Carl H. Johnson, Ph.D.
Stevenson Professor of Biological Sciences
Vanderbilt University Medical Center
Box 1634 Sta B
Nashville, TN 37232
Cellular and Molecular Biology of Biological Clocks
Organisms and even single cells have endogenous biological "clocks" that allow them to tell the time of day. Research in our laboratory is directed towards understanding the cellular and molecular bases of these fascinating timing mechanisms in a variety of organisms: cyanobacteria ("blue-green algae"), plants, and animals. To analyze the molecular nature of the clock in the prokaryotic cyanobacteria, we have developed a bioluminescent reporter strain that expresses a daily rhythm of light emission. Using this bioluminescence rhythm as a marker, clock mutants have been identified. We found that the essential clock gene, KaiC, is rhythmically expressed and forms ATP-dependent hexamers. In collaboration with the laboratory of Dr. Martin Egli, we have crystallized KaiC to determine its three-dimensional structure and discover its phosphorylation sites. The three key bacterial clock proteins (KaiA + KaiB + KaiC) will show circadian oscillations in a test tube! In collaboration with the laboratories of Drs. Phoebe Stewart and Hassane Mchaourab, we are applying electron microscopic and biophysical methods to explain how these proteins oscillate in vitro. Furthermore, we are using clock mutants of cyanobacteria to provide the first rigorous evidence for the adaptive significance of circadian clocks in fitness.
We also study the neuroscience of the circadian system of mammals. To measure circadian rhythms in brain slices in vitro, we use transgenic mice that express luciferase rhythmically. As a model system, we have also created a fibroblast cell line that is stably transfected with a luciferase reporter and glows rhythmically. Therefore, we use luminescence as a tool to monitor circadian rhythms in the brain. Future studies will focus upon understanding the signal transduction pathway of calcium to the clock and the role of clock genes in the fundamental mammalian clockwork.
We have recently extended our studies to the genetics of the human biological clock. We are examining clock gene polymorphisms in human populations to determine how the neurogenetics of the biological clock affects our ability to adapt to shiftwork cycles and how it can influence mental health (esp. depression). Because daily biological clocks control a myriad of fundamental cellular activities, including cell division, metabolism, gene expression, and ion channel, the elucidation of the timing mechanism will have ramifications for many aspects of temporal regulation, including mental health, cancer, and jet lag.
Finally, we have developed a new method for measuring protein-protein interactions based upon the resonance energy between a luciferase and a fluorescent protein. This method is called Bioluminescence Resonance Energy Transfer, or BRET. This technique has allowed us to develop novel reporters for intracellular calcium and hydrogen ions. We envision a bright future for this technique.
See our laboratory website at: http://www.cas.vanderbilt.edu/johnsonlab/
- Shi, SQ, Ansari, TS, McGuinness, OP, Wasserman, DH, Johnson, CH Circadian Disruption Leads to Insulin Resistance and Obesity. Curr Biol, 23372-381, 2013.
- Egli, M, Pattanayek, R, Sheehan, JH, Xu, Y, Mori, T, Smith, JA, Johnson, CH Loop-Loop Interactions Regulate KaiA-Stimulated KaiC Phosphorylation in the Cyanobacterial KaiABC Circadian Clock. Biochemistry, 52(7), 1208-20, 2013.
- Xu, Y, Ma, P, Shah, P, Rokas, A, Liu, Y, Johnson, CH Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature, 495(7439), 116-20, 2013.
- Egli, M, Mori, T, Pattanayek, R, Xu, Y, Qin, X, Johnson, CH Dephosphorylation of the core clock protein KaiC in the cyanobacterial KaiABC circadian oscillator proceeds via an ATP synthase mechanism. Biochemistry, 51(8), 1547-58, 2012.
- Edgar, R.S., E.W. Green, Y. Zhao, G. van Ooijen, M. Olmedo, X. Qin, Y. Xu, M. Pan, U.K. Valekunja, K.A. Feeney, E.S. Maywood, M.H. Hastings, N.S. Baliga, M. Merrow, A.J. Millar, C.H. Johnson, C.P. Kyriacou, J.S. Oâ€™Neill, A.B. Reddy. "Peroxiredoxins are conserved markers of circadian rhythms.." Nature, 485459-64, 2012.
- Zhang, Y, Xie, Q, Robertson, JB, Johnson, CH pHlash: a new genetically encoded and ratiometric luminescence sensor of intracellular pH. PLoS One, 7(8), e43072, 2012.
