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Ultrastructure Study on the T System and the Subcellular Localization of Calcium in Frog Skeletal Muscle

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Ultrastructure Study on the T System and the Subcellular Localization of Calcium in Frog Skeletal Muscle Loyola University Chicago Loyola eCommons Dissertations Theses and Dissertations 1971 Ultrastructure Study on the T System and the Subcellular Localization of Calcium in Frog Skeletal Muscle Lawrence P. McCallister Loyola University Chicago Follow this and additional works at: https://ecommons.luc.edu/luc_diss Part of the Medicine and Health Sciences Commons Recommended Citation McCallister, Lawrence P., "Ultrastructure Study on the T System and the Subcellular Localization of Calcium in Frog Skeletal Muscle" (1971). Dissertations. 1148. https://ecommons.luc.edu/luc_diss/1148 This Dissertation is brought to you for free and open access by the Theses and Dissertations at Loyola eCommons. It has been accepted for inclusion in Dissertations by an authorized administrator of Loyola eCommons. For more information, please contact [email protected]. This work is licensed under a Creative Commons Attribution-Noncommercial-No Derivative Works 3.0 License. Copyright © 1971 Lawrence P. McCallister ULTRASTRUCTURE STUDY ON THS T SYSTEM AND TH3 SUi3CELLUIAR LOCP.LIZA TION OF CALCIUM IN FROG SKELE.?AL MUSCLE by Lawrence P. McCallister A Dissertation Submitted to the Fac~lty of the Graduate School of Loyola Unive<rsity :tn Partial. Fulfilment of th~ Requirements f o~ the Degree of Doctor of Philosophy Juns. 1971 BIOORAPHY Lawrence P. McCallister was born on March 27, 19l~J, :ln Chicago, Illinois. He was graduated from Lake View High School in Chicago, in Fetruary, 1961; and continued his studies at Wright Jr. College, Chica.go, Ill., where he received the degree of Associa to of Ar.ts in Biolog~r in 1964·. He completed his undergraduate studies at the University f':f.' Illinois, Champtdgn, Urbana, and received the degree of Bachelor of Science in Zoology in I<\:ib:ru­ ary, 1966. In September of 1966 he began zraduate studies i.'1 the Dapartn:Gnt cf' Anatomy, l.oyola University, Str1.tch School of Hedicina, Chicago, Illinois ... He was awarded a National Defense Education Act Fellowship in the Dep:1rt­ ment of Anatomy from 1967 to 1970; and he was admitted as an associate men:ber in the Society of Sigma Xi in }fa.y, 1969. During the writing of his dissertation he w.;.s a.wn:r·ded a o. s. Public Health Fellowship :..n the Departments of Hodicine and Cardiology at the University of Chicago, Chicago, Illinois. ii ----------------------------------.....·------- ACKNOWLED:J 2:1-ENTS The author will always be indebted to his advisor, Dr. Robert F.adek, for unfailing support, encouragement, and scientific criticism throughout the preparation of this manuscript. Special thanks are also due to the Department of Pharmacology of Loyola University, and Dr. L. c. Blaber, who provided pharmacology equip-~ ment. A major portion of this work would not have been possible '!lrithout. the cooperation of Engis Equipment Co., Morton Grove, Illinois, which supplied the Cambridge Stereoscan used in the experiments. iii TABLE OF co~~T Ei~T s Page I. INTRODUCTION • • • • • • • • • • • • • • • • . • • • 1 A. PAin' I: THZ T SYSTEM • • • • • • • • • • • • • • • • 1 B. PART II: THE SU.DCELLULAR LOCALIZATIOJ.'l OF CALCIUM • • 3 II. REVI.d;'d OF THE P.EIATED LITERATURE • • • . • • • • • • • 6 A. THEORIES OF CONTRACTION. • • . • • • • • • • . 