Combinatorial and computational approaches to identify interactions of macrophage colony-stimulating factor (M-CSF) and its receptor c-FMS

Journal of Biological Chemistry

Volumn 290, Issue 43, 2015, Pages 26180-26193

  Rosenfeld, Lior ^a   Shirian, Jason ^a   Zur, Yuval ^a,b   Levaot, Noam ^b   Shifman, Julia M ^a   Papo, Niv ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; MACROPHAGES; PROTEINS;

COLONY-STIMULATING FACTOR; COMBINATORIAL LIBRARY; COMPUTATIONAL APPROACH; COMPUTATIONAL PREDICTIONS; INTERMOLECULAR INTERACTIONS; MACROPHAGE COLONY STIMULATING FACTORS; TYROSINE-KINASE RECEPTORS; YEAST SURFACE DISPLAYS;

BINS;

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR RECEPTOR; PROTEIN BINDING;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL SELECTION; CELL SURFACE DISPLAY; CONTROLLED STUDY; DIMERIZATION; FLOW CYTOMETRY; MOLECULAR INTERACTION; MOLECULAR LIBRARY; MUTATIONAL ANALYSIS; PREDICTION; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; RESIDUE ANALYSIS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; SURFACE PROPERTY; CHEMISTRY; COMBINATORIAL CHEMISTRY; HUMAN; METABOLISM; PROTEIN CONFORMATION;

COMBINATORIAL CHEMISTRY TECHNIQUES; FLOW CYTOMETRY; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR;

EID: 84944937241     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.671271     Document Type: Article

References (66)