- Xie, Q, Soutto, M, Xu, X, Zhang, Y, Johnson, CH Bioluminescence resonance energy transfer (BRET) imaging in plant seedlings and mammalian cells. Methods Mol Biol, 6803-28, 2011.
- Pattanayek, R, Williams, DR, Rossi, G, Weigand, S, Mori, T, Johnson, CH, Stewart, PL, Egli, M Combined SAXS/EM based models of the S. elongatus post-translational circadian oscillator and its interactions with the output His-kinase SasA. PLoS One, 6(8), e23697, 2011.
- Robertson, JB, Johnson, CH Luminescence as a continuous real-time reporter of promoter activity in yeast undergoing respiratory oscillations or cell division rhythms. Methods Mol Biol, 73463-79, 2011.
- Gamble, KL, Motsinger-Reif, AA, Hida, A, Borsetti, HM, Servick, SV, Ciarleglio, CM, Robbins, S, Hicks, J, Carver, K, Hamilton, N, Wells, N, Summar, ML, McMahon, DG, Johnson, CH Shift work in nurses: contribution of phenotypes and genotypes to adaptation. PLoS One, 6(4), e18395, 2011.
- Johnson, CH, Stewart, PL, Egli, M The cyanobacterial circadian system: from biophysics to bioevolution. Annu Rev Biophys, 40143-67, 2011.
- Shi, S, Hida, A, McGuinness, OP, Wasserman, DH, Yamazaki, S, Johnson, CH Circadian clock gene Bmal1 is not essential; functional replacement with its paralog, Bmal2. Curr Biol, 20(4), 316-21, 2010.
- Johnson, CH Circadian clocks and cell division: What's the pacemaker?. Cell Cycle, 9(19), 2010.
- Qin, X, Byrne, M, Xu, Y, Mori, T, Johnson, CH Coupling of a core post-translational pacemaker to a slave transcription/translation feedback loop in a circadian system. PLoS Biol, 8(6), e1000394, 2010.
- Qin, X, Byrne, M, Mori, T, Zou, P, Williams, DR, McHaourab, H, Johnson, CH Intermolecular associations determine the dynamics of the circadian KaiABC oscillator. Proc Natl Acad Sci U S A, 107(33), 14805-10, 2010.
- J.L. Ditty, S.R. Mackey, C.H. Johnson, editors "Bacterial Circadian Programs." , 333 pages, 2009.
- Xu, X, Graeff, R, Xie, Q, Gamble, KL, Mori, T, Johnson, CH Comment on "The Arabidopsis circadian clock incorporates a cADPR-based feedback loop". Science, 326(5950), 230; author reply 230, 2009.
- Xu, Y, Mori, T, Qin, X, Yan, H, Egli, M, Johnson, CH Intramolecular regulation of phosphorylation status of the circadian clock protein KaiC. PLoS One, 4(11), e7509, 2009.
- Robertson, JB, Zhang, Y, Johnson, CH Light-emitting diode flashlights as effective and inexpensive light sources for fluorescence microscopy. J Microsc, 236(1), 1-4, 2009.
- Pattanayek, R, Mori, T, Xu, Y, Pattanayek, S, Johnson, CH, Egli, M Structures of KaiC circadian clock mutant proteins: a new phosphorylation site at T426 and mechanisms of kinase, ATPase and phosphatase. PLoS One, 4(11), e7529, 2009.
- Johnson, CH, Mori, T, Xu, Y A cyanobacterial circadian clockwork. Curr Biol, 18(17), R816-R825, 2008.
- Ciarleglio, CM, Ryckman, KK, Servick, SV, Hida, A, Robbins, S, Wells, N, Hicks, J, Larson, SA, Wiedermann, JP, Carver, K, Hamilton, N, Kidd, KK, Kidd, JR, Smith, JR, Friedlaender, J, McMahon, DG, Williams, SM, Summar, ML, Johnson, CH Genetic differences in human circadian clock genes among worldwide populations. J Biol Rhythms, 23(4), 330-40, 2008.
- Robertson, JB, Stowers, CC, Boczko, E, Johnson, CH Real-time luminescence monitoring of cell-cycle and respiratory oscillations in yeast. Proc Natl Acad Sci U S A, 105(46), 17988-93, 2008.
- Vougogiannopoulou, K, Ferandin, Y, Bettayeb, K, Myrianthopoulos, V, Lozach, O, Fan, Y, Johnson, CH, Magiatis, P, Skaltsounis, AL, Mikros, E, Meijer, L Soluble 3'',6-substituted indirubins with enhanced selectivity toward glycogen synthase kinase -3 alter circadian period. J Med Chem, 51(20), 6421-31, 2008.
