Carl H. Johnson

Last updated
Carl H. Johnson
Carl H. Johnson.tif
Born
Washington, D.C.
NationalityAmerican
Alma mater University of Texas at Austin
Stanford University
Harvard University
Scientific career
Fields Biology, Circadian rhythm
Institutions Vanderbilt University
Doctoral advisor David Epel
Colin Pittendrigh
Other academic advisors Michael Menaker

Carl Hirschie Johnson is an American-born biologist who researches the chronobiology of different organisms, most notably the bacterial circadian rhythms of cyanobacteria. [1] Johnson completed his undergraduate degree in Honors Liberal Arts at the University of Texas at Austin, and later earned his PhD in biology from Stanford University, where he began his research under the mentorship of Dr. Colin Pittendrigh. [2] Currently, Johnson is the Stevenson Professor of Biological Sciences at Vanderbilt University. [3]

Contents

Personal life

Carl Johnson was born in Washington D.C. When he first began college at the University of Texas at Austin, he planned to go to medical school rather than pursue research. [2] However, he quickly developed a passion for research after working as an undergraduate student in a chronobiology lab directed by Dr. Michael Menaker. Johnson asserts that "music led [him] to science," as he originally began his research job with Menaker to pay for classical voice lessons. Classical music has remained a major avocation, as he continues to sing music with the chorus of the Nashville Symphony Orchestra. [4] Also in his free time, he enjoys yoga. [2]

Scientific career

Early career and education

Johnson graduated with a B.A. in Honors Liberal Arts (the Plan II Honors program [5] ) at the University of Texas at Austin in 1976. During this time, he became involved in undergraduate research under the mentorship of Dr. Michael Menaker, whose lab was studying biological clocks in birds and rodents. [6] [7] [8] Johnson's exposure to the practice of experimental research in Dr. Menaker's lab inspired him to go to graduate school instead of following his original plan to become a physician. [2] He went on to earn his Ph.D. in biology in 1982 at Stanford University, first working under the renowned leader in chronobiology, Colin Pittendrigh and then moving to David Epel's laboratory to finish his degree. Subsequently, Johnson conducted postdoctoral work in Cell & Developmental Biology at Harvard University, which he completed in 1987, with Dr. J.W. 'Woody' Hastings (John Woodland Hastings), a biologist famous for his work on bioluminescence in many organisms, including algae. [9] Hastings became a close friend and mentor to Johnson. In 1987, Johnson came to Vanderbilt University to initiate an independent research program, and he has been a biology professor at Vanderbilt since then. [2] [3]

Research beginnings

Johnson's initial foray into research was as an undergraduate in Menaker's lab, which was working on the pineal gland in birds [7] [10] and other chronobiology projects in vertebrates. [8] In graduate school at Stanford under Colin Pittendrigh, Johnson attempted to discover circadian rhythms in a variety of organism such as leeches and cockroaches. He also worked with earthworms to see whether they would completely recover circadian rhythms upon regeneration of lesioned parts of their brains. He also developed a method to measure the pH levels inside cells in search of rhythmic acid/base relationships. However, only one of these projects ultimately resulted in a publication, namely a paper about the clock's control over the pH in the bread mould Neurospora crassa. [11] Johnson switched to David Epel's marine biology lab [12] in his fourth year of graduate school, because their work on the pH change in sea urchin and starfish eggs upon fertilization was an excellent system in which to apply the method he had developed earlier to measure the pH levels inside cells. [13] [14] He successfully published a number of papers on this topic. [15] [16] In his postdoctoral studies with Hastings, Johnson returned to the biological clocks field and worked mainly on rhythms in the bioluminescent alga Gonyaulax polyedra [17] [18] and later in the algal model system for genetics, Chlamydomonas reinhardtii. [19]