6 1. THE ROLE 01? IACTIC ACID AND ORGAiUC PHOSPHATES • 6 2. STRUCTURAL PROTZINS FOUND Di MUSCLE. • • • • • • 7 3. SLIDD~G FILA.Mi.i;NT TH.:!:ORY OF co.~TRl\.CTio:~ • • • • • 8 B. CALCIUN ION r:~ cmTRACTIOl'l • • • • • • • • . 8 c. EXCITATIO~I-CONTrtA.CTIOri COUPLING. • • • • • . 10 D. A?FR.OACHES TO TliE STUDY OF MUSCLE CALCIUH. 11 1. EARLY WORK • • • • • • • • • • • • • • • • • • • 11 2. RADIOCALCIUH EFFJ,UX. • • • • • • • • • • J2 J. CALCIUM i:HNDrnG DYES • • • • • • • • • • • • l'.3 #. FP...4.GME:?~TED SAHCOP:I..t-<SlHC REl'ICULU,;:·i. • • • • • • • lJ 5. AUTORADICDRAPiiIC STUDI&S • • • • • • • • • • • • 14 6. OXALATE PR3CIPITATIO.:f. • • • • • • • • • • • 15 7. LOC:\LIZ~_TION a:;· CALCIUM BY PO'l'ASSIUM PYROANTirl~ONAT E • • • • • • • • • • • • • • • • • 15 III. MAT ER.IAI.S AND M.:!:rHODS . 18 A. TIE MUSCLE •• • • Cl • • • • • • . 18 B. E,{?EBDrEi~TS Oi'l' T:E T SYSTEM: . • • • • • • • • • • 18 l. FIY.ATIO:~ AND DS:tYDT&"..TIO~~ • . 18 2. THA3SNI.$SIW ELEc1·:rw:i HICROSCOPY • • • • • • • • 19 J. SCA2{Hr~J ~LECfROi~ ViICROSCOPY • • • • • • • • • • 19 C. THE PHYSIOLOGY OF THZ C1iF'FEINE-INDUCED CWTP.ACTURE • 19 1. MUSCLE; PR~?AFWI'IC:I AND RECORDING APPARA.TUS • • • 20 2. SOl.UTIC.JS • • • • • • • • • • • • • • _. • . 20 J. PRCCLDURS . 21 iv Page D. SUBCELLUIAR LOCALIZATION OF CALCIUM • • • • • • • • 21 1. MUSCL~ EXPOSED TO l 0 -RINGER 1S SOLUTION, Cl1LCIUM F.RIB RING.i:R' S SOLU'l.'IO!~, OR RL'IJGE:cl' S SOLUTION CONTAINING CALCilr.·1 CHEIJ.Til'~G AG.GNTS • • • • 22 2. MUSCLES IN WHICH THE CAFFEINE-INDUCED CONTRti.CTURE WAS ARHS.::il' ED • • • • • • • • • • • • 22 IV. RESULTS: THE T SYST Ei·1 • • • • • • . 23 A. TRANSMISSION ELECTRON MICROSCOPY • • • • • • • • • • 2J 1. GEJ.'l.B;RAL MORPHOLOGY • • • • • • • • • • • • • • • 23 2. TJE SARCOPUcSHIC R3'.l'ICULUM • • • • • • • 24 J. ASSOCIATION OF THE T SYSTEM WITH THE F:GER SU~1.FACE • • • • • • • • • • • • • • • • • • • • 25 4. THE ZNTRA.NCE OF IANTH.fl..NUM INTO THE T SYST3M • • 26 B. SCANNING ELECTRON ¥.ICROSCOPY •• • • . 27 1. GENEP.AL MORPHOLCGY • • • • • • • • • • • • • • • 27 2. THE M1JSCLE SURI•'ACB OF EXT.RAFUSAL FIBERS • • • • 28 IV. RESULTS: THE SU.t3CELLUIAR LOCAJ.J:ZATION Oli' CALCIUH PY:KOA.NTDfONATE • • • • • • • • • • . A. PHYSIOlffiY OF THE CAFF~~JNE:-INDUCED CC'NTRA.CTURE IN CALCitJN-FRIB RINGER 1 S SQ1,ljI'IOl'~ • • • • • • • • • • • 30 B. ELECT RON MICROSCOPY OF I~USCIE.3 FIXED IN Os04 WTrHOUT POTASSIUN PYiWA.NTIEO.N'ATE • • • • • • • • 32 c. MUSCLES FIX3D Ii'l 1% Os04 CWTAIIUNG A 2;.o co:1Ci1NTHA- Tim~ OF POl'ASSIUH PYROANTIHWATE • • • • • • • • • • J2 D. MUSCLES £XPOSED TO CALCIUd-FiGB RINGER'S SOLUTIO~, AND RINGZR Is SOJ_,UTION co2nAINING CALCIUM CIBLADG AG E~~fr S • • • • • • • • • • • • • • • • • • • • • • • 34 E. NUSCL&S Ii~ ~·iHICH THE CAFFEINi-ItWGCED CONTR~CTURE WAS ARREST E:D IN CALCIUli-FRIB R.Il'lG ~P. 1 S SOLUTION • • • J4 F. MUSCLES IN WHICH THE CA!i'FEINE-TIWUC:SD co~~TrlAC:'l'URE WA.S A.:1RES'l'.2D Ill CALCIU~·l-fR.2:~ ?..Il-JGEP. 1S SOLUTION 1 I''LJr. I/. ,-,"'~A. A:"D '1 r;Y"_TA CONr· a 1\l ·\ u 5 m. i r... 11 r.. ...11.. ...., 5 tr.J."' .u..;i • .. • • • .. • • • 35 v p Page v. DISCUSSIO~~ • • • • • • . • • . A. GENER.\L MOR?HOLOGY . • • • • • • . :a. THE T SYSTEA ••• . • • • 1. ASSOCIATION WITd TH~ FIBER SURFACE • • • • • • • J6 2. FACTORS INFLUE;;:~CL'iG THE CO'.