The Campbell Lab at the University of Alberta

Engineering optogenetic tools for cell biology and neuroscience

Lifetime numbering; Trainees in bold; corresponding author(s) indicated with *.

61. P. Zou (equal contribution), Y. Zhao (equal contribution), A.D. Douglass, D.R. Hochbaum, D. Brinks, C.A. Werley, D.J. Harrison, R.E. Campbell (*correspondence regarding the library screen), A.E. Cohen*, “Bright and fast multi-colored voltage reporters via electrochromic FRET (eFRET)”, Nat. Commun., 2014, Accepted July 8, 2014. [Funding from NSERC Discovery, CIHR MOP 123514, and graduate scholarships from the University of Alberta and Alberta Innovates to Y.Z.]

60. B.G. Oscar, W. Liu, Y. Zhao, L. Tang, Y Wang, R.E. Campbell, and C. Fang*, “Excited state structural dynamics of a dual-emission calmodulin-green fluorescent protein sensor for calcium ion imaging”, Proc. Natl. Acad. Sci. U.S.A., 2014, Accepted June 6, 2014. [Supplementary Material; Funding from NSERC Discovery, CIHR MOP 123514, and graduate scholarships from the University of Alberta and Alberta Innovates to Y.Z.]

59. D.R. Hochbaum (equal contribution), Y. Zhao (equal contribution), S.L. Farhi, N. Klapoetke, C.A. Werley, V. Kapoor, P. Zou, J.M. Kralj, D. Maclaurin, N. Smedemark-Margulies, J. Saulnier, G.L. Boulting, Y. Cho, M. Melkonian, G.K-S. Wong, D.J. Harrison, V.N. Murthy, B. Sabatini, E.S. Boyden (equal contribution), R.E. Campbell (equal contribution; *correspondance related to directed evolution), and A.E. Cohen*, “All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins”, Nat. Methods, 2014. Accepted May 29, 2014. [Supplementary Material; Sample requests; Funding from NSERC Discovery, CIHR MOP 123514, and graduate scholarships from the University of Alberta and Alberta Innovates to Y.Z.; Highlighted by Science Media Centre of Canada]

58. Y. Zhao, A.S. Abdelfattah, Y. Zhao, A. Ruangkittisakul, K. Ballanyi, R.E. Campbell*, D.J. Harrison*, “Microfluidic cell sorter-aided directed evolution of a protein-based calcium ion indicator with an inverted fluorescent response”, Integr. Biol. (Camb), 2014, 6(7), 714-725. [Open Access PDF; Supplementary material, Movie 1, Movie 2; Funding from NSERC Discovery, CIHR MOP 123514, and graduate scholarships from the University of Alberta (Y.Z) and Alberta Innovates to (Y.Z. and A.S.A)]

57. H-w. Ai, M.A. Baird, Y. Shen, M.W. Davidson*, and R.E. Campbell*, “Engineering and characterizing monomeric fluorescent proteins for live-cell imaging applications”. Nat. Protocols, 2014, 9, 910-928. [Funding from University of Alberta, CFI, NSERC Discovery grant, and Alberta Ingenuity (Scholarship to Y.S. and a New Faculty Award to R.E.C.)]

56. A.S.F. Belal, B.R. Sell, H. Hoi, M.W. Davidson, and R.E. Campbell*, “Optimization of a Genetically Encoded Biosensor for Cyclin B1-Cyclin Dependent Kinase 1”. Mol. Biosyst., 2014, 10(2), 191-195. [Open Access PDF; Supplementary material; Funded by NSERC]

55. H. Hoi, Y. Ding, and R.E. Campbell*, “FRET with Fluorescent Proteins”, in FRET - Förster Resonance Energy Transfer: From Theory to Applications. Eds. Igor Medintz and Niko Hildebrandt. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, November 2013, pages 431-473. [Google book preview; Funded by NSERC Discovery and CIHR NHG 99085]

54. H. Hoi, E.S. Howe, Y. Ding, W. Zhang, M.A. Baird, B.R. Sell, J.R. Allen, M.W. Davidson, and R.E. Campbell*, “An engineered monomeric Zoanthus sp. yellow fluorescent protein”, Chem. Biol., 2013, 20, 1296-1304. [Highlighted in the same issue; Supplementary Material; Funded by NSERC Discovery and Alberta Innovates Technology Futures (AITF) Scholarship to W.Z.]