Major contributions

Circadian system in cyanobacteria

Prior to the late 1980s, most chronobiologists believed that bacteria were too "simple" to express circadian rhythms. [20] Johnson did not accept this dogma, and as early as 1978, he was examining haloarchaea for the possible presence of biological clocks. While the studies of haloarchaea were not productive, when other studies suggested the possibility of circadian rhythms in cyanobacteria, [21] [22] Johnson along with colleagues and collaborators used a luciferase reporter system to prove that Synechococcus elongatus, of the phylum cyanobacteria, showed evidence of daily bacterial circadian rhythms (with circa-24 hour cycles). [23] Synechococcus expressed free-running rhythms, temperature compensation, and ability to entrain, which are the defining properties of circadian rhythms. [1] These organisms also regulate cell division with forbidden and allowed phases. [24] Therefore, Johnson and coworkers challenged the original belief that bacteria do not have daily biological cycles. Moreover, they identified the central elements of the bacterial clock, namely the KaiABC gene cluster, and determined their structure. [25] Currently, the idea that bacterial circadian rhythms exist in at least some prokaryotes is well accepted by the chronobiology community, and prokaryotes are an important model system for studying rhythmicity. [26]

Bioluminescence Resonance Energy Transfer (BRET)

In 1999, Johnson and his team developed and patented a new method of studying the interaction of molecules based on Förster resonance energy transfer (FRET), also known as Fluorescent Resonance Energy Transfer (FRET). [27] They modified the existing technique of FRET so that instead of using light to activate fluorophores attached to the proteins of interest, they employed bioluminescent proteins with luciferase activity. BRET eliminates the need for light excitation and so avoids changes that light generally causes in circadian clocks, such as resetting the clock phase. Because it avoids light excitation (as in the case of FRET), BRET can also be helpful (1) when tissues are autofluorescent, (2) when light excitation causes phototoxicity, photoresponses (as in retina), or photobleaching, and (3) in partnership with optogenetics. [28] This new method for measuring protein-protein interactions gives researchers the ability to develop novel reporters for intracellular calcium and hydrogen ions. This method is projected to be extremely useful for researchers dealing with live cell cultures, cell extracts and purified proteins.

Current work

The Johnson Lab is currently applying biophysical methods to explain how the central bacterial clock proteins (KaiA + KaiB + KaiC) oscillate in vitro. [26] [29] [30] Together with the laboratory of Dr. Martin Egli, Dr. Johnson's lab has led a concerted effort to apply structural biology techniques for insight into circadian clock mechanisms. [25] [31] The lab has also used mutants and codon bias in cyanobacteria to provide the first rigorous evidence for the adaptive significance of biological clocks in fitness. [32] [33] [34] The Johnson lab is expanding the study of bacterial circadian rhythms from cyanobacteria to purple bacteria. [26] [35] Currently the lab is also conducting studies on the circadian system of mammals in vivo and in vitro, by using luminescence as a tool to monitor circadian rhythms in the brain. [28] Finally, Johnson and his lab is studying circadian and sleep phenotypes of mouse models of the serious human neurodevelopmental disorder called Angelman syndrome. The lab hopes to find chronotherapeutic ways to ameliorate the sleep disorders of patients with this syndrome. [36]

Timeline of accomplishments

Positions and honors

See also

Related Research Articles

<span class="mw-page-title-main">Circadian rhythm</span> Natural internal process that regulates the sleep-wake cycle

A circadian rhythm, or circadian cycle, is a natural oscillation that repeats roughly every 24 hours. Circadian rhythms can refer to any process that originates within an organism and responds to the environment. Circadian rhythms are regulated by a circadian clock whose primary function is to rhythmically co-ordinate biological processes so they occur at the correct time to maximise the fitness of an individual. Circadian rhythms have been widely observed in animals, plants, fungi and cyanobacteria and there is evidence that they evolved independently in each of these kingdoms of life.

