Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise

Bryon R. McKay; Joshua P. Nederveen; Stephen A. Fortino; Tim Snijders; Sophie Joanisse; Dinesh A. Kumbhare; Gianni Parise

doi:10.1139/apnm-2019-0501

Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise

Bryon R. McKay, Joshua P. Nederveen, Stephen A. Fortino, Tim Snijders, Sophie Joanisse, Dinesh A. Kumbhare, Gianni Parise^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Muscle satellite cell (SC) regulation is a complex process involving many key signalling molecules. Recently, the neurotrophin brain-derived neurotropic factor (BDNF) has implicated in SC regulation in animals. To date, little is known regarding the role of BDNF in human SC function in vivo. Twenty-nine males (age, 21 +/- 0.5 years) participated in the study. Muscle biopsies from the thigh were obtained prior to a bout of 300 maximal eccentric contractions (Pre), and at 6 h, 24 h, 72 11, and 96 h postexercise. BDNF was not detected in any quiescent (Pax7(+)/MyoD(-))SCs across the time-course. BDNF colocalized to 39% +/- 5% of proliferating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 84% +/- 3% by 96 h (P < 0.05). BDNF was only detected in 13% +/- 5% of differentiating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 67% +/- 4% by 96 h (P < 0.05). The number of myogenin(+) cells increased 95% from Pre (1.6 +/- 0.2 cells/100 myofibres (MF)) at 24 h (3.1 +/- 0.3 cells/100 MF) and remained elevated until 96 h (cells/100 MF), P < 0.05. The proportion of BDNF+/mnyogenin(+) cells was 26% +/- 0.3% at Pre, peaking at 24 11 (49% +/- 3%, P < 0.05) and remained elevated at 96 h (P < 0.05). These data are the first to demonstrate an association between SC proliferation and differentiation and BDNF expression in humans in vivo, with BDNF colocalization to SCs increasing during the later stages of proliferation and early differentiation.

Novelty

BDNF is associated with SC response to muscle injury.

BDNF was not detected in nonactivated (quiescent) SCs.

BDNF is associated with late proliferation and early differentiation of SCs in vivo in humans.

Original language	English
Pages (from-to)	581-590
Number of pages	10
Journal	Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme
Volume	45
Issue number	6
DOIs	https://doi.org/10.1139/apnm-2019-0501
Publication status	Published - Jun 2020

Keywords

Pax7
satellite cells
brain-derived neurotrophic factor
muscle
damage
myogenic regulatory factors
SKELETAL-MUSCLE
STEM-CELL
GENE-EXPRESSION
BDNF
REGENERATION
POTENTIATION
CONTRACTION
ACTIVATION
EXPANSION
SURVIVAL

Access to Document

10.1139/apnm-2019-0501

Cite this

McKay, B. R., Nederveen, J. P., Fortino, S. A., Snijders, T., Joanisse, S., Kumbhare, D. A., & Parise, G. (2020). Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise. Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme, 45(6), 581-590. https://doi.org/10.1139/apnm-2019-0501

@article{33218898a374402d80b732994b97cd5f,

title = "Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise",

abstract = "Muscle satellite cell (SC) regulation is a complex process involving many key signalling molecules. Recently, the neurotrophin brain-derived neurotropic factor (BDNF) has implicated in SC regulation in animals. To date, little is known regarding the role of BDNF in human SC function in vivo. Twenty-nine males (age, 21 +/- 0.5 years) participated in the study. Muscle biopsies from the thigh were obtained prior to a bout of 300 maximal eccentric contractions (Pre), and at 6 h, 24 h, 72 11, and 96 h postexercise. BDNF was not detected in any quiescent (Pax7(+)/MyoD(-))SCs across the time-course. BDNF colocalized to 39% +/- 5% of proliferating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 84% +/- 3% by 96 h (P < 0.05). BDNF was only detected in 13% +/- 5% of differentiating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 67% +/- 4% by 96 h (P < 0.05). The number of myogenin(+) cells increased 95% from Pre (1.6 +/- 0.2 cells/100 myofibres (MF)) at 24 h (3.1 +/- 0.3 cells/100 MF) and remained elevated until 96 h (cells/100 MF), P < 0.05. The proportion of BDNF+/mnyogenin(+) cells was 26% +/- 0.3% at Pre, peaking at 24 11 (49% +/- 3%, P < 0.05) and remained elevated at 96 h (P < 0.05). These data are the first to demonstrate an association between SC proliferation and differentiation and BDNF expression in humans in vivo, with BDNF colocalization to SCs increasing during the later stages of proliferation and early differentiation.NoveltyBDNF is associated with SC response to muscle injury.BDNF was not detected in nonactivated (quiescent) SCs.BDNF is associated with late proliferation and early differentiation of SCs in vivo in humans.",

