James W. Truman

Last updated
James "Jim" W. Truman
Born
Akron, Ohio, U.S.
Alma mater University of Notre Dame, Harvard University
Known forCircadian rhythms in silkmoth eclosion
Spouse Lynn Riddiford
Scientific career
Fields Entomology, neurobiology, chronobiology, endocrinology
Institutions University of Washington, Howard Hughes Medical Institute's Janelia Research Campus
Thesis The control of ecdysis in silkmoths (1970)
Doctoral advisor Lynn Riddiford
Website www.biology.washington.edu/people/profile/james-w-truman

James "Jim" William Truman is an American chronobiologist known for his seminal research on circadian rhythms in silkmoth (Saturniidae) eclosion, particularly the restoration of rhythm and phase following brain transplantation. He is a professor emeritus at the University of Washington and a former senior fellow at Howard Hughes Medical Institution Janelia Research Campus. [1]

Contents

Background

Truman was introduced to biological research as an undergraduate at the University of Notre Dame in the laboratory of George B. Craig. He was intrigued by Craig's discoveries relating to the hormonal regulation of mosquito mating behavior. [1] As a graduate student, he continued to study hormonal control of insect behavior at Harvard University where he received his PhD in 1970. His doctoral advisor was Lynn Riddiford, whom he later married. He began his research in chronobiology as a junior fellow at Harvard University and continued this work when he established his own laboratory in 1973 at the University of Washington. [1]

Truman took three sabbaticals from the University of Washington. [1] The first, in 1986, was to Cambridge University, where he studied Drosophila neurobiology under Mike Bate. In the second half of this sabbatical he then traveled to Kenya, where he spent time researching tsetse fly development. On his second sabbatical in 1993, Truman traveled to the Australian National University in Canberra, Australia, to research grasshopper metamorphosis hormones with Eldon Ball. In his final sabbatical, he returned to Cambridge University to study evolutionary developmental biology with Michael Akam.

In 2007, after 34 years at University of Washington, Truman retired from the university in order to study insect neuronal stem cells as a group leader at the Howard Hughes Medical Institute's Janelia Research Campus, in Ashburn, Virginia. [1] In 2016, he retired from the Howard Hughes Medical Institute and returned to the University of Washington to pursue research at Friday Harbor Laboratories. His current research focuses on the development and evolution of insect and crustacean nervous systems. [2]

Research contributions

Discovery of the eclosion hormone

While still in graduate school at Harvard, Truman identified an insect neurohormone now known as the eclosion hormone, which mediates moth ecdysis. [1] He demonstrated that injecting eclosion hormone (EH) into moths elicits a stereotyped sequence of ecdysis behaviors. [3] In future studies of silkmoth eclosion, Truman went on to confirm the role of EH in mediating ecdysis. Later studies also implicated a brain-based circadian clock as the regulator controlling the release of EH.

Studies of silkmoth eclosion

As a junior fellow in the Harvard Society of Fellows, [1] Truman studied the underlying mechanisms of silkmoth eclosion, mainly focusing on the role of the circadian clock in driving time of day rhythms in eclosion. Truman demonstrated that eclosion rhythms persist in Hyalophora cecropia moths that have had their compound eyes, corpora cardiaca, and corpora allata surgically removed. [4] Eclosion rhythms were only abolished with the removal of the brain, indicating that the circadian clock is located within the brain. [4] Further experiments involving brain transplantation and selective illumination of different parts of the body revealed that the circadian photoreceptors, which are responsible for receiving light information to entrain the circadian clock, are also located in the brain.

More brain transplant experiments in Hyalophora cecropia and Antheraea pernyi showed that both entrained and free-running eclosion rhythms can be rescued in debrained moths that have had brains transplanted into their abdomens. [4] These restored eclosion rhythms in the debrained moths matched in phase angle with the eclosion rhythms observed in the donor moths prior to brain transplantation. These results confirmed Truman's previous findings that the circadian clock is located within the brain and that the factor mediating eclosion behavior is hormonal. Similar experiments focusing on the role of the circadian clock in regulating flight rhythms confirmed that extraretinal photoreceptors in the brain are responsible for entraining a brain-based circadian clock. [5]

Further studies on eclosion in Drosophila

In 2008, Truman went on to discover that eclosion rhythms, which are mediated by the circadian release of the neurohormone EH, can be masked. [6] In chronobiology, masking refers to the apparent coupling of an observable biological rhythm with an external environmental time cue, without affecting the underlying circadian clock that mediates the observed rhythm. Truman and colleagues observed increased eclosion in adult Drosophila flies immediately following a lights-on signal, which lead to their subsequent discovery that light triggers rapid eclosion in Drosophila on the condition that there was prior EH release. This occurs through the convergence of parallel neurosecretory pathways, both of which are activated by EH. These two EH activated pathways oppose each other; one is an excitatory behavioral pathway and one is inhibitory. Truman and colleagues found that the presence of light can result in the inhibition of the inhibitory pathway, leading to a greater net effect of the excitatory pathway. This light-mediated response promotes more rapid Drosophila eclosion and as a result masks the circadian eclosion rhythms. Further work with Drosophila resulted in the finding that masking of circadian eclosion rhythms can also occur through the inhibition of eclosion. In 2008, Truman and colleagues found that expression of the light chain of tetanus toxin (UAS-TNT) can affect the release of EH from EH releasing cells in the fly brain. [7] This inhibition of EH release results in the inhibition of eclosion—pointing to another way to mask circadian eclosion in Drosophila.