<span class="mw-page-title-main">Chronobiology</span> Field of biology

Chronobiology is a field of biology that examines timing processes, including periodic (cyclic) phenomena in living organisms, such as their adaptation to solar- and lunar-related rhythms. These cycles are known as biological rhythms. Chronobiology comes from the ancient Greek χρόνος, and biology, which pertains to the study, or science, of life. The related terms chronomics and chronome have been used in some cases to describe either the molecular mechanisms involved in chronobiological phenomena or the more quantitative aspects of chronobiology, particularly where comparison of cycles between organisms is required.

<span class="mw-page-title-main">Suprachiasmatic nucleus</span> Part of the brains hypothalamus

The suprachiasmatic nucleus or nuclei (SCN) is a small region of the brain in the hypothalamus, situated directly above the optic chiasm. The SCN is the principal circadian pacemaker in mammals, responsible for generating circadian rhythms. Reception of light inputs from photosensitive retinal ganglion cells allow the SCN to coordinate the subordinate cellular clocks of the body and entrain to the environment. The neuronal and hormonal activities it generates regulate many different body functions in an approximately 24-hour cycle.

A circadian clock, or circadian oscillator, is a biochemical oscillator that cycles with a stable phase and is synchronized with solar time.

<span class="mw-page-title-main">CLOCK</span> Protein-coding gene in the species Homo sapiens

CLOCK is a gene encoding a basic helix-loop-helix-PAS transcription factor that is known to affect both the persistence and period of circadian rhythms.

Bacterial circadian rhythms, like other circadian rhythms, are endogenous "biological clocks" that have the following three characteristics: (a) in constant conditions they oscillate with a period that is close to, but not exactly, 24 hours in duration, (b) this "free-running" rhythm is temperature compensated, and (c) the rhythm will entrain to an appropriate environmental cycle.

<span class="mw-page-title-main">John Woodland Hastings</span>

John Woodland "Woody" Hastings, was a leader in the field of photobiology, especially bioluminescence, and was one of the founders of the field of circadian biology. He was the Paul C. Mangelsdorf Professor of Natural Sciences and Professor of Molecular and Cellular Biology at Harvard University. He published over 400 papers and co-edited three books.

<i>KaiC</i> Gene found in cyanobacteria

KaiC is a gene belonging to the KaiABC gene cluster that, together, regulate bacterial circadian rhythms, specifically in cyanobacteria. KaiC encodes for the KaiC protein, which interacts with the KaiA and KaiB proteins in a post-translational oscillator (PTO). The PTO is cyanobacteria master clock that is controlled by sequences of phosphorylation of KaiC protein. Regulation of KaiABC expression and KaiABC phosphorylation is essential for cyanobacteria circadian rhythmicity, and is particularly important for regulating cyanobacteria processes such as nitrogen fixation, photosynthesis, and cell division. Studies have shown similarities to Drosophila, Neurospora, and mammalian clock models in that the kaiABC regulation of the cyanobacteria slave circadian clock is also based on a transcription translation feedback loop (TTFL). KaiC protein has both auto-kinase and auto-phosphatase activity and functions as the circadian regulator in both the PTO and the TTFL. KaiC has been found to not only suppress kaiBC when overexpressed, but also suppress circadian expression of all genes in the cyanobacterial genome.

<span class="mw-page-title-main">Takao Kondo</span> Japanese biologist (1948–2023)

Takao Kondo was a Japanese biologist and professor of biological science at Nagoya University in Nagoya, Japan. He is best known for reconstituting the circadian clock in vitro.

Arnold Eskin was a professor of chronobiology at the University of Houston in Houston, Texas. He attended Vanderbilt University, where he received a degree in physics. He later attended University of Texas at Austin, where he received his Ph.D. in zoology in 1969. He is recognized in the term Eskinogram, and has been a leader in the discovery of mechanisms underlying entrainment of circadian clocks.

