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NASA TECHNICAL MEMQRANDUM NASA TM-76283

ULTRASTRUCTURAL STUDIES OF THE MITOCHONDRIAE I N THE

STRIATED MUSCLES OF BIRDS WITH REGARD TO EXPERIMENTAL

HYPOKINE,CIS

M , Belak, J. Kocisova and K , Bod1a

T r a n s l a t i o n of "Studium d e r U l t r a s t r u k t u r von Mitochondrien i n d e r q u e r g e s t r e i f t e n Muskulatur d e r W g e l u n t e r Berucks ich t igung d z r experiment- e l l he rvor~gerufenen Hypokineseu , Archiv f u e r Exper imente l l e Ve te r inae rmediz in ( L e i p z i g ) , Vol. 31, Ju ly 4 , 1977, pp. 537-546.

( N A S A-TM-76283) DLTRASTHUCTURAL STUDXES OF N81- 1 3 b l 6 T h E MXTOCHUNDRIAE I N TBE STRXATED MUSCLES OF B I R D S GJITH HEGAHD TO EXPBBIM.ENTAL HP'POKLNBSTS ( N a t i o n a l Aeronautics and S p a c e U n c l a s A.c"ministration) ' 14 p HC AC)2/HF A')? CSCL O 6 C G3151 29455

NATIONAL AERONAUTICS AND SPACE ADMINISTRATION WASHINGTON DC 20546 JULY 1980

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Ulta-nstxtueLura% S tud ie s of the Mitochondria in the Y t r l a t o d Muscles sf Birds w i t h Regard t o Esycr-

ittlcntnl l iypaleisesis

Thc ~ t r i a t * o ~ i ttzusclcs s f bird8 had been n subJec t of re- c t ~ l ~ t e l e c k r o t ~ 11~j1~34t~~s~lr~pt ilzvesf;if2;~_qt;ita118. XII pak7ti~u3m~'tl8 Lhe

el~?llzcllta o r ~nyo? ~ b r i l s 41awc brdu s LuJi ed, such n8, f o r example, t.hp (11 i'fr>~-cnttes i n t h~ orgtt:risation of' t h e T-system between t h e S'l*o!~t nmi ,lbtai\lc nlusc~3,t~s o f tAe b:lcka or' c?hlclcs (Pnkye, b g e g ) , ant1 1.11~ breas t . 111u;i~ hc's oi' poult x3y f btrndul, 191 J 1 , lEllclda (137,!) w t \ t t i t t % : i \lsc\ sftrv.\t:t3ulbt? o f tn t? t ;~pe t t - , \2k a ~ u s c l o s 3.11 gi@;eerrs, Adall, jl:l';.3) ~ t ~ u ~ l i t l s 't,iltl st;twt?t u ~ e of tho Ib;~tstnfusnl musel.c, :uld fIt\p;nr~t.y , G-2, ( 1'1'; 3 ) ::2.ut3 L C S ~ t,hc:! ~~n~t*c~rl l t \ r~c\s 3.11 bix*cis

rind p:tt*':k>\:~ -1 11 Z * ~ C L X ~ B I L W ~ f a , %tlle~l:a :1)1t1 J i ~ * ~ ~ i t l ~ ) o v t t i l g f 5 ) , ntrd J t rmmuuav:~, r t t~ci Ec l c r l l : ~ ( Il:l'/ 3 ) 1 n ~ t ~ s l ~ S ~ c . t t c d t ~ e u t r u p h i l i~it,t'r-nc:t.!oll:r :rl,rl r t l ~ ~ : ; ~ ~ Z t \ irit;t\psalty i r l t,llt: 111tisclrs ilf ohlt:ks.