Studies on neuronal remodeling during insect metamorphosis

Some of Truman's most influential work outside of chronobiology involves how hormones alter the nervous system to influence behavior in insect models. Notably, Truman and colleagues have studied neuronal remodeling during insect metamorphosis. Their model organism, the hornworm moth ( Manduca sexta ), was chosen because it has a well-studied endocrinology and its large size allows for the use of standard electrophysiological and neuroanatomical techniques. [8] In 1986, Truman found that accompanying the bodily changes of the hornworm moth was an extensive reorganization of the moth's central nervous system (CNS). Among many changes was the finding that upon onset of metamorphosis, vast cell death sweeps through nests of larvae that are at the end of larval life. These nest cells were previously in an arrested state, but after this metamorphosis-induced cell death, the surviving nest cells can then differentiate. These cells become functional adult CNS neurons.

Discoveries on the insect nervous system

Following his interest in the evolution of metamorphosis, Truman began conducting research on the evolution of the insect nervous system at the Janelia Research Campus. Working in Drosophila model systems, he corroborated his findings from his work in Manduca sexta and discovered that as the adult insect CNS develops during metamorphosis, neuronal stem cells (neuroblasts) differentiate based on specific, highly conserved lineages. He also identified that the peripheral nervous system and motor neurons develop during the embryonic stage and are only partially remodeled during metamorphosis. [9] Furthermore, Truman and his colleagues identified that neuroblasts in the ventral nerve cord originate specific neuronal lineages extending to different regions of the insect body, and that these neuroblasts are characterized by position, size, and manner in which they divide. [10] Currently, Truman and his colleagues at the University of Washington are focusing on characterizing these neuronal lineages in the Drosophila CNS.

Awards

Notable publications

Related Research Articles

<span class="mw-page-title-main">Nervous system</span> Part of an animal that coordinates actions and senses

In biology, the nervous system is the highly complex part of an animal that coordinates its actions and sensory information by transmitting signals to and from different parts of its body. The nervous system detects environmental changes that impact the body, then works in tandem with the endocrine system to respond to such events. Nervous tissue first arose in wormlike organisms about 550 to 600 million years ago. In vertebrates it consists of two main parts, the central nervous system (CNS) and the peripheral nervous system (PNS). The CNS consists of the brain and spinal cord. The PNS consists mainly of nerves, which are enclosed bundles of the long fibers or axons, that connect the CNS to every other part of the body. Nerves that transmit signals from the brain are called motor nerves or efferent nerves, while those nerves that transmit information from the body to the CNS are called sensory nerves or afferent. Spinal nerves are mixed nerves that serve both functions. The PNS is divided into three separate subsystems, the somatic, autonomic, and enteric nervous systems. Somatic nerves mediate voluntary movement. The autonomic nervous system is further subdivided into the sympathetic and the parasympathetic nervous systems. The sympathetic nervous system is activated in cases of emergencies to mobilize energy, while the parasympathetic nervous system is activated when organisms are in a relaxed state. The enteric nervous system functions to control the gastrointestinal system. Both autonomic and enteric nervous systems function involuntarily. Nerves that exit from the cranium are called cranial nerves while those exiting from the spinal cord are called spinal nerves.

<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">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. It is the principal circadian pacemaker in mammals and is necessary 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.

In vertebrates, a neuroblast or primitive nerve cell is a postmitotic cell that does not divide further, and which will develop into a neuron after a migration phase. In invertebrates such as Drosophila, neuroblasts are neural progenitor cells which divide asymmetrically to produce a neuroblast, and a daughter cell of varying potency depending on the type of neuroblast. Vertebrate neuroblasts differentiate from radial glial cells and are committed to becoming neurons. Neural stem cells, which only divide symmetrically to produce more neural stem cells, transition gradually into radial glial cells. Radial glial cells, also called radial glial progenitor cells, divide asymmetrically to produce a neuroblast and another radial glial cell that will re-enter the cell cycle.

<span class="mw-page-title-main">Ventral nerve cord</span>

The ventral nerve cord is a major structure of the invertebrate central nervous system. It is the functional equivalent of the vertebrate spinal cord. The ventral nerve cord coordinates neural signaling from the brain to the body and vice versa, integrating sensory input and locomotor output. Because arthropods have an open circulatory system, decapitated insects can still walk, groom, and mate—illustrating that the circuitry of the ventral nerve cord is sufficient to perform complex motor programs without brain input.

Bursicon is an insect hormone which mediates tanning in the cuticle of adult flies.