<span class="mw-page-title-main">Douglas G. McMahon</span>

Douglas G. McMahon is a professor of Biological Sciences and Pharmacology at Vanderbilt University. McMahon has contributed several important discoveries to the field of chronobiology and vision. His research focuses on connecting the anatomical location in the brain to specific behaviors. As a graduate student under Gene Block, McMahon identified that the basal retinal neurons (BRNs) of the molluscan eye exhibited circadian rhythms in spike frequency and membrane potential, indicating they are the clock neurons. He became the 1986 winner of the Society for Neuroscience's Donald B. Lindsley Prize in Behavioral Neuroscience for his work. Later, he moved on to investigate visual, circadian, and serotonergic mechanisms of neuroplasticity. In addition, he helped find that constant light can desynchronize the circadian cells in the suprachiasmatic nucleus (SCN). He has always been interested in the underlying causes of behavior and examining the long term changes in behavior and physiology in the neurological modular system. McMahon helped identifying a retrograde neurotransmission system in the retina involving the melanopsin containing ganglion cells and the retinal dopaminergic amacrine neurons.

kaiA is a gene in the "kaiABC" gene cluster that plays a crucial role in the regulation of bacterial circadian rhythms, such as in the cyanobacterium Synechococcus elongatus. For these bacteria, regulation of kaiA expression is critical for circadian rhythm, which determines the twenty-four-hour biological rhythm. In addition, KaiA functions with a negative feedback loop in relation with kaiB and KaiC. The kaiA gene makes KaiA protein that enhances phosphorylation of KaiC while KaiB inhibits activity of KaiA.

Steve A. Kay is a British-born chronobiologist who mainly works in the United States. Dr. Kay has pioneered methods to monitor daily gene expression in real time and characterized circadian gene expression in plants, flies and mammals. In 2014, Steve Kay celebrated 25 years of successful chronobiology research at the Kaylab 25 Symposium, joined by over one hundred researchers with whom he had collaborated with or mentored. Dr. Kay, a member of the National Academy of Sciences, U.S.A., briefly served as president of The Scripps Research Institute. and is currently a professor at the University of Southern California. He also served on the Life Sciences jury for the Infosys Prize in 2011.

KaiB is a gene located in the highly-conserved kaiABC gene cluster of various cyanobacterial species. Along with KaiA and KaiC, KaiB plays a central role in operation of the cyanobacterial circadian clock. Discovery of the Kai genes marked the first-ever identification of a circadian oscillator in a prokaryotic species. Moreover, characterization of the cyanobacterial clock demonstrated the existence of transcription-independent, post-translational mechanisms of rhythm generation, challenging the universality of the transcription-translation feedback loop model of circadian rhythmicity.

The Society for Research on Biological Rhythms (SRBR) is an international chronobiological research society with three key goals:

  1. to promote the advancement and dissemination of basic and applied research in all aspects of biological rhythms.
  2. to enhance the education and training of students and researchers in the field.
  3. to foster interdisciplinary communication and an international exchange of ideas.

Susan Golden is a Professor of molecular biology known for her research in circadian rhythms. She is currently a faculty member at UC San Diego.

Jennifer Loros, also known as J.J. Loros, is a chronobiologist leading the field in the study of circadian rhythms in Neurospora. Her research focuses on circadian oscillators and their control of gene expression in living cells. Currently, Loros is a professor of Biochemistry, Cell Biology, and Molecular and Systems Biology at the Giesel School of Medicine.

<span class="mw-page-title-main">John S. O'Neill</span> British biologist

John Stuart O’Neill is a British molecular and circadian biologist. O’Neill is currently a Principal Investigator at the MRC Laboratory of Molecular Biology in Cambridge, United Kingdom. His work focuses on the fundamental mechanisms that sustain circadian rhythms in eukaryotic cells.

Jay Dunlap is an American chronobiologist and photobiologist who has made significant contributions to the field of chronobiology by investigating the underlying mechanisms of circadian systems in Neurospora, a fungus commonly used as a model organism in biology, and in mice and mammalian cell culture models. Major contributions by Jay Dunlap include his work investigating the role of frq and wc clock genes in circadian rhythmicity, and his leadership in coordinating the whole genome knockout collection for Neurospora. He is currently the Nathan Smith Professor of Molecular and Systems Biology at the Geisel School of Medicine at Dartmouth. He and his colleague Jennifer Loros have mentored numerous students and postdoctoral fellows, many of whom presently hold positions at various academic institutions.