53. H.J. Carlson and R.E. Campbell*, “Mutational analysis of a red fluorescent protein-based calcium ion indicator”, Sensors, 2013, 13(9), 11507-11521. [Open Access PDF; Supplementary Material; Funded by NSERC Discovery, NSERC PGSM, and Alberta Ingenuity Scholarship]

52. H.J. Carlson and R.E. Campbell*, “Circular permutated red fluorescent proteins and calcium ion indicators based on mCherry”, Protein Eng. Des. Sel., 2013, 26(12): 763-772. [Supplementary Material; Funded by NSERC Discovery, NSERC PGSM, and Alberta Ingenuity Scholarship]

51. E.M. Lynes, A. Raturi, M. Shenkman, C.O. Sandova, M.C. Yap, J. Wu, A. Janowicz, N. Myhill, M.D. Benson, R.E. Campbell, L. G. Berthiaume, G.Z. Lederkremer and T. Simmen*, "Palmitoylation is the Switch that Assigns Calnexin to Quality Control or ER Calcium Signaling", J. Cell Sci., 2013, 126, 3893-3903. [Supplementary Material; Funded by CIHR NHG 99085]

50. J. Wu, L. Liu, T. Matsuda, Y. Zhao, A. Rebane, M. Drobizhev, Y-F. Chang, S. Araki, Y. Arai, K. March, T. E. Hughes, K. Sagou, T. Miyata, T. Nagai*, W-h. Li*, R. E. Campbell*, “Improved orange and red Ca2+ indicators and photophysical considerations for optogenetic applications”, ACS Chem. Neurosci., 2013, 4(6), 963-972. [Supplementary Material; Funded by CIHR NHG 99085, CIHR MOP 123514, NSERC Discovery, and Alberta Ingenuity Nanotechnology Scholarship to Y.Z.; Highlighted at OpenOptogenetics]

49. H. Hoi, T. Matsuda, T. Nagai, and R.E. Campbell*, “Highlightable Ca2+ indicators for live cell imaging”, J. Am. Chem. Soc., 2013, 135(1), 46-49. [Supplementary Material; Funded by NSERC Discovery; Highlighted at OpenOptogenetics]

48. S.C. Alford, J. Wu, Y. Zhao, R.E. Campbell, and T. Knöpfel*, “Optogenetic Reporters”. Biol. Cell., 2013, 105, 14-29. [Funded by CIHR NHG 99085, NSERC Discovery, NSERC CGSD3 to S.C.A., Alberta Ingenuity Ph.D. Scholarship to S.C.A., and Alberta Ingenuity Nanotechnology Scholarship to Y.Z.; Highlighted at ChemistryViews]

47. A.L. McEvoy*, H. Hoi, M. Bates, E. Platonova, P.J. Cranfill, M.A. Baird, M.W. Davidson, H. Ewers, J. Liphardt, and R.E. Campbell*, “mMaple: a photoconvertible fluorescent protein for use in multiple imaging modalities”. PLoS ONE, 2012, 7(12): e51314. [Open Access PDF; Supplementary Material; Funded by NSERC Discovery]

46. S.C. Alford, Y. Ding, T. Simmen, and R.E. Campbell*, “Dimerization-Dependent Green and Yellow Fluorescent Proteins”. ACS Synth. Biol., 2012, 1(12), 569-575. [Cover art; Supplementary Material; Author Feature; Funded by CIHR NHG 99085, NSERC Discovery, NSERC CGSD3 to S.C.A., and Alberta Ingenuity Ph.D. Scholarship to S.C.A]

45. M. Funes-Huacca,  A. Wu,  E. Szepesvari,  P. Rajendran,  N. Kwan-Wong,  A. Razgulin,  Y. Shen,  J. Kagira,  R.E. Campbell and R. Derda*, “Portable self-contained cultures for phage and bacteria made of paper and tape”. Lab Chip, 2012, 12, 4269-4278. [Funded by NSERC Discovery and Alberta Ingenuity Nanotechnology Scholarship to Y.S]

44. P. Tewson, M. Westenberg, Y. Zhao, R.E. Campbell, A.M. Quinn, T.E. Hughes,* “Simultaneous detection of Ca2+ and diacylglycerol signaling in living cells”. PLoS ONE, 2012, 7(8): e42791. [Open Access PDF; Funded by CIHR NHG 99085 and Alberta Ingenuity Nanotechnology Scholarship to Y.Z.]

