Time-delimited signaling of MET receptor tyrosine kinase regulates cortical circuit development and critical period plasticity

Chen, Ke; Ma, Xiaokuang; Nehme, Antoine; Wei, Jing; Cui, Yan; Cui, Yuehua; Yao, Dezhong; Wu, Jie; Anderson, Trent; Ferguson, Deveroux; Levitt, Pat; Qiu, Shenfeng

doi:10.1038/s41380-019-0635-6

Cited by 17 publications

(38 citation statements)

References 61 publications

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“…Multisensory integration deficits have also been described in several mouse models of ASD (154). Low MET expression, an autism gene, yields a "timing mosaic" in the cortex due to accelerated maturation of AMPA/NMDA receptor ratio and precocious CP closure (155).…”

Section: Consequences For Mental Illness and Brain Injurymentioning

confidence: 99%

Critical period regulation across multiple timescales

Reh

Dias

Nelson

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

329

267

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Brain plasticity is dynamically regulated across the life span, peaking during windows of early life. Typically assessed in the physiological range of milliseconds (real time), these trajectories are also influenced on the longer timescales of developmental time (nurture) and evolutionary time (nature), which shape neural architectures that support plasticity. Properly sequenced critical periods of circuit refinement build up complex cognitive functions, such as language, from more primary modalities. Here, we consider recent progress in the biological basis of critical periods as a unifying rubric for understanding plasticity across multiple timescales. Notably, the maturation of parvalbumin-positive (PV) inhibitory neurons is pivotal. These fast-spiking cells generate gamma oscillations associated with critical period plasticity, are sensitive to circadian gene manipulation, emerge at different rates across brain regions, acquire perineuronal nets with age, and may be influenced by epigenetic factors over generations. These features provide further novel insight into the impact of early adversity and neurodevelopmental risk factors for mental disorders.

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Section: Consequences For Mental Illness and Brain Injurymentioning

confidence: 99%

Critical period regulation across multiple timescales

Reh

Dias

Nelson

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

329

267

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“…The first is the identification of molecular and cellular accelerators and brakes that regulate onset, duration, and cessation. 103,104 This led to the discovery that the balance between neuronal excitation and inhibition is highly conserved, including in humans. This balance is essential for the ability to process complex information and has been shown to be disrupted in certain mental illnesses.…”

Section: Timementioning

confidence: 99%

Genes, Environments, and Time: The Biology of Adversity and Resilience

et al. 2021

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Exposures to adverse environments, both psychosocial and physicochemical, are prevalent and consequential across a broad range of childhood populations. Such adversity, especially early in life, conveys measurable risk to learning and behavior and to the foundations of both mental and physical health. Using an interactive gene-environment-time (GET) framework, we survey the independent and interactive roles of genetic variation, environmental context, and developmental timing in light of advances in the biology of adversity and resilience, as well as new discoveries in biomedical research. Drawing on this rich evidence base, we identify 4 core concepts that provide a powerful catalyst for fresh thinking about primary health care for young children: (1) all biological systems are inextricably integrated, continuously “reading” and adapting to the environment and “talking back” to the brain and each other through highly regulated channels of cross-system communication; (2) adverse environmental exposures induce alterations in developmental trajectories that can lead to persistent disruptions of organ function and structure; (3) children vary in their sensitivity to context, and this variation is influenced by interactions among genetic factors, family and community environments, and developmental timing; and (4) critical or sensitive periods provide unmatched windows of opportunity for both positive and negative influences on multiple biological systems. These rapidly moving frontiers of investigation provide a powerful framework for new, science-informed thinking about health promotion and disease prevention in the early childhood period.

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“…Recent work from our laboratory and others have demonstrated that prenatally, subsets of developing vagal motor neurons express the Met receptor tyrosine kinase (MET) (Isabella et al, 2020;Kamitakahara et al, 2017;Wu and Levitt, 2013), positioning it as a candidate for distinguishing motor neuron types. MET is a pleiotropic receptor, known to be important in synapse maturation and critical period development in the cerebral cortex (Chen et al, 2020;Ma and Qiu, 2019;Xie et al, 2016) and for the differentiation of several different motor neuron pools in the brainstem and spinal cord (Caton et al, 2000;Ebens et al, 1996;Tallafuss and Eisen, 2008;Wong et al, 1997). For example, upon binding its only known ligand, hepatocyte growth factor (HGF), MET confers neuronal survival in developing spinal motor neurons innervating the pectoralis minor muscle (Lamballe et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

MET Receptor Tyrosine Kinase Regulates Vagal Laryngeal Motor Neuron Development and Lifespan Ultrasonic Vocal Communication

Kamitakahara

Ghoddousi

Lanjewar

et al. 2020

Preprint

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The vagal motor nucleus ambiguus (nAmb) innervates the intrinsic muscles of the larynx, providing direct motor control over vocal production in humans and rodents. Here, we demonstrate that early developmental signaling through the MET receptor tyrosine kinase (MET) is required for proper formation of the nAmb. Embryonic deletion of Met in the developing brainstem resulted in a loss of one-third of motor neurons in the nAmb. While the remaining neurons were able to establish connections with target muscles in the larynx, advanced signal processing analyses revealed severe deficits in ultrasonic vocalization in early postnatal life. Abnormal vocalization patterns persisted into adulthood in the majority of mice tested. Interestingly, 28% of adult mice recovered the ability to vocalize demonstrating heterogeneity in circuit restitution. Together, the data establish MET as a factor necessary for development of a specific subset of neurons in the nAmb required for normal ultrasonic vocalization.

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Time-delimited signaling of MET receptor tyrosine kinase regulates cortical circuit development and critical period plasticity

Abstract: , A. et al. Time-delimited signaling of MET receptor tyrosine kinase regulates cortical circuit development and critical period plasticity. Mol Psychiatry (2020).

Cited by 17 publications

References 61 publications

Critical period regulation across multiple timescales

Critical period regulation across multiple timescales

Genes, Environments, and Time: The Biology of Adversity and Resilience

MET Receptor Tyrosine Kinase Regulates Vagal Laryngeal Motor Neuron Development and Lifespan Ultrasonic Vocal Communication

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