The Transcriptional Signature of a Runner's High

Steven D. Hicks, Paige Jacob, Omar Perez, Matthew Baffuto, Zofia Gagnon, Frank A. Middleton

Research output: Contribution to journalArticle

Abstract

Introduction: Endorphins, endocannabinoids, monoamines, and neurotrophins have all been implicated in the euphoric response to endurance running, known as a runner's high (RH). The epitranscriptional mechanisms regulating this effect have not been defined. Here, we investigate peripheral micro-ribonucleic acid (miRNA) changes unique to athletes experiencing postrun euphoria, yielding insights into gene networks that control an RH. Methods: A cohort study involving 25 collegiate runners (48% females, age = 20 ± 1 yr) examined salivary RNA levels before and after a long-distance run. Participants were divided into RH and nonrunner's high (NRH) groups based on surveys of four criteria (mood, lost sense of time, run quality, and euphoria). Physiological measures were also recorded (temperature, heart rate, blood pressure, pupillary dilatation, and salivary serotonin). Levels of miRNAs and their messenger RNA targets were compared across pre- and postrun samples from RH and NRH groups with two-way ANOVA. Representation of opioid, gamma-aminobutyic acid (GABA), endocannabinoid, neurotrophin, serotonergic, and dopaminergic pathways was assessed in DIANA miRPath. Pearson's correlation analyses examined relationships between miRNAs and RH indices. Results: RH participants (n = 13) demonstrated postrun mydriasis (P = 0.046) and hypothermia (P = 0.043) relative to NRH participants (n = 12) but had no difference in serotonin dynamics (P = 0.88). Six miRNAs (miR-194-5p, miR-4676-3p, miR-4254, miR-4425, miR-1273-3p, miR-6743-5p) exhibited significant effects (false discovery rate P value < 0.05) across pre- or postrun and RH/NRH groups. These miRNAs displayed target enrichment for opioid (P = 2.74E-06) and GABA (P = 0.00016) pathways. miR-1237-3p levels were related with lost sense of time (R = 0.40). Mitogen-activated protein kinase (MAPK11), an endocannabinoid target of miR-1273-3p, was nominally elevated in RH participants (false discovery rate P value = 0.11). Conclusions: Unique dynamics in miRNA concentration occur in athletes with subjective/objective evidence of RH, targeting genes implicated endorphin, endocannabinoid, and GABAergic signaling.

Original languageEnglish (US)
Pages (from-to)970-978
Number of pages9
JournalMedicine and science in sports and exercise
Volume51
Issue number5
DOIs
StatePublished - May 1 2019

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Endocannabinoids
MicroRNAs
Endorphins
Nerve Growth Factors
RNA
Athletes
Opioid Analgesics
Mitogen-Activated Protein Kinase 11
Serotonin
Mydriasis
Acids
Gene Targeting
Gene Regulatory Networks
Hypothermia
Dilatation
Analysis of Variance
Cohort Studies
Heart Rate
Blood Pressure
Messenger RNA

All Science Journal Classification (ASJC) codes

  • Orthopedics and Sports Medicine
  • Physical Therapy, Sports Therapy and Rehabilitation

Cite this

Hicks, Steven D. ; Jacob, Paige ; Perez, Omar ; Baffuto, Matthew ; Gagnon, Zofia ; Middleton, Frank A. / The Transcriptional Signature of a Runner's High. In: Medicine and science in sports and exercise. 2019 ; Vol. 51, No. 5. pp. 970-978.
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title = "The Transcriptional Signature of a Runner's High",
abstract = "Introduction: Endorphins, endocannabinoids, monoamines, and neurotrophins have all been implicated in the euphoric response to endurance running, known as a runner's high (RH). The epitranscriptional mechanisms regulating this effect have not been defined. Here, we investigate peripheral micro-ribonucleic acid (miRNA) changes unique to athletes experiencing postrun euphoria, yielding insights into gene networks that control an RH. Methods: A cohort study involving 25 collegiate runners (48{\%} females, age = 20 ± 1 yr) examined salivary RNA levels before and after a long-distance run. Participants were divided into RH and nonrunner's high (NRH) groups based on surveys of four criteria (mood, lost sense of time, run quality, and euphoria). Physiological measures were also recorded (temperature, heart rate, blood pressure, pupillary dilatation, and salivary serotonin). Levels of miRNAs and their messenger RNA targets were compared across pre- and postrun samples from RH and NRH groups with two-way ANOVA. Representation of opioid, gamma-aminobutyic acid (GABA), endocannabinoid, neurotrophin, serotonergic, and dopaminergic pathways was assessed in DIANA miRPath. Pearson's correlation analyses examined relationships between miRNAs and RH indices. Results: RH participants (n = 13) demonstrated postrun mydriasis (P = 0.046) and hypothermia (P = 0.043) relative to NRH participants (n = 12) but had no difference in serotonin dynamics (P = 0.88). Six miRNAs (miR-194-5p, miR-4676-3p, miR-4254, miR-4425, miR-1273-3p, miR-6743-5p) exhibited significant effects (false discovery rate P value < 0.05) across pre- or postrun and RH/NRH groups. These miRNAs displayed target enrichment for opioid (P = 2.74E-06) and GABA (P = 0.00016) pathways. miR-1237-3p levels were related with lost sense of time (R = 0.40). Mitogen-activated protein kinase (MAPK11), an endocannabinoid target of miR-1273-3p, was nominally elevated in RH participants (false discovery rate P value = 0.11). Conclusions: Unique dynamics in miRNA concentration occur in athletes with subjective/objective evidence of RH, targeting genes implicated endorphin, endocannabinoid, and GABAergic signaling.",
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Hicks, SD, Jacob, P, Perez, O, Baffuto, M, Gagnon, Z & Middleton, FA 2019, 'The Transcriptional Signature of a Runner's High', Medicine and science in sports and exercise, vol. 51, no. 5, pp. 970-978. https://doi.org/10.1249/MSS.0000000000001865

The Transcriptional Signature of a Runner's High. / Hicks, Steven D.; Jacob, Paige; Perez, Omar; Baffuto, Matthew; Gagnon, Zofia; Middleton, Frank A.

