Skeletal Muscle Metabolism and Performance During Heavy ... · SKELETAL MUSCLE METABOLISM AND...
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SKELETAL MUSCLE METABOLISM
AND PERFORMANCE DURING HEAVY
MUSCULAR CONTRACTION IN THE
ISOLATED PERFUSED RAT HINDQUARTER
by
LAWRENCE L. SPRIET, M.Sc •
.A Thesis
Submitted to the School of Gr'aduate Studiesin Partial Fulfilment of the Requirements
for theoegreeDoctor of Philosophy
McMaster University
@JUly, 1984
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MUSCLE METABOLISM AND PERFORMANCE DURING
HEAVY CONTRACTION
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DOCTOR DF PHILOSOPHY (1984)(Medical Science)
MCMASTER UNIVERSITYHamilton, Ontario
TITLE:
AUTHOR:
Skeletal Muscle Metabolism and Perform~ce
During Heavy Muscular Contraction in the'Isolated Perfused Rat Hindquarter '
Lawrence L. Spriet, B.Sc. (Waterloo university)
M.Sc. (York"University)
SUPERVISOR: Dr. N.L. Jones
NUMBER OF"PAGES: x, 226
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ABSTRACT
~\
. ~
Direct assessments of the relative contribut ions of•
th~ major energy releasing pathways in human skeletal muscle
during heavy exercise
invasive measurements
are difficult to obtain dpe to the..-....required. With an isolated muscle
,preparation the muscles' environment is carefully controlled
and all metabolic measurements are directly obtained. For
this reason the isolated perfused rat hindquarter model,
previously used to study resting muscle metabolism, was
developed to examine the metabolism and performance
heavily contracting skeletal muscle.
of\
Energy calculations based upon measurements of 02
uptake (aerobic metabolism), lactate product ion (anaerobic
glycolysis) and CP hydrolysis (alactic anaerobiosis) were
made during 20 minutes of repetitive tetanic stimulation.
During the initial 5 minut~s of stimulation isometric tension
production was high but fatigued rapidly and anaerobic
involvement in energy production was large (30%), especially
in the fast-twitch glycolytic muscle fibers. Muscle
glycogenolysis provided the majority of substrate for both
anaerobic glycolysis and aerobic metabolism. During the
final 15 minutes of stimulation aerobic metabolism dominated
(90%) while 60% of peak tension was held, mainly by the
fast-twitch oxida'tiv~, glycolytic muscle fibers. Glycogen
utilization was minimal and intramuscular triacylglycerol•
became the dominant fuel for oxidat ive metaboli'sm,
;; ;
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contributing 62% of the energy produced.
Perfusions with acidotic· mediums (metabol ic and
respiratory) reduced muscle glycogenolys is . and lactate
accumulation ~ .. -35% during the initial 5 minutes of
stimulation. '-The decreased glycolytic flux reduced the
availability oL carbohydrate substrate for aerobic metabolism
and 02 uptake decreased. The-associated reduction in energy
release produced an increased rate of tens ion decay. Total
energy release and tension production were also reduced
during acidosis in the final 15 minutes of stimulation. The
decreased glycolyt ic flux appeared to be due· to an earlier
fall in muscle pH during acidosis and subsequent inhibition
of key regulatory enzymes such as phosphorylase and
phosphofructokinase. However an alternate hypothesis is that
acidosis exerted a direct negative effect on the•
excitation-contraction coupling mechanism, thereby reducing
the need for energy production •
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\ ACKNOWLEDGEMENTS
I am extremely grateful to my supervisor, Dr. Norman~
L. Jones and my committee members, Dr. George J.F.
Heigenhauser and Dr. C.J. Toews for their assistance and
guidance during this project. The early work with this
hindquarter model by Gus Matsos and Sandra J. Peters and
their helpful discussions and technical expertise as
co-workers in the laboratory are great fully acknowledged.
The completion of this wo-rk is a tribute to my wife
Anne, for her undaunt ing support, understand ipg and Cassistance throughout the project.
