EVTDENCE FOR STEI{ CELLS IN THE ]\IESODER}I OF HENSEN'S NODE
A^"D THEIR ROLtr I\' trN{ARYONIC PATTERN FORNIATION
li{ark A.J. Selleck' and Claudio D. Stem
p - - L sR o - J .O \ t o r d O X t 1 e \ . t K
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r ed e r i r o n
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d . 3 . h ' c r c n ' n tgr r h e f u n - e . . ' L d - t( r d ^ . t < r . r o J c r n ,i r \ r - b . n e d l h
r h e e D i b t a slrL.
elongarescrnnially over rhe ncxt t hours. whlle a goove apiers atong irs l€nith in rh€
midline; cells migrare lfteraly from ir ro form rle eirty mesiitenn ana ite defin-itive(sut)
e r d o d e r mA. r r h e , l c f i r . . \ e . n e J . r - ; e , l ^ l 8 l o r i r a u b l r o n . . r , g er , r n e s m , t e r r e ' n a .
e . n r n , nsrr o \ r r .l ,) r n a p r A l e n u r r o r \ . . p t r . 1 n d . . o r c e . . t e n n e d H e r . e r . n o d e .
ll er vrllor llil.en {lo li^r de\ oed t r,.l^:o.
M r n \ L n e \o i e ! : J c r . e : u e g er r d I t c r . p n . n ^ d e3 \ r h e u r g d 1 i . e .u t r h e- n n , o r e
e r n o t o . . r r . c . r c . ' n I n J u . er h e t o m . r o r n f J \ e c ^ n ue r n b r y o l i cJ \ r . r t g r x t r e di n l o x h ^ . 1
e l h r \ o n L c r ^ l k cr 1 eJ , r . | . , o . r r h e b l J r o p o , . . . , , e , m p . t r , " n , r o r * i i . * . , . i 1 * i r " r ,
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o n r ' . , , o r g : r n r . eer r p e n r i r e n ra,r d h - i .
r . d r ) ^ ^ o r k f l. / \ d l - f l I r ^ < C J . , e r J .t q 7 l . \ t . c J l i o r n d S t n o " ,
, ' . : r r . , . : r 1 ds c t 4 ( r q o l t ' ) " 0 ) f r f l r e - . . - - . v l e 1 l h e l o J e
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r ( n J i r . s : r L ,r 1 ^ . ec e . o f l S , n , t r . J h c l t e dF. L f l h r m u r er. 1 ( , . . " " , " "
:K-\:,,,l,ri l! u c !
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Fig. L Diagran illustratingthe faie of mesodennceils widin diffcrent reqions
o f H e n c e nJ n o d ea n d r o , r , l t r i T i v e , l r e d t d t r t e J e f i n i u v ep n m n v e , n e a l
n d g e t n d V ^ h a r c d m . d l . n e; s i o n o f r h en o d e ,m e s o d e m. ' e t t :w r c o n r r i b r . r e
only ro nobchord, whil. in more taleral rcqions, cells wil contribure to thc
m e d r d lh a l v e . o i . o m r r e s . T h e d o r s 3 lp a , . ro f r h e I r r e r r l r o d e s e c t o rd L o
contarnspresunptive nobchord cells (not shown).The laterdlpans of somires
f f e d e r i \ e d i r o n m o r c . a u a a lr e f i o n . o t t l - ep n m i ! e \ $ r d t .
(stage4),_prospective
notochordcells arEconrainedwirhin a V-shapedmedial secror,and in
r h e d o r : J l p a r r so i l a , e r a l. e c o - . r t - . s . 1 , . T h e m e s d e r m o f r h i t r L e - a t. e c r o r s , o n r a n r
D r o s p € c t ' \m
e c d n l s o m r e. e l l \ . * h i l e r h et d r e ' J h
1 a . v e so r . o m e . d r c d . r i r e d i r o m r r c s r o n
o r r o - o d r p i r u \ e r r e a l : j r u 3 l e d b r h : n J r h e n o d e , l - i g . l ) . T h e r e , L t r , o b r a r r e df r o m
r n j . c r r o no t L K D r n l o s i n g t ec e t l c\ u g C e . rl h r r r t - e, e g r o n sj n l r ^ e n i n g b e r q r e nl h e m e d i - ld n d
rarerdrsecror{ r-onrirIn jnrerm.Ltia.ecetts. qhose progeny can conmb.Ie to borh nolochonl
. t J 8 f . 1 - 1 - . t r r en o d ea l s o c o n t a i n sp r o \ p e c r r v e r d o d e r mL f l l \ .
