Multiplex quantification identifies novel exercise-regulated myokines/cytokines in plasma and in glycolytic and oxidative skeletal muscle

Hannah C. Little, Stefanie Y. Tan, Francesca M. Cali, Susana Rodriguez, Xia Lei, Andrew Wolfe, Christopher Hug, Guang William Wong

Research output: Contribution to journalArticle

Abstract

Exercise is known to confer major health benefits, but the underlying mechanisms are not well understood. The systemic effects of exercise on multi-organ systems are thought to be partly because of myokines/cytokines secreted by skeletal muscle. The extent to which exercise alters cytokine expression and secretion in different muscle fiber types has not been systematically examined. Here, we assessed changes in 66 mouse cytokines in serum, and in glycolytic (plantaris) and oxidative (soleus) muscles, in response to sprint, endurance, or chronic wheel running. Both acute and shortterm exercise significantly altered a large fraction of cytokines in both serum and muscle, twenty-three of which are considered novel exercise-regulated myokines. Most of the secreted cytokine receptors profiled were also altered by physical activity, suggesting an exercise-regulated mechanism that modulates the generation of soluble receptors found in circulation. A greater overlap in cytokine profile was seen between endurance and chronic wheel running. Between fiber types, both acute and chronic exercise induced significantly more cytokine changes in oxidative compared with glycolytic muscle. Further, changes in a subset of circulating cytokines were not matched by their changes in muscle, but instead reflected altered expression in liver and adipose tissues. Last, exercise-induced changes in cytokine mRNA and protein were only minimally correlated in soleus and plantaris. In sum, our results indicate that exercise regulates many cytokines whose pleiotropic actions may be linked to positive health outcomes. These data provide a framework to further understand potential crosstalk between skeletal muscle and other organ compartments.

Original languageEnglish (US)
Pages (from-to)1546-1563
Number of pages18
JournalMolecular and Cellular Proteomics
Volume17
Issue number8
DOIs
StatePublished - Aug 1 2018

Fingerprint

Muscle
Skeletal Muscle
Cytokines
Plasmas
Muscles
Running
Wheels
Durability
Health
Exercise
Cytokine Receptors
Fibers
Insurance Benefits
Crosstalk
Serum
Liver
Adipose Tissue
Tissue
Messenger RNA
Proteins

ASJC Scopus subject areas

  • Analytical Chemistry
  • Biochemistry
  • Molecular Biology

Cite this

Multiplex quantification identifies novel exercise-regulated myokines/cytokines in plasma and in glycolytic and oxidative skeletal muscle. / Little, Hannah C.; Tan, Stefanie Y.; Cali, Francesca M.; Rodriguez, Susana; Lei, Xia; Wolfe, Andrew; Hug, Christopher; Wong, Guang William.

In: Molecular and Cellular Proteomics, Vol. 17, No. 8, 01.08.2018, p. 1546-1563.

Research output: Contribution to journalArticle

Little, Hannah C. ; Tan, Stefanie Y. ; Cali, Francesca M. ; Rodriguez, Susana ; Lei, Xia ; Wolfe, Andrew ; Hug, Christopher ; Wong, Guang William. / Multiplex quantification identifies novel exercise-regulated myokines/cytokines in plasma and in glycolytic and oxidative skeletal muscle. In: Molecular and Cellular Proteomics. 2018 ; Vol. 17, No. 8. pp. 1546-1563.
@article{5d238967bc344605933a893d103b76df,
title = "Multiplex quantification identifies novel exercise-regulated myokines/cytokines in plasma and in glycolytic and oxidative skeletal muscle",
abstract = "Exercise is known to confer major health benefits, but the underlying mechanisms are not well understood. The systemic effects of exercise on multi-organ systems are thought to be partly because of myokines/cytokines secreted by skeletal muscle. The extent to which exercise alters cytokine expression and secretion in different muscle fiber types has not been systematically examined. Here, we assessed changes in 66 mouse cytokines in serum, and in glycolytic (plantaris) and oxidative (soleus) muscles, in response to sprint, endurance, or chronic wheel running. Both acute and shortterm exercise significantly altered a large fraction of cytokines in both serum and muscle, twenty-three of which are considered novel exercise-regulated myokines. Most of the secreted cytokine receptors profiled were also altered by physical activity, suggesting an exercise-regulated mechanism that modulates the generation of soluble receptors found in circulation. A greater overlap in cytokine profile was seen between endurance and chronic wheel running. Between fiber types, both acute and chronic exercise induced significantly more cytokine changes in oxidative compared with glycolytic muscle. Further, changes in a subset of circulating cytokines were not matched by their changes in muscle, but instead reflected altered expression in liver and adipose tissues. Last, exercise-induced changes in cytokine mRNA and protein were only minimally correlated in soleus and plantaris. In sum, our results indicate that exercise regulates many cytokines whose pleiotropic actions may be linked to positive health outcomes. These data provide a framework to further understand potential crosstalk between skeletal muscle and other organ compartments.",
author = "Little, {Hannah C.} and Tan, {Stefanie Y.} and Cali, {Francesca M.} and Susana Rodriguez and Xia Lei and Andrew Wolfe and Christopher Hug and Wong, {Guang William}",
year = "2018",
month = "8",
day = "1",
doi = "10.1074/mcp.RA118.000794",
language = "English (US)",
volume = "17",
pages = "1546--1563",
journal = "Molecular and Cellular Proteomics",
issn = "1535-9476",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "8",