<span class="mw-page-title-main">Ganglion mother cell</span>

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Ronald J. Konopka (1947-2015) was an American geneticist who studied chronobiology. He made his most notable contribution to the field while working with Drosophila in the lab of Seymour Benzer at the California Institute of Technology. During this work, Konopka discovered the period (per) gene, which controls the period of circadian rhythms.

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<i>Cycle</i> (gene)

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<span class="mw-page-title-main">Michael Rosbash</span> American geneticist and chronobiologist (born 1944)

Michael Morris Rosbash is an American geneticist and chronobiologist. Rosbash is a professor and researcher at Brandeis University and investigator at the Howard Hughes Medical Institute. Rosbash's research group cloned the Drosophila period gene in 1984 and proposed the Transcription Translation Negative Feedback Loop for circadian clocks in 1990. In 1998, they discovered the cycle gene, clock gene, and cryptochrome photoreceptor in Drosophila through the use of forward genetics, by first identifying the phenotype of a mutant and then determining the genetics behind the mutation. Rosbash was elected to the National Academy of Sciences in 2003. Along with Michael W. Young and Jeffrey C. Hall, he was awarded the 2017 Nobel Prize in Physiology or Medicine "for their discoveries of molecular mechanisms controlling the circadian rhythm".

<span class="mw-page-title-main">Jeffrey C. Hall</span> American geneticist and chronobiologist (born 1945)

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<i>Drosophila</i> circadian rhythm

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<span class="mw-page-title-main">Eclosion assay</span> Procedure to study insect hatching or emergence from pupa

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References

  1. 1 2 3 4 5 6 7 "Jim Truman | Janelia Research Campus". www.janelia.org. Retrieved April 11, 2019.
  2. ↑ "Researchers at FHL | Friday Harbor Laboratories" . Retrieved April 25, 2019.
  3. ↑ Žitňan, Dušan & Daubnerová, Ivana. (2016). Chapter 76 "Eclosion Hormone", Editors: Yoshio Takei, Hironori Ando, Kazuyoshi Tsutsui, Handbook of Hormones, Academic Press, Pages 459-e76-2, ISBN   9780128010280. doi : 10.1016/B978-0-12-801028-0.00076-3
  4. 1 2 3 Saunders, D. S. (2002-10-28). Insect Clocks (3 ed.). Elsevier. ISBN   9780080534718.
  5. ↑ Tomioka, Kenji; Matsumoto, Akira (December 25, 2009). "A comparative view of insect circadian clock systems". Cellular and Molecular Life Sciences. 67 (9): 1397–1406. doi:10.1007/s00018-009-0232-y. PMID   20035363. S2CID   6547927.
  6. ↑ Taghert, Paul H.; Nitabach, Michael N. (October 2012). "Peptide Neuromodulation in Invertebrate Model Systems". Neuron. 76 (1): 82–97. doi:10.1016/j.neuron.2012.08.035. PMC   3466441 . PMID   23040808.
  7. ↑ Venken, Koen J.T.; Simpson, Julie H.; Bellen, Hugo J. (October 2011). "Genetic Manipulation of Genes and Cells in the Nervous System of the Fruit Fly". Neuron. 72 (2): 202–230. doi:10.1016/j.neuron.2011.09.021. PMC   3232021 . PMID   22017985.
  8. ↑ Weeks, J. C.; Levine, R. B. (1990). "Postembryonic Neuronal Plasticity and its Hormonal Control During Insect Metamorphosis". Annual Review of Neuroscience. 13 (1): 183–194. doi:10.1146/annurev.ne.13.030190.001151. PMID   2183673.
  9. ↑ Sokol, Nicholas S. (August 2012). "Small temporal RNAs in animal development". Current Opinion in Genetics & Development. 22 (4): 368–373. doi:10.1016/j.gde.2012.04.001. PMC   3419770 . PMID   22578317.
  10. ↑ Kim, Dongwook W.; Hirth, Frank (October 2009). "Genetic mechanisms regulating stem cell self-renewal and differentiation in the central nervous system of Drosophila". Cell Adhesion & Migration. 3 (4): 402–411. doi:10.4161/cam.3.4.8690. ISSN   1933-6926. PMC   2802756 . PMID   19421003.
  11. ↑ "Newcomb Cleveland Prize Recipients". American Association for the Advancement of Science. Retrieved 2019-04-25.
  12. ↑ "John Simon Guggenheim Foundation | All Fellows". Archived from the original on 2019-03-22. Retrieved 2019-04-25.
  13. ↑ "Winners of the ESA Founders' Memorial Award". Entomological Sociert of America. Retrieved 2019-04-11.
  14. ↑ "The Wigglesworth Memorial Lecture and Award". Royal Entomological Society. 2017-05-26. Retrieved 2019-04-25.
  15. ↑ "James William Truman". American Academy of Arts & Sciences. Retrieved 2019-04-25.
  16. ↑ "2022 NAS Election". www.nasonline.org. Retrieved 2022-05-13.
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