a n o ,m e ( r l a r r l
_ . n me . A t
A l l : t e r s r x g e .r 5 - a l . t \ e m e d i d lV . . e L r o rb e c o m e sn a r r o w e d
r s p r e . u m p u v en o r o c t . o r\de l s
are lost from lhe node, and rhe proponion of prospecrivesomird cells ;ithin ir increases.
t
Commitmenl of node mcsoderm c€ttsto their fates
T o r e \ l t \ c c o r n m i r r e n ro t c c . r o r t - e r fr a r e s i.l i { n e c e \ s a 4l o c h a e n s el h e t r r e r J t
.
rhecellsin Jirrercnrenvronmenr.. w. I rre ped.med e\pe,i-en,sio i"i;snq"i; ;i.;i;.;,;;
I
p r o s p e c r r \neo t ^ ( h o d d n d . o m , r el ' r l . q . r h i n H e n . e nr n o d e$ e r o m m i l l e db y h e r ( r o t o D i ,
gr^afiingbetweenvarious secrorsof the node and rosnat primjrive streak (Selt"it
I
l o o 2 r .T h e c e i l . o f r h es a f r r o e l d b e l l e dw i r h D . t r o f u l t ; $ r h e i ri ; c ; ; o m i i o r i i " , . ""J_St"'.".
a
i
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i
.
*
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,
r r \ u e \ : n o l o c h o r dq a . i J e l l i l ( d u . r n gd . p e c i f r c a n r r b o d yr N o r t . y a . r J d J e r a l . , I v o t ) . A l
s
r n e c e l r n r h v e\ t r J r y i p e . t r c s p e .r j \ e n o r o lh o r dc e l l sa p | c a rr o b e c o m m r , r e Jl o r h e i rf , r e ,
b r ( a u . e , r l l sr n r h er r e dJ l r o d e . e c r o ' a t w a t \ ( o n r n b L r t e r o n o t o . h ^ r J o r f o m \ o l t - D o . i r . r e
n o r ( ] c n o r d - r rs\ eo L c r L , r e$.h r n F r d f t r Ji n r od . i i e r e n p
l o s i r h , 1 i.n r h e( m b n o I n c u n r i d , rl.n e
p r c . u n r p t r r e \ o n r r e , r . d r e r b l c r o c o n r i b u r e r o n o r . \ h o - d d 1 , 1 n " r q . r h \ o r t . . h o $ i r g r 1 , Il l
rney are not conrmittcdto a somilic fale.
fi
Wc were unable lo deremrine the time ar which nobchord ce s firsr become
r o - n r n r r l e r Il r . . J I f r c u l rl o p e r f o r mg - a l D l g c \ p e r i m e n r .l o i n r c " l i r d r r r h : . d r \ l o e r J o r
e d r l . e r s. r r c e l h e n o r u L h o f d
c e l l , c r e . n r e a Ll jh r o , . g \ r o urrt - en o o e ,i ; r e m r n e t e d$ i l i o r h e r
p r o s p eILr e c e t t t ) o . . . I t r s e v e r .r , I c et i n e so I e \ r d e r c es u g g F , Irn , l J r l e r r r o l n ep r o . n e r! i v e
notochord cells bccome commilted to their frte in Henscn,s nodc. The fust ii rhai sorne
i n d i ! i d u a lr r l l . r n r h ec t r b l r n . t r f e n o d . , : n p o p L l l r eb o r hr h en o r o ,h u , dr n d r h i n c L r J tr u h .