This research was supported by the Medical Research
Council of Canada.
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TABLE OJ!' CONTENTS
Section
) Title Page
Descriptive Note
Abstract
ACkno(~,edgements
Table 'of Contents ,List of Figures,
"List of Tables
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ii
iH
v
vi
viii
x
43444445474849505354
) 6061
(
1.1.11.21.31.4
1.,51.61. 6. 11. 6.21. 6.31. 6. 41. 6. 51. 6. 6
. 1. 71.8
1.9
2.
2.12.1.12.1. 22.1. 32.1.42.1. 52.22.32.42.52.6
HISTORICAL INTRODUCTION 1Introduction ' 1The Hill-Meyerhof Theory of Muscle Metabolism 3Phosphate Compounds in Muscle 4Additional Findings Contradicting the
Hill-Meyerhof Theory 7Summary 10Fuel Sources for Muscle Metabolism 11Early Research 11Circulating Free Fatty Acids 15Intramuscular Triacylglycerol' 19Circulat ing Glucose, 22Intramuscular Glycogen 25The Interaction of Fat and Carbohydrate
Fuels in Muscle 27 'Anaerobic Metabolism 30The Effects of Acidosis on Muscle Metabolism
and Performance 35Purpose of the Thesis 40
DEVELOPMENT OF THE ISOLATED PERFUSED RATHINPQUARTER MODEL
Early per-fusionsPerfusion ProtocolHindquarter PerformanceOxygen DeliveryNon-Recirculating Perfusion SystemCollection of Fresh Red Blood CellsPerfusion Related Alterations
• Surgical AlterationsHindquarter Stimulation and Performan~Measurement 'Related Improvement sSummary
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c
' .. "'-- ..
•
Section
3 •
3.13.23.2.13.2.23.2.33 .2.43.2.53.2.63.2.73.2.83.2.93.33.4
4 .
4.14.24.34.4
5.5.15.25.3
A1-2.
a.b.c.d.e.
3.
BC
'DEF
.J
MUSCLE METABOLISM AND PERFORMANCE DORINGHEAVY EXERCISE IN THE PERFOSED RATHINDQUARTER
IntroductionMethodsAnimalsPerfusion MediumHindquarter Surgical PreparationPerfusion ApparatusStimulation of Perfused Skeletal MuscleSampling of Perfused Skeletal MusclePerfusion ProtocolAnalytical MethodsStatisticsResul tsDiscussion
EFFECTS OF ACIDOSIS ON RAT MUSCLE METABOLISMAllD PERFORMAllCE DURING HEAVY EXERC ISE
IntroductionMethodsResul tsDiscussion
GENERAL SUMMARYIntroductionObservations and Conclusions of the ThesisQuestions for Future Repearch
APPENDICES.CalculationsOxygen Uptake CalculationsEnergy Release CalculationsTotal Oxygen UtilizedLactate ProducedCreatine Phosphate UtilizedGlycogen utilization and Glucose uptakeSummaryCa~culation of Contribution of Energy· .. Subst~ates for Aerobic Metabolism During
the Final 15 min of StimulationCharacterization Study Mean MU$cle DataCharacterization Study Individual DataAcidosis Study Mean Muscle Metabolite' DataAcidosis Study Individual Data'Rat Hindquarter Dye Perfusion Data
~
6262636363646667697072767689
,.