- Johnson, CH, Egli, M, Stewart, PL Structural insights into a circadian oscillator. Science, 322(5902), 697-701, 2008.
- Pattanayek, R, Williams, DR, Pattanayek, S, Mori, T, Johnson, CH, Stewart, PL, Egli, M Structural model of the circadian clock KaiB-KaiC complex and mechanism for modulation of KaiC phosphorylation. EMBO J, 27(12), 1767-78, 2008.
- Bonneau, R, Facciotti, MT, Reiss, DJ, Schmid, AK, Pan, M, Kaur, A, Thorsson, V, Shannon, P, Johnson, MH, Bare, JC, Longabaugh, W, Vuthoori, M, Whitehead, K, Madar, A, Suzuki, L, Mori, T, Chang, DE, Diruggiero, J, Johnson, CH, Hood, L, Baliga, NS A predictive model for transcriptional control of physiology in a free living cell. Cell, 131(7), 1354-65, 2007.
- Johnson, CH Bacterial circadian programs. Cold Spring Harb Symp Quant Biol, 72395-404, 2007.
- Woelfle, MA, Xu, Y, Qin, X, Johnson, CH Circadian rhythms of superhelical status of DNA in cyanobacteria. Proc Natl Acad Sci U S A, 104(47), 18819-24, 2007.
- Fan, Y, Hida, A, Anderson, DA, Izumo, M, Johnson, CH Cycling of CRYPTOCHROME proteins is not necessary for circadian-clock function in mammalian fibroblasts. Curr Biol, 17(13), 1091-100, 2007.
- Xu, X, Hotta, CT, Dodd, AN, Love, J, Sharrock, R, Lee, YW, Xie, Q, Johnson, CH, Webb, AA Distinct light and clock modulation of cytosolic free Ca2+ oscillations and rhythmic CHLOROPHYLL A/B BINDING PROTEIN2 promoter activity in Arabidopsis. Plant Cell, 19(11), 3474-90, 2007.
- Mori, T, Williams, DR, Byrne, MO, Qin, X, Egli, M, McHaourab, HS, Stewart, PL, Johnson, CH Elucidating the Ticking of an In Vitro Circadian Clockwork. PLoS Biol, 5(4), e93, 2007.
- Xu, X, Soutto, M, Xie, Q, Servick, S, Subramanian, C, von Arnim, AG, Johnson, CH Imaging protein interactions with bioluminescence resonance energy transfer (BRET) in plant and mammalian cells and tissues. Proc Natl Acad Sci U S A, 104(24), 10264-9, 2007.
- Subramanian, C, Woo, J, Cai, X, Xu, X, Servick, S, Johnson, CH, NebenfÃ¼hr, A, von Arnim, AG A suite of tools and application notes for in vivo protein interaction assays using bioluminescence resonance energy transfer (BRET). Plant J, 48(1), 138-52, 2006.
- Pattanayek, R, Williams, DR, Pattanayek, S, Xu, Y, Mori, T, Johnson, CH, Stewart, PL, Egli, M Analysis of KaiA-KaiC protein interactions in the cyano-bacterial circadian clock using hybrid structural methods. EMBO J, 25(9), 2017-28, 2006.
- Johnson, C.H., and S.S. Golden "Circadian Rhythms in Cyanobacteria." In: Nature Encyclopedia of Life Sciences, Nature Publishing Group, London: www.els.net, 2006.
- Woelfle, MA, Johnson, CH No promoter left behind: global circadian gene expression in cyanobacteria. J Biol Rhythms, 21(6), 419-31, 2006.
- Izumo, M, Sato, TR, Straume, M, Johnson, CH Quantitative analyses of circadian gene expression in mammalian cell cultures. PLoS Comput Biol, 2(10), e136, 2006.
- Johnson, C.H., R. Shingles, and W.F. Ettinger "Regulation and role of Ca++ fluxes in the chloroplast." In: The Structure and Function of Plastids, Chapter 20, 23403-416, 2006.
- Johnson, C.H. "Reminiscences from Pittendrigh's last Ph.D. student." Resonance, 1122-31, 2006.
- Soutto M., Y. Xu, and C. H. Johnson "Bioluminescence RET (BRET): techniques and potential." In: Molecular Imaging: FRET Microscopy and Spectroscopy, 260-271, 2005.