Martin R. Ralph is a circadian biologist who serves as a professor in the Psychology Department at the University of Toronto. His research primarily focuses on circadian rhythmicity in the fields of neuroscience, psychology, and endocrinology. His most notable work was has been on the suprachiasmatic nucleus, now recognized as the central circadian pacemaker in mammals, but has also investigated circadian rhythms in the context of time, memory, and light.

References

  1. 1 2 Johnson, C.H. "From Skepticism to Prominence: Circadian Clocks in Bacteria". Microbe 4(9). Sept, 2009
  2. 1 2 3 4 5 "Carl Hirschie Johnson." Current Biology, vol. 24, no. 3, 2014, pp. R100-R102.
  3. 1 2 "Department of Biological Sciences - Carl H. Johnson". Vanderbilt University. http://as.vanderbilt.edu/biosci/bio/carl-johnson. Accessed 29 Nov, 2016.
  4. ↑ "Nashville Symphony Chorus Roster". https://www.nashvillesymphony.org/about/chorus/roster%5B%5D. Accessed 29 Nov, 2016.
  5. ↑ Plan II Honors Program, University of Texas at Austin. https://liberalarts.utexas.edu/plan2/. Accessed 29 Nov, 2016.
  6. ↑ Michael Menaker. University of Virginia College and Graduate School of Arts & Sciences, 2015, bio.as.virginia.edu/people/mm7e. Accessed 29 Nov. 2016.
  7. 1 2 Gaston, S; Menaker, M. (1968). "Pineal function: the biological clock in the sparrow?". Science. 160 (3832): 1125–1127. Bibcode:1968Sci...160.1125G. doi:10.1126/science.160.3832.1125. PMID   5647435. S2CID   36220489.
  8. 1 2 Stetson, M. H.; Elliott, J.A.; Menaker, M. (1975). "Photoperiodic regulation of Hamster testis: circadian sensitivity to the effects of light". Biology of Reproduction. 13 (3): 329–339. doi: 10.1095/biolreprod13.3.329 . PMID   1218198.
  9. ↑ Hastings Lab Home Page. Harvard University Biological Laboratories, Sept. 2006, labs.mcb.harvard.edu/hastings/dino.html. Accessed 29 Nov. 2016.
  10. ↑ Takahashi, J. S.; Hamm, H.; Menaker, M. (1980). "Circadian rhythms of melatonin release from individual superfused chicken pineal glands in vitro". Proc. Natl. Acad. Sci. USA. 77 (4): 2319–2322. Bibcode:1980PNAS...77.2319T. doi: 10.1073/pnas.77.4.2319 . PMC   348706 . PMID   6929552.
  11. ↑ Johnson, C. H. (1983). "Changes of intracellular pH are not correlated with the circadian rhythm of Neurospora". Plant Physiol. 72 (1): 129–133. doi: 10.1104/pp.72.1.129 . PMC   1066181 . PMID   16662945.
  12. ↑ David Epel. Stanford University Hopkins Marine Station, http://hopkinsmarinestation.stanford.edu/people/david-epel. Accessed 29 November 2016.
  13. ↑ Johnson, C. H.; Epel, D. (1981). "Intracellular pH of sea urchin eggs measured by the dimethyloxazolidinedione (DMO) method". J. Cell Biol. 89 (2): 284–291. doi: 10.1083/jcb.89.2.284 . PMC   2111700 . PMID   7195903.
  14. ↑ Johnson, C. H., and D. Epel. 1982. Starfish oocyte maturation and fertilization: intracellular pH is not involved in activation. Devel. Biol. 92: 461-469.