1. Zhao, Y., Muir, T. W., Kent, S. B., Tischer, E., Scardina, J. M., and Chait, B. T. (1996) Mapping protein-protein interactions by affinity-directed mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 93, 4020-4024
2. Chakrabarti, P., and Janin, J. (2002) Dissecting protein-protein recognition sites. Proteins Struct. Funct. Genet. 47, 334-343
3. Erijman, A., Rosenthal, E., and Shifman, J. M. (2014) How structure defines affinity in protein-protein interactions. PLoS ONE 9, e110085
4. Murciano-Calles, J., McLaughlin, M. E., Erijman, A., Hooda, Y., Chakravorty, N., Martinez, J. C., Shifman, J. M., and Sidhu, S. S. (2014) Alteration of the C-terminal ligand specificity of the Erbin PDZ domain by allosteric mutational effects. J. Mol. Biol. 426, 1-9
5. Lefèvre, F., Rémy, M. H., and Masson, J. M. (1997) Alanine-stretch scanning mutagenesis: a simple and efficient method to probe protein structure and function. Nucleic Acids Res. 25, 447-448
6. Weiss, G. A., Watanabe, C. K., Zhong, A., Goddard, A., and Sidhu, S. S. (2000) Rapid mapping of protein functional epitopes by combinatorial alanine scanning. Proc. Natl. Acad. Sci. U. S. A. 97, 8950-8954
7. Cortese, R., Felici, F., Galfre, G., Luzzago, A., Monaci, P., and Nicosia, A. (1994) Epitope discovery using peptide libraries displayed on phage. Trends Biotechnol. 12, 262-267
8. Fack, F., Hügle-Dörr, B., Song, D., Queitsch, I., Petersen, G., and Bautz, E. K. (1997) Epitope mapping by phage display: random versus gene-fragment libraries. J. Immunol. Methods. 206, 43-52
9. Pál, G., Kouadio, J. L., Artis, D. R., Kossiakoff, A. A., and Sidhu, S. S. (2006) Comprehensive and quantitative mapping of energy landscapes for proteinprotein interactions by rapid combinatorial scanning. J. Biol. Chem. 281, 22378-22385
10. Boder, E. T., and Wittrup, K. D. (2000) Yeast surface display for directed evolution of protein expression, affinity, and stability. Methods Enzymol. 328, 430-444
11. Chao, G., Lau, W. L., Hackel, B. J., Sazinsky, S. L., Lippow, S. M., and Wittrup, K. D. (2006) Isolating and engineering human antibodies using yeast surface display. Nat. Protoc. 1, 755-768
12. Gai, S. A., and Wittrup, K. D. (2007) Yeast surface display for protein engineering and characterization. Curr. Opin. Struct. Biol. 17, 467-473
13. Boder, E. T., and Wittrup, K. D. (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat. Biotechnol. 15, 553-557
14. Taylor, E. W., Fear, A. L., Bohm, A., Kim, S. H., and Koths, K. (1994) Structure-function studies on recombinant human macrophage colonystimulating factor (M-CSF). J. Biol. Chem. 269, 31171-31177
15. Tanner, W., and Lehle, L. (1987) Protein glycosylation in yeast. Biochim. Biophys. Acta 906, 81-99
16. Brooks, S. A. (2004) Appropriate glycosylation of recombinant proteins for human use: implications of choice of expression system. Mol. Biotechnol. 28, 241-255
17. Cochran, J. R., Kim, Y. S., Olsen, M. J., Bhandari, R., and Wittrup, K. D. (2004) Domain-level antibody epitope mapping through yeast surface display of epidermal growth factor receptor fragments. J. Immunol. Methods 287, 147-158
18. Mata-Fink, J., Kriegsman, B., Yu, H. X., Zhu, H., Hanson, M. C., Irvine, D. J., and Wittrup, K. D. (2013) Rapid conformational epitope mapping of anti-gp120 antibodies with a designed mutant panel displayed on yeast. J. Mol. Biol. 425, 444-456
19. Levy, R., Forsyth, C. M., LaPorte, S. L., Geren, I. N., Smith, L. A., and Marks, J. D. (2007) Fine and domain-level epitope mapping of botulinum neurotoxin type A neutralizing antibodies by yeast surface display. J. Mol. Biol. 365, 196-210
20. Sharabi, O., Erijman, A., and Shifman, J. M. (2013) Computational methods for controlling binding specificity. Methods Enzymol. 523, 41-59
21. Sharabi, O., Shirian, J., and Shifman, J. M. (2013) Predicting affinity- and specificity-enhancing mutations at protein-protein interfaces. Biochem. Soc. Trans. 41, 1166-1169
22. Filchtinski, D., Sharabi, O., Rüppel, A., Vetter, I. R., Herrmann, C., and Shifman, J. M. (2010) What makes Ras an efficient molecular switch: a computational, biophysical, and structural study of Ras-GDP interactions with mutants of Raf. J. Mol. Biol. 399, 422-435
23. Aizner, Y., Sharabi, O., Shirian, J., Dakwar, G., Abvraham, O., Risman, M., and Shifman, J. M. (2014) Mapping the binding landscape of a picomolar protein-protein complex through computation and experiment. Structure 22, 1-10
24. Sharabi, O., Shirian, J., Grossman, M., Lebendiker, M., Sagi, I., and Shifman, J. (2014) Affinity- and specificity-enhancing mutations are frequent in multispecific interaction between MMP14 and its inhibitor TIMP2. PLoS ONE 9, e93712