a . l a l ea ss l o e e4 . \ h l ' w l n l t h . r lt h e ) c i r l o l y e rb f J o m n . r l r dt o e l h e r t r r e ( 5 e l l e c kd n d S , . r r .
r s y r ) s e ( o l d . r h c p ' o s e n )o f r i n E l e . e t t . t y g b r r w e c . r t . em e d i r td n d t : l c r u tn o d e . e c r n r .
c o n r n D u l teo b o l h n o r o c h o rrdr J , o m i e l S e t t e r ka n dS r e m ,t q o l , . T h e l t r d D i e c eo . e v r J F n c .
r \ l n a t p r o s p e c u \ e. . m i e c e l l , i n t \ e t a e u . n o d e. e c l o r s, : r r b e c o n r e
noto.horJ.c \ $nen
S t " f l c d. n r ou r em e d i r l . e c l o r .q n i c h s J t S e . r .l h a rm e c , r l n r . r nt., r J l. D e c i f \! c l L $ n o t & n o d
d e r l r l l o f c r J f i n dr r l h i \ s t a r e( \ e l t e c t d r d S t e r 1 .t 9 9 ) r .
I r s e e m .| l ( l ) t l p r e . J np \ e n o r f f h u r uc e l t \ b e L o m ec o r u D e J w t e n r h e r e n r ( r
.
I n e m e d . d rr € c t o ro l l h e n d l c . W h J t ( u u l d b e l h e m r c h a n . , m tA n r p h : b i a ne m b n c i c o L , o
provide ptn of th€ answer.Lr Xsn,pJr', facton relatea to rCrp, especiattl,f"
".ti,i"r, "r"
24
(r
fr
I
F
Fi
in
da
lhr
(F
induce ectodermcclls 1o becomenotochord(Greenand Snilh, 1990: Snirh ct al.. 19901Van
den Eiinden Van Raaij et al.. 1990;Greenand Smith, 1991).They operatein a concentrarion
give dse to notochord(Greenand Snirh. 1990;
dependenrmanne. the highestconcentrations
'orgdniser'
activity when mixed wirh untrert€d
Smirh et a1..1991) ard to cells that display
cells (Greenand Smith. 1990).I! has beensuggested(Smith et d., 1985;Srewanand Gerhan.
1991) that organisercells are responsiblefor the induction of nobchord. lf the norochordis
specifiedin a snnilar way in the chick, ihen one might expectrha!cells with organiseractivity
will be locatcd in llensen's node.
If'organiser'cetls are presenrinrhenode.and servero commit notochod celts!o their
f u l e .w h c , eJ o r h e yc o m ei r o n f ' B o r h t u r et r r p s r n d s p e c i f i c a l i onnu p s o f r h ee p i b l d . la r p l t s . n . J t . r d g . . p l a c er h ep r e :J m p r \ e r o r o (l o r d c e l l sr i r h ec c n r r eo f r l i e b h . r o J c | m\ R u d n r c k ,
19.18;Waddingron, 1952j Balinsky, 1975), which may indicale rhar tlresecells ar€ alreadv
commited to noto.hod. Iiowever, rhis nnding is also consisrenlwith the vjew rhai this resio;
containsorgMiserceus.Whenisolared,sornecells;ndrisregionwouldfonnnobcho,u;der
'lhis
the inflLrenceof lhe orgaDjsercells.
conclusionsuggestslhar lhe tip of the etongating
s i F : . k b . r s e e n . r . , g e ' 2 J n J I d o e , n . r y e r c o n r J i n o r e . , n i . e rc e l t s . 3 n d r h . ' e r o r e n ;
p - o . p e c r i v en o r o c \ o r dc e l l s .T h e, c . e 1 . . c r n o n \ b € r e c f l , i r e dw h e n r l e u p o r r h e \ n e , l
' e a c h e sr h ec e n l r co f r h eb l J s r o J c r r . . ra b o J rn l s e . 1 .I h r \ r r r e e sw i l h t h et n d i r p r o t N i c o _ e r
I l a 1 0 ' . q h o i o I n J r \ r r r 1 e r i p o t L n e. r r e r ka r s i r g c 2 d o e . - n o tr o n r i b L r er o r f ; n o r f f h u , J .
chordcells
andStern,
o differcnt
1991).