  15. ↑ Johnson, C. H., and D. Epel. 1983. Heavy metal chelators prolong motility and viability of sea urchin sperm by inhibiting spontaneous acrosome reactions. J. Exp. Zool. 226: 431-440.
  16. ↑ Johnson, C. H., D. L. Clapper, M. W. Winkler, H. C. Lee, and D. Epel. 1983. A volatile inhibitor immobilizes sea urchin sperm in semen by depressing the intracellular pH. Devel. Biol. 98: 493-501.
  17. ↑ Johnson, C. H.; Roeber, J. F.; Hastings, J. W. (1984). "Circadian changes of enzyme concentration account for rhythm of enzyme activity in Gonyaulax". Science. 223 (4643): 1428–1430. Bibcode:1984Sci...223.1428H. doi:10.1126/science.223.4643.1428. PMID   17746055. S2CID   1488579.
  18. ↑ Johnson, C. H.; Hastings, J. W. (1989). "Circadian phototransduction: phase-resetting and frequency of the circadian clock of Gonyaulax cells in red light". J. Biol. Rhythms. 4 (4): 417–437. doi: 10.1177/074873048900400403 . PMID   2519604. S2CID   21817404.
  19. ↑ Johnson, C. H.; Kondo, T.; Hastings, J. W. (1991). "Action spectrum for resetting the circadian phototaxis rhythm in the CW15 strain of Chlamydomonas. II. Illuminated cells". Plant Physiol. 97 (3): 1122–1129. doi: 10.1104/pp.97.3.1122 . PMC   1081131 . PMID   16668498.
  20. ↑ Johnson, CH; Golden, SS; Ishiura, M; Kondo, T (1996). "Circadian clocks in prokaryotes". Mol Microbiol. 21 (1): 5–11. doi:10.1046/j.1365-2958.1996.00613.x. PMID   8843429. S2CID   40431382.
  21. ↑ Huang, T-C; Grobbelaar, N (1995). "The circadian clock in the prokaryote Synechococcus RF-1". Microbiology. 141 (3): 535–540. doi: 10.1099/13500872-141-3-535 .
  22. ↑ Sweeney, BM; Borgese, MB (1989). "A circadian rhythm in cell division in a prokaryote, the cyanobacterium Synechococcus WH7803". J. Phycol. 25: 183–186. doi:10.1111/j.0022-3646.1989.00183.x. S2CID   83576869.
  23. ↑ Kondo, T.; Strayer, C. A.; Kulkarni, R. D.; Taylor, W.; Ishiura, M.; Golden, S. S.; Johnson, C. H. (1993). "Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria". Proc. Natl. Acad. Sci. USA. 90 (12): 5672–5676. Bibcode:1993PNAS...90.5672K. doi: 10.1073/pnas.90.12.5672 . PMC   46783 . PMID   8516317.
  24. ↑ Mori, T.; Binder, B.; Johnson, C.H. (1996). "Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours". Proc. Natl. Acad. Sci. USA. 93 (19): 10183–10188. Bibcode:1996PNAS...9310183M. doi: 10.1073/pnas.93.19.10183 . PMC   38358 . PMID   8816773.
  25. 1 2 Pattanayek, R.; Wang, J.; Mori, T.; Xu, Y.; Johnson, C.H.; Egli, M. (2004). "Visualizing a circadian clock protein: crystal structure of KaiC and functional insights". Molecular Cell. 15 (3): 375–388. doi: 10.1016/j.molcel.2004.07.013 . PMID   15304218.
  26. 1 2 3 Johnson, Carl Hirschie; Zhao, Chi; Xu, Yao; Mori, Tetsuya (April 2017). "Timing the day: what makes bacterial clocks tick?". Nature Reviews. Microbiology. 15 (4): 232–242. doi:10.1038/nrmicro.2016.196. ISSN   1740-1534. PMC   5696799 . PMID   28216658.
