Expanding the utility of β-galactosidase complementation: Piece by piece

Molecular Pharmaceutics

Volumn 7, Issue 1, 2010, Pages 60-74

  Broome, Ann Marie ^a,b   Bhavsar, Nihir ^a   Ramamurthy, Gopalakrishnan ^b   Newton, Gail ^c   Basilion, James P ^a,b,d  

^a Case Western Reserve University   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

galactosidase; Complementation; Enzyme fragments; Targeted reporter complex

Indexed keywords

BETA GALACTOSIDASE; CELL SURFACE RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; POLYPEPTIDE; TRANSFERRIN RECEPTOR;

ARTICLE; BACTERIAL CELL; ENZYME ACTIVITY; FRAGMENTATION REACTION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

ANIMALS; BETA-GALACTOSIDASE; CELL LINE, TUMOR; ESCHERICHIA COLI K12; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; GLIOMA; HUMANS; PEPTIDE FRAGMENTS; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, TRANSFERRIN; TRANSFECTION; TUMOR MARKERS, BIOLOGICAL;

EID: 76249116272     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp900188e     Document Type: Article

References (58)

1. Stephen, R. M.; Gillies, R. J. Promise and progress for functional and molecular imaging of response to targeted therapies. Pharm. Res. 2007, 24 (6), 1172-1185.
2. Alper, O.; Bergmann-Leitner, E. S.; Bennett, T. A.; Hacker, N. F.; Stromberg, K.; Stetler-Stevenson, W. G. Epidermal growth factor receptor signaling and the invasive phenotype of ovarian carcinoma cells. J. Natl. Cancer Inst. 2001, 93 (18), 1375-1384.
3. Magkou, C.; Nakopoulou, L.; Zoubouli, C.; Karali, K.; Theohari, I.; Bakarakos, P.; Giannopoulou, I. Expression of the epidermal growth factor receptor (EGFR) and the phosphorylated EGFR in invasive breast carcinomas. Breast Cancer Res. 2008, 10 (3), R49.
4. Hoelzinger, D. B.; Mariani, L.; Weis, J.; Woyke, T.; Berens, T. J.; McDonough, W. S.; Sloan, A.; Coons, S. W.; Berens, M. E. Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets. Neoplasia 2005, 7 (1), 7-16.
5. Nakada, M.; Nakada, S.; Demuth, T.; Tran, N. L.; Hoelzinger, D. B.; Berens, M. E. Molecular targets of glioma invasion. Cell. Mol. Life Sci. 2007, 64 (4), 458-478.
6. Krahn, G.; Leiter, U.; Kaskel, P.; Udart, M.; Utikal, J.; Bezold, G.; Peter, R. U. Coexpression patterns of EGFR, HER2, HER3 and HER4 in non-melanoma skin cancer. Eur. J. Cancer 2001, 37 (2), 251-259.
7. Hogemann-Savellano, D.; Bos, E.; Blondet, C.; Sato, F.; Abe, T.; Josephson, L.; Weissleder, R.; Gaudet, J.; Sgroi, D.; Peters, P. J.; Basilion, J. P. The transferrin receptor: a potential molecular imaging marker for human cancer. Neoplasia 2003, 5 (6), 495-506.
8. Habashy, H. O.; Powe, D. G.; Staka, C. M.; Rakha, E. A.; Ball, G.; Green, A. R.; Aleskandarany, M.; Paish, E. C.; Douglas, M. R.; Nicholson, R. I.; Ellis, I. O.; Gee, J. M. Transferrin receptor (CD71) is a marker of poor prognosis in breast cancer and can predict response to tamoxifen. Breast Cancer Res. Treat., submitted.
9. Liu, T. F.; Tatter, S. B.; Willingham, M. C.; Yang, M.; Hu, J. J.; Frankel, A. E. Growth factor receptor expression varies among high-grade gliomas and normal brain: epidermal growth factor receptor has excellent properties for interstitial fusion protein therapy. Mol. Cancer Ther. 2003, 2 (8), 783-787.