Tine : - t m ~ j \ ~ ~ l t ol' m i t ot*lxolrtIl*i:r d f f ? f t ' ~ s :trtlc?.'rl~g t tl~e t1.i.f ~ ' P X V I ~ C

t>,ypes (5 f muPc l t k s . Yhc ~ v l t t t i o n ~3 f 1114, t o ~ h o n ~ i t y i n nuti m y t l f l b ~ i l s

t t j c:teli ot.ht>rb cwI+nJ,t1:1 -Lrls; 'k\r*111nt;ion :.tbtlut 1310 ~ ' ~ ~ t q \ t t " l t ? y ~51' II~USCLC c ~ ~ n l ; ~ * t t ~ t 1 tmii :it111 I lltt i 1' : : L I ~ ~ ~ ~ G L I I . Thc tt l t>~*t\ ~nyt ,ec~fl~~t~ttr l ia 111 t h e

nlusa3.c . I ' l b t ~ ~ * a , ~ A L Q nlok7t? f ~+~q\i t \ t lL 1:1m c ,?on t ~ o c t 1 0118 . \rlllc\x~ moa*t? t n y k i , r r ' d , i ~ ~ Y i i Js nr*t,? prbt\stwi. , t,11t? ttnlsncity i r l c v a ~ s t > s , but; tehe Fre- clut\lley i 5 ; /+c~l i i~od. S'tl gtttlr?~?n3- , ~ n y t utallolldria. BPC I ? u H c c ~ V ~ T " ~ Z ; Q ~

p t ? ~ ~ i l r \ ~ u l t ~ n t ~ c ill ~ k r * i : \ t ~ i x d ~ I I \ ~ s c ~ c ? ; , but t;llcy :.txte RLSO faulld i n t.t?ll mc~tllbt~ntlt\s nnc.2 m,vot'il~x*,t.fa, Tho lit;t;ti\ ovnid tnyt;ocIat~ndx*in tltv t1s:iunl ly t'uilk~tl I n p:liLrs , i2nd are located s yr t l~ t~e t i~* l i ?~ tZI~r new3 1:he ::-l.1 nes In t h t ~ l~yc; tb o f t he I-bnnds (I\IcNnugl:l~l;ar~, 1974 ) . Nc~sI. of' t,lre I:~r+gt\x*, S'ilait!ek?teus mi1 .~a l r snJ1+l~ RPC %iLunt4rd t\rl bhout; aw;k:npti I.0 Z;llu2 1% svol,?t;:l~?lz t o t:hc d i i ' f t ? r ' t a n t snxicomcro

u n i t s .

I n view o f t h e f a c t ti'lnt tila mitsatlt~ond~ia of' the slcalctal ~nust.,lcs, t f i ~ ~ t i g l i % h e i r ~t~embraneaus %tt;ruc@ure, Parltl an tatrerlye&ic r~cautnulat ion (?enter nrrd, in t h a t they a r e tr$ghSy s e n s i t i v e t a t h e inf ' luenee of' changed physiohag:r,ical states, i t ; becalztc the 8031 df thLs st,ud;y to I t lves tLgate t h e u l t r a s t ~ ~ u c . ~ u u , s o f 611eae orgratlcl&os i n t o t o i n .the a r s a sf t h e t h i g h akad b r e t ~ s t inuscles tviL11 ~ e g a v d t o experimet?tal. I'lypokix~esis,

Me t i ~ a d s and M a t e r i a l s

lr[7-il,zy o l d ..idnpancse qua i l s werta tkstld f u r the c l ~ c t r a l ~ I I I ~ C P O -

kjaopc s t u d y . A t t h e np;o o f 71 days , t h e y were p l aced i n cages ~ L ? V SIX 1 1 0 ~ ~ s bf' each 1-n the f ol lotving 100 d a y s , i n such a way that a l l n~uvc'alolrt was i l l l l lb i t cd . 177 q u a i l s were lqalsed nortnal- Ly nnil were u s ~ d fax1 t i :0111;~~~1 p u ~ ~ p 0 8 e s . The' necpssnl*y excisions w u ~ s talcell frurr~ %11t? M e p ~ ? ~ t ~ r a l d . s t . t ~ e l ~ ~ ~ i t ! u s a119 cfrolt~ t.he hi. i l i a t i - bidkh ~i38 t~1 \ l01* . Q ~ C S I I ~ U S C ? ~ ~ ? ~tl*i&\ WrtS ~0s~ltC.d fol* L' @C?l'iod of cwn t ~ a u ~ s i n :I, 3.5% fixill&: ssolutitlxl (aftex. S a b n t l n i , 99b3). Es- c i s i o n s mcnaul?illg 1 x 1 ma I n s l z u ivcue subseigurk1t2.y talcen Prom tlresc s t ~ i p s . They 'ruere washed i n a 0.1 sace>dyl,zto bufft'cr,