Ar
rheirfates
tl positive
nage3 or
The organise. cells found at the centre of the blaslodem mav orisinate from the
p o se n o r e n d o l r \ e e r n b r l o .a r o r n e d rr h e p o s r e r i om
r a r A i n a,l " n . ,
ctril.o -poe-s ro
h a r 6 s i g , . ; r . . q u : l i r i e ' r J c h d . c o n n o l t i n sr h e o r i e n L r o n o f r h e o"nr 'r i I l \ e , r r e u t ir E r r l C . l J d . l n J S t r d . l o o 5 : A / r J r d E y r l - G i l J d i t. q 7 o .t a 8 l i M , n r n : e ri t . t o c l i ( l r n e r e i d t .
1985; Khaner and Eyal Clladi, 1986; 1989: Eyal-Giladi and Khaner, 1989i Stern, 1990).
ClJbunpdni.le rrkrnc exFnmenr\ rSlmrr. tolo) .hos rhJrbriolE rfe nrimilve srrcat
. , p p e 1 r rc. e l l \ d r l h c p o n e r i o r e n J o f r h f b l d s t o d e n .nl q r a l e r c s r r . . \ . t h i s f i n d r n s r s
c o m p a u b l es i r h c m o r e m e n lo f o r g a n i s eLr e . t sr n t \ e e p i - o t . stl o s x J d sr r r ec e n r e o t - r h e
b l J . r o d e r mp n o r l o s l r e i l o m a r r o n ,a n d m a y r n d n a r er \ J r o r g a n . s ecr e . p l a ) d i t f e , e r r
controlling roles a! differenr sragesof development.
HENSEN'S NODE AND THE GENERATION OF PATTERN
Periodic contribution of node-deriy€d cels to notochord and somite
O n e s r i k i r g f i n d i n gu b r a i n e di r o m o u r \ i n g l e c € l i n e a g ee \ p e r i m e n r s , S ee c k _ n J
^
5 r e m . l e wr l r \ r h 3 t I n s o . n ec a s e . .t h e p r o F e n yo t \ i r g l e L R D - l a b e t l e(dc l l . q e r e a r r r n g e Ji n
a p e n o d r cr a c n r o nI n r h e r o l o r h o r d a l d r L J m j l er.F r g 2 d ) . S e r e m tg r o . r p so f l c b e | e d c e t .
r o u l d b e f o u l d a l o n gr h el e n F r hn f r h r n o r o c h o r de.r . r s e p a r a r ebdy i b o u i : , o m r r ei n r e r a t s .
l n s p e c r m e n \$ h e r e . . n 8 l e . e l l . i r H e n . e n\ n o d e p o p u t r r e dt h e . o m e c . a b o L r 2 _ J
c o r s e c U I ! e\ o m i t e ss e r e l ! b e l . e da f i g 2 d r . { . r \ J D e n o d r c i ioyt a b o u l5 6 s o n r i r e iA \ r m r t a l
l r r d r n g q a ' n d r j e q h F l D j l l d b e l l r J l d r e m tn ^ l e r e c l o r sw e r ep t J c e di n r h e m e d i r l s e c t o r
r S e l l e . kr q J S t e m . l q o 2 : I r g 2 b . c r :t : r b ( l l e u. e l t s p o p r t : r r e Jr i e n o r o . h o r di n a D e n o d . c
I n . ' r i o l T ' l e ' e f i n d r n g sr r e c o n , : s l e n lw i r r ' e r d p ; r h J t H e n : e nr n o d e m c ! L o n l a i l
p r e ( u m t l r t en o l o c h o r dr n d , o n r e ' o u r d e rL e l l s ,w h . l e m - c e l t - l i t es,e l L r e n e q
ins ,bilnv
Founder cells and stem cetts in the node?
