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GDNF Content And NMJ Morphology Are Altered In Recruited Muscles Following High‐speed And Resistance Wheel Training

A. Gyorkos, J. Spitsbergen
Published 2014 · Medicine

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Glial cell line‐derived neurotrophic factor (GDNF) may play a role in delaying the onset of aging and help compress morbidity by preventing motor unit degeneration. Exercise has been shown to alter GDNF expression differently in slow‐ and fast‐twitch myofibers. The aim was to examine the effects of different intensities (10, 20, ~30, and ~40 m·min−1) of wheel running on GDNF expression and neuromuscular junction (NMJ) plasticity in slow‐ and fast‐twitch myofibers. Male Sprague‐Dawley Rats (4 weeks old) were divided into two sedentary control groups (CON4 week, n = 5 and CON6 week, n = 5), two involuntary running groups, one at a low velocity; 10 m/min (INVOL‐low, n = 5), and one at a higher velocity; 20 m/min (INVOL‐high, n = 5), and two voluntary running groups with resistance (VOL‐R, n = 5, 120 g), and without resistance (VOL‐NR, n = 5, 4.5 g). GDNF protein content, determined by enzyme‐linked immunosorbent assay (ELISA), increased significantly in the recruited muscles. Plantaris (PLA) GDNF protein content increased 174% (P < 0.05) and 161% (P < 0.05) and end plate‐stained area increased 123% (P < 0.05) and 72% (P < 0.05) following VOL‐R, and VOL‐NR training, respectively, when compared to age‐matched controls. A relationship exists between GDNF protein content and end plate area (r = 0.880, P < 0.01, n = 15). VOL‐R training also resulted in more dispersed synapses in the PLA muscle when compared to age‐matched controls (P < 0.05). Higher intensity exercise (>30 m/min) can increase GDNF protein content in fast‐twitch myofibers as well as induce changes in the NMJ morphology. These findings help to inform exercise prescription to preserve the integrity of the neuromuscular system through aging and disease.
This paper references
10.1113/jphysiol.1991.sp018550
Effects of enhanced activity on synaptic transmission in mouse extensor digitorum longus muscle.
M. Dorlöchter (1991)
10.1002/CNE.902690309
Medial gastrocnemius motor nucleus in the rat: Age‐related changes in the number and size of motoneurons
K. Hashizume (1988)
10.1093/GERONA/60.3.324
Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons.
M. Visser (2005)
10.1152/JAPPL.1989.66.3.1250
Variations in running activity and enzymatic adaptations in voluntary running rats.
K. Rodnick (1989)
10.1002/(SICI)1096-9861(19981221)402:3<303::AID-CNE2>3.0.CO;2-I
Prominent expression of glial cell line–derived neurotrophic factor in human skeletal muscle
H. Suzuki (1998)
The loss of skeletal
B. H. Goodpaster (2006)
10.1152/JAPPL.1986.60.5.1623
Muscle lipoprotein lipase activity in voluntarily exercising rats.
G. Bagby (1986)
10.1126/SCIENCE.8493557
GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons.
L. Lin (1993)
10.1016/0014-4886(80)90006-0
Effects of aging on nerve sprouting and regeneration
A. Pestronk (1980)
Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society
(2014)
10.1006/anbe.1998.0836
Voluntary wheel running: a review and novel interpretation
C. M. Sherwin (1998)
10.1126/SCIENCE.7973664
GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle.
C. E. Henderson (1994)
10.1007/BF01186990
Plasticity of presynaptic and postsynaptic elements of neuromuscular junctions repeatedly observed in living adult mice
R. R. Hill (1991)
10.1152/JAPPL.1977.43.2.288
Glycogen, lactate, and alanine changes in muscle fiber types during graded exercise.
K. Baldwin (1977)
10.1111/J.1748-1716.1990.TB08974.X
Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds.
H. Klitgaard (1990)
10.1007/s00421-004-1061-1
Effects of prolonged voluntary wheel-running on muscle structure and function in rat skeletal muscle
F. Kariya (2004)
10.1016/j.neuroscience.2010.11.016
Glial cell line-derived neurotrophic factor protein content in rat skeletal muscle is altered by increased physical activity in vivo and in vitro
M. Mccullough (2011)
10.1093/jn/127.5.990S
Sarcopenia: origins and clinical relevance.
I. Rosenberg (1997)
10.1152/JAPPL.1998.84.6.2183
Hypertrophy of rat plantaris muscle fibers after voluntary running with increasing loads.
A. Ishihara (1998)
10.1056/NEJM198007173030304
Aging, natural death, and the compression of morbidity.
J. Fries (1980)
10.1111/j.1532-5415.1977.tb00274.x
Histochemical and Ultrastructural Changes in Senile Human Skeletal Muscle
M. Tomonaga (1977)
10.1152/JAPPL.1982.53.4.844
Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle.
G. Dudley (1982)
10.1212/WNL.19.5.469
The histographic analysis of human muscle biopsies with regard to fiber types
M. Brooke (1969)
J. Histochem. Cytochem
10.1001/JAMA.1989.03420180087036
Risk factors for recurrent nonsyncopal falls. A prospective study.