Pixed i n (I kX BsDq ~ ~ L u L l o l l , I I ~ 1 1 y d ~ a b e J i l l a graded series ol' t ' tbai lols , ixud f i n a l l y c~inbaddcti i l l Durcupan. t3ltrn-tq2li1r sec t ions wcrp proSuc.ed w i t h ttlc t l l t r o t s m LKB; Chest were t:olar*ed w i t h a c!ornbitlat ion AP urnny l ncc t a t s (Writ son, 1958) s ~ d Icad c i b r ~ t ' e 1 5 3 0 (He;vllelds, lgb3), and tllen sxatilltlocl. under n. Tes ln 513 e l e c t r o n m i c17sasilope : ~ n d p h u % o g r a p l ~ ~ d .

'nlc. ~ n y ~ \ P i b r i i s af the stx*iaeed breast and tl'lbgk r~ruscLLes of 1:lu.l e o n t r o l animals fo~n~ccl rspest;Sng uniform sarkc~mcl*s, vhf ch are dcf inod as ~segmonta bcCwi+cn t h e t ~ v o I't'sSlawl ng 2-lines, and wllich

c o n t a i n t h e A-bands and h a l f o f t h e c o n n e c t e d I -bands . The H-

zonc w i t h t h e nar row M-line r u n s t h r o u g h t h e midd le o f t h e A-band

(b'lk:ure 1) . Two t y p e s o f myof i l amen t s were d i s t l n ~ u l s h a b l c : one

compr i sed t h i n n c t i n f i l a m e n t s r u n n i n g f rom t h e Z - l i n e s t o t h e

I -bands ; t h e s econd t y p e c o n s i s t e d o f t h i c k e r myosin f i l a m e n t s

whicti r z n i n t o t h e A-bands. The i n t e r f i b r i l a r s p a c e c o n t a i n e d

t u b u l a r and vesicular s t , r u c t u r , e s .

I.'lt:ur*e 1. Lonh;i:.udlnal s e c t i o n t h r o u g h t h e t h i c h musc le of' a q u , r ~ i l from t h c c o n t r o l g roup . The M-zone (H) w l t h 3 nar row M-line r u n s t h r o u g h t h e midti le o f t h e A- band. The f i l a m e n t o u s m i t o c h o n d r i a m:iintain a well- p re se rv t>d and c l e a r l y d e f i n e d i n t e r m 1 1 structure. b:8;.;5ific?:lt,ion: 28500 x .

Two s h a p c s o f n i t , o c h o n d r i n a p p e a r e d I n out* r e su1 t . s . Those

in t.hc b r e a s t musc1t.s wcrc main ly f i l a m e n t o u s , r . ' h i l ~ > t h o s e o f

t h e thi!:tl n u s c l c s r n n p d from s n n l l and round t c ) o v o i d s h a p e s .

T h e i r l r l n c r s t , r * u c t u ~ * e c o n t a i n e d a l a r g e number ctf c l o s e l y a l i g n e d

c r i s t a e , whlch rat: v e r t i c a l t o t h e l o n e c r a x i s o f t h e mitochon-

d r i a .

I n c o n p a r i s o n t o t h e ~ > o n t r o l 1:roup. t h e mi:ochondria o f t h e

b r -cas t rriuscles of hypoklnc t i z q u a i l s showed d i s : ; i nz t c h n n ~ e s .

