Translational profiling of dorsal root ganglia and spinal cord in a mouse model of neuropathic pain

Highlights • Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established. • ERK is a central hub of both transcriptionally and translationally controlled genes. • Changes in translation efficiency and mRNA levels occur in the opposite direction for multiple mRNAs....

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Published inNeurobiology of pain Vol. 4; pp. 35 - 44
Main Authors Uttam, Sonali, Wong, Calvin, Amorim, Inês S, Jafarnejad, Seyed Mehdi, Tansley, Shannon N, Yang, Jieyi, Prager-Khoutorsky, Masha, Mogil, Jeffrey S, Gkogkas, Christos G, Khoutorsky, Arkady
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.08.2018
Elsevier
Subjects
Original Research
Pain Medicine
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Abstract Highlights • Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established. • ERK is a central hub of both transcriptionally and translationally controlled genes. • Changes in translation efficiency and mRNA levels occur in the opposite direction for multiple mRNAs.
AbstractList Acute pain serves as a protective mechanism, guiding the organism away from actual or potential tissue injury. In contrast, chronic pain is a debilitating condition without any obvious physiological function. The transition to, and the maintenance of chronic pain require new gene expression to support biochemical and structural changes within the pain pathway. The regulation of gene expression at the level of mRNA translation has emerged as an important step in the control of protein expression in the cell. Recent studies show that signaling pathways upstream of mRNA translation, such as mTORC1 and ERK, are upregulated in chronic pain conditions, and their inhibition effectively alleviates pain in several animal models. Despite this progress, mRNAs whose translation is altered in chronic pain conditions remain largely unknown. Here, we performed genome-wide translational profiling of dorsal root ganglion (DRG) and spinal cord dorsal horn tissues in a mouse model of neuropathic pain, spared nerve injury (SNI), using the ribosome profiling technique. We identified distinct subsets of mRNAs that are differentially translated in response to nerve injury in both tissues. We discovered key converging upstream regulators and pathways linked to mRNA translational control and neuropathic pain. Our data are crucial for the understanding of mechanisms by which mRNA translation promotes persistent hypersensitivity after nerve injury.
• Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established. • ERK is a central hub of both transcriptionally and translationally controlled genes. • Changes in translation efficiency and mRNA levels occur in the opposite direction for multiple mRNAs. Acute pain serves as a protective mechanism, guiding the organism away from actual or potential tissue injury. In contrast, chronic pain is a debilitating condition without any obvious physiological function. The transition to, and the maintenance of chronic pain require new gene expression to support biochemical and structural changes within the pain pathway. The regulation of gene expression at the level of mRNA translation has emerged as an important step in the control of protein expression in the cell. Recent studies show that signaling pathways upstream of mRNA translation, such as mTORC1 and ERK, are upregulated in chronic pain conditions, and their inhibition effectively alleviates pain in several animal models. Despite this progress, mRNAs whose translation is altered in chronic pain conditions remain largely unknown. Here, we performed genome-wide translational profiling of dorsal root ganglion (DRG) and spinal cord dorsal horn tissues in a mouse model of neuropathic pain, spared nerve injury (SNI), using the ribosome profiling technique. We identified distinct subsets of mRNAs that are differentially translated in response to nerve injury in both tissues. We discovered key converging upstream regulators and pathways linked to mRNA translational control and neuropathic pain. Our data are crucial for the understanding of mechanisms by which mRNA translation promotes persistent hypersensitivity after nerve injury.
•Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established.•ERK is a central hub of both transcriptionally and translationally controlled genes.•Changes in translation efficiency and mRNA levels occur in the opposite direction for multiple mRNAs. Acute pain serves as a protective mechanism, guiding the organism away from actual or potential tissue injury. In contrast, chronic pain is a debilitating condition without any obvious physiological function. The transition to, and the maintenance of chronic pain require new gene expression to support biochemical and structural changes within the pain pathway. The regulation of gene expression at the level of mRNA translation has emerged as an important step in the control of protein expression in the cell. Recent studies show that signaling pathways upstream of mRNA translation, such as mTORC1 and ERK, are upregulated in chronic pain conditions, and their inhibition effectively alleviates pain in several animal models. Despite this progress, mRNAs whose translation is altered in chronic pain conditions remain largely unknown. Here, we performed genome-wide translational profiling of dorsal root ganglion (DRG) and spinal cord dorsal horn tissues in a mouse model of neuropathic pain, spared nerve injury (SNI), using the ribosome profiling technique. We identified distinct subsets of mRNAs that are differentially translated in response to nerve injury in both tissues. We discovered key converging upstream regulators and pathways linked to mRNA translational control and neuropathic pain. Our data are crucial for the understanding of mechanisms by which mRNA translation promotes persistent hypersensitivity after nerve injury.
Highlights • Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established. • ERK is a central hub of both transcriptionally and translationally controlled genes. • Changes in translation efficiency and mRNA levels occur in the opposite direction for multiple mRNAs.
Author Uttam, Sonali
Gkogkas, Christos G
Jafarnejad, Seyed Mehdi
Prager-Khoutorsky, Masha
Mogil, Jeffrey S
Amorim, Inês S
Yang, Jieyi
Tansley, Shannon N
Wong, Calvin
Khoutorsky, Arkady
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Snippet Highlights • Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established. • ERK is a central hub of both transcriptionally...
•Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established.•ERK is a central hub of both transcriptionally and...
Acute pain serves as a protective mechanism, guiding the organism away from actual or potential tissue injury. In contrast, chronic pain is a debilitating...
• Translational landscape in DRG and spinal cord in SNI assay of neuropathic pain was established. • ERK is a central hub of both transcriptionally and...
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Title Translational profiling of dorsal root ganglia and spinal cord in a mouse model of neuropathic pain
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