102102103106122
lJ7137137141
145145145145145146148148149
149151156178186210
BIBLIOGRAPHY
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212-226
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I
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'0
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LIST Ol!' l!'IGURES
•
, l!'igure
1 Contribution of major energy releasing pathwaysto tota energy supply ~ith exercise (Keulet al, 1 i!) 12
2 Tension prod tion by the rat hindquarte~'undervarying cond' ions and in previousinvestigations 46
c,
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4
5
6
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,8
9
10
11
12
13
14
15
16
17
Rat hindquarter stabilization and tendonattachment
Rat hindquarter perf~sion apparatus
Perfusion protocol
Tensi9n generation by the ,hindquarter
Hindquarter oxygen uptake and perfusionpressure
Hindquarter lactate release and glucoseuptake
Hindquarter free fatty acid and glycerolrelease
Muscle glycogen and lactate concentrationsfollowing the perfusions
,Muscle CP and ATP concentrations followingthe perfusions
Muscle triacylglycerol con~ent before andafter 20 min of stimulation
Perfusion pressure during acidosis
Tension generation during acidosis
Oxygen uptake during acidosis
Lactate release during acidosis
GlucQse uptake during acidosis
viii
•
56
68
71
79
81,
82
84,
86
87
90
108
109
111
112
113'
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~..Figure .~~
...18 Muscle glycogen utilization and lactate
accumulation following 5 min ofst~ulation during acidosis . 116
•
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19
20
21
22
23
Muscle CP and ATP concentra~ons following5 min of stimulation dqri~ acidosis
Muscle glycogen utilization and lactateaccumulation following 20 min of 'stimulation during acidosis
Muscle CP and ATP concentrations following20 min of.stimulation during acidosis
Relative lactate release from working muscleduring 5 min of stlmulation during acidosisand control conditions
Lactate release normalized for tensionproduction during acidosis and control
.. conditions
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ix
'.
117
120
121
134
135
.. .
.J
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r
Table
1
2
3
4
5
6
LIST OF TABLES
~pmance variables at selected workloads
Effects'of fasting on muscle glycogen yont~nt
Characteristics of the perfusion mediums,Electroiyte ,data at rest and during
stimulationI
Energy released'during 20 min o~ stimulation
sources\and fa'tes of gll,lc~seduring.20minof sttmulation "....
p~ge
58
59
77
78
95
9,6
Energy released during acidotic stimulation
Contribution Of energy substrates to aerobicmetabolism ?,uring the fin'al 15.m'in ofstimulatio~
• Characterist~c~ ,of t~' ac.idos,isperfus~.nl.med,iums '\
•
7
8
9
10
\
Electrolyte data during: acidosis , .
99
105
107. V-
126'
.;(52-155.'
11
12
13-16
. .Sources and fates of g'lucose during acidotic ..
stimulation
, Muscle lacirate, lactate released from muscle. and total l'actate produced during, acidotic
stimulation '
Characterization study mean musclemetabolite data
•127
c
133 ,
17 37
38-44
45-67
6,8
Characterization study individual data
Acidosis study mean muscle metaboiitedata
Acidosis study individual data
Rat hindquarter dye perfusion data
••
157-177
179-185
187-210
211 \
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1.
1.1
HISTORICAL INTRODUCTION
Introduct ion
Man'is capa.l'le of performing large amounts of
external work through the conversion of chemical to
~-' mechanical energy in the skeletal muscles' of the body. The
required chemic~l energy is ultimately provided through the
ingestion of foodstuffs and their subsequent uptake and
metabolism by the muscles. Our ing per iods of phys ical
exertion the metabolism of the'entire body is
the me~abolism of the working muscles. ~
dominated by
.The study of muscle metabolism originated soon after
the discovery and isolation of oxygen (0 2 ) in the late
eighteenth century and the subsequent development of methods...,..""..-\
to examine the amQunt of substances taken up'and released by
living organisms (Asmussen, 1971).. Over the course of the
, .
next century work centeJ:ed on. attempts to determine the
nature ~f the foodstuffs responsibl~ for the energy utilized•
at rest and during physical work. 'Studies by Pettenkofer and
"Voit (1862) examining the urinary nitrogen (N 2 ) output
stlggested that protein was not a major source of fuel dur ing
work (Asmussen, 1971)."
Zuntz and colle~gues (1894) believed
that work was performed through the comb\l.st ion of both fat
a~d carbohydrate fuels as at rest, while Chauveau and
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\
2•
coworkers (1896) maint~that carbohydrate -was the sole
energy source for muscular contraction (Asmussen, 1971).