Bo t." ,ill and larger enclosed vacuoles and a fading matrix were

found in some of the filamentous mitochondria, which were often

perinucleated (Figure 2, 3). Sometimes these formations filledthe entire organelle. The larger vacuoles are probably generated

through the fusion of several small and lighter formations.

Destruction and even disappearance of the mitochondrlal crist-

ae occur-red at the location of the vacuole opening. Finally,

a total decay of the mitochondria occurred as a consequence of

there alterations (Figure 5).

.^ `X

F1 gure 2. Longitudinal section through the breast muscle of /539hypokinetic quails. The filamentous mitochondria(Mi) show a clearly defined internal structure whichIs only occasionally disturbed by little vacuoles.a ,ni fi,cation: ,1^b5^x.

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At

Figure 3. Longitudinal section through the breast muscle ofhypokinetic quails. The large mitochondria (Mi),

4

which are squeezed in between the myofibrils are largerthan the sarcomer•es ar.d do not suffer damage in theirouter membranes. These are large vacuoles in the matrixand the cristae show occasional changes. The Z-line (Z)is slightly shifted. ,p a ir.: 19650x.

Fig,:re 4. The Zristae of the filament and ovoid mitochondria /540

lose their continuity. `the mitochondria (MI) grow in size andare filled by large vacuoles (V), which probably generate fromthe fusion of smaller vacuoles. Among the mitochondria and my-filaments are numerous osmiofile granula (G). Mag: 19650x.

t• ,

i

i

4 240

Figure 1). Longitudinal section through the breast muscle ofhypokinetic quails. The membranes of the cristac within themitochondria (MI) lose their characteristic internal structure;the outer membrane is damaged as well. Mag.: 19650x.

5

^t

r .^

Rp

Figure 6. Longitudinal section through the breast muscle ofhypokinetic quails. On both poles of the altered mitochondrion(Mi) are fat part i cles (P) measuring 0.8 um. Mai;: 19650x.

n

/541

6

t• .s;..sr•. ^,^. . M • `^" •,.y •r.T-t • •r• '• N's. 1e r.... ^.^.t ^S}

^ 4

r'igure 7. Longitudinal section through the t rt. a:,t muscle ofhypokinetic quails. The inner membrane of those mitochondriawhich lie in close proximity to each other (Mi) are vacuolated.The large fat particles (P) are occasionally located in a lateralposition. MaF.: 20750x.

Figure 8. Lon t;ituditial section through the thigh muscles of /542hypokinetic quails. The cristae disappeared in the middleof the altered mitochondrion (MI), but the outer membrane isstill intact. The H-zone is characterized by the alternatingpresence of light and dark filaments. A slight shift of LheZ-lines is noticeable. Mag.: 1b000X.

t 7 ,

^r'S•

r ^^ r t

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Figure 9. Longitudinal section through the thigh muscle of hypo-kinetic quails. There is a destroyed mitochondrion (Mi), theouter membrane of which is not destroyed. There is a triad (T) inthe vicinity of thr Z-lines. Mag.: 16000x.

A further interesting finding concerned the fat particles,

which were approximately 0.8 um in size, and were localized

primarily at the poles of altered mitochondria (Figure 6). oc-

casionally, they were also observed in lateral locations.

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The mitochondria of the th igh n~usc les o f t h e t e s t animals 1543 ,

showed changes similar t o those of t h e breas t muscles. The fox- lawing c h a r a c t e r i s t i c f ea tu res ware observed: i l lunt ina t ion o r the matrix, disappearance of o r i ~ t a e , and the! des t ruc t ion o r crist;ae without damage t o the out;e?r n~ambranes (Figure 8, 9).

