Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: A functional and proteomic analysis

Julien Gondin, Lorenza Brocca, Elena Bellinzona, Giuseppe D'Antona, Nicola A. Maffiuletti, Danilo Miotti, Maria A. Pellegrino, Roberto Bottinelli

Research output: Contribution to journalArticle

80 Citations (Scopus)

Abstract

The aim of the present study was to define the chronic effects of neuromuscular electrical stimulation (NMES) on the neuromuscular properties of human skeletal muscle. Eight young healthy male subjects were subjected to 25 sessions of isometric NMES of the quadriceps muscle over an 8-wk period. Needle biopsies were taken from the vastus lateralis muscle before and after training. The training status, myosin heavy chain (MHC) isoform distribution, and global protein pattern, as assessed by proteomic analysis, widely varied among subjects at baseline and prompted the identification of two subgroups: an "active" (ACT) group, which performed regular exercise and had a slower MHC profile, and a sedentary (SED) group, which did not perform any exercise and had a faster MHC profile. Maximum voluntary force and neural activation significantly increased after NMES in both groups (+∼30% and +∼10%, respectively). Both type 1 and 2 fibers showed significant muscle hypertrophy. After NMES, both groups showed a significant shift from MHC-2X toward MHC-2A and MHC-1, i.e., a fast-to-slow transition. Proteomic maps showing ∼500 spots were obtained before and after training in both groups. Differentially expressed proteins were identified and grouped into functional categories. The most relevant changes regarded 1) myofibrillar proteins, whose changes were consistent with a fast-to-slow phenotype shift and with a strengthening of the cytoskeleton; 2) energy production systems, whose changes indicated a glycolytic-to-oxidative shift in the metabolic profile; and 3) antioxidant defense systems, whose changes indicated an enhancement of intracellular defenses against reactive oxygen species. The adaptations in the protein pattern of the ACT and SED groups were different but were, in both groups, typical of both resistance (i.e., strength gains and hypertrophy) and endurance (i.e., a fast-to-slow shift in MHC and metabolic profile) training. These training-induced adaptations can be ascribed to the peculiar motor unit recruitment pattern associated with NMES.

Original languageEnglish
Pages (from-to)433-450
Number of pages18
JournalJournal of Applied Physiology
Volume110
Issue number2
DOIs
Publication statusPublished - Feb 2011

Fingerprint

Myosin Heavy Chains
Proteomics
Electric Stimulation
Skeletal Muscle
Phenotype
Metabolome
Quadriceps Muscle
Hypertrophy
Proteins
Neurophysiological Recruitment
Exercise
Muscles
Needle Biopsy
Cytoskeleton
Reactive Oxygen Species
Healthy Volunteers
Protein Isoforms
Antioxidants

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype : A functional and proteomic analysis. / Gondin, Julien; Brocca, Lorenza; Bellinzona, Elena; D'Antona, Giuseppe; Maffiuletti, Nicola A.; Miotti, Danilo; Pellegrino, Maria A.; Bottinelli, Roberto.

In: Journal of Applied Physiology, Vol. 110, No. 2, 02.2011, p. 433-450.

Research output: Contribution to journalArticle

Gondin, Julien ; Brocca, Lorenza ; Bellinzona, Elena ; D'Antona, Giuseppe ; Maffiuletti, Nicola A. ; Miotti, Danilo ; Pellegrino, Maria A. ; Bottinelli, Roberto. / Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype : A functional and proteomic analysis. In: Journal of Applied Physiology. 2011 ; Vol. 110, No. 2. pp. 433-450.
@article{2a0cb3ee396d4bc5b4422ffe1c125999,
title = "Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: A functional and proteomic analysis",
abstract = "The aim of the present study was to define the chronic effects of neuromuscular electrical stimulation (NMES) on the neuromuscular properties of human skeletal muscle. Eight young healthy male subjects were subjected to 25 sessions of isometric NMES of the quadriceps muscle over an 8-wk period. Needle biopsies were taken from the vastus lateralis muscle before and after training. The training status, myosin heavy chain (MHC) isoform distribution, and global protein pattern, as assessed by proteomic analysis, widely varied among subjects at baseline and prompted the identification of two subgroups: an {"}active{"} (ACT) group, which performed regular exercise and had a slower MHC profile, and a sedentary (SED) group, which did not perform any exercise and had a faster MHC profile. Maximum voluntary force and neural activation significantly increased after NMES in both groups (+∼30{\%} and +∼10{\%}, respectively). Both type 1 and 2 fibers showed significant muscle hypertrophy. After NMES, both groups showed a significant shift from MHC-2X toward MHC-2A and MHC-1, i.e., a fast-to-slow transition. Proteomic maps showing ∼500 spots were obtained before and after training in both groups. Differentially expressed proteins were identified and grouped into functional categories. The most relevant changes regarded 1) myofibrillar proteins, whose changes were consistent with a fast-to-slow phenotype shift and with a strengthening of the cytoskeleton; 2) energy production systems, whose changes indicated a glycolytic-to-oxidative shift in the metabolic profile; and 3) antioxidant defense systems, whose changes indicated an enhancement of intracellular defenses against reactive oxygen species. The adaptations in the protein pattern of the ACT and SED groups were different but were, in both groups, typical of both resistance (i.e., strength gains and hypertrophy) and endurance (i.e., a fast-to-slow shift in MHC and metabolic profile) training. These training-induced adaptations can be ascribed to the peculiar motor unit recruitment pattern associated with NMES.",
author = "Julien Gondin and Lorenza Brocca and Elena Bellinzona and Giuseppe D'Antona and Maffiuletti, {Nicola A.} and Danilo Miotti and Pellegrino, {Maria A.} and Roberto Bottinelli",
year = "2011",
month = "2",
doi = "10.1152/japplphysiol.00914.2010",
language = "English",
volume = "110",
pages = "433--450",
journal = "Journal of Applied Physiology",
issn = "8750-7587",
publisher = "American Physiological Society",
number = "2",