In: Medicine and science in sports and exercise, Vol. 51, No. 5, 01.05.2019, p. 970-978.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The Transcriptional Signature of a Runner's High

AU - Hicks, Steven D.

AU - Jacob, Paige

AU - Perez, Omar

AU - Baffuto, Matthew

AU - Gagnon, Zofia

AU - Middleton, Frank A.

PY - 2019/5/1

Y1 - 2019/5/1

N2 - Introduction: Endorphins, endocannabinoids, monoamines, and neurotrophins have all been implicated in the euphoric response to endurance running, known as a runner's high (RH). The epitranscriptional mechanisms regulating this effect have not been defined. Here, we investigate peripheral micro-ribonucleic acid (miRNA) changes unique to athletes experiencing postrun euphoria, yielding insights into gene networks that control an RH. Methods: A cohort study involving 25 collegiate runners (48% females, age = 20 ± 1 yr) examined salivary RNA levels before and after a long-distance run. Participants were divided into RH and nonrunner's high (NRH) groups based on surveys of four criteria (mood, lost sense of time, run quality, and euphoria). Physiological measures were also recorded (temperature, heart rate, blood pressure, pupillary dilatation, and salivary serotonin). Levels of miRNAs and their messenger RNA targets were compared across pre- and postrun samples from RH and NRH groups with two-way ANOVA. Representation of opioid, gamma-aminobutyic acid (GABA), endocannabinoid, neurotrophin, serotonergic, and dopaminergic pathways was assessed in DIANA miRPath. Pearson's correlation analyses examined relationships between miRNAs and RH indices. Results: RH participants (n = 13) demonstrated postrun mydriasis (P = 0.046) and hypothermia (P = 0.043) relative to NRH participants (n = 12) but had no difference in serotonin dynamics (P = 0.88). Six miRNAs (miR-194-5p, miR-4676-3p, miR-4254, miR-4425, miR-1273-3p, miR-6743-5p) exhibited significant effects (false discovery rate P value < 0.05) across pre- or postrun and RH/NRH groups. These miRNAs displayed target enrichment for opioid (P = 2.74E-06) and GABA (P = 0.00016) pathways. miR-1237-3p levels were related with lost sense of time (R = 0.40). Mitogen-activated protein kinase (MAPK11), an endocannabinoid target of miR-1273-3p, was nominally elevated in RH participants (false discovery rate P value = 0.11). Conclusions: Unique dynamics in miRNA concentration occur in athletes with subjective/objective evidence of RH, targeting genes implicated endorphin, endocannabinoid, and GABAergic signaling.

AB - Introduction: Endorphins, endocannabinoids, monoamines, and neurotrophins have all been implicated in the euphoric response to endurance running, known as a runner's high (RH). The epitranscriptional mechanisms regulating this effect have not been defined. Here, we investigate peripheral micro-ribonucleic acid (miRNA) changes unique to athletes experiencing postrun euphoria, yielding insights into gene networks that control an RH. Methods: A cohort study involving 25 collegiate runners (48% females, age = 20 ± 1 yr) examined salivary RNA levels before and after a long-distance run. Participants were divided into RH and nonrunner's high (NRH) groups based on surveys of four criteria (mood, lost sense of time, run quality, and euphoria). Physiological measures were also recorded (temperature, heart rate, blood pressure, pupillary dilatation, and salivary serotonin). Levels of miRNAs and their messenger RNA targets were compared across pre- and postrun samples from RH and NRH groups with two-way ANOVA. Representation of opioid, gamma-aminobutyic acid (GABA), endocannabinoid, neurotrophin, serotonergic, and dopaminergic pathways was assessed in DIANA miRPath. Pearson's correlation analyses examined relationships between miRNAs and RH indices. Results: RH participants (n = 13) demonstrated postrun mydriasis (P = 0.046) and hypothermia (P = 0.043) relative to NRH participants (n = 12) but had no difference in serotonin dynamics (P = 0.88). Six miRNAs (miR-194-5p, miR-4676-3p, miR-4254, miR-4425, miR-1273-3p, miR-6743-5p) exhibited significant effects (false discovery rate P value < 0.05) across pre- or postrun and RH/NRH groups. These miRNAs displayed target enrichment for opioid (P = 2.74E-06) and GABA (P = 0.00016) pathways. miR-1237-3p levels were related with lost sense of time (R = 0.40). Mitogen-activated protein kinase (MAPK11), an endocannabinoid target of miR-1273-3p, was nominally elevated in RH participants (false discovery rate P value = 0.11). Conclusions: Unique dynamics in miRNA concentration occur in athletes with subjective/objective evidence of RH, targeting genes implicated endorphin, endocannabinoid, and GABAergic signaling.

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