M. Nevitt (1989)
10.1113/jphysiol.1991.sp018833
Effects of age on physiological, immunohistochemical and biochemical properties of fast‐twitch single motor units in the rat.
L. Larsson (1991)
Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure. Scand
P Aagaard (2010)
10.1001/jama.2009.681
Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis.
S. Kodama (2009)
10.1093/GERONA/61.10.1059
The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study.
B. Goodpaster (2006)
Effects of age on physiological
L Larsson (1991)
10.1152/japplphysiol.01313.2012
I am 80 going on 18: exercise and the fountain of youth.
M. Joyner (2013)
10.1152/JAPPLPHYSIOL.00861.2003
Strength training reduces force fluctuations during anisometric contractions of the quadriceps femoris muscles in old adults.
B. Tracy (2004)
10.3945/ajcn.2009.28047
Longitudinal study of muscle strength, quality, and adipose tissue infiltration.
M. Delmonico (2009)
10.1089/10430349950017536
Intramuscular grafts of myoblasts genetically modified to secrete glial cell line-derived neurotrophic factor prevent motoneuron loss and disease progression in a mouse model of familial amyotrophic lateral sclerosis.
M. Mohajeri (1999)
10.1002/AJA.1001710303
Muscle fiber type composition of the rat hindlimb.
R. Armstrong (1984)
[Fractures of the proximal end of the femur].
J. C. Birkenhäger (1982)
10.1007/BF01637652
Effects of endurance exercise on the morphology of mouse neuromuscular junctions during ageing
M. Andonian (1987)
10.1007/BF00581173
Oxygen uptake of rats at different work intensities
R. Shepherd (2004)
10.1016/j.neuroscience.2013.10.068
Glial cell line-derived neurotrophic factor (GDNF) expression and NMJ plasticity in skeletal muscle following endurance exercise
A. Gyorkos (2014)
10.1002/mus.10179
GDNF is regulated in an activity‐dependent manner in rat skeletal muscle
Erica A. Wehrwein (2002)
10.1016/j.apmr.2008.09.565
Age-associated changes in motor unit physiology: observations from the Baltimore Longitudinal Study of Aging.
S. Ling (2009)
10.1113/expphysiol.2007.041244
Voluntary resistance running wheel activity pattern and skeletal muscle growth in rats
K. Legerlotz (2008)
10.1093/gerona/gls241
Elderly men and women benefit equally from prolonged resistance-type exercise training.
M. Leenders (2013)
10.1007/BF00590489
Glycogen depletion in rat skeletal muscle fibers at different intensities and durations of excercise
R. Armstrong (2004)
10.1139/H01-006
Origins and clinical relevance of sarcopenia.
R. Roubenoff (2001)
10.1016/0022-510X(90)90138-D
Quantitative and qualitative morphological properties of the soleus motor nerve and the L5 ventral root in young and old rats: Relation to the number of soleus muscle fibres
T. Ansved (1990)
J. Neurocytol
10.1007/BF00174949
Different effects of physical training on the morphology of motor nerve terminals in the rat extensor digitorum longus and soleus muscles
O. Wærhaug (2004)
10.1016/j.neuroscience.2005.10.042
Increased and decreased activity elicits specific morphological adaptations of the neuromuscular junction
M. Deschenes (2006)
10.1038/373341A0
In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons
Q. Yan (1995)
10.1097/00005072-198903000-00001
Morphometric Alteration of Rat Myelinated Fibers with Aging
C. A. Knox (1989)
10.1097/00003086-198412000-00025
Impaired muscle function with aging. A background factor in the incidence of fractures of the proximal end of the femur.
A. Aniansson (1984)
10.1046/j.1532-5415.2002.50216.x
Low Relative Skeletal Muscle Mass (Sarcopenia) in Older Persons Is Associated with Functional Impairment and Physical Disability
I. Janssen (2002)
10.1111/j.1600-0838.2009.01084.x
Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure
P. Aagaard (2010)
J. Neuropathol. Exp. Neurol
Spitsbergen GDNF Content and NMJ Altered in Recruited Muscles
A M Gyorkos
10.1074/jbc.M106116200
Regulation of Neuromuscular Synapse Development by Glial Cell Line-derived Neurotrophic Factor and Neurturin*
Chang-Yu Wang (2002)
Effects of age on physiological, immunohistochemical GDNF Content and NMJ Altered in Recruited Muscles Spitsbergen and biochemical properties of fast-twitch single motor units in the rat
L Larsson (1991)
Impaired muscle function with aging
A. Aniansson (1984)
10.1016/j.arr.2010.03.004
Resistance exercise for muscular strength in older adults: A meta-analysis
M. Peterson (2010)
10.1113/jphysiol.1972.sp009691
Fatigue of maintained voluntary muscle contraction in man
J. Stephens (1972)
10.1212/WNL.19.3.221
The histographic analysis of human muscle biopsies with regard to fiber types
M. Brooke (1969)
10.1006/exnr.2001.7753
Overexpression of GDNF Induces and Maintains Hyperinnervation of Muscle Fibers and Multiple End-Plate Formation
M. Zwick (2001)
10.1073/pnas.111152298
Changes in the prevalence of chronic disability in the United States black and nonblack population above age 65 from 1982 to 1999
K. Manton (2001)
10.1007/BF01181487
The effects of exercise training of different intensities on neuromuscular junction morphology
M. Deschenes (1993)
10.1001/JAMA.1990.03440220053029
High-intensity strength training in nonagenarians. Effects on skeletal muscle.