}

TY - JOUR

T1 - Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype

T2 - A functional and proteomic analysis

AU - Gondin, Julien

AU - Brocca, Lorenza

AU - Bellinzona, Elena

AU - D'Antona, Giuseppe

AU - Maffiuletti, Nicola A.

AU - Miotti, Danilo

AU - Pellegrino, Maria A.

AU - Bottinelli, Roberto

PY - 2011/2

Y1 - 2011/2

N2 - The aim of the present study was to define the chronic effects of neuromuscular electrical stimulation (NMES) on the neuromuscular properties of human skeletal muscle. Eight young healthy male subjects were subjected to 25 sessions of isometric NMES of the quadriceps muscle over an 8-wk period. Needle biopsies were taken from the vastus lateralis muscle before and after training. The training status, myosin heavy chain (MHC) isoform distribution, and global protein pattern, as assessed by proteomic analysis, widely varied among subjects at baseline and prompted the identification of two subgroups: an "active" (ACT) group, which performed regular exercise and had a slower MHC profile, and a sedentary (SED) group, which did not perform any exercise and had a faster MHC profile. Maximum voluntary force and neural activation significantly increased after NMES in both groups (+∼30% and +∼10%, respectively). Both type 1 and 2 fibers showed significant muscle hypertrophy. After NMES, both groups showed a significant shift from MHC-2X toward MHC-2A and MHC-1, i.e., a fast-to-slow transition. Proteomic maps showing ∼500 spots were obtained before and after training in both groups. Differentially expressed proteins were identified and grouped into functional categories. The most relevant changes regarded 1) myofibrillar proteins, whose changes were consistent with a fast-to-slow phenotype shift and with a strengthening of the cytoskeleton; 2) energy production systems, whose changes indicated a glycolytic-to-oxidative shift in the metabolic profile; and 3) antioxidant defense systems, whose changes indicated an enhancement of intracellular defenses against reactive oxygen species. The adaptations in the protein pattern of the ACT and SED groups were different but were, in both groups, typical of both resistance (i.e., strength gains and hypertrophy) and endurance (i.e., a fast-to-slow shift in MHC and metabolic profile) training. These training-induced adaptations can be ascribed to the peculiar motor unit recruitment pattern associated with NMES.

AB - The aim of the present study was to define the chronic effects of neuromuscular electrical stimulation (NMES) on the neuromuscular properties of human skeletal muscle. Eight young healthy male subjects were subjected to 25 sessions of isometric NMES of the quadriceps muscle over an 8-wk period. Needle biopsies were taken from the vastus lateralis muscle before and after training. The training status, myosin heavy chain (MHC) isoform distribution, and global protein pattern, as assessed by proteomic analysis, widely varied among subjects at baseline and prompted the identification of two subgroups: an "active" (ACT) group, which performed regular exercise and had a slower MHC profile, and a sedentary (SED) group, which did not perform any exercise and had a faster MHC profile. Maximum voluntary force and neural activation significantly increased after NMES in both groups (+∼30% and +∼10%, respectively). Both type 1 and 2 fibers showed significant muscle hypertrophy. After NMES, both groups showed a significant shift from MHC-2X toward MHC-2A and MHC-1, i.e., a fast-to-slow transition. Proteomic maps showing ∼500 spots were obtained before and after training in both groups. Differentially expressed proteins were identified and grouped into functional categories. The most relevant changes regarded 1) myofibrillar proteins, whose changes were consistent with a fast-to-slow phenotype shift and with a strengthening of the cytoskeleton; 2) energy production systems, whose changes indicated a glycolytic-to-oxidative shift in the metabolic profile; and 3) antioxidant defense systems, whose changes indicated an enhancement of intracellular defenses against reactive oxygen species. The adaptations in the protein pattern of the ACT and SED groups were different but were, in both groups, typical of both resistance (i.e., strength gains and hypertrophy) and endurance (i.e., a fast-to-slow shift in MHC and metabolic profile) training. These training-induced adaptations can be ascribed to the peculiar motor unit recruitment pattern associated with NMES.

UR - http://www.scopus.com/inward/record.url?scp=79851505708&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79851505708&partnerID=8YFLogxK

U2 - 10.1152/japplphysiol.00914.2010

DO - 10.1152/japplphysiol.00914.2010

M3 - Article

C2 - 21127206

AN - SCOPUS:79851505708

VL - 110

SP - 433

EP - 450

JO - Journal of Applied Physiology

JF - Journal of Applied Physiology

SN - 8750-7587

IS - 2

ER -