- Johnson, C.H. and C.P. Kyriacou "Clock evolution and adaptation: whence and whither?." In: Endogenous Plant Rhythms , (Chapter 10), 237-260, 2005.
- Johnson, CH Testing the adaptive value of circadian systems. Methods Enzymol, 393818-37, 2005.
- Johnson, C.H "Testing the adaptive value of circadian systems." Methods in Enzymology, 393818-837, 2005.
- Mittag, M, Kiaulehn, S, Johnson, CH The circadian clock in Chlamydomonas reinhardtii. What is it for? What is it similar to. Plant Physiol, 137(2), 399-409, 2005.
- Johnson, C.H. As time glows by in bacteria. Nature , 430(1), 23-24, 2004.
- Johnson, Carl Hirschie Global orchestration of gene expression by the biological clock of cyanobacteria. Genome Biol, 5(4), 217, 2004.
- Xu, Y, Mori, T, Pattanayek, R, Pattanayek, S, Egli, M, Johnson, CH Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc Natl Acad Sci U S A, 101(38), 13933-8, 2004.
- Subramanian, C, Xu, Y, Johnson, CH, von Arnim, AG In vivo detection of protein-protein interaction in plant cells using BRET. Methods Mol Biol, 284271-86, 2004.
- Min, H, Liu, Y, Johnson, CH, Golden, SS Phase determination of circadian gene expression in Synechococcus elongatus PCC 7942. J Biol Rhythms, 19(2), 103-12, 2004.
- Johnson, Carl Hirschie Precise circadian clocks in prokaryotic cyanobacteria. Curr Issues Mol Biol, 6(2), 103-10, 2004.
- Subramanian, C, Kim, BH, Lyssenko, NN, Xu, X, Johnson, CH, von Arnim, AG The Arabidopsis repressor of light signaling, COP1, is regulated by nuclear exclusion: mutational analysis by bioluminescence resonance energy transfer. Proc Natl Acad Sci U S A, 101(17), 6798-802, 2004.
- Woelfle, MA, Ouyang, Y, Phanvijhitsiri, K, Johnson, CH The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Curr Biol, 14(16), 1481-6, 2004.
- Johnson, C.H. and M. Egli Visualizing a biological clockwork's cogs. Nature Structural and Molecular Biology, 11(7), 584-585, 2004.
- Pattanayek, R, Wang, J, Mori, T, Xu, Y, Johnson, CH, Egli, M Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol Cell, 15(3), 375-88, 2004.
- Hastings, JW, Johnson, CH Bioluminescence and chemiluminescence. Methods Enzymol, 36075-104, 2003.
- Xu, Yao, Kanauchi, Akihito, von Arnim, Albrecht G, Piston, David W, Johnson, Carl Hirschie Bioluminescence resonance energy transfer: monitoring protein-protein interactions in living cells. Methods Enzymol, 360289-301, 2003.
- Izumo, Mariko, Johnson, Carl Hirschie, Yamazaki, Shin Circadian gene expression in mammalian fibroblasts revealed by real-time luminescence reporting: temperature compensation and damping. Proc Natl Acad Sci U S A, 100(26), 16089-94, 2003.
- Xu, Yao, Mori, Tetsuya, Johnson, Carl Hirschie Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J, 222117-26, 2003.
- Johnson, Carl Hirschie, Elliott, Jeffrey A, Foster, Russell Entrainment of circadian programs. Chronobiol Int, 20(5), 741-74, 2003.
- Schoenhard, John A, Smith, Layton H, Painter, Corrie A, Eren, Mesut, Johnson, Carl H, Vaughan, Douglas E Regulation of the PAI-1 promoter by circadian clock components: differential activation by BMAL1 and BMAL2. J Mol Cell Cardiol, 35473-81, 2003.
- Schoenhard, John A, Eren, Mesut, Johnson, Carl H, Vaughan, Douglas E Alternative splicing yields novel BMAL2 variants: tissue distribution and functional characterization. Am J Physiol Cell Physiol, 283C103-14, 2002.
- Xu, Yao, Johnson, Carl Hirschie, Piston, David Bioluminescence resonance energy transfer assays for protein-protein interactions in living cells. Methods Mol Biol, 183121-33, 2002.
- Mori, Tetsuya, Saveliev, Sergei V, Xu, Yao, Stafford, Walter F, Cox, Michael M, Inman, Ross B, Johnson, Carl H Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci U S A, 9917203-8, 2002.