_ Fu.ther evidence rhat the node conrains stem cel_like celh that crn sive ise ro
n o r o lh o - d L r t e f i l J n s r s e e c k a n d s r e r 1 . t a q l I o f a g r o , p
. . r L i r , " ,i i " i i p i r " , . r r , i
r n r r c i e n e l n o r t h e r o r . { t - o r d . t ) . n g b e r " e € n r h e n r r r J t r 1 d" t t : r e r : t r o d - s c i r d r , . T h e s c
.
r
o
t
o
(hord
u D s e n a r r u nl sg g e s t r h J t t \ e l o J c c o n r x i n ra p n p r t . o n o r
r o L l J e rc e . L f a , .
n g . l r q . r r 5 r e n r c e l l p r o f e ( i e sI e: , c h d i v i \ r o n o f u n c o f t h e . e . ( l l . , o n e d : r L e h r e r r e m i ] l n j
I n I m n o d c a n d b e c o r r e s( h e p r o p e no r o . . u b \ e q u e r l g r o u p so f c r l l s , u h l r t r f e
ol\er
a r u g e f g r \ e s n . e r o a s r l g l e . m o r e r n r e n o rg o u p o f L e l l . . A r e r c l d i r i . i ^ n o f d t o J n d . - l
c e r " I n c r e r o r er .h et l e . t e J . e l l a n d i r . p r o S e n yo c c J p ys u c c e s s r v eTt yo r e p o . r e f l o rt e \ e t , . l
r 1 c n n r o . r o r d s r l h ( t L \ . e r s . i f r J l e d b y a b o u r2 - J s o r n e l e n q . t - s
l,1{yrtT) fhe di\t.n.e
m N e c n - L c c e . . . \ ec l . f r c ' . $ o J l J h e d e r e . m r n ebdy r i e r . r e o f , l i \ , . i o n . f r \ e r o . n d . r
. el
I r ( ^ r . $ l r . l e r t e l e n . r ho t e d c h r l J r e rd e p e n d .
o n l h e m r eo t , j i \ i . r o n o r i r d : r J e f . e . s .
24
25
!,i.
26
Fig.3. Djagmm illustrating a stem cell and founderceU mcchanismthat mav
. .r e n'r. 1 1 , , \ l S C r l l r n g
c r o o . p a r r e r ;i u l r l ( r o r \ h . J , r l s o r n r r e S
betlveenthe rnediil and latcrnl node secton give rise to diughter cells !hr!
populate borh areas. There d:rughrer cells arc founders for prospcctive
notochordor so'nirecells (FC. and FC" respectivcly).The ceU cycle dnre of
rhe notochordfoundercells i\ different fron thar of somite founder cells. The
cell clcle tine of thc founder cell\ will control lhe periodlcty in allocationof
cells ro thcir mcsodermstruclrrcs,
Nledial sonrLlecells also secn ro be denvedfrom foundercells in Hensen'snode(FCr:
L r J ' . S | ; l c L r t c l l c d . e l | . g r v ( r i . r r o p r c r e n yr h ] l f f e , i n r i t t r t ) d r r a g e o i l r o r t J . ( e | sr n
r h e r c d i : l h | \ c ' l r h < . o m . r e : . e ^ r L u . r ebre . n 8. o n c I ) , o r n : r el s. 1 g r " o u - rr 0 0 j 0 o L l . r
Fjg. ld) nnd $lth a stacing of about 5 6 sonites (800pm).Thc differEncein spacingbctween
clunen in norochod and somitesindicaresthat erch kind offounder cel hrs a chtacteristic
. Singlecellslying be6veenthe ncdial and lareralnodesecrorsare abtero populrte borh
norochordand sonires.Theretirre,fiese nrxy represenra populrri{)nof nmlriporini sremcc s
(,\rr.SC:
Fig. 3), which sives rise ro rhe foundc. cetlsof borh ti\\ucs (FC. adl FCs).Thc re
o ' d i / , . i . 1 o 1 . J ' L g h r e ro. r \ 1 . , , , ' r ) b e
, rd rh.\ .re.pc.irrca.