M. Fiatarone (1990)
10.1016/j.exger.2010.03.007
Remodeling of the neuromuscular junction precedes sarcopenia related alterations in myofibers
M. Deschenes (2010)
10.1590/S0042-96862002000300012
Aging, natural death, and the compression of morbidity. 1980.
J. Fries (2002)
10.1177/21.1.51
HINDLIMB MUSCLE FIBER POPULATIONS OF FIVE MAMMALS
M. Ariano (1973)
10.1152/ajpendo.1999.277.1.E118
Resistance exercise training increases mixed muscle protein synthesis rate in frail women and men ≥76 yr old.
K. Yarasheski (1999)
10.1523/JNEUROSCI.21-16-06136.2001
Glial Cell Line-Derived Neurotrophic Factor Administration in Postnatal Life Results in Motor Unit Enlargement and Continuous Synaptic Remodeling at the Neuromuscular Junction
C. Keller-Peck (2001)
10.1093/GERONA/61.1.72
Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort.
A. Newman (2006)
10.1016/0022-510X(77)90069-7
The numbers of limb motor neurons in the human lumbosacral cord throughout life
B. Tomlinson (1977)
10.1002/(SICI)1097-4598(199908)22:8<1022::AID-MUS3>3.0.CO;2-F
Age‐related changes in fastest and slowest conducting axons of thenar motor units
F. Wang (1999)



This paper is referenced by
10.1186/s13104-015-1644-4
Effects of exercise on neuromuscular junction components across age: systematic review of animal experimental studies
Walter Krause Neto (2015)
10.3390/ijms22010136
How to Build and to Protect the Neuromuscular Junction: The Role of the Glial Cell Line-Derived Neurotrophic Factor
Serena Stanga (2020)
10.15698/cst2018.02.123
Rejuvenation of the aged neuromuscular junction by exercise
Tabita Kreko-Pierce (2018)
10.26773/MJSSM.190906
The Effects of High-Intensity Interval Training on Skeletal Muscle Morphological Changes and Denervation Gene expression of Aged Rats
S. M. Tayebi (2019)
The Effect of High-Intensity Exercise Training on Gene Expression of Semaphorin 3A in Extensor Digitorum Longus Muscles of Aged C57bl/6 Mice
(2018)
10.1016/j.neuroscience.2016.01.044
Exercise modulates synaptic acetylcholinesterase at neuromuscular junctions
E. Blotnick (2016)
10.1016/j.neuroscience.2015.12.004
Effects of exercise training on neuromuscular junction morphology and pre- to post-synaptic coupling in young and aged rats
M. Deschenes (2016)
تاثیر یک دوره تمرین ورزشی با شدت بالا بر بیان ژن سمافورین 3A در عضله بازکننده طویل انگشتان پای موشهای پیر C57BL/6
(2019)
Implication des cellules gliales dans la modulation de l’activité synaptique à la jonction neuromusculaire sénescente
Ayman Moustaine (2019)
10.1016/j.molmet.2017.11.001
Neurturin is a PGC-1α1-controlled myokine that promotes motor neuron recruitment and neuromuscular junction formation
Richard Mills (2018)
10.1016/j.exger.2019.03.007
The effect of resistance exercise upon age-related systemic and local skeletal muscle inflammation
A. K. Ziegler (2019)
GDNF content and NMJ plasticity in slow and fast twitch myofibers follows recruitment in exercise
A. Gyorkos (2014)
Regulation of Glial Cell Line-Derived Neurotrophic Factor (GDNF) Production in Voluntary and Involuntary Muscle
John-Mary Vianney (2015)
10.1016/j.physbeh.2015.04.012
Comparing interval and continuous exercise training regimens on neurotrophic factors in rat brain
Mohammad Esmaiel Afzalpour (2015)
10.1016/B978-0-12-805094-1.00009-5
Biochemichal Mechanism Associated With Exercise-Induced Neuroprotection in Aging Brains and Related Neurological Diseases
M. Shanmugam (2017)
10.14336/AD.2015.0506
Mechanisms of Muscle Denervation in Aging: Insights from a Mouse Model of Amyotrophic Lateral Sclerosis.
K. Park (2015)
Effects of Creatine, Leucine, and Ethanol on Glial Cell Line-Derived Neurotrophic Factor in C2C12 Skeletal Muscle Cells
D. Waters (2016)
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