}

TY - JOUR

T1 - Multiplex quantification identifies novel exercise-regulated myokines/cytokines in plasma and in glycolytic and oxidative skeletal muscle

AU - Little, Hannah C.

AU - Tan, Stefanie Y.

AU - Cali, Francesca M.

AU - Rodriguez, Susana

AU - Lei, Xia

AU - Wolfe, Andrew

AU - Hug, Christopher

AU - Wong, Guang William

PY - 2018/8/1

Y1 - 2018/8/1

N2 - Exercise is known to confer major health benefits, but the underlying mechanisms are not well understood. The systemic effects of exercise on multi-organ systems are thought to be partly because of myokines/cytokines secreted by skeletal muscle. The extent to which exercise alters cytokine expression and secretion in different muscle fiber types has not been systematically examined. Here, we assessed changes in 66 mouse cytokines in serum, and in glycolytic (plantaris) and oxidative (soleus) muscles, in response to sprint, endurance, or chronic wheel running. Both acute and shortterm exercise significantly altered a large fraction of cytokines in both serum and muscle, twenty-three of which are considered novel exercise-regulated myokines. Most of the secreted cytokine receptors profiled were also altered by physical activity, suggesting an exercise-regulated mechanism that modulates the generation of soluble receptors found in circulation. A greater overlap in cytokine profile was seen between endurance and chronic wheel running. Between fiber types, both acute and chronic exercise induced significantly more cytokine changes in oxidative compared with glycolytic muscle. Further, changes in a subset of circulating cytokines were not matched by their changes in muscle, but instead reflected altered expression in liver and adipose tissues. Last, exercise-induced changes in cytokine mRNA and protein were only minimally correlated in soleus and plantaris. In sum, our results indicate that exercise regulates many cytokines whose pleiotropic actions may be linked to positive health outcomes. These data provide a framework to further understand potential crosstalk between skeletal muscle and other organ compartments.

AB - Exercise is known to confer major health benefits, but the underlying mechanisms are not well understood. The systemic effects of exercise on multi-organ systems are thought to be partly because of myokines/cytokines secreted by skeletal muscle. The extent to which exercise alters cytokine expression and secretion in different muscle fiber types has not been systematically examined. Here, we assessed changes in 66 mouse cytokines in serum, and in glycolytic (plantaris) and oxidative (soleus) muscles, in response to sprint, endurance, or chronic wheel running. Both acute and shortterm exercise significantly altered a large fraction of cytokines in both serum and muscle, twenty-three of which are considered novel exercise-regulated myokines. Most of the secreted cytokine receptors profiled were also altered by physical activity, suggesting an exercise-regulated mechanism that modulates the generation of soluble receptors found in circulation. A greater overlap in cytokine profile was seen between endurance and chronic wheel running. Between fiber types, both acute and chronic exercise induced significantly more cytokine changes in oxidative compared with glycolytic muscle. Further, changes in a subset of circulating cytokines were not matched by their changes in muscle, but instead reflected altered expression in liver and adipose tissues. Last, exercise-induced changes in cytokine mRNA and protein were only minimally correlated in soleus and plantaris. In sum, our results indicate that exercise regulates many cytokines whose pleiotropic actions may be linked to positive health outcomes. These data provide a framework to further understand potential crosstalk between skeletal muscle and other organ compartments.

UR - http://www.scopus.com/inward/record.url?scp=85051004905&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85051004905&partnerID=8YFLogxK

U2 - 10.1074/mcp.RA118.000794

DO - 10.1074/mcp.RA118.000794

M3 - Article

C2 - 29735541

AN - SCOPUS:85051004905

VL - 17

SP - 1546

EP - 1563

JO - Molecular and Cellular Proteomics

JF - Molecular and Cellular Proteomics

SN - 1535-9476

IS - 8

ER -