keywords = "Pax7, satellite cells, brain-derived neurotrophic factor, muscle, damage, myogenic regulatory factors, SKELETAL-MUSCLE, STEM-CELL, GENE-EXPRESSION, BDNF, REGENERATION, POTENTIATION, CONTRACTION, ACTIVATION, EXPANSION, SURVIVAL",

author = "McKay, {Bryon R.} and Nederveen, {Joshua P.} and Fortino, {Stephen A.} and Tim Snijders and Sophie Joanisse and Kumbhare, {Dinesh A.} and Gianni Parise",

note = "Funding Information: We would like to acknowledge Dr. Jonathan P Little (The University of British Columbia, Kelowna, B.C., Canada) for his assistance with the BDNF mRNA primers. The Pax7 hybridoma cells developed by Dr. A. Kawakami and the F5D cells developed by Dr. W. E. Wright were obtained from the Developmental Studies Hybridoma Bank, created by the National Institute of Child Health and Human Development, and maintained at Department of Biology of The University of Iowa (Iowa City, Iowa, USA). This work was supported by operating grants from Natural Sciences and Engineering Research Council (NSERC) and Canadian Institutes of Health Research (CIHR) to Dr. G. Parise. Publisher Copyright: {\textcopyright} 2020, Canadian Science Publishing. All rights reserved.",

year = "2020",

month = jun,

doi = "10.1139/apnm-2019-0501",

language = "English",

volume = "45",

pages = "581--590",

journal = "Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme",

issn = "1715-5312",

publisher = "Canadian Science Publishing, NRC Research Press",

number = "6",

}

McKay, BR, Nederveen, JP, Fortino, SA, Snijders, T, Joanisse, S, Kumbhare, DA & Parise, G 2020, 'Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise', Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme, vol. 45, no. 6, pp. 581-590. https://doi.org/10.1139/apnm-2019-0501

Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise. / McKay, Bryon R.; Nederveen, Joshua P.; Fortino, Stephen A. et al.
In: Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme, Vol. 45, No. 6, 06.2020, p. 581-590.

Research output: Contribution to journal › Article › Academic › peer-review

TY - JOUR

T1 - Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise

AU - McKay, Bryon R.

AU - Nederveen, Joshua P.

AU - Fortino, Stephen A.

AU - Snijders, Tim

AU - Joanisse, Sophie

AU - Kumbhare, Dinesh A.

AU - Parise, Gianni

N1 - Funding Information: We would like to acknowledge Dr. Jonathan P Little (The University of British Columbia, Kelowna, B.C., Canada) for his assistance with the BDNF mRNA primers. The Pax7 hybridoma cells developed by Dr. A. Kawakami and the F5D cells developed by Dr. W. E. Wright were obtained from the Developmental Studies Hybridoma Bank, created by the National Institute of Child Health and Human Development, and maintained at Department of Biology of The University of Iowa (Iowa City, Iowa, USA). This work was supported by operating grants from Natural Sciences and Engineering Research Council (NSERC) and Canadian Institutes of Health Research (CIHR) to Dr. G. Parise. Publisher Copyright: © 2020, Canadian Science Publishing. All rights reserved.

