental Validation of a Fragment Library for Lead Discovery Using SPR Biosensor Technology J. Biomol. Screening 2011, 16, 15-25
67. Kabsch, W. XDS Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 125-132
68. Evans, P. Scaling and assessment of data quality Acta Crystallogr., Sect. D: Biol. Crystallogr. 2005, 62, 72-82
69. McCoy, A. J.; Grosse-Kunstleve, R. W.; Adams, P. D.; Winn, M. D.; Storoni, L. C.; Read, R. J. Phasercrystallographic software J. Appl. Crystallogr. 2007, 40, 658-674
70. Emsley, P.; Lohkamp, B.; Scott, W. G.; Cowtan, K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 486-501
71. Murshudov, G. N.; Skubák, P.; Lebedev, A. A.; Pannu, N. S.; Steiner, R. A.; Nicholls, R. A.; Winn, M. D.; Long, F.; Vagin, A. A. REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr., Sect. D: Biol. Crystallogr. 2011, 67, 355-367
72. Lebedev, A. A.; Young, P.; Isupov, M. N.; Moroz, O. V.; Vagin, A. A.; Murshudov, G. N. JLigand: A graphical tool for the CCP4 template-restraint library Acta Crystallogr., Sect. D: Biol. Crystallogr. 2012, 68, 431-40
73. Schüttelkopf, A. W.; van Aalten, D. M. F. PRODRG: A tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 1355-63
74. Chen, V. B.; Arendall, W. B.; Headd, J. J.; Keedy, D. A.; Immormino, R. M.; Kapral, G. J.; Murray, L. W.; Richardson, J. S.; Richardson, D. C. MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 2010, 66, 12-21
75. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank Nucleic Acids Res. 2000, 28, 235-42 Development