43. R.E. Campbell*, “New Bioanalytical Tools and Devices: Chemistry leads the way”. Biotechnology Focus (Bioscienceworld), 2012, 16(4), 7-9. [Highlighting the research of Drs. Gibbs-Davis, Serpe, and Derda; Interactive PDF]

42. K.D. Daze,  T. Pinter,  C.S. BesharaA. Ibraheem,  S.A. Minaker,  M.C.F. Ma,  R.J.M. Courtemanche,  R.E. Campbell, and F. Hof*, “Supramolecular hosts that recognize methyllysines and disrupt the interaction between a modified histone tail and its epigenetic reader protein”. Chem. Sci., 2012, 3, 2695-2699. [Supplementary Material; Funded by Alberta Cancer Board and NSERC Discovery]

41. S.C. Alford, A.S. Abdelfattah, Y. Ding, and R.E. Campbell*, “A Fluorogenic Red Fluorescent Protein Heterodimer”. Chem. Biol., 2012, 19, 353-360. [Cover Art; Highlighted in Nature Methods ; Supplementary Material; Funded by CIHR NHG 94487 and 99085, NSERC Discovery, NSERC CGSD3 to S.C.A., and Vanier CGS to A.S.A.]

40. Y. Ding, H-w. Ai, H. Hoi, R.E. Campbell*, “FRET-based biosensors for multiparameter ratiometric imaging of Ca2+ dynamics and caspase-3 activity in single cells”. Anal. Chem., 2011, 83, 9687–9693. [Supplementary Material; Funded by CIHR NHG 94487 and 99085 and NSERC Discovery]

39. A. Ibraheem, H. Yap, Y. Ding, R.E. Campbell*, “A bacteria colony-based screen for optimal linker combinations in genetically encoded biosensors”. BMC Biotechnol., 2011, 11, 105. [Open Access PDF; Supplementary Material; Funded by Alberta Cancer Board]

38. Y. Zhao, S. Araki, J. Wu, T. Teramoto, Y-F. Chang, M. Nakano, A.S. Abdelfattah, M. Fujiwara, T. Ishihara, T. Nagai, and R.E. Campbell*, “An Expanded Palette of Genetically Encoded Ca2+ Indicators”, Science, 2011, 333, 1888-1891. [Press release; Highlighted by C&EN Concentrates, Biophotonics, and Science Signaling; Supplementary Material; Funded by CIHR NHG 94487 and 99085, NSERC Discovery, Alberta Ingenuity Nanotechnology Scholarship to Y.Z., and Vanier CGS to A.S.A.]

37. H. Hoi, N.C. Shaner, M.W. Davidson, C.W. Cairo, J. Wang, R.E. Campbell*, “A Monomeric Photoconvertible Fluorescent Protein for Imaging of Dynamic Protein Localization”. J. Mol. Biol., 2010, 401, 776-791. [Supplementary Material; Funded by NSERC Discovery]

36. H.J. Carlson, D. Cotton, and R.E. Campbell*, “Circularly permuted monomeric red fluorescent proteins with new termini in the β-sheet”, Protein Sci., 2010, 19, 1490-1499. [Funded by NSERC Discovery, NSERC USRA to D.C., NSERC PGSM to H.J.C., and Alberta Ingenuity Scholarship to H.J.C.]

35. R.E. Campbell and M.W. Davidson*, “Fluorescent reporter proteins”, Molecular Imaging with Reporter Genes. Eds. Sanjiv S. Gambhir and Shahriar S. Yaghoubi. Cambridge University Press, New York, NY, July 2010: 3 - 40. [Google book preview]

34. A. Ibraheem and R.E. Campbell*, “Designs and applications of fluorescent protein-based biosensors”, Curr. Opin. Chem. Biol., 2010, 14, 30-36. [Funded by Alberta Cancer Board]

33. R.E. Campbell* and C.J. Chang*, "Molecular Imaging: Editorial Overview", Curr. Opin. Chem. Biol., 2010, 14, 1-2. [Co-editor for this Special issue of the journal which had 15 invited reviews.]