25. Schymkowitz, J. W., Rousseau, F., Martins, I. C., Ferkinghoff-Borg, J., Stricher, F., and Serrano, L. (2005) Prediction of water and metal binding sites and their affinities by using the Fold-X force field. Proc. Natl. Acad. Sci. U. S. A. 102, 10147-10152
26. Dahiyat, B. I., Sarisky, C. A., and Mayo, S. L. (1997) De novo protein design: toward fully automated sequence selection. J. Mol. Biol. 273, 789-796
27. Kim, D. E., Chivian, D., and Baker, D. (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32, W526-W531
28. Bartelmez, S. H., Bradley, T. R., Bertoncello, I., Mochizuki, D. Y., Tushinski, R. J., Stanley, E. R., Hapel, A. J., Young, I. G., Kriegler, A. B., and Hodgson, G. S. (1989) Interleukin 1 plus interleukin 3 plus colony-stimulating factor 1 are essential for clonal proliferation of primitive myeloid bone marrow cells. Exp. Hematol. 17, 240-245
29. Douglass, T. G., Driggers, L., Zhang, J. G., Hoa, N., Delgado, C., Williams, C. C., Dan, Q., Sanchez, R., Jeffes, E. W., Wepsic, H. T., Myers, M. P., Koths, K., and Jadus, M. R. (2008) Macrophage colony stimulating factor: not just for macrophages anymore! A gateway into complex biologies. Int. Immunopharmacol. 8, 1354-1376
30. Stanley, E. R., and Chitu, V. (2014) CSF-1 receptor signaling in myeloid cells. Cold Spring Harb. Symp. Quant. Biol. 6, 1-21
31. Tushinski, R. J., Oliver, I. T., Guilbert, L. J., Tynan, P. W., Warner, J. R., and Stanley, E. R. (1982) Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell 28, 71-81
32. Yasuda, H., Shima, N., Nakagawa, N., Yamaguchi, K., Kinosaki, M., Mochizuki, S., Tomoyasu, A., Yano, K., Goto, M., Murakami, A., Tsuda, E., Morinaga, T., Higashio, K., Udagawa, N., Takahashi, N., and Suda, T. (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. U. S. A. 95, 3597-3602
33. Wiktor-Jedrzejczak, W., Bartocci, A., Ferrante, A. W., Jr., Ahmed-Ansari, A., Sell, K. W., Pollard, J. W., and Stanley, E. R. (1990) Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. U. S. A. 87, 4828-4832
34. Yoshida, H., Hayashi, S., Kunisada, T., Ogawa, M., Nishikawa, S., Okamura, H., Sudo, T., Shultz, L. D., and Nishikawa, S. (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345, 442-444
35. Dai, X. M., Ryan, G. R., Hapel, A. J., Dominguez, M. G., Russell, R. G., Kapp, S., Sylvestre, V., and Stanley, E. R. (2002) Targeted disruption of the mouse CSF-1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies and reproductive defects. Blood 99, 111-120
36. Chockalingam, S., and Ghosh, S. S. (2014) Macrophage colony-stimulating factor and cancer: a review. Tumour Biol. 35, 10635-10644
37. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555
38. Laoui, D., Van Overmeire, E., De Baetselier, P., Van Ginderachter, J. A., and Raes, G. (2014) Functional relationship between tumor-associated macrophages and macrophage colony-stimulating factor as contributors to cancer progression. Front. Immunol. 5, 1-15
39. Lin, E. Y., Gouon-Evans, V., Nguyen, A. V., and Pollard, J. W. (2002) The macrophage growth factor CSF-1 in mammary gland development and tumor progression. J. Mammary Gland Biol. Neoplasia. 7, 147-162
40. Murray, L. J., Abrams, T. J., Long, K. R., Ngai, T. J., Olson, L. M., Hong, W., Keast, P. K., Brassard, J. A., O'Farrell, A. M., Cherrington, J. M., and Pryer, N. K. (2003) SU11248 inhibits tumor growth and CSF-1R-dependent osteolysis in an experimental breast cancer bone metastasis model. Clin. Exp. Metastasis. 20, 757-766
41. Escamilla, J., Schokrpur, S., Liu, C., Priceman, S. J., Moughon, D., Jiang, Z., Pouliot, F., Magyar, C., Sung, J. L., Xu, J., Deng, G., West, B. L., Bollag, G., Fradet, Y., Lacombe, L., Jung, M. E., Huang, J., and Wu, L. (2015) CSF1 receptor targeting in prostate cancer reverses macrophage-mediated resistance to androgen blockade therapy. Cancer Res. 75, 950-962
42. Sluijter, M., van der Sluis, T. C., van der Velden, P. A., Versluis, M., West, B. L., van der Burg, S. H., and van Hall, T. (2014) Inhibition of CSF-1R supports T-cell mediated melanoma therapy. PLoS ONE 9, e104230
43. Gronski, P., Badziong, W., Habermann, P., List, W., Müllner, H., Neurohr, K. J., Tripier, D., and Seiler, F. R. (1988) E. coli derived human granulocytemacrophage colony-stimulating factor (rh GM-CSF) available for clinical trials. Behring Inst. Mitt. 83, 246-249
44. Liu, H., Leo, C., Chen, X., Wong, B. R., Williams, L. T., Lin, H., and He, X. (2012) The mechanism of shared but distinct CSF-1R signaling by the non-homologous cytokines IL-34 and CSF-1. Biochim. Biophys. Acta. 1824, 938-945
45. Colby, D. W., Kellogg, B. A., Graff, C. P., Yeung, Y. A., Swers, J. S., and Wittrup, K. D. (2004) Engineering antibody affinity by yeast surface display. Methods Enzymol. 388, 348-358