10. Gazdar, A. F. Activating and resistance mutations of EGFR in non-small-cell lung cancer: role in clinical response to EGFR tyrosine kinase inhibitors. Oncogene 2009, 28 (Suppl. 1), S24-S31.
11. Suzuki, M.; Shigematsu, H.; Hiroshima, K.; Iizasa, T.; Nakatani, Y.; Minna, J. D.; Gazdar, A. F.; Fujisawa, T. Epidermal growth factor receptor expression status in lung cancer correlates with its mutation. Hum. Pathol. 2005, 36 (10), 1127-1134.
12. Gillies, R. J.; Hoffman, J. M.; Lam, K. S.; Menkens, A. E.; Piwnica-Worms, D. R.; Sullivan, D. C.; Weissleder, R. Meeting report: high-throughput technologies for in vivo imaging agents. Mol. Imaging 2005, 4 (2), 98-103.
13. Gal-Yam, E. N.; Saito, Y.; Egger, G.; Jones, P. A. Cancer epigenetics: modifications, screening, and therapy. Annu. Rev. Med. 2008, 59, 267-280.
14. Sharma, S.; Kelly, T. K.; Jones, P. A. Epigenetics in Cancer. Carcinogenesis, submitted.
15. Chen, B.; O' Connell, C. D.; Boone, D. J.; Amos, J. A.; Beck, J. C.; Chan, M. M.; Farkas, D. H.; Lebo, R. V.; Richards, C. S.; Roa, B. B.; Silverman, L. M.; Barton, D. E.; Bejjani, B. A.; Belloni, D. R.; Bernacki, S. H.; Caggana, M.; Charache, P.; Dequeker, E.; Ferreira-Gonzalez, A.; Friedman, K. J.; Greene, C. L.; Grody, W. W.; Highsmith, W. E., Jr.; Hinkel, C. S.; Kalman, L. V.; Lubin, I. M.; Lyon, E.; Payne, D. A.; Pratt, V. M.; Rohlfs, E.; Rundell, C. A.; Schneider, E.; Willey, A. M.; Williams, L. O.; Willey, J. C.; Winn-Deen, E. S.; Wolff, D. J. Developing a sustainable process to provide quality control materials for genetic testing. Genet. Med 2005, 7 (8), 534-549.
16. Gregg, J. P.; Grody, W. W. Molecular pathology and cancer genetic screening. West. J. Med 1995, 162 (5), 449-450.
17. Grody, W. W. Molecular genetic risk screening. Annu. Rev. Med. 2003, 54, 473-490.
18. Maddox, C. B.; Rasmussen, L.; White, E. L. Adapting Cell-Based Assays to the High Throughput Screening Platform: Problems Encountered and Lessons Learned. JALA 2008, 13 (3), 168-173.
19. Borloo, J.; De, S. L.; Vergauwen, B.; Van Beeumen, J. J.; Devreese, B. A beta-galactosidase-based bacterial two-hybrid system to assess protein-protein interactions in the correct cellular environment. J. Proteome Res. 2007, 6 (7), 2587-2595.
20. Galarneau, A.; Primeau, M.; Trudeau, L. E.; Michnick, S. W. Betalactamase protein fragment complementation assays as in vivo and in vitro sensors of protein protein interactions. Nat. Biotechnol. 2002, 20 (6), 619-622.
21. Luker, K. E.; Piwnica-Worms, D. Optimizing luciferase protein fragment complementation for bioluminescent imaging of proteinprotein interactions in live cells and animals. Methods Enzymol. 2004, 385, 349-360.
22. Remy, I.; Michnick, S. W. Clonal selection and in vivo quantitation of protein interactions with protein-fragment complementation assays. Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (10), 5394-5399.
23. Gong, H.; Zhang, B.; Little, G.; Kovar, J.; Chen, H.; Xie, W.; Schutz-Geschwender, A.; Olive, D. M. beta-Galactosidase activity assay using far-red-shifted fluorescent substrate DDAOG. Anal. Biochem. 2009, 386 (1), 59-64.
24. Ho, N. H.; Weissleder, R.; Tung, C. H. A self-immolative reporter for beta-galactosidase sensing. ChemBioChem 2007, 8 (5), 560-566.