,Both groups arrived at their conclusions through measurements
of the respiratory exchange ratio (R), defined as the ratio
of carbon dioxide (C0 2 ) produced over 02 utilized by the body
as measured /f~dir'ectly from the inspired and expired.. air.
/Direct ~asurements of the CO 2 produced and 02 utilized
_/
dur irlg complete combust ion of carbohydrate and fat produced
rat\'OS/f 1.0 and 0.7, respectively... When direct
measuremfnts are made the ratio is referred to as t~e
respi-r£~ory quotient (RQ). With the beginning of the/,/' \
/~entieth centu~~fhis uncertainty persis\ed and would not be
\ resOlv~d for another 40 years.
~ At the same time a new and more direct line .of
research in muscle metabolism began wlth the classic study of
•
F],etcher and Hopkins (1907). using improved techniques for
extracting
demonstrated
resting
ctic acid from amphibian muscle they
~ existence of lactic acid in surviving'
and the product ion of lact ic acid by work'ing
muscle. An insufficient 02 supply to resting or working
mutcle increased lactic acid production while the
administration of '02 caused the lactic acid to disappear.
Muscle fat ig,ue was always greatest in t:'he presence of lact ic
acid and least in its absence. Fletcher and Hopkins (1907)
also maintained that carbohydrate, in the form of glycogen
was the precurser ~c acid formation.
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3
In the following 20 years work in l'luscle physiology·
and metab"olism was dominated by two individuals; Otto
Meyerhof working in Germany and A. V. Hill in England, who
shared the 1922 Nobel prize for physiology for their work
with frog muscles. Meyerhof integrated his chemical findings
with the thermodynamic and mechanical findings of the time to
formulate an hypothesis explaining the physiology of muscular
contraction (Sacks and Sacks, 1933). Hill combined his
myothermic find.ing·s with those of the biochemists· and
published his explanation of muscular exertion (Hill and
Lupton, 1923; Hill et al, 1924). The Hill-Meyerhof theory
seemed to explain most of the mechanical and metabolic
changes produced by muscular contraction.
1.2 The Hltl-MeyerhOf Theory of Muscle Metabolism
The primary event in a contracting muscle was held to
be the anaerobic breakdown of glycogen to lact ic ac id wh ich
evoked the muscle's mechanical response. During exercise
CO 2 was driven off, the heat release was proportional to the
lactic acid product ion and the hydrogen ion (H+) content of
the muscle increased. This acidification was mentioned as
the pass ible mechan ism for the act i vat ion of the cont ract ile
proteins. During recovery in the presence· of 02'
approximately one-fifth of the produced lactic acid was
ox id i zed, to prov ide the ene-rgy for the reconvers ion of the
remaining lactic acid to glycogen. During recovery from
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------- ..~---_.
4,
exercise the 02 uptake did not immediately return to resting
levels. This additional 02 uptake was referred to a~ the 02
debt since it was used to remove the lact ic ac id wh ich had
accumulated early in the exercise before the circulation
responded to the work load by increasing 02 delivery. In
prolonged exercise a steady state was attained when available
lactic acid production matched the aerobic removal, resulting
in a constant blood lactic acid concentratiort.
Although Hill and Lupton (1923) were aware that 02
was ultimately used in the combustion of foodstuffs to supply
the energy required for body functions, they felt it was not
used in the primary breakdown processes, only in the recovery. . .
processes. Additionally! at that time most researchers
believed carbohydrate was the sole precursor for energy
production and lactic' acid was a central intermediary in
metabolism with points of contact with carbohydrate, fat and
protein metabolism (Jervell, 1923).
1.3 Phosphate Compounds in Muscle
While the Hill-Meyerhof theory dominated the thinking
concerning skeletal muscle physiology for a number of years,
~vidence was accumulating to suggest the theory was incorrect
or too simpl ist ic. Two groups of investigators working
independently published results demonstrating the existence
of a phosphate co~pound as a substance in muscle. Eggle':..9"
and Eggleton (1927) in London improved l:he existing methods
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