32. M.W. Davidson and R.E. Campbell*, “Engineered fluorescent proteins: innovations and applications”, Nat. Methods, 2009, 6, 713-717. [Invited Commentary for 5th Anniversary issue.]

31. W.B. Frommer*, M.W. Davidson, R.E. Campbell* Genetically encoded biosensors based on engineered fluorescent proteins”, Chem. Soc. Rev., 2009, 38, 2833-2841. [Supplementary Material]

30. D.E. Johnson, H-w. Ai, P. Wong, J.D. Young, R.E. Campbell*, and J.R. Casey* “Red fluorescent protein pH biosensor to detect concentrative nucleoside transport”, J. Biol. Chem., 2009, 284, 20499-20511. [Supplementary Material]

29. R.E. Campbell*, “Fluorescent Protein-Based Biosensors: Modulation of Energy Transfer as a Design Principle”, Anal. Chem., 2009, 81(15), 5972–5979. [Cover Art; Podcast]

28. Z. Cheng and R.E. Campbell*, “An engineered tryptophan zipper-type peptide as a molecular recognition scaffold”, J. Pept. Sci., 2009, 15, 523-532. [Supplementary Material]

27. H.J. Carlson, R.E. Campbell*, “Genetically encoded FRET-based biosensors for multiparameter fluorescence imaging”, Curr. Opin. Biotechnol., 2009, 20, 19-27.

26. R.E. Campbell*, “Fluorescent proteins”, Scholarpedia J., 2008, 3(7), 5410. [Open access; Article accessed more than 95,000 times as of July 2014]

25. H-w. Ai, K.L. Hazelwood, M.W. Davidson, and R.E. Campbell*, “Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors”, Nat. Methods, 2008, 5, 401-403. [Supplementary Material; Highlighted in October 2008 issue of Biophotonics]

24. H-w. Ai, S.G. Olenych, P. Wong, M.W. Davidson, and R.E. Campbell*, “Hue-shifted monomeric variants of Clavularia cyan fluorescent protein: identification of the molecular determinants of color and applications in fluorescence imaging”, BMC Biol., 2008, 6, 13. [Open Access PDF; Designated as a Highly Accessed article]

23. H-w. Ai, and R. E. Campbell*, “Teal fluorescent proteins: Characterization of a reversibly photoconvertible variant”, Proc. SPIE, 2008, 6868, 68680D.

22. Q.K. Timerghazin, H.J. Carlson, C. Liang, R.E. Campbell,* and A. Brown*, “Computational prediction of absorbance maxima for a structurally diverse series of engineered green fluorescent protein chromophores”, J. Phys. Chem B, 2008, 112, 2533-2541. [Supplementary Material]

21. Y. Li, A.M. Sierra, H.-w. Ai, and R.E. Campbell*, “Identification of sites within a monomeric red fluorescent protein that tolerate peptide insertion and testing of corresponding circular permutations”, Photochem. Photobiol., 2008, 84, 111–119. [Supplementary Material]

20. H-w. Ai and R.E. Campbell*, “More than just pretty colors: the growing impact of fluorescent proteins in the life sciences”, Biotechnology Focus (Bioscienceworld), 2007, issue 11, 16-18. [PDF]

19. Z. Cheng, M. Miskolzie, and R.E. Campbell*, “In vivo screening identifies a highly folded beta-hairpin peptide with a structured extension”, ChemBioChem, 2007, 8, 880-883. [Cover Art; Supplementary Material]

18. H.-w. Ai, N.C. Shaner, Z. Cheng, R.Y. Tsien, and R.E. Campbell*, “Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins”, Biochemistry, 2007, 46, 5904 - 5910. [Featured on the cover of the June 2007 issue of Biophotonics]

17. J.N. Henderson, H.-w. Ai, R.E. Campbell, and S.J. Remington*, “Structural basis for reversible photobleaching of a green fluorescent protein homologue”, Proc. Natl. Acad. Sci. U.S.A., 2007, 14, 6672-6677. [Supplementary Material; Featured in June 2007 issue of Biophotonics and April 2007 Science Daily online]

16. Z. Cheng and R.E. Campbell*, “Fluorescence-based characterization of genetically encoded peptides that fold in live cells: progress towards a generic hairpin scaffold”, Proc. SPIE, 2007, 6449, 64490S.

15. H-w. Ai, J.N. Henderson, S.J. Remington, and R.E. Campbell*, “Directed evolution of a monomeric, bright, and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging”, Biochem. J., 2006, 400, 531-540.