- Sai, Jiqing, Johnson, Carl Hirschie Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell, 141279-91, 2002.
- Suzuki, Lena, Johnson, Carl Hirschie Photoperiodic control of germination in the unicell Chlamydomonas. Naturwissenschaften, 89214-20, 2002.
- Xu, Y, Johnson, C H A clock- and light-regulated gene that links the circadian oscillator to LHCB gene expression. Plant Cell, 131411-25, 2001.
- Mori, T, Johnson, C H Circadian programming in cyanobacteria. Semin Cell Dev Biol, 12271-8, 2001.
- Johnson, C H Endogenous timekeepers in photosynthetic organisms. Annu Rev Physiol, 63695-728, 2001.
- Dassarma, S, Kennedy, SP, Berquist, B, Victor Ng, W, Baliga, NS, Spudich, JL, Krebs, MP, Eisen, JA, Johnson, CH, Hood, L Genomic perspective on the photobiology of Halobacterium species NRC-1, a phototrophic, phototactic, and UV-tolerant haloarchaeon. Photosynth Res, 70(1), 3-17, 2001.
- Mori, T, Johnson, C H Independence of circadian timing from cell division in cyanobacteria. J Bacteriol, 1832439-44, 2001.
- Xu, Y, Mori, T, Johnson, C H Circadian clock-protein expression in cyanobacteria: rhythms and phase setting. EMBO J, 19(13), 3349-57, 2000.
- Mori, T, Johnson, C H Circadian control of cell division in unicellular organisms. Prog Cell Cycle Res, 4185-92, 2000.
- Nikaido, S S, Johnson, C H Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem Photobiol, 71(6), 758-65, 2000.
- Xu, Y, Piston, D W, Johnson, C H A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc Natl Acad Sci U S A, 96(1), 151-6, 1999.
- Johnson, C H, Golden, S S Circadian programs in cyanobacteria: adaptiveness and mechanism. Annu Rev Microbiol, 53389-409, 1999.
- Sai, J, Johnson, C H Different circadian oscillators control Ca(2+) fluxes and lhcb gene expression. Proc Natl Acad Sci U S A, 96(20), 11659-63, 1999.
- Johnson, C H Forty years of PRCs--what have we learned. Chronobiol Int, 16(6), 711-43, 1999.
- Johnson, C H, Golden, S S, Kondo, T Adaptive significance of circadian programs in cyanobacteria. Trends Microbiol, 6(10), 407-10, 1998.
- Ishiura, M, Kutsuna, S, Aoki, S, Iwasaki, H, Andersson, CR, Tanabe, A, Golden, SS, Johnson, CH, Kondo, T Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science, 281(5382), 1519-23, 1998.
- Ouyang, Y, Andersson, C R, Kondo, T, Golden, S S, Johnson, C H Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A, 95(15), 8660-4, 1998.
- Golden, SS, Johnson, CH, Kondo, T The cyanobacterial circadian system: a clock apart. Curr Opin Microbiol, 1(6), 669-73, 1998.
- Golden, Susan S., Ishiura, Masahiro, Johnson, Carl Hirschie, Kondo, Takao CYANOBACTERIAL CIRCADIAN RHYTHMS. Annu Rev Plant Physiol Plant Mol Biol, 48327-354, 1997.
- Tsinoremas, NF, Ishiura, M, Kondo, T, Andersson, CR, Tanaka, K, Takahashi, H, Johnson, CH, Golden, SS A sigma factor that modifies the circadian expression of a subset of genes in cyanobacteria. EMBO J, 15(10), 2488-95, 1996.
- Johnson, C H, Golden, S S, Ishiura, M, Kondo, T Circadian clocks in prokaryotes. Mol Microbiol, 21(1), 5-11, 1996.
- Liu, Y, Tsinoremas, N F, Golden, S S, Kondo, T, Johnson, C H Circadian expression of genes involved in the purine biosynthetic pathway of the cyanobacterium Synechococcus sp. strain PCC 7942. Mol Microbiol, 20(5), 1071-81, 1996.
- Mori, T, Binder, B, Johnson, CH Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. Proc Natl Acad Sci U S A, 93(19), 10183-8, 1996.
- Jacobshagen, S, Kindle, K L, Johnson, C H Transcription of CABII is regulated by the biological clock in Chlamydomonas reinhardtii. Plant Mol Biol, 31(6), 1173-84, 1996.
- Liu, Y, Golden, S S, Kondo, T, Ishiura, M, Johnson, C H Bacterial luciferase as a reporter of circadian gene expression in cyanobacteria. J Bacteriol, 177(8), 2080-6, 1995.