  27. ↑ Xu, Y.; Piston, D. W.; Johnson, C. H. (1999). "A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins". Proceedings of the National Academy of Sciences. 96 (1): 151–156. Bibcode:1999PNAS...96..151X. doi: 10.1073/pnas.96.1.151 . PMC   15108 . PMID   9874787.
  28. 1 2 Yang, J.; Cumberbatch, D.; Centanni, S.; Shi, S.; Winder, D.; Webb, D.; Johnson, C.H. (2016). "Coupling Optogenetic Stimulation with NanoLuc-based Luminescence (BRET) Ca ++ Sensing". Nature Communications. 7: 13268. Bibcode:2016NatCo...713268Y. doi: 10.1038/ncomms13268 . PMC   5476805 . PMID   27786307.
  29. ↑ Johnson, C. H.; Egli, M. (2014). "Metabolic compensation and circadian resilience in prokaryotic cyanobacteria". Annu. Rev. Biochem. 83: 221–47. doi:10.1146/annurev-biochem-060713-035632. PMC   4259047 . PMID   24905782.
  30. ↑ Mori, T.; Williams, D.R.; Byrne, M.O.; Qin, X.; Mchaourab, H.S.; Egli, M.; Stewart, P.L.; Johnson, C.H. (2007). "Elucidating the Ticking of an in vitro Circadian Clockwork". PLOS Biology. 5 (4): e93. doi: 10.1371/journal.pbio.0050093 . PMC   1831719 . PMID   17388688.
  31. ↑ Johnson, C.H.; Egli, M.; Stewart, P.L. (2008). "Structural Insights into a Circadian Oscillator". Science. 322 (5902): 697–701. Bibcode:2008Sci...322..697J. doi:10.1126/science.1150451. PMC   2588432 . PMID   18974343.
  32. ↑ Ouyang, Y.; Andersson, C.R.; Kondo, T.; Golden, S.S.; Johnson, C.H. (1998). "Resonating circadian clocks enhance fitness in cyanobacteria". Proc. Natl. Acad. Sci. USA. 95 (15): 8660–8664. Bibcode:1998PNAS...95.8660O. doi: 10.1073/pnas.95.15.8660 . PMC   21132 . PMID   9671734.
  33. ↑ Xu, Y.; Ma, P.; Shah, P.; Rokas, A.; Liu, Y.; Johnson, C.H. (2013). "Non-optimal codon usage is a mechanism to achieve circadian clock conditionality". Nature. 495 (7439): 116–20. Bibcode:2013Natur.495..116X. doi:10.1038/nature11942. PMC   3593822 . PMID   23417065.
  34. ↑ Woelfle, M.A.; Ouyang, Y.; Phanvijhitsiri, K.; Johnson, C.H. (2004). "The adaptive value of circadian clocks: An experimental assessment in cyanobacteria". Current Biology. 14 (16): 1481–1486. doi: 10.1016/j.cub.2004.08.023 . PMID   15324665.
  35. ↑ Ma, P.; Mori, T.; Zhao, C.; Thiel, T.; Johnson, C.H. (2016). "Evolution of KaiC-dependent timekeepers: a proto-circadian timing mechanism confers adaptive fitness in the purple bacterium Rhodopseudomonas palustris". PLOS Genetics. 12 (3): e1005922. doi: 10.1371/journal.pgen.1005922 . PMC   4794148 . PMID   26982486.
  36. ↑ Shi, S.; Bichell, T.J.; Ihrie, R.A.; Johnson, C.H. (2015). "Ube3a Imprinting Impairs Circadian Robustness in Angelman Syndrome Models". Current Biology. 25 (5): 537–545. doi: 10.1016/j.cub.2014.12.047 . PMC   4348236 . PMID   25660546.
  37. ↑ "Previous SRBR Meetings".
  38. ↑ "Chancellor's Award for Research | Faculty Awards | Office of the Provost | Vanderbilt University". Archived from the original on 2016-05-26. Retrieved 2017-01-26.
  39. ↑ aschoff-honma.wixsite.com/ahmf/prize-winners
  40. ↑ "About the Chapter – Phi Beta Kappa – Alpha of Tennessee".
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.