46. Cregg, J. M., Barringer, K. J., Hessler, A. Y., and Madden, K. R. (1985) Pichia pastoris as a host system for transformations. Mol. Cell. Biol. 5, 3376-3385
47. Daly, R., and Hearn, M. T. (2005) Expression of heterologous proteins in Pichia pastoris: a useful experimental tool in protein engineering and production. J. Mol. Recognit. 18, 119-138
48. Macauley-Patrick, S., Fazenda, M. L., McNeil, B., and Harvey, L. M. (2005) Heterologous protein production using the Pichia pastoris expression system. Yeast 22, 249-270
49. Luo, Y., Yuan, Z., Luo, G., and Zhao, F. (2008) Expression of secreted His-tagged S-adenosylmethionine synthetase in the methylotrophic yeast Pichia pastoris and its characterization, one-step purification, and immobilization. Biotechnol. Prog. 24, 214-220
50. Cregg, J. M., Cereghino, J. L., Shi, J., and Higgins, D. R. (2000) Recombinant protein expression in Pichia pastoris. Mol. Biotechnol. 16, 23-52
51. Shi, X., Karkut, T., Chamankhah, M., Alting-Mees, M., Hemmingsen, S. M., and Hegedus, D. (2003) Optimal conditions for the expression of a single-chain antibody (scFv) gene in Pichia pastoris. Protein Expr. Purif. 28, 321-330
52. Ma, X., Lin, W. Y., Chen, Y., Stawicki, S., Mukhyala, K., Wu, Y., Martin, F., Bazan, J. F., and Starovasnik, M. A. (2012) Structural basis for the dual recognition of helical cytokines IL-34 and CSF-1 by CSF-1R. Structure 20, 676-687
53. Elegheert, J., Bracke, N., Pouliot, P., Gutsche, I., Shkumatov, A. V., Tarbouriech, N., Verstraete, K., Bekaert, A., Burmeister, W. P., Svergun, D. I., Lambrecht, B. N., Vergauwen, B., and Savvides, S. N. (2012) Allosteric competitive inactivation of hematopoietic CSF-1 signaling by the viral decoy receptor BARF1. Nat. Struct. Mol. Biol. 19, 938-947
54. Chen, X., Liu, H., Focia, P. J., Shim, A. H., and He, X. (2008) Structure of macrophage colony stimulating factor bound to FMS: diverse signaling assemblies of class III receptor tyrosine kinases. Proc. Natl. Acad. Sci. U. S. A. 105, 18267-18272
55. Gray, J. J., Moughon, S., Wang, C., Schueler-Furman, O., Kuhlman, B., Rohl, C. A., and Baker, D. (2003) Protein-protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations. J. Mol. Biol. 331, 281-299
56. Lyskov, S., Chou, F. C., Conchúir, S. Ó., Der, B. S., Drew, K., Kuroda, D., Xu, J., Weitzner, B. D., Renfrew, P. D., Sripakdeevong, P., Borgo, B., Havranek, J. J., Kuhlman, B., Kortemme, T., Bonneau, R., Gray, J. J., and Das, R. (2013) Serverification of molecular modeling applications: the Rosetta Online Server that includes everyone (ROSIE). PLoS ONE 8, e63906
57. Sharabi, O., Dekel, A., and Shifman, J. M. (2011) Triathlon for energy functions: Who is the winner for design of protein-protein interactions? Proteins 79, 1487-1498
58. Dunbrack, R. L., Jr., and Karplus, M. (1993) Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J. Mol. Biol. 230, 543-574
59. Desmet, J., De Maeyer, M., Hazes, B., and Lasters, I. (1992) The dead-end elimination theorem and its use in protein side-chain positioning. Nature 356, 539-542
60. Gordon, D. B., Hom, G. K., Mayo, S. L., and Pierce, N. A. (2003) Exact rotamer optimization for protein design. J. Comput. Chem. 24, 232-243
61. Chao, G., Cochran, J. R., and Wittrup, K. D. (2004) Fine epitope mapping of anti-epidermal growth factor receptor antibodies through random mutagenesis and yeast surface display. J. Mol. Biol. 342, 539-550
62. Van Blarcom, T., Rossi, A., Foletti, D., Sundar, P., Pitts, S., Bee, C., Melton Witt, J., Melton, Z., Hasa-Moreno, A., Shaughnessy, L., Telman, D., Zhao, L., Cheung, W. L., Berka, J., Zhai, W., et al. (2015) Precise and efficient antibody epitope determination through library design, yeast display, and next generation sequencing. J. Mol. Biol. 427, 1513-1534
63. Thompson, L. C., Walters, J., Burke, J., Parsons, J. F., Armstrong, R. N., and Dirr, H. W. (2006) Double mutation at the subunit interface of glutathione transferase rGSTM1-1 results in a stable, folded monomer. Biochemistry 45, 2267-2273
64. Schreiber, G., and Fersht, A. R. (1995) Energetics of protein-protein interactions: analysis of the barnase-barstar interface by single mutations and double mutant cycles. J. Mol. Biol. 248, 478-486
65. Selzer, T., Albeck, S., and Schreiber, G. (2000) Rational design of faster associating and tighter binding protein complexes. Nat. Struct. Biol. 7, 537-541
66. Doolan, K. M., and Colby, D. W. (2015) Conformation-dependent epitopes recognized by prion protein antibodies probed using mutational scanning and deep sequencing. J. Mol. Biol. 427, 328-340