n o r L r o r d f C . r o r s o m r r e( F C , f o L L n L !j (crt \
I I c n s € n ' sn o d e r n d t h c c o n t r o l o f s e g m c n t r r i o n
bur have
. .NIxn)*orke^ hl]veinvesrigxr.dltre role of lcnlcn.s node ilr somit(,gencsis,
r c l c h e dc o n f l i c r i f gc o n c l u s i o nass r o i r s i m l o n l n c e ( s e cB e l l a i r s ,1 9 6 3 iN j c ; i e r , 1 9 7 1 iS l e m
3nd tselhirs, 1981i Bcllairs. 1986). This mry bc dLre(o rhe absenceof deraitedinfonmti(nr
xboul lhe ccllLrlnrcontcnrsof (he nodc. N.Ioreorer,s(!nc workers have assum.d llrar $e node
compnsesonl! tfesumprile nobchord cells.
I ' r n o r , S . l c ,n : 1 J S r . r r .l a r . o r J , l l l l d L e D o , . : l J i n
. q. o ) / . 1 .r \ o r r r . : r e
. . l r d r d . l h . r ' i d . : r l . l J l .c - . ' ll : 1 . c . ! c i \ - d l I . n r s u \ J p r r , . e . o . . r c e . \ t : r ( r r t
,u,.eJno
rJrteno.lrimiti!e srerl, resFclivelyl suggesrsrhat ftis duai origin may pliy an nnponanr
rore.rn \ome aspeclof !)nrjtc developmenr.Howeler, de\fite a difterence in f.]le of nredial
. | ' r r , . 1 ' I c . e| | . Ir Ir | . c t . i , . , o 1 .t . \ , o p r . . r r o b e r . + i r r- t
ItJ L il. Jn I
u , 2 . t . r t r p . r n ( n . r i r , l . . . n t: r b u i \ i . i J , s o n i r . ,r . f l r . . . .
0 . 0 . . ) . . . r r . d f " r , r (t . n e r ' . , r . . r . e r . ..r. r i . - J c r r d t h . r t l , r r ^ r , e . L D c e . t , . e - l
'Iller. i
o rJ r r . r : \ \ l l l o e . B . i .
.rd\ii.
t o 8 r . e e| . o B . . i , . . q x o l d r c
Ide.lL.
k r ' r . . . " 0 ( p ' . . i l . r ' l - r r r l - 1 ' s l c h r ( c - i r . < l. r u r .
r e r : n - rc J o . r ' . . I t e . o d r r 'rr^r u T . o r r t , c v l r o p o . er f . r r n ( 1 u . , t e ro t . - c l
c:'(.
. . . 1 . l . i r ' r ' , ( r l - . . u . . . . , r r. r r r t t o n r , . 1 r0f r r \ . . r c , lnerd . e | .
m*c up cell numbersso that sLrfficientcells gathert{) form indilidud $nrircs.
-..,:r.;.,i
I
us;uu****'ru$*
'gr,*+*;l1;r$*p,5
l*
,,,lull,,,ti',l.;
irffir:*-*t
$g********g***
*nt*:#.ffi*.i*iil*
ffitr*nm*r$ffiN
2A
i
'
NODE EXTIRPATIO\
REGLLATION FOLLOIIING
has
that Hense.'s nodeconlainsorganisercelis and
TtreDreccdjnsdiscussion suggcsrcd
wilhin
ii
.ts
it
rcgre\ses,
r.tlhrr thln bcnrg nErely a passage*av for
;eixined
sten cetls
O c p r o o l e m ! i r \ r h . . r j s i . r \ - r r o d . f \ r i , T - r i ! 1 J r - . ' . r , l ifu \ e . r r e r k r o r . r . o n
. r " r i d . l o \ . n r o r e^ r 1 . . . l u r ' ,
R
Jc\clofrer . pro,rdeJIn.,r ,(
.hc u. ir''.
"{ ro L r d h . . l ' ( $ , J J . n g r o r . l o . 1 :\.l - _ . o - b r e .l ' 5 u . S p r - l r l.0 5 < . G m b$ . . i o : o : C . l l c r , .
- 9 o 5 , t , : o - r : b : G r l l ( r r r d \ i c o l e r . l o 7 / : H r r . a 8 ) | n d e -3 p o r o o n r r eo, r . i ^ n . .