- Liu, Y, Tsinoremas, N F, Johnson, C H, Lebedeva, N V, Golden, S S, Ishiura, M, Kondo, T Circadian orchestration of gene expression in cyanobacteria. Genes Dev, 9(12), 1469-78, 1995.
- Johnson, C H, Knight, M R, Kondo, T, Masson, P, Sedbrook, J, Haley, A, Trewavas, A Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science, 269(5232), 1863-5, 1995.
- Goto, K, Johnson, CH Is the cell division cycle gated by a circadian clock? The case of Chlamydomonas reinhardtii. J Cell Biol, 129(4), 1061-9, 1995.
- Kondo, T, Tsinoremas, NF, Golden, SS, Johnson, CH, Kutsuna, S, Ishiura, M Circadian clock mutants of cyanobacteria. Science, 266(5188), 1233-6, 1994.
- Jacobshagen, S, Johnson, C H Circadian rhythms of gene expression in Chlamydomonas reinhardtii: circadian cycling of mRNA abundances of cab II, and possibly of beta-tubulin and cytochrome c. Eur J Cell Biol, 64(1), 142-52, 1994.
- Johnson, C H Illuminating the clock: circadian photobiology. Semin Cell Biol, 5(5), 355-62, 1994.
- Johnson, C H, Nakaoka, Y, Miwa, I The effects of altering extracellular potassium ion concentration on the membrane potential and circadian clock of Paramecium bursaria. J Exp Biol, 197295-308, 1994.
- Kondo, T, Strayer, CA, Kulkarni, RD, Taylor, W, Ishiura, M, Golden, SS, Johnson, CH Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A, 90(12), 5672-6, 1993.
- Johnson, C H, Kondo, T Light pulses induce 'singular' behavior and shorten the period of the circadian phototaxis rhythm in the CW15 strain of Chlamydomonas. J Biol Rhythms, 7(4), 313-27, 1992.
- Johnson, CH, Kondo, T, Hastings, JW Action Spectrum for Resetting the Circadian Phototaxis Rhythm in the CW15 Strain of Chlamydomonas: II. Illuminated Cells. Plant Physiol, 97(3), 1122-1129, 1991.
- Kondo, T, Johnson, CH, Hastings, JW Action Spectrum for Resetting the Circadian Phototaxis Rhythm in the CW15 Strain of Chlamydomonas: I. Cells in Darkness. Plant Physiol, 95(1), 197-205, 1991.
- Johnson, C H, Nakashima, H Cycloheximide inhibits light-induced phase shifting of the circadian clock in Neurospora. J Biol Rhythms, 5(2), 159-67, 1990.
- Johnson, C H, Hastings, J W Circadian phototransduction: phase resetting and frequency of the circadian clock of Gonyaulax cells in red light. J Biol Rhythms, 4(4), 417-37, 1989.
- Johnson, C H, Miwa, I, Kondo, T, Hastings, J W Circadian rhythm of photoaccumulation in Paramecium bursaria. J Biol Rhythms, 4(4), 405-15, 1989.
- Broda, H, Johnson, CH, Taylor, WR, Hastings, JW Temperature dependence of phase response curves for drug-induced phase shifts. J Biol Rhythms, 4(3), 327-33, 1989.
- Olesiak, W, Ungar, A, Johnson, CH, Hastings, JW Are protein synthesis inhibition and phase shifting of the circadian clock in Gonyaulax correlated. J Biol Rhythms, 2(2), 121-38, 1987.
- Nicolas, MT, Nicolas, G, Johnson, CH, Bassot, JM, Hastings, JW Characterization of the bioluminescent organelles in Gonyaulax polyedra (dinoflagellates) after fast-freeze fixation and antiluciferase immunogold staining. J Cell Biol, 105(2), 723-35, 1987.
- Johnson, CH, InouÃ©, S, Flint, A, Hastings, JW Compartmentalization of algal bioluminescence: autofluorescence of bioluminescent particles in the dinoflagellate Gonyaulax as studied with image-intensified video microscopy and flow cytometry. J Cell Biol, 100(5), 1435-46, 1985.
- Nicolas, MT, Johnson, CH, Bassot, JM, Hastings, JW Immunogold labeling of organelles in the bioluminescent dinoflagellate Gonyaulax polyedra with anti-luciferase antibody. Cell Biol Int Rep, 9(9), 797-802, 1985.