25. Tung, C. H.; Zeng, Q.; Shah, K.; Kim, D. E.; Schellingerhout, D.; Weissleder, R. In vivo imaging of beta-galactosidase activity using far red fluorescent switch. Cancer Res. 2004, 64 (5), 1579-1583.
26. Ullmann, A.; JACOB, F.; MONOD, J. Characterization by in vitro complementation of a peptide corresponding to an operator-proximal segment of the beta-galactosidase structural gene of Escherichia coli. J. Mol. Biol. 1967, 24 (2), 339-343.
27. Jacobson, R. H.; Zhang, X. J.; DuBose, R. F.; Matthews, B. W. Three-dimensional structure of beta-galactosidase from E. coli. Nature 1994, 369 (6483), 761-766.
28. Jacobson, R. H.; Matthews, B. W. Crystallization of beta-galactosidase from Escherichia coli. J. Mol. Biol. 1992, 223 (4), 1177-1182.
29. Jacob, F.; Ullman, A.; Monod, J. The promotor, a genetic element necessary to the expression of an operon. C. R. Hebd. Seances Acad. Sci. 1964, 258, 3125-3128.
30. Villarejo, M. R.; Zabin, I. Beta-galactosidase from termination and deletion mutant strains. J. Bacteriol. 1974, 120 (1), 466-474.
31. Rossi, F.; Charlton, C. A.; Blau, H. M. Monitoring protein-protein interactions in intact eukaryotic cells by beta-galactosidase complementation. Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (16), 8405-8410.
32. Langley, K. E.; Fowler, A. V.; Zabin, I. Amino acid sequence of beta-galactosidase. IV. Sequence of an alpha-complementing cyanogen bromide peptide, residues 3 to 92. J. Biol. Chem. 1975, 250 (7), 2587-2592.
33. Mohler, W. A.; Blau, H. M. Gene expression and cell fusion analyzed by lacZ complementation in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 1996, 93 (22), 12423-12427.
34. Wehrman, T.; Kleaveland, B.; Her, J. H.; Balint, R. F.; Blau, H. M. Protein-protein interactions monitored in mammalian cells via complementation of beta -lactamase enzyme fragments. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (6), 3469-3474.
35. Paulmurugan, R.; Gambhir, S. S. Monitoring protein-protein interactions using split synthetic renilla luciferase protein-fragment-assisted complementation. Anal. Chem. 2003, 75 (7), 1584-1589.
36. Paulmurugan, R.; Gambhir, S. S. Firefly luciferase enzyme fragment complementation for imaging in cells and living animals. Anal. Chem. 2005, 77 (5), 1295-1302.
37. Fung, P.; Peng, K.; Kobel, P.; Dotimas, H.; Kauffman, L.; Olson, K.; Eglen, R. M. A homogeneous cell-based assay to measure nuclear translocation using beta-galactosidase enzyme fragment complementation. Assay Drug Dev. Technol. 2006, 4 (3), 263-272.
38. Hammer, M. M.; Wehrman, T. S.; Blau, H. M. A novel enzyme complementation-based assay for monitoring G-protein-coupled receptor internalization. FASEB J. 2007, 21 (14), 3827-3834.
39. Villalobos, V.; Naik, S.; Piwnica-Worms, D. Detection of protein-protein interactions in live cells and animals with split firefly luciferase protein fragment complementation. Methods Mol. Biol. 2008, 439, 339-352.
40. Nichtl, A.; Buchner, J.; Jaenicke, R.; Rudolph, R.; Scheibel, T. Folding and association of beta-galactosidase. J. Mol. Biol. 1998, 282 (5), 1083-1091.
41. Ozawa, T.; Takeuchi, T. M.; Kaihara, A.; Sato, M.; Umezawa, Y. Protein splicing-based reconstitution of split green fluorescent protein for monitoring protein-protein interactions in bacteria: improved sensitivity and reduced screening time. Anal. Chem. 2001, 73 (24), 5866-5874.