14. Z. Cheng and R.E. Campbell*, “Assessing the Structural Stability of Designed β-Hairpin Peptides in the Cytoplasm of Live Cells”, ChemBioChem, 2006, 7, 1147-1150.

13. R.E. Campbell*, “Realization of β-lactamase as a versatile fluorogenic reporter”, Trends Biotech., 2004, 22, 208-211.

Postdoctoral research at the University of California, San Diego

12. M.Z. Lin, M.R. McKeown, H.-L. Ng, T.A. Aguilera, N.C. Shaner, R.E. Campbell, S.R. Adams, L.A. Gross, W. Ma, T. Alber, R.Y. Tsien*, “Autofluorescent Proteins with Excitation in the Optical Window for Intravital Imaging in Mammals”, Chem. Biol., 2009, 16, 1169-1179.

11. N.C. Shaner, R.E. Campbell, P.A. Steinbach, B.N.G. Giepmans, A.E. Palmer, and R.Y. Tsien*, “Improved monomeric red, orange, and yellow fluorescent proteins derived from Discosoma red fluorescent protein”, Nat. Biotechnol., 2004, 22, 1567-1572.

10. J. Zhang, R.E. Campbell, A.Y. Ting and R.Y. Tsien*, “Creating New Fluorescent Probes for Cell Biology”, Nat. Rev. Mol. Cell Biol., 2002, 3, 906-918.

9. R.E. Campbell, O. Tour, A.E. Palmer, P.A. Steinbach, G.S. Baird, D.A. Zacharias and R.Y. Tsien*, “A Monomeric Red Fluorescent Protein”, Proc. Natl. Acad. Sci. U.S.A., 2002, 99, 7877-7882.

8. S.R. Adams, R.E. Campbell, L.A. Gross, B.R. Martin, G.K. Walkup, Y. Yao, J. Llopis and R.Y. Tsien*, “New Biarsenical Ligands and Tetracysteine Motifs for Protein Labeling in Vitro and in Vivo: Synthesis and Biological Applications”, J. Am. Chem. Soc., 2002, 124, 6063-6076.

7. O. Griesbeck, G.S. Baird, R.E. Campbell, D.A. Zacharias and R.Y. Tsien*, “Reducing the Environmental Sensitivity of Yellow Fluorescent Protein: Mechanism and Applications”, J. Biol. Chem., 2001, 276, 29188-29194.

Graduate research at the University of British Columbia

6. R.E. Campbell, S.C. Mosimann, M.E. Tanner*, and N.C.J. Strynadka*, “The Structure of UDP-N-Acetylglucosamine 2-Epimerase Reveals Homology to Phosphoglycosyl Transferases”, Biochemistry, 2000, 39, 14993-15001.

5. R.E. Campbell, S.C. Mosimann, I. van de Rijn, M. E. Tanner, and N.C.J. Strynadka*, “The First Structure of UDP-Glucose Dehydrogenase Reveals the Catalytic Residues Necessary for the Two-fold Oxidation”, Biochemistry, 2000, 39, 7012-7023.

4. R.E. Campbell and M.E. Tanner*, “UDP-Glucose Analogues as Inhibitors and Mechanistic Probes of UDP-Glucose Dehydrogenase”, J. Org. Chem., 1999, 64, 9487-9492.

3. X. Ge, R.E. Campbell, I. van de Rijn, and M.E. Tanner*, “Covalent Adduct Formation with a Mutated Enzyme: Evidence for a Thioester Intermediate in the Reaction Catalyzed by UDP-Glucose Dehydrogenase”, J. Am. Chem. Soc., 1998, 120, 6613-6614.

2. R.E. Campbell and M.E. Tanner*, “Uridine diphospho-alpha-D-gluco-hexodialdose: Synthesis and kinetic competence in the reaction catalyzed by UDP-glucose dehydrogenase”, Angew. Chem. Int. Ed. Eng. 1997, 36, 1520-1522.

1. R.E. Campbell, R.F. Sala, I. van de Rijn and M.E. Tanner*, “Properties and kinetic analysis of UDP-glucose dehydrogenase from group A streptococci. Irreversible inhibition by UDP-chloroacetol”, J. Biol. Chem., 1997, 272, 3416-22.