. - . 1 - . , , b q . ' o n . n o r G - \ o r d 3 d o m . l e sI .r : r l l , . i d c . e e \ | e i T e r r ' r ' r e e r n h r r o . l o ,
a remarkablcability to compensalefor the loss of Hensen'snode or for a large disturbance
in its posirionor odemarion.Il rhereare specialcclls !vi!h organiserard sren cell prolerrie\
in the node,1henlhesecells and propertiesmust be mnintnjnedas a resLrltof interactionsltirh
ltre neighbouringcells, and rheseinreractionsmusrcontinueat leastundl rhe dennitive sre*
srage.
CONCLT,SIONS
Ilensen s rode appean to contain a popuhtion oi organiscrcells reslonsible for ttre
connDixnentof rotolhord ceLlsro their fares,lnd a popularionof srenvfoLrnder
cetts rhrt
contribL[eto somitcsand ro rhe notochofd.SonriticfoLrnderce]ls ame!. to be responsibl€for
conrrollingthe spacingof the segnrntrl patrem of somites.
ACKNOWLEDGEMENTS
I rhe
The frre nrapplng and conrmirnrentexperinrcDrsdescribedin this
raper were s pponed by a wellcome liust Prizc srudentship.
will
- o ' L \ e r . . , . . n lt . . - : r h . J .t c p n | | r i \ .
\\","a b'e M. o.n |
. .. n ' i.l
' r ' . t 1 11 1 1 , . ! 1 1 l r . , h . \ \ . . l , { I H ' 1 t r t - . r r i
-tt.
\/.'r. Y. . lJ F.-1.. L r
..=4. it:-t
/.
ll
t c p n - r i . . \ , r - J ^. r o J ! . r ;
c " r l o nr r ' l c t r i r ' \ L r " l " r n l . r . ' .I l n r o r r . l \ r v o - ! r . . 5 1 . - \ - a r
\.
\ . . 1 J . \ , c ; . , , r i . t , . ' . r . i n , r . , r r o r . o t , o t o . . *. r. , I . o o o t - - r l i l - i T , m . o
. .n o r
thc pnmitivc strelk md the ernbryonicrris in rhe chjck. as releated by hypobtast
. o t . u i o ne x p c r i m e n NJ,. I l n r b r v o le. x p l \ j o l ' ! ) h . , 6 l : 1 3 11 . 1 1 .
Balinskv, B.L,,L9tj, tntroductic,nto enbr$rog).!r-.!rir Edn., Saunden. phjladerphia.
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I l 6 t 7- 7 t J
Bellairs, R, 191i6,1he rail bud .]nd cEssarionof segmentatjonjn lhe chick embryo,
I!:
-\on
r r ' i ' d e r i l o p i l !t si . n o . . R t { c t . . . r . . t J . \ . F J ( 1 r J J $ . L a , h e d . . p t e r r r l
(.
rrc
LonLlI r
Bcllai^. R. and Venri. 1.1.. 198.1,Experinrcnratan. ysis of conrrcl nrechannmsjn soDite
segme aron in a'ian embryos.II. Reductjonof materiri jn the gasrula slagesof the
r? lf
lbv
:'*
,
ircs
the
.f i-1. J. f:_!r.-!:r
l&_!r.'"
tsj j0,
I t . , . . \ l S . , r r S c. n i r
.
" o l t C . a . . l . ! , ) f n m x | | ^ n o f e . l u p i cn e L r e p . r l (nt i n . L . k
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,, /o e rrd pdT,,.\e rerr
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n s p r r A-. iI o) e vB. r t ] .l l l t : 2 1 - 5 - l l l
I I G i l , d .l.l
5 p r . , .\ , J r . t ' , - r . I e e , n D r \ . - . r r . r t s N r r c . e . o
r ht F ) , , - , g . i . . r
b t r . t c a J F 1 r ^ . - \ p \ t , , nt . l : t n - - : 7 1
u } e r . r . . , ! ' , : . h \ c r , r c t l r . . n . p t . , ru
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.
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