42. Lehming, N. Analysis of protein-protein proximities using the split-ubiquitin system. Briefings Funct. Genomic Proteomic 2002, 1 (3), 230-238.
43. Reichel, C.; Johnsson, N. The split-ubiquitin sensor: measuring interactions and conformational alterations of proteins in vivo. Methods Enzymol. 2005, 399, 757-776.
44. Muller, J.; Johnsson, N. Split-ubiquitin and the split-protein sensors: chessman for the endgame. ChemBioChem 2008, 9 (13), 2029-2038.
45. Piwnica-Worms, D.; Luker, K. E. Imaging protein-protein interactions in whole cells and living animals. Ernst Schering Res. Found. Workshop 2005, (49), 35-41.
46. Luker, K. E.; Smith, M. C.; Luker, G. D.; Gammon, S. T.; Piwnica-Worms, H.; Piwnica-Worms, D. Kinetics of regulated protein-protein interactions revealed with firefly luciferase complementation imaging in cells and living animals. Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (33), 12288-12293.
47. Michnick, S. W.; Remy, I.; Campbell-Valois, F. X.; Vallee-Belisle, A.; Pelletier, J. N. Detection of protein-protein interactions by protein fragment complementation strategies. Methods Enzymol. 2000, 328, 208-230.
48. Shiba, K.; Schimmel, P. Functional assembly of a randomly cleaved protein. Proc. Natl. Acad. Sci. U.S.A. 1992, 89 (5), 1880-1884.
49. Dibya, D.; Sander, S.; Smith, E. A. Identifying cytoplasmic proteins that affect receptor clustering using fluorescence resonance energy transfer and RNA interference. Anal. Bioanal. Chem., submitted.
50. Guo, C.; Levine, H. A thermodynamic model for receptor clustering. Biophys. J. 1999, 77 (5), 2358-2365.
51. Eglen, R. M.; Singh, R. Beta galactosidase enzyme fragment complementation as a novel technology for high throughput screening. Comb. Chem. High Throughput Screening 2003, 6 (4), 381-387.
52. Stahl, P. D.; Barbieri, M. A. Multivesicular bodies and multivesicular endosomes: the "ins and outs" of endosomal traffic. Sci. STKE 2002, 2002 (141), e32.
53. Pastan, I.; Hanover, J.; Willingham, M. The cellular entry of EGF and transferrin: a problem in intracellular sorting. Curr. Top. Cell Regul. 1985, 26, 17-25.
54. Dargemont, C.; Le, B. A.; Rothenberger, S.; Iacopetta, B.; Kuhn, L. C. The internalization signal and the phosphorylation site of transferrin receptor are distinct from the main basolateral sorting information. EMBO J. 1993, 12 (4), 1713-1721.
55. Roberts, R. L.; Fine, R. E.; Sandra, A. Receptor-mediated endocytosis of transferrin at the blood-brain barrier. J. Cell Sci. 1993, 104 (2), 521-532.
56. Leonard, D.; Hayakawa, A.; Lawe, D.; Lambright, D.; Bellve, K. D.; Standley, C.; Lifshitz, L. M.; Fogarty, K. E.; Corvera, S. Sorting of EGF and transferrin at the plasma membrane and by cargo-specific signaling to EEA1-enriched endosomes. J. Cell Sci. 2008, 121 (Pt 20), 3445-3458.
57. Handl, H. L.; Vagner, J.; Han, H.; Mash, E.; Hruby, V. J.; Gillies, R. J. Hitting multiple targets with multimeric ligands. Expert Opin. Ther. Targets 2004, 8 (6), 565-586.
58. Xu, L.; Vagner, J.; Josan, J.; Lynch, R. M.; Morse, D. L.; Baggett, B.; Han, H.; Mash, E. A.; Hruby, V. J.; Gillies, R. J. Enhanced targeting with heterobivalent ligands. Mol. Cancer Ther. 2009, 8 (8), 2356-2365.