PY - 2020/6

Y1 - 2020/6

N2 - Muscle satellite cell (SC) regulation is a complex process involving many key signalling molecules. Recently, the neurotrophin brain-derived neurotropic factor (BDNF) has implicated in SC regulation in animals. To date, little is known regarding the role of BDNF in human SC function in vivo. Twenty-nine males (age, 21 +/- 0.5 years) participated in the study. Muscle biopsies from the thigh were obtained prior to a bout of 300 maximal eccentric contractions (Pre), and at 6 h, 24 h, 72 11, and 96 h postexercise. BDNF was not detected in any quiescent (Pax7(+)/MyoD(-))SCs across the time-course. BDNF colocalized to 39% +/- 5% of proliferating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 84% +/- 3% by 96 h (P < 0.05). BDNF was only detected in 13% +/- 5% of differentiating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 67% +/- 4% by 96 h (P < 0.05). The number of myogenin(+) cells increased 95% from Pre (1.6 +/- 0.2 cells/100 myofibres (MF)) at 24 h (3.1 +/- 0.3 cells/100 MF) and remained elevated until 96 h (cells/100 MF), P < 0.05. The proportion of BDNF+/mnyogenin(+) cells was 26% +/- 0.3% at Pre, peaking at 24 11 (49% +/- 3%, P < 0.05) and remained elevated at 96 h (P < 0.05). These data are the first to demonstrate an association between SC proliferation and differentiation and BDNF expression in humans in vivo, with BDNF colocalization to SCs increasing during the later stages of proliferation and early differentiation.NoveltyBDNF is associated with SC response to muscle injury.BDNF was not detected in nonactivated (quiescent) SCs.BDNF is associated with late proliferation and early differentiation of SCs in vivo in humans.

AB - Muscle satellite cell (SC) regulation is a complex process involving many key signalling molecules. Recently, the neurotrophin brain-derived neurotropic factor (BDNF) has implicated in SC regulation in animals. To date, little is known regarding the role of BDNF in human SC function in vivo. Twenty-nine males (age, 21 +/- 0.5 years) participated in the study. Muscle biopsies from the thigh were obtained prior to a bout of 300 maximal eccentric contractions (Pre), and at 6 h, 24 h, 72 11, and 96 h postexercise. BDNF was not detected in any quiescent (Pax7(+)/MyoD(-))SCs across the time-course. BDNF colocalized to 39% +/- 5% of proliferating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 84% +/- 3% by 96 h (P < 0.05). BDNF was only detected in 13% +/- 5% of differentiating (Pax7(+)/MyoD(-)) cells at Pre, which increased to 67% +/- 4% by 96 h (P < 0.05). The number of myogenin(+) cells increased 95% from Pre (1.6 +/- 0.2 cells/100 myofibres (MF)) at 24 h (3.1 +/- 0.3 cells/100 MF) and remained elevated until 96 h (cells/100 MF), P < 0.05. The proportion of BDNF+/mnyogenin(+) cells was 26% +/- 0.3% at Pre, peaking at 24 11 (49% +/- 3%, P < 0.05) and remained elevated at 96 h (P < 0.05). These data are the first to demonstrate an association between SC proliferation and differentiation and BDNF expression in humans in vivo, with BDNF colocalization to SCs increasing during the later stages of proliferation and early differentiation.NoveltyBDNF is associated with SC response to muscle injury.BDNF was not detected in nonactivated (quiescent) SCs.BDNF is associated with late proliferation and early differentiation of SCs in vivo in humans.

KW - Pax7

KW - satellite cells

KW - brain-derived neurotrophic factor

KW - muscle

KW - damage

KW - myogenic regulatory factors

KW - SKELETAL-MUSCLE

KW - STEM-CELL

KW - GENE-EXPRESSION

KW - BDNF

KW - REGENERATION

KW - POTENTIATION

KW - CONTRACTION

KW - ACTIVATION

KW - EXPANSION

KW - SURVIVAL

U2 - 10.1139/apnm-2019-0501

DO - 10.1139/apnm-2019-0501

M3 - Article

C2 - 31661631

SN - 1715-5312

VL - 45

SP - 581

EP - 590

JO - Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme

JF - Applied Physiology Nutrition and Metabolism-Physiologie appliquee nutrition et metabolisme

IS - 6

ER -

Brain-derived neurotrophic factor is associated with human muscle satellite cell differentiation in response to muscle-damaging exercise

Abstract

Keywords

Access to Document

Fingerprint

Cite this