The sarcomez1es of the b r e a s t and t h l g h musclee of t h e hypa- lcinetic q u a l l s wcpe chrrracterized by tile constant exchange of A- and X-bands. The Z-lines, however, did not form a coherent zone, b u t showed a s l i gh t ; shift I n some cases,

Discussion

Our i n v e s t i g s t i o n s allawed t h a t t h e mitochondria J.n t h e M. p e c t o r a l i s thorac ius 8f Japanese q u a i l s a r c numerous and cons i s t of Large fi9amentous and small ovoid rnil;achondria. They a m locai:eci per5.nuclent;e and 211 the c e l l membrane; sometitnes they a r e between t h e rnyofibrils. The M, iX io tLb ia l I s p o s t e r i o r con- %&ins f ewer rttktachondria than tile M. Fec to rn l i s thorac icus , and conta ins mare small round and ovoid mitochondria. These &re mainly loca l i ced i n the l ayer o f t h e i s a t r o p zone of the ~ a x ~ c o ~ n e r e .

I n t h e Iczngitudi~ial sectiom of the th igh niuscles of hypc- k i n e t i c q u a i l s , t h e 2-lines which separa te t h e snrcomeres (Allen, 2.973) cauld nat; be found i n otie Xayer. rat he^, they made the impllession Lhst they were s h i f t e d . Th i s phenomenon could stem from an ndaption of' t h e t~ iya f ib r i l s t o a l t e r e d condi t ions (Zelcna and Jirmanova, 1973) . Tile funct ion of the r n i t o ~ h o ~ a d ~ i a , defined by t h e i r enzymic content , i s t h e f r r o l e i n c e l l r e s p i r a t i o n , o r oxida t ion , i . e , , , t h e t r anspar t of e l ec t rons froni t h e diffez*- an t s u b s t r a t a ta t h e f i n a l oxygen source. Aside frorn t h e i r job of d e l i v e r i n g energy f o r c e l l funct ions, these organel les a l s o use energy to keep t he c e l l s t r u c t u r e s i n t h e i r normal s t a t e (Bsozmat~, 1965). They a r e very complicated u n i t s and are h i g h l y s e n s i t i v e t o t h e impact of a l t e r a t i o n s . Diculesca and Fopesca (1973) suggest t l~at ; they a l s o f o r ~ n ar'l accumulation zone

far calcium i n %he s t r i a t a d muscZe systam. Barta, 1973, Devine, e t ax., 1973, th ink t h a t thia hagpenu when t h e r e As a surplus of a tored calcium i n t h t ? b ~ E ~ u $ c S & ~ . The calcium 1 rs probably t ranspor ted through t h e Cu,tdiis.trcreal channels af the mitochondria,

The e leccron mieroseopc st t ~ d i e s of t h e mitochondria af bhe bveast and $high musc?es of Japanese qualla w i t h regard t o experimental hypokinesis have shown that t h e changes which are caused by t h i s s t a t e can b2 observed on singbc mitochondria witbout a l l of' them being af'fected.

During fiyymkinesis, t he b r e a s t musc1.ess exhib i ted mainly orthodox forms of organelle^, whose typic81 s t r u c t u r e was maintained, and which was charac ter ized b y t h e formation of numerous long m i t a c h ~ q d r i d c r i s t a e , t h e l a t t e r f i l l i n g t h e gap 5eBwesn the o u t e r men;branes. The forntatiorc of c r l s t a e

i s a measure of t h e ~nagnltude oS energy production, shown i n t h e arnaunt of ATP foraned by t;he iaitochondria.

In some of t h e mitochondria, small l$ght vacuoles could /544 be observed; these were general ly loca ted i n the inner periphery of the o u t e r metnbranc, A comparison of t h e electragrams proved tha t the Al te ra t l ens probably manifest themselves a s a fusion of small vacuolcs i n t o lapger ones, which means t h a t t h e contin- u i t y of t h e mitochcrndrial c r i s t a e was d is turbed and t h e matrix i l luminated. Tt i s i n t e r e s t i n g t h a t , i n t h i s atat;e, no dis-

turbance of t he ou te r c e l l cotnpartment occurs. The only a l t e r - a t i o n observed i n these nlltochondria was a d i f f e r e r ~ t grade of hydration. The f i n a l r e s u l t of t h e a l t e r a t i o n s was, i n some cases , a t o t a l d e s t r u c t i c n of t h e mitochondrha whereby the outer cor tex dAsappeared e n t i r e l y ,

It appears t h a t a s long as the ou te r membrane of t h e mito-

chondrionis maintained, t h i s process i s reversLble, and can

bhercfore be regarded as t h e minimal barnagti which can occur t h r ~ u g h lhak af axygen caused by inac t iv2 ty .