\TINUITY OF THE T SYST2l•1 WITH 1'1E EXTRAC2LLUL'\.R SPACE IN CON­ VENTIONAL ELECTrW~~ NICROORAPP.S • • • • • • • • • 38 c. THE JUNCTro:~ 3EI'iJEEi~ TIE T SYSTEM AND Tffi: SAR.CO- PLASMIC HErICULUl•I • • • • • • • • • • • • • • • • • 40 D. SPI~DLE-LI.t<3 STftUCIUP3S . 42 E. THE LOCALIZA'l'IOi1 OF CAlCIUM BY POTASSIUM PYROANTL\10- l~TE • • • • • • • • • • • • • . 43 1. D~·rRACZLLUL\R PRECIPITATE . 4J 2. EXTRACELLU.I.AR PR3:CIPITAT Z • • • • • • • • • • • 46 J. PRECIPITATE I~~ HUSCL2S t:XPOSED TO CALCIU11I-FREE SOLUTIOi~S Aim SOLUTIO~~s CWTAI2UNG CALCIUM C:iIElA.TING AG&.~TS • • • • • • • • • • •••••• 47 4. PRECIPITATE IN ~cHJSCLES IN '.'i'HICH THE CAFFEINE­ INDUC!i:D CON'l'&\CTUitE WAS ARREST3D •••••••• 48 VI. SU:•J·1ARY' Ai.rn CQ;:JCLUSIO:~s . 53 l3IrlLIOGR.\Pifi • • • • . • • • • • • . 56 PLATES AND FIGU;tES • . • • • • • • • • • • 66 vi • LIST OF TABLES Page TABLE I. EXPERil1ENT S ON THE T SYST El1 • • • • • • • • • • • • 19a TABLE II._,,,~PEK[l1E.NTS ON THE SlJBCELLUIAR LOCALIZATION OF W\.il;li.h·1 • • • • • • • • • • • • • • • • • • . • • 22a vii • r, LOSS;\l~Y OF TER~IS ADP adenosine dirhosphate ATP a<lenosine triphosnhate EDTJ\ ethylencdiaminc tetraacetic acid EGTA cthyleneglycol bis tetraacctic acid Os0 osmium tetroxide 4 viii • 1 I. IN'TRODUCTION This study had two goals; (~) to establish whether a direct continuity exists between the T system and the surface membrane in frog skeletal muscle; and (B) to observe and study the localization of calcium in skeletal muscle cells using potassium pryoanti.~onate as a reactant. .. .:l. • PART I: T'I:z T .SY7!'Z·: Transmission electron microscopy has demonstrated the continuity between th'3 membrc.nes of the T systero and the sarcolemma in a number of striated muscle cells (Franzini-Armstrong and Porter, 1961.~; Jasper, 1967; Rayns et al., 1968; Smith, 1966). A not<:d. exception, ho·:raver, is adult frog skeletA.l ::rnu:;cle in which the T system fo:r.ms complex terminations at the f.i'.:>ar surface, obscuring any direct co~tinui..ty between the wall of the T tubules and the sa.rcolemma (Peachey, 19~5). On the other hand, several stu::lies have demonstrated the free diffusion of substances between the e:Ktracellular space and the central elements of the triads in at>1phibian rn.wcle. For example, 2ndo ( 19:S!t-) traced the diffusj.0:1 of a fluorescent dye, Lisa.mine Rohda:irl.ne B 200, in isolated fibers of the semitendi- nosus muscle of the frog. In his experiments the dye was consistently otserved in the cente1• of the I band, without appea.rinz in the major portion of t".-le .r. l i. ioer. Using aul:.o~adio:-:,raphy, Hill (1964) localized tho uptake of trit:i.at.ed sertt:n a.lburnin to the central compo::ient of the triads in amphibian muscle; and both Huxley (19&'+) and Peisc~ (199~) '!:ave demo:1strated the uptake of ferritin :i.n T tubnles of frog sartc::--ius r:iuscle.:;. All indicatin6 a possibility of direct continu.i.ty between the T tuhulBs aZ'ld the muscle cell sm.•face. p • 2 Despite this indirect evidence, only two investigators, L.D. Peachey (1965) and R.I. Eirks (1965), have published transmisston electron micro­ gra.phs of frog skeleta.l muscle showine terminations of T tubules which could be interp1·eted as having a possible continuity with the extracellular space. However, due to the complicated termination of the T tubules, and their infre­ quent occurrence along the cell membrane, such evidence has been subsequently regarded as inconclusive (Bianchi, 1968; Eisenberg and E:tsenberg, 1968; Smith, 1966; Fra.nzini-Armsb~onc, 1970).
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