T t i s aacumed t h a t p a r t i c u l a r l y t h e b r e a s t muscles of f l y i n g b i r d s are metabolicaLly much more ac-t;ivc, and have 8

higher rate of oxiddtlon a c t i v i t i e 8 . Similar condit ions, al- I

though l e s a a c t i v e , seem t o p r e v a i l I n t h e th igh muscles, Therefore, a f t e r lengthy subdectian t o hypokinetlc condi t ions, energy l n s u f f l c ~ e n c y and, as a consequence, hydration of' t h e mit;ochondri&, w i l l occur. The i n i t i a l a l te ra t ionts concern the mitochoneria crSs*ae, where t h e enzyme systems of t h e oxi- daeion phosphorylation and of t h e e l e c t r o n t r anspor t a r e lo- cated. The penet ra t ion of water Znto the mitochondria removes OP destroys these enzyme systems. Consequently, the requi red energy can not be produced, which causes f u r t h e r damage of t h e micochsndria (David, 1967, Krolenko and Svinka, 1974).

During ext;ensive r e s t r i c t e d 1 2 f t i n g movements of the l i m b s

of dogs, Kuprjanov e t a l . (1975) observed a reduct ion i n the s i z e of the mitochandria, whereby small nound farms w&th a reduc- ed number o f c r i s t a e and a thickened matrix were t h e majori ty . The mitochondria only decayed i n p laces where myof ibr i l s under- went t h e l a r g e s t a l t e r a t i o n s .

A moderate increase of p a r t i c l e s normally located at t h e pa les of t h e mitochondria, o r a t l a t e r a l loca t lons , a l s o ind i - ca tes a c e r t a i n lack of oxygen.

It can be concluded from our i n v e s t i g a t i o n s t h a t t h e a l t e r - a t i a n s of' mitachondria of the b reas t and th igh muscles of Japanese q u a i l s wi th regard t o experimental hypokinesis a r e probably caused by energet ic $nsuff iciency followed by hydration of t h e organel les . Because of t h e damage of t h e mftochondpia c r i s - t a e and t h e matrix, the funct ion of t h e enzyme system of t h e my- tachondria i s dis turbed. A s a consequence, c e r t a i n ca tabo l i c

aXtera t iona i n t h e ox ida t ion and r e d u c t i o n procesa I n muscle a c t i v i t y can occur,

E lec t ron microscopic s t u d i e s have been c a r r i e d o u t on t h e mitochondria of t h e t r a n s v e r s e l y s t r i a t e d muscles wi th r ega rd t o e x p e ~ i m e n t a l hypokineais . A s compared t o t h e c e n t r a l group t h e mitochondria o f m. peetorallej, t f ~ o r a c i c u s and t h e m. i l i o t - i b i a l i s p o s t e r i o r i n hypofcinetic b i r d s r e v e a l marked changes. Sn f i lamentous and ovoid mitochondria vacuoles can be abserved which i n some cases produced Larger l i g h t formations wi th f o l - lowing disappearance o f t h e c r i s t a e and d e s t r u c t i o n o f mitochon- a F a t p a r t i c l e s l o c a t e d a t .tihe p o l e s of %he a l t e r e d mito- chondria, spo rad ica l ly s c c w p ~ a l ~ o l a t e l t a l l y , p resen ted another f i nd ing , The Z-lines of t h e Sarcomre d i d no t form a cont inuous l i n e , bu t were somewhat s h i f t e d .

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